Marine biology in time and space - Vliz

marine ecology an evolutionary perspective

^

»

EDI TORI AL

Mar'ne Ecology- ISSN °173-9565

Marine biology in tim e and space

Introduction T his v olum e com prises a n u m b e r o f th e papers presented at th e 44th E uro p ean M arin e Biology S ym posium (EMBS) hosted by th e U niversity o f Liverpool in Septem ber 2009. T he them e o f th e science p ro g ram m e was ‘M arin e Biology in T im e an d Space’. The papers focused o n describing p a t­ terns across a variety o f spatial a n d tem p o ral scales b u t w ith the em phasis o n seeking u n d e rsta n d in g a n d explana­ tio ns for those pattern s. T im e a n d space define the four dim ensions in w hich scientific observations are g rounded. Indeed V ito V olterra’s first m odel o f coupled tem p o ral in teractions was developed b y U m b erto D ’A ncona to stu d y the in teractio n betw een fishery stocks a n d fishing effort, a m o m e n t considered b y som e to b e th e starting p o in t for m o d e rn ecology (B oero 2009; G atto 2009). In th e 21st century, new observational techniques, from D N A genetic profiling to data storage tags an d rem o te sensing, have been developed to d o cu m e n t these pattern s, w hile experim ental a n d m odelling approaches are being applied to develop u n d e rstan d in g o f th e factors resp o n si­ ble for them . T he 44th EMBS therefore to o k as its them e ‘M arine Biology in T im e an d Space’ w ith th e aim o f co n ­ sidering recent advances in o u r u n d e rsta n d in g o f th e driv­ ers o f long term change in m arin e organism com m unities an d ecosystems, th e causes o f spatial p attern s in ecology an d the consequences o f catastrophic p h en o m e n a in m a r­ ine systems. Papers w ere p resented u n d e r these th ree m ain them es, th o u g h in reflection o f th e n atu rally in ter-d isci­ plin ary n atu re o f m arin e biology, m an y o f th em co ntained elem ents from m o re th a n one them e.

T h em e 1: Long-Term D ynam ics T he U niversity o f Liverpool h ad previously hosted the E uropean M arine Biology Sym posium (EMBS13) in 1978. A t th a t m eeting th e th em e was ‘Cyclic P h en o m en a in M arine P lants an d A nim als’ (N aylor & H a rtn o ll 1979) an d tem p o ral dynam ics reap p eared as one o f th e them es for th e 44th m eeting. T em poral change in m arin e systems occurs o n long, m ulti-decadal, tim e scales. The im p o r­ tance o f collecting an d m ain tain in g lo n g -term data sets of the m arin e en v iro n m en t is well recognised (D ucklow et al. 2009), an d several o f th e presented papers hig h ­ lighted this (e.g. Ligas et al. 2011; Spencer et al. 2011).

Marine Ecology 32 (Suppl. 1) (2011) v-vii © 2011 Blackwell Verlag GmbH

In d eed for th e stu d y o f long-lived organism s such as cetaceans, lo n g -term an d extensive d ata sets are necessary to derive even th e m o st fu n d am en tal life-history traits (A rrigoni et al. 2011). It is clear th a t m arin e systems m ay be influenced by large scale enviro n m en tal p h e n o m en a such as clim atic variatio n s a n d h u m a n activities, especially in heavily exploited areas such as th e M ed iterran ean Sea (Ligas et al. 2011). It is also beco m ing increasingly clear th a t w hile we strive to u n d e rsta n d th e m echanism s co ntrolling the dynam ics o f m arin e com m unities, th e co m m u n ities th e m ­ selves, such as tho se a ro u n d th e U K are changing over tim e (Spencer et al. 2011). In contrast, surveys o f th e rel­ atively u n m o dified W h ite Sea indicate an absence o f su b ­ stantial change in th e stru ctu re o f b en th ic com m unities d u rin g th e past 50 years (Solyanko et al. 2011). It is p ro b ­ ably m o st im p o rta n t to assess th e im pacts o f lo n g -term change o n species com p o sitio n (Spencer et al. 2011) or ecosystem fu n ctio n in g (N e u m a n n & K röncke 2011). H ow ever, at a finer scale, species-specific studies in dicated differential variability to different sources o f an th ro p enicin d u ced change (Ligas et al. 2011), an im p o rta n t consid­ eratio n in th e m an ag em en t o f com m ercially im p o rta n t species. A ssessm ent o f ecosystem fu n ctio n in g is an increasingly im p o rta n t to o l for a n u m b e r o f m an ag em ent p u rp o ses b u t, for b en th ic systems at least, it is essential th a t m ethodologies be consistent an d consider biological traits as well as sim ple c o u n t an d biom ass m etrics (A arnio et al. 2011).

T h em e 2: Spatial Patterns A n u n d e rsta n d in g o f p attern s o f species d istrib u tio n an d co m m u n ity co m p o sitio n can also be gained b y studies of spatial variability, an d th e presented papers also h igh­ lighted th e im p o rtan ce o f considering a range o f scales. D esignation o f M arine P rotected Areas (M PAs) to effec­ tively p ro te ct vulnerable hab itats fro m exploitative activi­ ties an d preserve biodiversity should be based on know ledge o f spatial factors such as d istrib u tio n an d dis­ persal (K inlan & Gaines 2003). H ow ever M PAs will n o t be able to pro v ide p ro tec tio n fro m extrem e clim atic events (H uete-S tauffer et al. 2011). A t a regional scale, such as in th e English C hannel, the tro p h ic stru ctu re o f b enth ic ecosystem s appears to be

V

Editorial

d eterm ined by sed im en tary conditions, w hatever th e geo­ graphic area (G arcia et al. 2011), show ing th e im p o rtan ce o f abiotic factors. It is possible to consider h o w species d istrib u tio n s are controlled b y spatial factors at m icro to regional scales, an d th eir in teractio n s, w ith in single stu d ­ ies. For exam ple, b o th specific fro n d segm ents an d envi­ ro n m en tal factors o f salinity an d wave exposure are im p o rta n t in d eterm in in g th e co m p o sitio n o f epiphyte and m obile fauna co m m u n ities o n h ab ita t fo rm in g m acro algae (K ersen et al. 2011). A t local scales such as estuarine habitats, th e coexistence o f sym patric an d seem ingly co m ­ p e tito r species can be explained b y p artitio n in g of resources. In th e case o f juvenile plaice a n d flo un d er, b o th flexibility and heterogeneity o f diets appears to reduce niche overlap a n d b rin g o rd er to an ap p aren tly chaotic h ab itat (M ariani et a í 2011). Finally, a key req u irem en t in exam ining spatial effects is th e establishm ent o f discrete p opulations, a process w hich is rap id ly being facilitated by m olecular techniques (Luis et a í 2011).

T h em e 3: C o n se q u en ce s o f C atastroph ic Events Finally, b o th tem p o ral an d spatial factors collide w hen considering the im pacts an d influence o f catastrophic events. This will becom e increasing im p o rta n t if th e in c i­ dence o f these events continues to increase in frequency a n d /o r m ag n itu d e (C erran o & Bavestrello 2009). Mass m o rtality events can lead to change in ecosystem stru ctu re and function, p articu larly if th e subjects affected are eco­ system engineers (H uete-S tauffer et a í 2011). In th e case o f M ed iterranean corals, high tem p eratu re ap peared to precipitate a m ass-ex tin ctio n event w hich was exacerbated b y o p p o rtu n istic bacterial in fection (H uete-S tauffer et a í 2011). C atastrophic events m ay o f course also be p re d ic t­ able an d avoidable. O n tidal m udflats, com m ercial d red g ­ ing for cockles can cause d isru p tio n o f benthic com m unities. H ow ever these systems can recover to th eir original state if dredging occurs at an a p p ro p riate in te n ­ sity an d frequency (W ijnhoven e t al. 2011).

P ersp ectives As ever in the stu d y o f biology, it is w o rth considering th e w ork o f C harles D arw in. As well as his m o re w idely-publi­ cised w ork, D arw in ’s studies o f barnacles rem ain a u th o rita ­ tive (R ainbow 2011). In th e b icentennial o f his b irth , a consideration o f th e influence o f m arin e biology o n the w ork o f D arw in reveals th e im p o rtan ce o f detailed observa­ tion, critical th in k in g an d experim ents to test ideas an d ultim ately co m m u n icate th e results (R ainbow 2011). These principles clearly co n tin u e to u n d e rp in th e w o rk o f m arine biologists an d th e w o rk presen ted at th e 44th E uropean M arine Biology Sym posium was a testam en t to this.

vi

G re e n , P a ra m o r, R o b in so n , S p e n c e r, W a tts & Frid

J. A. Green1, O. A. L. Paramor1’3, L. A. Robinson1, M. Spencer1, P. C. W atts2 & C. L. J. Frid1 1School o f Environm ental Sciences, University o f Liverpool, Liverpool L69 3GP, UK; 2Institute o f Integrative Biology, Biosciences Building, University o f Liverpool, Liverpool L69 7BX, UK; 3University o f N ottingham Ningbo, China, Environm ental Sciences, 199 Taikang East Road, N ingbo 315100, Zhejiang, P.R. China

R eferen ces Aarnio K., Mattila J., Tornroos A., Bonsdorff E. (2011) Zoobenthos as an environmental quality element: the ecological significance of sampling design and functional traits. Marine Ecology, 32(Suppl. 1), 58-71. Arrigoni M., Manfredi P., Panigada S., Bramanti L., Santangelo G. (2011) Life-history tables of the Mediterranean fin whale from stranding data. Marine Ecology, 32(Suppl. 1), 1-9. Boero F. (2009) Recent innovations in marine biology. Marine Ecology, 30, 1-12. Cerrano C., Bavestrello G. (2009) Mass mortalities and extinc­ tions. In: W ahl M. (Ed.), Marine Hard Bottom Communities. Springer, Berlin: 295-307. Ducklow H.W., Doney S.C., Steinberg D.K. (2009) C ontribu­ tions of long-term research and time-series observations to marine ecology and biogeochemistry. Annual Review of Mar­ ine Science, 1(1), 279-302. Garcia C., Chardy P., Dewarumez J.M., Dauvin J.C. (2011) Assessement o f benthic ecosystem functioning through trophic web modelling: the example of the eastern basin of the Eng­ lish Channel and the Southern Bight of the N orth Sea. Mar­ ine Ecology, 32(Suppl. 1), 72-86. Gatto M. (2009) On Volterra 8c D ’Ancona’s footsteps: the tem ­ poral and spatial complexity o f ecological interactions and networks. Italian Journal o f Zoology, 76(1), 3-15. Huete-Stauffer C., Vielmini I., Palma M., Navone A., Panzalis P., Vezulli L., Misic C., Cerrano C. (2011) Paramuricea clav­ ata (Anthozoa, Octoralia) loss in the Marine Protected Area of Tavolara (Sardinia, Italy) due to a mass mortality event. Marine Ecology, 32(Suppl. 1), 107-116. Kersen P., Kotta J., Martynas B., Kolesova N., Dekere Z. (2011) Epiphytes and associated fauna on the brown alga Fucus vesiculosus in the Baltic and the N orth Seas in relation to different abiotic and biotic variables. Marine Ecology, 32(Suppl. 1), 87-95. Kinlan B.P., Gaines S.D. (2003) Propagule dispersal in marine and terrestrial environments: a comm unity perspective. Ecol­ ogy, 84(8), 2007-2020. Ligas A., Sartor P., Colloca F. (2011) Trends in population dynamics and fishery o f Parapenaeus longirostris and Nephr­ ops norvegicus in the Tyrrehenian Sea (NW Mediterranean): the relative importance o f fishery and environmental variables. Marine Ecology, 32(Suppl. 1), 25-35.

Marine Ecology 32 (Suppl. 1 ) (2011 ) v -v ii © 2011 Blackwell Verlag GmbH

G re e n , P a ra m o r, R o b in so n , S p e n c e r, W a tts & Frid

Luis J.R., Comesafia A.S., Sanjuan A. (2011) mtDNA differentiation in the mussel Mytilus galloprovincalis Lmk. on the Iberian Peninsula coast: first results. Marine Ecology, 32(Suppl. 1), 102-106. Mariani S., Boggan C., Balata D. (2011) Food resource use in sympatric juvenile plaice and flounder in estuarine habitats. Marine Ecology, 32(Suppl. 1), 96-101. Naylor E., Hartnoll R.G. (1979) Cyclic phenomena in marine animals and plants. Proceedings o f the 13th European Marine Biology Symposium Isle o f Man, 27 September-4 October 1978. Pergamon Press, Oxford: p. 477. Neumann H., Kröncke I. (2011) The effect o f temperature var­ iability on ecological functioning o f epifauna in the German Bight. Marine Ecology, 32(Suppl. 1), 49-57. Rainbow P.S. (2011) Charles Darwin and marine biology. Marine Ecology, 32(Suppl. 1), 130-134.

Marine Ecology 32 (Suppl. 1) (2011 ) v -v ll © 2011 Blackwell Verlag GmbH

Editorial

Solyanko K., Spiridonov V., Naumov A. (2011) Biomass, com ­ monly occurring and dom inant species o f macrobenthos in Onega Bay (White Sea, Russia): data from three different decades. Marine Ecology, 32(Suppl. 1), 36-48. Spencer M., Birchenough S.N.R., Mieszkowska N., Robinson L.A., Simpson S.D., Burrows M.T., Capasso E., Cleall-Harding P., Crummy J., Duck C., Eloire D., Frost M., Haii A.J., Hawkins S.J., Johns D.G., Sims D.W., Smyth T.J., Frid L.J. (2011) Temporal change in UK marine communities: trends or regime shifts? Marine Ecology, 32(Suppl. 1), 10-24. W ijnhoven S., Escaravage V., Herman P.M.J., Smaal A.C., Hummel H. (2011) Short and mid-long term effects of cockle-dredging on non-target macrobenthic species: a before-after-control-impact experiment on a tidal mudflat in the Oosterschelde (The Netherlands). Marine Ecology, 32 (Suppl. 1), 117-129.

marine ecology an evolutionary perspective

^

»

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

Life-history tables of th e M editerranean fin whale from stranding data M assim o A r r ig o n i1,2, P iero M a n fr e d i3, S im o n e P a n ig a d a 2, L o ren zo B r a m a n ti1,4 & G io v a n n i S a n t a n g e lo 1 1 D epartm ent of Biology, University of Pisa, Pisa, Italy 2 Tethys Research Institute, Milan, Italy 3 D epartm ent of Statistics and Mathematics Applied to Economics, University of Pisa, Pisa, Italy 4 Institut de Ciencias del Mar, CSIC, Barcelona, Spain

K eywords Conservation; demography; M editerranean Sea; Mysticeta. C orrespondence Giovanni Santangelo, Departm ent of Biology, University of Pisa, Via Volta 6, 1-56126 Italy, Pisa. E-mail: [email protected] Accepted: 15 December 2010 doi: 10.1111/j. 1439-0485.2011,00437.x

A bstract The conservation o f long-lived species requires extensive, in -d e p th know ledge o f th e ir p o p u la tio n stru ctu re an d vital rates. In this p a p er we exam ine the stru ctu re o f th e M ed iterran ean fin w hale (Balaenoptera physalus) p o p u la tio n based o n the available m o rtality figures fro m E u ro p ean stran d in g netw o rk d ata­ bases com piled over th e past 22 years. Such d ata has enabled us to lay o u t a first life-history (m ortality) table o f th e p o p u la tio n using a sim ple age-struc­ tu re d dem ographic m odel w ith th ree life-tables: calf, im m a tu re a n d m ature. O u r results reveal a high m o rtality rate in th e first stage o f life (77% p er year), w hich decreases d u rin g th e im m atu re stage a n d falls fu rth e r d u rin g th e m atu re ad u lt stage. In ad d itio n , we have calculated th e co rresp o n d in g life expectancies at b irth (e0), at en try in th e im m a tu re stage ( e j an d a t m a tu rity (e2) u n d er different hypotheses o n survival at th e m ax im u m age o f 90 years (s90) ranging betw een 0.1 a n d 3% o f new borns still alive. T he life expectancy at b irth (e0) at th e low er b o u n d o f th e chosen range (s90 = 0.001) is a b o u t 6 years, entry in th e im m a tu re stage ( e j is 8.2 years, an d e n try in th e m atu re stage (e2) is a b o u t 15.6 years. This large increase is th e consequence o f th e h igher m o rtality in the first tw o stages com p ared w ith th e m a tu re one. T he life expectancies are 10.1, 14.3, an d 37.8 years for s90 at th e u p p e r b o u n d o f th e chosen range (s90 = 0.03). T he resulting p o p u la tio n in trin sic grow th rates (r) ranged betw een - 1 .3 . a n d +1.7 p er year. H igh juvenile m o rtality p attern s im ply th a t th e sta­ tio n ary rep ro d u ctiv e value (th e n u m b e r o f fem ale offspring p ro d u ce d b y each fem ale after a given age x) at th e sta rt o f m a tu rity reaches a value a b o u t seven tim es h igher th a n at b irth . O nly optim istically high survival p attern s o f older individuals w o u ld allow positive intrinsic grow th rates, th ereb y en hancing the chances o f th e p o p u latio n survival.

Introduction Surprisingly, th e fin w hale (Balaenoptera physalus), w hich is the w o rld ’s second largest cetacean a n d one o f its longest-lived m am m als (Lockyer et a í 1977), is also one o f th e least-know n M ysticetes in dem ographic term s (N o tarb arto lo di Sciara et a í 2003).

Marine Ecology 32 (Suppl. 1) (2011) 1 -9 © 2011 Blackwell Verlag GmbH

W hile som e d em ographic studies have been con d u cted u sing in d u strial w haling d ata o n N o rth east A tlantic p o p u ­ lations (A guilar & Lockyer 1987), little is k n o w n a b o u t th e d em o g rap h y o f th e ir c o u n terp arts in th e M ed iterra­ n ean, w here in d u strial w haling has never been practised (N o tarb arto lo di Sciara et a í 2003). A lthough th e data fro m A guilar & Lockyer (1987) are a fu n d am ental

1

D e m o g r a p h y o f fin w h a l e s from stran din gs

c o n trib u tio n to th e u n d e rstan d in g o f th e d em o g rap h y of the fin w hale, n o p o p u la tio n dynam ics m odel has ever been developed for this species. M oreover, as th e M ed i­ terran ean fin w hale p o p u la tio n is genetically d istinct from its N o rth east A tlantic c o u n terp a rt (the nearest p o p u latio n in geographic term s; B érubé et al. 1998; Palsboll et al. 2004), it therefore represents a separate u n it o f conserva­ tion, requiring ad hoc studies. A ccording to th e IU C N Red data book criteria (Reeves and N o tarb arto lo di Sciara, 2006), th e conservation status o f this M ed iterran ean species has been ju d g ed data defi­ cient due to th e lack o f dem ographic in fo rm atio n . H o w ­ ever, a m o re recen t assessm ent, still u n d e r review b y th e Red List A uthority, has classified th e M ed iterran ean p o p ­ u latio n as vulnerable (Panigada, pers. com m .) T he survival o f this p o p u la tio n is th reaten ed b y m an y sources o f m o rtality a n d enviro n m en tal stress (N o tarb a r­ tolo di Sciara & G o rd o n 1997; N o tarb arto lo di Sciara et a í 2002), the m o st im p o rta n t o f w hich are ship collisions (P anigada et a í, 2006), fishing gear entanglem ent, h u m a n in duced n atu ral h ab itat d egradation, unreg u lated w halew atching (A iroldi et al. 1999), a n d acoustic disturbance (N o tarb arto lo di Sciara et al. 2003; A bdulla et al. 2008). A lthough som e ecological features, such as seasonal a b u n ­ dance (Forcada et al. 1996), h ab itat use (P anigada et a í 2005, P anigada et al. 2008; M onestiez et al. 2006; L aran & G annier 2008), site fidelity, diving profiles (P anigada et a l 1999) an d co n tam in atio n b y p o llu tio n (Fossi et al. 2003) have been investigated, n o p o p u la tio n dynam ics stu d y has been p erform ed o n fin w hale p o p u latio n s to date. O nly recently have th e dem ographic m odels w idely used in studying o th er anim al a n d p la n t p o p u latio n s (E bert 1998; Caswell 2001; Santangelo & B ram anti 2006) been applied to th e stu d y o f cetaceans (B uckland 1990; Fujiw ara & Caswell 2001). Tw o different approaches are com m only applied in dem ographic studies; these are based on static o r cohort life-tables. A th ird ap p ro ach is to com pile m ortality tables (C aughley 1966; C aughley & Sin­ clair 1994; E bert 1999), w hich p rovide precise in fo rm a­ tio n a b o u t size/age a n d sex o f dead individuals. H erein we have ad o p ted this latter ap p ro ach , w hich to date has never been applied to cetaceans, b y using stran d in g data. O u r aim is to develop a d em ographic m odel for th e M ed ­ iterran ean fin w hale p o p u la tio n based o n a life-history table (m o rtality table sensu Bergher 1990; Ricklefs an d M iller 2001) b u ilt o n M ed iterran ean stran d in g records.

M aterial and m e th o d s Stranding data O u r dem ographic m odel has been based o n all available data on fin w hale strandings reco rd ed o n M ed iterran ean coasts betw een 1986 an d 2007. T he in fo rm atio n o n

2

A rrig o n i, M a n fre d i, P a n ig a d a , B ra m a n ti & S a n ta n g e lo

strandings along th e Italian coasts has been draw n from th e CSC (C etacean Study C enter) database, available online a t CIBRA (2010). T he Spanish an d French coast stran d in g data have been collected respectively from the MEDACES database (2009) an d th e French N ational S tranding N etw ork RNE (2008). F u rth er data fro m M ed i­ terran ean countries w ith o u t dedicated stran d in g databases w ere fo u n d in th e scientific literatu re (N o tarb arto lo di Sciara et al. 2003). In o u r analyses we used th e stranded anim als’ sex an d length at death. U nfortunately, th e in fo r­ m a tio n is n o t u n ifo rm , as in m an y cases sex was n o t d eterm in ed an d exact size m easu rem en ts are possible only for recently dead anim als due to th eir rap id decom posi­ tion.

Basic life-history data Fin whales are characterized b y fast grow th in the first p a rt o f th e ir life, w hich th e n slows as th ey reach full phys­ ical m a tu rity at a b o u t 25 years o f age (A guilar & Lockyer 1987). As a first step, w e tran sfo rm ed th e size d istrib u tio n o f th e stran d ed w hales in to a size-stage d istrib u tio n , and th e n in to an age d istrib u tio n b y stage. This was carried o u t using th e grow th an d rep ro d u ctiv e param eters m ea­ sured in th e N o rth east A tlantic p o p u latio n (Lockyer 1984; A guilar & Lockyer 1987; A guilar et al. 1988), criteria w hich yielded th e follow ing th ree age-stages: C alf (0-0.5) years, Im m a tu re (0.5-7.5) years, a n d M atu re (7.5-90) years. T he value o f 90 years represents th e m ax im u m life­ sp an for fin whales estim ated b y Lockyer et al. (1977). As a p relim in ary assu m p tio n we hypothesized th a t stran d in g d ata rep resen t a faithful descrip tio n o f th e real m o rtality by stage. This, how ever, holds only if th e p ro b a ­ bility o f stran d in g is equal in all life-tables. Indeed, only u n d e r such circum stances w o u ld we expect th e relative d istrib u tio n o f stran d in g by stage to b e th e sam e as the tru e u n derlying d istrib u tio n o f deaths b y stage. As precise in fo rm atio n in this regard is lacking, such an assu m p tio n is therefore necessary to co m p u te th e m o rtality table.

The mortality table To b u ild u p a com plete m o rtality table for th e p o p u latio n we used a sim ple dem ographic m o d el based o n th e three above-defined life-tables, w ith c o n tin u o u s age d istrib u tio n an d co n stan t m o rtality rates w ith in each stage, u n d e r the assu m p tio n o f p o p u la tio n statio n arity [i.e. th e p o p u latio n is assum ed to be co n stan t in n u m b er an d age stru ctu re over tim e). As w e assum ed th a t n o anim als survive b eyond th e age o f 90, to apply th e m odel w ith co n stan t m o rtality rates, it is necessary to know th e fractio n (s90) o f n ew b o rn in d i­ viduals th a t survive u p to th e m ax im u m age cu = 90.

M arine Ecology 32 (Suppl. 1) (2011 ) 1 -9 © 2011 Blackwell Verlag GmbH

D e m o g r a p h y o f fin w h a l e s from stran d in g s

A rrig o n i, M a n fre d i, P a n ig a d a , B ra m a n ti & S a n ta n g e lo

G iven th e lack o f in fo rm a tio n o n this quantity, w e p e r­ fo rm ed a detailed analysis o f th e sensitivity o f the lifetable to different assu m p tio n s o n survival rates u p to the m ax im u m age (ranging betw een 0.1 an d 3% ). T his has enabled us to co m p u te th e m o rtality rates (o r m o rtality risks) /( for each age-stage (a¡_1, a¡) via th e equation:

In equation 1, th e age interval (a;-!, a;) denotes th e ith age-stage. T hus, as p er th e definitions in th e previous section, th e calf stage is defined b y (a0 = 0, a : = 0.5 years), the im m a tu re stage b y (a : = 0.5 years, a2 = 7.5 years), and th e difference h¡ = a; - a;_! is the corresponding class length. Finally, s(a¡)denotes th e frac­ tio n o f n ew born individuals still alive at precisely age a; [i.e. a t the m o m e n t o f tran sitio n fro m stage i to stage (i + 1)]. The assu m p tio n o f c o n stan t m o rtality rates w ith in each age group im plies th a t th e corresp o n d in g survival curve has th e follow ing exponential form :

o n average one offspring every 2 2 -2 4 m o n th s (Lockyer 1984). This corresponds to an age-specific fem ale fertility rate o f a b o u t 0.25-0.28 fem ales p er year, assum ing a sex ratio a t b irth o f 1:1 (Z anardelli et a í 1999). By co m bining this assu m p tio n w ith o u r m o rtality table, we have calcu­ lated th e stan d ard re p ro d u c tio n m easures: th e n et re p ro ­ ductive n u m b e r (Ro), th e m ean age o f m o th ers at re p ro d u ctio n in th e co rresp o n d ing statio n ary p o p u la tio n (T ), th e p o p u la tio n intrinsic grow th rate (r, Keyfitz & Caswell 2007) a n d th e rep ro d u ctiv e value a t each age in a statio n ary p o p u la tio n (SRV). The n e t rep ro d u ctiv e rate R0 represents th e average n u m b e r o f fem ale offspring a fem ale expects to have d u rin g h er entire life u n d e r the m o rtality described b y th e given life-table (so th a t the value R0 = 1 represents th e th resh o ld betw een p o p u la tio n grow th an d decline). T he statio n ary rep ro d u ctiv e value (SRV) represents th e n u m b e r o f fem ale offspring rem ain ­ ing to b e b o rn to a fem ale m o th e r after an y given age x. F u rth er details are rep o rte d in A ppen d ix 1.

R esults Stranded population structure

s(a) = s(a i_ i)e -"-(a- a' ^

a¡_i < a
(2)

E q uation 2 m eans th a t th e fraction(s) surviving at any given age a in each age gro u p can be c o m p u ted fro m the fraction surviving a t th e age o f entry in to th e gro u p an d reducing this fractio n b y th e m o rtality risk /(¡, w hich ‘accum ulates’ as th e in d ividual grows older. It is w o rth ­ while n o tin g th a t eq u atio n 1 is easily derived b y setting a = a; in eq u atio n 2 an d solving for / í¡. In ad d itio n , we have calculated o th e r sta n d a rd life-table statistics, such as th e life expectancy at b irth (e0) a n d the life expectancies u p o n en try in to sub seq u en t stages (e¡). T he life expectancy at b irth , w hich is easily co m p u ted as the area below the survival curve (2), represents th e n u m ­ b er o f years th a t a n ew b o rn in d ividual is expected to live if exposed d u ring its lifetim e to th e m o rta lity risks described by the m o rtality table (Keyfitz & Caswell 2007). A sim ilar in terp re ta tio n is a ttrib u te d to th e life expectancy at th e m o m e n t o f en try in to th e m a tu re stage e2: this re p ­ resents the n u m b e r o f years th a t an in dividual ju st e n ter­ ing the m atu re stage is expected to live if exposed durin g the rest o f its life to th e m o rtality risks described b y the m o rtality table. Such m easures p rovide a useful su m m ary view o f m ortality.

Reproduction parameters

T he final dataset includes 134 individuals o f k n o w n size, b u t w hose sex was identified only in 73 cases (33 males an d 40 fem ales). The hypothesis o f a balanced sex ratio in th e subsam ple o f k n o w n sex was n o t rejected (C hisqu ared test, y 2 = 0.0833 NS). H ow ever, given th e sm all figures for each gender, we decided to co m p u te a u n iq u e m o rtality table for th e tw o sexes. T he tim e d istrib u tio n o f to tal strandings (Fig. 1) does n o t suggest an y evident tren d . Figure 2 rep o rts th e d istri­ b u tio n o f strandings b y life-table in tw o distinct 11-year subperiods: 1986-96 a n d 1997-2007 an d th ro u g h o u t the

9r B -

O'

^2- n

Marine Ecology 32 (Suppl. 1) (2011) 1 -9 © 2011 Blackwell Verlag GmbH

n

J l 1 1 1 1 1 lui 1 1 1 1 y 11 n Ini

1985

T he fertility rates for females have been draw n fro m the literature using th e sta n d a rd assu m p tio n th a t a m a tu re fem ale th a t has n o t been subjected to m o rta lity p roduces

i—i

1990

1995

Year

2000

2005

2010

Fig. 1. M editerranean fin whale: distribution of total strandings over the period 1986-2007.

3

D e m o g r a p h y o f fin w h a l e s from stran din gs

A rrig o n i, M a n fre d i, P a n ig a d a , B ra m a n ti & S a n ta n g e lo

eo I

01

S 30

50

50

30

30

20

20

11988-2007

Fig. 2. Mediterranean fin whale: distribution of strandings by life-stage over two different periods: (A) 1986-96, (B) 1997-2007, and (C)

10 0 C aR Im m atura M atura

CaH

Im m atura M atura

entire period. T here was a statistically significant differ­ ence in the p o p u la tio n m o rtality stru ctu re betw een th e tw o 11-year periods (o m n ib u s-ty p e likelihood ratio test o n the m u ltin o m ial d istrib u tio n significant at 1%), sug­ gesting th a t som e change in m o rtality could have occurred in the m o re recen t p erio d (1997-2007). H o w ­ ever, even th o u g h th e d ata suggest th e possibility o f a change in th e m o rtality stru ctu re, we calculated a single m o rtality table for th e en tire p erio d to avoid th e exces­ sively sm all sam ple size th a t w o u ld result b y sp litting th e data. This was su p p o rted b y th e lack o f an y evident trends in th e d istrib u tio n o f to tal strandings over tim e (Fig. 1), as well as b y som e evidence o f stability suggested b y th e m o n oton ically decreasing stru ctu re o f th e n o rm a l­ ized data (Table 1, Fig. 3).

Mortality table As a second step we b u ilt a new m o rtality table (Table 1) based on the strandings according to occurrence in the three discrete life-tables in to w hich th e species life cycle has been divided (calf, im m a tu re a n d m atu re). In this perspective, th e to tal n u m b e r o f strandings (134) can be in terp reted as th e n u m b e r o f new borns in a hypothetical b irth cohort, o f w hich 43 die d u rin g th e calf stage, 66 d u ring the im m a tu re stage, an d th e rem ain in g 25 in d iv id ­ uals d u ring the m atu re stage (Table 1 co lu m n 5). In te r­ pretin g th e d ata is sim plified b y using a hypothetical

CaR Im m atura M atura

the entire m easurem ent period: 1986-2007.

co h o rt o f 1000 (instead o f 134) recruits, as show n in T able 2, co lu m n 3: o f 1000 recruits, only 679 (67.9% ) enter th e im m atu re stage a n d only 186 enter th e m atu re stage. U n d er th e statio n arity hypothesis, this represents th e living p o p u la tio n structure. Clearly, th e d istrib u tio n o f individuals b y life-tables is biased b y th e different d u ra tio n s o f th e stages. To correct for this, we norm alized th e d istrib u tio n to th e d u ra tio n o f th e first stage (6 m o n th s), w hich is th e shortest (Table 1). U sing eq u atio n 1, we c o m p u ted th e c o n tin u o u s m o rta l­ ity rates /í¡ inside each stage. For calves, /q was 0.774 per year, w hile for im m a tu re individuals, ß 2 was 0.184 per year, less th a n a q u arter o f th e calf rate. For m atu re whales th e m o rtality rate ranged betw een 0.063 per year for P 90 = 0.001 a n d 0.022 p er year for P 90 = 0.03. Figure 3 show s th e co rresp o n d in g survival curves co m ­ p u te d according to eq u atio n 2 using th e values P90 = 0.001 an d P 90 = 0.03. T he p lo tted survival curves differ fro m each o th er only in th e th ird age-stage (7.5— 90 years), a consequence o f th e different assu m p tions on th e fractio n surviving at 90 years. T he curves fu rth erm o re show first an exponentially decreasing p a tte rn w ith in each age-stage, a result o f th e assu m p tio n o f co n stan t-rate m o rtality in each stage, an d secondly a m arked difference in th e rate o f decline in th e different stages, w hich is co n ­ sistent w ith th e different m o rtality rates in th e various stages.

Table 1. M editerranean fin whale: mortality table by life-stages.

Life-table

No. of deaths

(years)

No. of deaths normalized by stage duration ( y e a r 1)

Calf Immature Mature

43 66 25

0.5 7.0 82.5

86 9.42 0.30

Stage duration

4

No. of survivors at onset of each stage

No. of survivors a t onset of each stage (per 1000)

134 91 25

1000 679 186

M arine Ecology 32 (Suppl. 1) (2011 ) 1 -9 © 2011 Blackwell Verlag GmbH

D e m o g r a p h y o f fin w h a l e s from stran d in g s

A rrig o n i, M a n fre d i, P a n ig a d a , B ra m a n ti & S a n ta n g e lo

B 0.9

1 0.9

0.8

0.8

p 90 = 0 .0 ° 1

cl

Fig. 3. M editerranean fin whale: age-specific survival curves under tw o different assum ptions on the probability of survival to maximum age: (A): p90 = 0.001; (B)

0.7

0.7

0.6

0.6

0.5

0.5

0.4

0.4

0.3

0.3

0.2

0.2

0.1

0.1

0

0

20

40

60

0 0

80

20

Age (years)

P9 0 = 0.03.

T he life expectancies at th e age o f o n set o f th e various stages (Fig. 4) show a m arked increasing tren d as a func­ tio n o f b o th th e age o f en try an d th e fractio n surviving at age 90. In particular, fo r s90 a t th e low er b o u n d o f the chosen range (s90 = 0.001), th e life expectancy a t b irth (e0) is a b o u t 6 years, w hereas th e life expectancy u p o n onset o f th e im m a tu re stage ( e j is 8.2 years, a n d th e life expectancy entering in to th e m a tu re stage (e2) is a b o u t 15.6 years. T his large increase follows fro m th e very high m o rtality in th e first tw o stages as com p ared w ith the m a tu re stage. A t the u p p e r b o u n d o f th e chosen range (s90 = 0.03) th e respective life expectancies are 10.1, 14.3, and 37.8 years.

40

60

80

Age (years)

R eproduction param eters By co m b in in g o u r set o f m o rtality tables w ith fertility d ata w e can develop scenarios o f lo n g -term p o p u latio n tren d s. T h e n e t rep ro d u ctiv e rate Ro ranges fro m a value well below o n e (0.73) for th e s90 = 0.001 hypothesis, to a value considerably above u n ity (1.77) fo r s90 = 0.03. T he m ean age o f m o th ers at re p ro d u ctio n correspondingly ranges betw een 22.8 and 36.8 years (Fig. 5). Finally, the co rresp o n d ing in trin sic p o p u la tio n grow th rate (r) ranges betw een -1 .3 % a n d +1.7% year-1 (Fig. 6). Figure 7 show s th e tren d o f th e SRV w ith the age o f the m o th er. In p ar­ ticular, th e value at sexual m a tu rity is ab o u t seven tim es higher th a n th e value at b irth , d u e to the huge m o rtality d u rin g p re-rep ro d u ctiv e ages.

2

9_

0

0.005

0.01

0.015

0.02

0.025

0.03

Fraction alive at maximal ag e © (© = 90 years)

0 0

0.005

0.01

3.015

0.02

0.025

0.03

Fig. 4. M editerranean fin w hale: life expectancies a t the age of entry into the various stages as functions of the fraction surviving a t age 90

Fraction alive at maximal a g e © (© = 90 years)

(ranging betw een 0.001 and 0.03); e0 = life expectancy a t birth, e-i = life expectancy a t onset of the im mature stage, e 2 = life expec­ tancy a t onset of maturity.

Fig. 5. Mediterranean fin whale: net reproduction rate R0 (left verti­ cal axis) and the corresponding mean age of m others at reproduction T (right vertical axis) as functions of the fraction surviving at age 90.

Marine Ecology 32 (Suppl. 1) (2011) 1 -9 © 2011 Blackwell Verlag GmbH

5

D e m o g r a p h y o f f in w h a l e s f r o m s t r a n d i n g s

A rrig o n i, M a n fre d i, P a n ig a d a , B ra m a n ti & S a n ta n g e lo

0.02

0.015

0.01

5

0.005

-0.005

-

0.01

-0.015

0

0.005

0.01

0.015

0.02

Fraction alive at maximal age ® (® = 90 years) Fig. 6. M editerranean fin whale: the population Intrinsic growth rate as a function of the fraction surviving a t age 90.

SRV

A ge (y e a r s) Fig. 7. M editerranean fin whale: change in the stationary reproduc­ tive value (SRV) with age; a2 Is the age at sexual maturity.

D iscussion This study seeks to describe th e stru ctu re o f th e M ed iter­ ran ean fin w hale p o p u la tio n b y analyzing stran d in g records from th e p erio d 1986-2007. As th e ecological characteristics o f this species m ake d ata collection a t sea particularly difficult (fin whales usually live far fro m th e coast an d are difficult to observe d u e to w eather co n ­ straints an d th e high costs o f dedicated research vessels), strandings m ay prove to be an alternative source of dem ographic d ata (O rsi R elini et al. 2004). T his stu d y is the first to analyze th e dem ographic features o f th e M ed i­ terran ean fin w hale p o p u la tio n an d , to o u r know ledge, the first to set o u t a m o rta lity table based o n cetacean stran d in g data. T he dataset exam ined does n o t reveal an y significant divergence from a balanced sex ratio in th e strandings. W e are therefore unab le to confirm th e n a tu ral bias

6

tow ards fem ale m o rtality previously suggested for this species (C lark 1982; De La M are 1985). O u r results show th a t th e first stage o f th e life cycle is th e m o st life-threatening, w ith a yearly risk o f death o f a b o u t 77% , w hereas in th e im m a tu re stage, death is nearly fo u r tim es less likely (18% ). This indicates a strong im pact, n a tu ral a n d /o r an th ro p o g en ic, o n calves and im m a tu re anim als, w hich prevents th eir reaching sexual m atu rity . O n th e o th er h an d , th e risk o f death o f m atu re individuals is m u ch lower: u n d e r th e m o st pessim istic scenario it is still only a b o u t 6.3% p er year. These results confirm a p a tte rn c o m m o n to several m am m als: high m o rtality in th e youngest age classes an d low ones in m atu re stages (C aughley 1966; Em elen 1970). N o n eth e­ less, a very low p ro p o rtio n o f new borns reach sexual m atu rity, w hich m ay rep resen t a serious th re a t for the survival o f this p o p u latio n . Indeed, even u n d e r very o p ti­ m istic hypotheses o n th e length o f th e m ax im u m lifespan a n d prolo n g ed fertility, th e intrinsic grow th rate r is likely to be positive only if th e percentage o f offspring surviving u p to m ax im u m age is q u ite high {i.e. well above 0.005). T he SRV clearly show s th a t th e c o n trib u tio n to th e p o p u ­ latio n in term s o f survival is biased to w ard adults: m ost calves an d y o u n g w hales do n o t co n trib u te to re p ro d u c­ tio n because th ey will never reach sexual m aturity. In co n d u ctin g this stu d y we exam ined all th e available d ata o n strandings. H ow ever, these are far fro m represen­ tative o f all M ed iterran ean strandings. In ad d itio n , only som e o f th e available d ata w ere suitable for analysis, as ind icatio n s o n sex are lacking in a b o u t h alf th e cases and th e re p o rted size is often ap p ro x im ate o r even missing. To m ake u p for this lack o f data u niform ity, w e resorted to som e necessary assu m p tio n s (p o p u la tio n statio n arity a n d identical stran d in g probabilities in each stage). A lthough th e p ro p o sed m odel is rath er sim ple, th e study nevertheless suggests th a t stran d in g data an d th e use o f dem ographic m odels m ay well allow enhancing o u r cu r­ ren tly lim ited know ledge o f th e dem ographics o f this im p o rta n t cetacean. F u ture w o rk to im p ro v e o u r ongoing stud y o f fin w hale p o p u latio n s will focus o n co m paring th e ap p ro ach applied h erein w ith analyses o f p h o to -id en tification d ata reco rd ed b y th e Tethys R esearch In stitu te o n th e live p o p u la tio n in h ab itin g th e w aters o f the Pelagos Sanctuary. W e also p lan to investigate p o p u latio n dynam ics u n d e r different conservation scenarios, and th ereby assess its cu rren t status an d risk o f extinction. A t present, in spite o f th e existence o f th e Pelagos Sanctuary (N o tarb arto lo di Sciara et a í 2007), an M PA specifically designated to p ro te c t cetaceans an d w hich represents th e m o st im p o rta n t feeding g ro u n d s for the M ed iterran ean fin w hale (N o tarb arto lo di Sciara et a í 2003), n o specific regulation is cu rren tly in force for p ro te c tio n o f this species. R egulation o f naval traffic and

M arine Ecology 32 (Suppl. 1) (2011 ) 1 -9 © 2011 Blackwell Verlag GmbH

A rrig o n i, M a n fre d i, P a n ig a d a , B ra m a n ti & S a n ta n g e lo

w hale-w atching activities could enhance this p o p u la tio n ’s chances o f survival (P anigada et a í, 2006). O u r findings suggest th a t m itig atio n m easures targeted to reproductive adults, p articu larly addressed to increase the m ean age o f m o th ers at rep ro d u c tio n , are likely to be the m o st effective a n d need to be taken in to a c co u n t in designing p ro p er conservation plans. The discovery of breeding grounds w here calves m ay enjoy greater p ro te c­ tio n , could fu rth er increase survival rates. O n an o th e r track, special naval traffic regulations, aim ed at reducing m o rtality rates fro m ship collisions, could enhance the survival o f m atu re fem ales a n d calves. M itigating o th er sources o f m o rtality an d stress, such as chem ical an d acoustic p o llution, w hale-w atching activities a n d n atu ral h ab itat d egradation, could fu rth e r im p ro ve th e p o p u la ­ tio n ’s chances o f survival.

A c k n o w le d g e m e n ts W e w ish to th a n k th e Italian N ation al Strandings D ata­ base, CIBRA, U niversity o f Pavia an d Italian M in istry of the E nvironm ent. W e are also grateful to th e M ed iterra­ nean D atabase o f C etacean Strandings (MEDACES) at the U niversity o f V alencia (Spain), w hich is su p p o rte d b y the Spanish M inistry o f th e E nv iro n m en t, a n d th e French N ational S tranding N etw o rk (RN E), C entre de R echerche sur les M am m ifères M arins - U niversité de La Rochelle. W e also th an k C. C aro ta o f th e Statistics D ept, o f T u rin U niversity for statistical references an d A. Cafazzo for his revision o f the English text. T his research was su p p o rted b y the Italian M in istry o f E d u catio n a n d Scientific R esearch PR IN 2007 p ro ject 200777BW EP. M athem atical p o p u latio n th eo ry an d L.B. w ere su p p o rte d b y a M arieC urie IEF (CO RG ARD , p ro ject no. 221072). W e also th a n k tw o referees an d th e E ditor, w hose useful sugges­ tio ns im proved the m an u scrip t.

R eferen ces Abdulla A., Gornei M., Maison E., Piante C. (2008) Status o f Marine Protected Areas in the Mediterranean Sea. IUCN, Malaga and WWF France, Paris: 152 pp. Aguilar A., Lockyer C.H. (1987) Growth, physical maturity, and mortality of fin whales (Balaenoptera physalus) inhabit­ ing the temperate waters of the northeast Atlantic. Canadian Journal of Zoology, 65, 253-264. Aguilar A., Oimos M., Lockyer C.H. (1988) Sexual maturity of fin whales (Balaenoptera physalus) caught off Spain. Report of the International Whaling Commission, 38, 317-322. Airoldi S., Azzellino A., Nani B., Ballardini M., Bastoni C., Notarbartolo di Sciara G., Sturlese A. (1999) Whale-watching in Italy: results of the first three years of activity. European Research on Cetaceans, 13, 153-156.

Marine Ecology 32 (Suppl. 1) (2011) 1 -9 © 2011 Blackwell Verlag GmbH

D e m o g r a p h y o f fin w h a l e s from stran d in g s

Bergher J. (1990) Persistence of different-sized populations: an empirical assessment o f rapid extinction in Bighorn sheep. Conservation Biology, 4, 91-98. Bérubé M., Aguilar A., Dendanto D., Larsen F., Notarbartolo di Sciara G., Sears R., Sigurjonsson J., Urban-Ramirez J., Palsboll P.J. (1998) Population genetic structure of N orth Atlantic, Mediterranean Sea and Sea of Cortez fin whales, Balaenoptera physalus (Linnaeus, 1758): analysis of mitochondrial and nuclear loci. Molecolar Ecology, 7, 585600. Buckland S.T. ( 1990) Estimation of survival rates from sight­ ings o f individually identifiable whales. Report of the Interna­ tional Whaling Commission, Special Issue 12, 149-154. Caswell H. (2001) Matrix Population Models: Construction, Analysis and Interpretation, 2nd edn. Sinauer Associates, Sunderland, MA: 722 pp. Caughley C. (1966) Mortality patterns in mammals. Ecology, 47, 906-918. Caughley G., Sinclair A.R.E. (1994) Wildlife Ecology and M an­ agement. Blackwell Scientific Publishing, Oxford. CIBRA Centro Interdisciplinare di Bioacustica e Ricerche Ambientali. (2010) University o f Pavia http://www.cibra.unipv.it/ spiaggiamenti.html (last modified lanuary 2010). Clark W.G. (1982) Historical rates o f recruitment to Southern Hemisphere fin whale stocks. Report of the International Whaling Commission, 32, 305-324. De La Mare W.K. ( 1985) On the estimation of mortality rates from whale age data, with particular reference to mink whales (Balaenoptera acutorostrata) in the Southern Hemisphere. Report o f the International Whaling Commis­ sion, 35, 239-250. Ebert T.A. (1998) Plant and Animal Populations: Methods in Demography. Academic Press, New York. Entelen J.M. (1970) Age specificity and ecological theory. Ecol­ ogy, 51, 588-601. Forcada J., Aguilar A., H am m ond P., Pastor X., Aguilar R. (1996) Distribution and abundance o f fin whales (Balaenop­ tera physalus) in the western Mediterranean Sea during the summer. Journal o f Zoology London, 238, 23-34. Fossi M.C., Marsili L., Neri G., Natoli A., Politi E., Panigada S. (2003) The use of a non-lethal tool for evaluating toxicological hazard of organochlorine contaminants in M editerra­ nean cetaceans: new data 10 years after the first paper published in MPB. Marine Pollution Bulletin, 46, 972-982. Fujiwara M., Caswell H. (2001) Demography of the endan­ gered N orth Atlantic right whale. Nature, 414, 537-541. Keyfitz N., Caswell H. (2007) Applied Mathematical Demogra­ phy. Springer-Verlag, New York: 505 pp. Laran S., Gannier A. (2008) Spatial and temporal prediction of fin whale distribution in the northwestern Mediterranean Sea. ICES (International Council for the Exploration of the Seas) Journal of Marine Science, 65, 1260-1269. Lockyer C.H. (1984) Review of Baleen Whale (Mysticeti) Repro­ duction and Implications for Management. Report o f the International Whaling Commission, Special Issue 12.

7

D e m o g r a p h y o f fin w h a l e s from stran din gs

Lockyer C.H., Gambell R., Brown S.G. (1977) Notes on age data of fin whale taken off Iceland, 1967-74. Report o f the International Whaling Commission, 27, 427-450. MEDACES Mediterranean Database o f Cetacean Strandings (2009) University o f Valencia, http://www.medaces.uv.es (last modified September 2009). Monestiez P., Dubroca L., Bonnin E., Durbec J.P., Guinet C. (2006) Geostatistical modelling of spatial distribution o f Bal­ aenoptera physalus in the Northwestern Mediterranean Sea from sparse count data and heterogeneous observation efforts. Ecological Modelling, 193, 615-628. Notarbartolo di Sciara G., Gordon J. (1997) Bioacoustics: a tool for the conservation o f cetaceans in the Mediterranean Sea. Marine and Freshwater Behaviour and Physiology, 30, 125-146. Notarbartolo di Sciara G., Aguilar A., Bearzi G., Birkun A., Frantzis A. (2002) Overview o f known or presumed impact on the different species o f cetaceans in the Mediterranean and Black Seas. In Notarbartolo di Sciara G. (ed.), Cetaceans in the Mediterranean and Black Seas: State o f Knowledge and Conservation Strategies. Report to the ACCOBAMS Secretar­ iat, Monaco, February 2002, pp. 194-196, 219pp. Notarbartolo di Sciara G., Zanardelli M., Jahoda M., Panigada 5., Airoldi S. (2003) The fin whale Balaenoptera physalus (L. 1758) in the Mediterranean Sea. M ammal Review, 33, 105150. Notarbartolo di Sciara G., Agardy T., Hyrenbach D., Scovazzi T., Van Klaveren P. (2007) The Pelagos Sanctuary for Medi­ terranean marine mammals. Aquatic Conservation: Marine Freshwater Ecosystem, 18, 367-391. Orsi Relini L., Palandri G., Garibaldi F., Lantieri L. (2004) Note about some population parameters o f the fin whale Balaenoptera phisalns (Linneo 1758). Biol. Marine Med., 11, 138-154. Palsboll J., Bérubé M., Aguilar A., Notarbartolo di Sciara G., Nielsen R. (2004) Discerning between recurrent gene flow and recent divergence under a finite-site m utation model applied to North-Atlantic and Mediterranean sea fin whale (Balaenoptera physalus) populations. Evolution, 58, 670-675. Panigada S., Zanardelli M., Canese S., Jahoda M. (1999) How deep can baleen whales dive? Marine Ecology Progress Series, 187, 309-311. Panigada S., Notarbartolo di Sciara G., Zanardelli M., Airoldi 5., Borsani J.F., Jahoda M. (2005) Fin whales (Balaenoptera physalus) summering in the Ligurian Sea: distribution, encounter rate, mean group size and relation to physio­ graphic variables. Journal o f Cetacean Research Management, 7, 137-145. Panigada S., Pesante G., Zanardelli M., Capoulade F., Gannier A, Weinrich M.T. (2006) Mediterranean fin whales at risk from fatal ship strikes. Marine Pollution Bulletin, 52, 12871298. Panigada S., Zanardelli M., MacKenzie M., Donovan C., Mélin F., H am m ond P.S. (2008) Modelling habitat preferences for fin whales and striped dolphins in that Pelagos Sanctuary

8

A rrig o n i, M a n fre d i, P a n ig a d a , B ra m a n ti & S a n ta n g e lo

(Western Mediterranean Sea) with physiographic and remote sensing variables. Remote Sensing o f the Environment, 112, 3400-3412. Reeves R., Notarbartolo di Sciara G. (eds) (2006) The Status and Distribution o f Cetaceans in the Black Sea and Mediterra­ nean Sea. Iucn Centre for Mediterranean Cooperation, Malaga, Spain, 137 pp. Ricklefs R.E., Miller L.G. ( 1999) Ecology VI. Freeman and Co., New York. 822 pp. RNE Réseau National d ’échouage (2008) Université de La Rochelle et le Groupe d ’Etudes des Cétacés de Méditerranée http://crmm.univ-lr.fr/index.php/ff/echouages/carte (last modified 2010). Santangelo C., Bramanti L. (2006) Ecology through time; an overview. Biology Forum, 99, 395-424. Zanarddelli M., Panigada S., Airoldi S., Borsani J.F., Jahoda M., Notarbartolo di Sciara G. (1999) Site fidelity, seasonal residence and sex ratio of fin whales (Balaenoptera physalus) in the Ligurian Sea feeding grdouns. European Research on Cetaceans, 12, 24.

A p p en d ix W e re p o rt som e technical details o n th e various d em o ­ graphic m easures used in th e paper.

The mathematical model o f the mortality table T he m o rtality table is based o n th e follow ing piecewise co n stan t m o rtality rate over th e various (co n tin u o u s) agestages [ai_!,ai) /((a) = ( ( oo

- a an = cu

(A Í)

In particu lar, all individuals alive at th e m axim al age an = cu are assum ed to suddenly die, w hich am o u n ts to assum ing a m o rtality rate equal to infinity. In th e sim pli­ fied m odel described in th e p ap er th ere are only three age-stages (a0, a i) , ( a í , as), (ay ,a¡ = cu) represen ting the calf, th e im m atu re, an d th e m a tu re stages. T he co rresp o n d in g survival fu n ctio n , w hich represents th e prob ab ility th a t a n ew b o rn individual dies after age a (an d therefore ‘survives’ a t least u n til age a) an d relates to th e m o rta lity rate b y th e general relation s(a) = exp — fy /í(fí)d fíj, is given in o u r m o d el by , , _ ƒ s(ai_ 1)e-''i
a¡_! < a an

w hich defines a piecewise exponential survival fun ctio n over each age-stage. Let h¡ = a¡ - a;_j d en o te th e size o f th e i-th age-stage. T he life expectancy a t b irth , i.e. th e life expectancy at entry in th e stage o f calf, is given b y :

M arine Ecology 32 (Suppl. 1) (2011 ) 1 -9 © 2011 Blackwell Verlag GmbH

D e m o g r a p h y o f fin w h a l e s from stran d in g s

A rrig o n i, M a n fre d i, P a n ig a d a , B ra m a n ti & S a n ta n g e lo

1 (1 (A3) £ e A i=i Sim ilar equations can be derived for th e life expectan­ cies at th e age o f entry in th e im m atu re an d m a tu re stages, d enoted b y e!, e2 in th e m ain text. For exam ple the life expectancy at th e age a2 o f en try in th e m a tu re stage is given by: e0 =

/ s(a)d a = ^

a^=co

es- /32

(', 4 )

By com bining th e life-table w ith suitable assum ptions o n age-specific fertility rates o f fem ale w hales (taken as given) we can co m p u te a variety o f re p ro d u ctio n indices. Follow ing th e assu m p tio n a d o p ted in th e text, the age-

surviving u n til th e m a tu re stage tim es th e life expectancy in th e m a tu re stage. T he co rresp o n d in g m ean age of m o th ers a t th e b irth o f th eir fem ale offspring (co m p u ted w ith reference to th e statio n ary p o p u la tio n o f b irth d en­ sity R0"1m (a )p (a )) is given by; / 1\ e-P3(ffl-32) T — I a2 H I — (oj — a2) -------------------

(^3V)

T he intrin sic grow th rate r o f th e p o p u latio n , w hich represents th e speed o f grow th or decay th a t th e p o p u la ­ tio n w ould achieve in th e lo n g -term o n th e a ssu m ption th a t th e vital rates are m ain tain ed co n stan t over tim e, is given as: r = m Fp (a 2) e - ra2 ( l - e-
(A 8 )m l0

specific fertility rate is given by:

m p (a) = { 7

ekew here

i.e. it is u n changin g over tim e an d co n stan t w hole m a tu re stage. T herefore, it quickly follows that:

(A5) over the

In th e p ap er we also c o m p u ted a q u an tity th a t we called th e Stationary R eproductive V alue (SRV), w hich represents, o n th e a ssu m p tio n th a t th e p o p u la tio n is sta­ tionary, th e n u m b e r o f fem ale calves rem ain in g to be b o rn to a fem ale after an y given age a. This fu n ctio n is defined as: CO

Ro = mps2e2

(A6)

SRV =

f s(x) . . _ / —r— m F(x)dx ./ s(a)

i.e. th a t the N et R ep ro d u ctio n N u m b er Rofactorises as the p ro d u c t o f the fertility rates tim es th e pro b ab ility of

Marine Ecology 32 (Suppl. 1) (2011) 1 -9 © 2011 Blackwell Verlag GmbH

9

marine ecology

an evolutionary perspective

»

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

Temporal change in UK marine communities: trends or regime shifts? M. S p e n c e r 1*, S. N. R. B ir c h e n o u g h 2*, N. M ie sz k o w sk a 3*, L. A. R o b in s o n 1*, S. D. S im p so n 4*, M. T. B u rrow s5, E. C a p a sso 3,6, P. C lea ll-H a rd in g 6, J. C rum m y7, C. D uck 8, D. E loire9,10, M. F rost3, A. J. Haii8, S. J. H aw k in s3'6, D. G. J o h n s11, D. W . Sim s3'12, T. J. S m y th 9 & C. L. J. Frid1* 1 School of Environmental Sciences, University of Liverpool, Liverpool, UK 2 3 4 5

Cefas Laboratory, Pakefleld Road, Lowestoft, Suffolk, UK Marine Biological Association of the United Kingdom, The Laboratory, Citadel HUI, Plymouth, UK School of Biological Sciences, University of Bristol, Bristol, UK The Scottish Association for Marine Science, Dunstaffnage Marine Laboratory, Oban, Argyll, UK

6 School of Ocean Sciences, Bangor University, Menai Bridge, Ynys Mon, UK 7 British Geological Survey, Murchison House, Edinburgh, UK 8 Sea Mammal Research Unit, Scottish Oceans Institute, University of St Andrews, St Andrews, UK 9 Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth, Devon, UK 10 Laboratoire Ecosystème Lagunaire, UMR B119, CNRS - Université Montpellier II - IRD - IFREMER, CC093, Montpellier, France 11 Sir Allster Hardy Foundation for Ocean Science, Plymouth, UK 12 Marine Biology and Ecology Research Centre, Marine Institute, School of Marine Sciencesand Engineering, University of Plymouth, Drake Circus, Plymouth, UK

K eywords Abundance; population trends; principal

A bstract

com ponents; regime shift detection; regime

A regim e shift is a large, su d d en , an d long-lasting change in th e dynam ics o f an ecosystem , affecting m u ltip le tro p h ic levels. T here are a grow ing n u m b e r o f papers th a t re p o rt regim e shifts in m arin e ecosystems. H ow ever, th e evidence for regim e shifts is equivocal, because th e m eth o d s used to detect th e m are n o t yet well developed. W e have collated over 300 biological tim e series fro m seven m arin e regions a ro u n d th e UK, covering th e ecosystem fro m p h y to p la n k to n to m arin e m am m als. Each tim e series consists o f a n n u al m easures o f ab undance for a single gro u p o f organism s over several decades. W e su m m arised the data for each region using th e first p rincipal co m p o n en t, w eighting either each tim e series o r each biological co m p o n en t (e.g. p lan k to n , fish, b enthos) equally. W e th e n searched for regim e shifts using R o d io n o v ’s regim e shift detectio n (RSD) m eth o d , w hich fo u n d regim e shifts in th e first prin cip al co m p o n e n t for all seven m arin e regions. H ow ever, th ere are consistent tem p o ral tren d s in the data for six o f th e seven regions. Such tren d s violate th e assu m p tio n s o f RSD. T hus, th e regim e shifts detected b y RSD in six o f th e seven regions are likely to be artefacts caused b y tem p o ral trends. W e are th erefore developing m o re a p p ro p riate tim e series m odels for b o th single p o p u latio n s an d w hole c o m m u ­ nities th a t will explicitly m odel tem p o ral tren d s a n d should increase o u r ability to detect tru e regim e shift events.

shifts; time series; UK marine ecosystems. C orrespondence M atthew Spencer, School of Environmental Sciences, University of Liverpool, Liverpool L69 7ZB, UK. E-mail: [email protected] *These authors wish to be considered as joint first authors. Accepted: 16 November 2010 doi : 10.1111/j.1439-0485.2010.00422.x

Introduction A grow ing n u m b e r o f studies re p o rt m ajo r changes in biological systems (Reid et a í 2001; R u d n ick & Davis 2003; Lees et a í 2006; B eaugrand et al. 2008; C arp enter &

10

L athrop 2008; G reene et al. 2008; H agerthey et al. 2008; H eath & Beare 2008; H em ery et al. 2008; Petersen et al. 2008). These, often high profile, observations have co n ­ trib u te d to a m ove tow ards m o re holistic a n d integrated ‘ecosystem -based’ enviro n m en tal m an ag e m en t (U nited

Marine Ecology 32 (Suppl. 1) (2011) 1 0 -2 4 © 2 0 1 0 Blackwell Verlag GmbH

S p e n c e r, B irc h e n o u g h , M ie s z k o w s k a , R o b in so n , S im p so n , Frid

et al.

T em pora l c h a n g e in UK m arin e c om m u nities

N ations 1992). Several such studies have highlighted rela­ tively large-scale change in aspects o f the system over a sh o rt p eriod o f tim e (e.g. H are 8c M an tu a 2000; Reid et al. 2001; Chavez et al. 2003; W eijerm an et al. 2005; D askalov et al. 2007). Such p h e n o m e n a have been referred to as ecological regim e shifts an d have been seen as evidence o f n o n -lin ear interactions an d feedbacks in the ecological system, w ith the p o ten tial for hysteresis (Beisner et al. 2003; P otts et al. 2006). A large n u m b er o f such events have been d o cu m en ted (Folke et al. 2004). For exam ple, the T hresholds database (accessed 27 F eb ru ­ ary 2010) contains 102 instances o f regim e shifts in terrestrial, freshw ater an d m arin e ecosystem s (Resilience A lliance, Santa Fe In stitu te 2004). Lees et al. (2006) provide a review o f m an y o f th e ‘regim e shift’ papers published p rio r to 2005 an d em phasise th a t for changes actually to constitu te a regim e shift, th e change m u st

H owever, it seems im p o rta n t to evaluate w h eth er the assu m p tio n o f statio n arity in m ean except at discrete shift p o in ts is ap p ro p riate for a b ro a d range o f biological tim e series. Here, we apply RSD to a large collection o f m arine biological tim e series fro m seven regions a ro u n d th e B rit­ ish Isles. W e argue th a t m an y o f th e ap p aren t shifts fo u n d by RSD are in fact th e consequence o f gradual, rather th a n sudden, changes over tim e. W e th in k th a t such g rad ­

propagate across m ultiple physical an d biological c o m p o ­ nents o f the ecosystem.

D ata

In the m ajority o f cases w here a regim e shift was p o s­ tu lated it was attrib u te d to changes in th e clim atic system (Lees et al. 2006). T here is little d o u b t th a t p lanetary w arm ing is occurrin g an d th e te m p eratu re records suggest th a t this has been m o st rap id in th e last th ree decades, w ith a w arm ing tre n d a p p aren t in m o st atm o sp h eric an d sea surface tem p eratu re datasets (IPCC 2007, section 1.1). M any published analyses o f biological d ata focus on regim e shifts th a t m ay have been caused by e n v iro n m en ­ tal change (e.g. Reid et al. 2001; W eijerm an et al. 2005; B eaugrand et al. 2008). This raises th e fu n d am en tal ques­ tion: do biological interactions generally result in d isco n ­ tin u o u s dynam ics at th e system level? The answ er has p ro fo u n d im plications for u n d erstan d in g an d p redicting

ual changes are biologically interesting, an d are im p o rta n t because they fo rm a dynam ic baseline o f genuine and som etim es large changes in m arin e ecosystem s (H ardm a n -M o u n tfo rd et al. 2005). H ow ever, they do n o t fall w ith in th e usual definition o f regim e shifts.

M aterial and M eth o d s

The U K ’s M arine E n v iro n m en tal C hange N etw ork (M ECN ) links research un its an d universities th a t hold lo n g -term o r h istoric d ata o n aspects o f UK m arin e eco­ systems. The M EC N dataset com piled for this study includes 324 biological tim e series o f an n u al observations from seven m arin e regions (Fig. 1). The series cover five biological co m p o n en ts (plan k to n , infaunal b enthos, rocky shore invertebrates, fish, an d m arin e m am m als), although n o t all co m p o n en ts were represented in every region. All series w ith in a region were reduced to the length o f the shortest series fro m th a t region (from 19 to 30 years, fin ­ ishing in 2006: Table 1). Som e c o m p o n en ts were sam pled

the im pacts o f global clim ate change. A n u m b er o f studies have exam ined tim e series o f b io ­ logical and physical variables sim ultaneously (H are 8c M an tu a 2000; W eijerm an et al. 2005), often by su m m ariz­ ing m an y tim e series using prin cip al com p o n en ts. S tatisti­ cal m ethods can th e n be used to lo o k for su d d en changes in the levels o f th e prin cip al com ponents. The regim e shift detection (RSD) algorithm is one such m e th o d (R o­ dio n o v 2004, 2005, 2006). RSD was initially developed for clim atic data such as th e Pacific D ecadal O scillation (R o­ dio n o v 2004, 2005), b u t has subsequently been applied to biological data such as the abundances o f organism s in several tro p h ic levels in th e Black Sea ecosystem (D aska­ lov et al. 2007), fish stocks in fo u r m arin e ecosystems (Link et al. 2009) an d p lan k to n in th e N o rth e rn A driatic Sea (K am burska 8c F o n d a-U m an i 2009). RSD assum es th a t th e univariate tim e series o f interest (such as the first prin cip al co m p o n e n t o f a m u ltivariate dataset) is stationary in m ean except at an u n k n o w n

Fig. 1. UK marine regions used in this study. The regions are the standard continuous plankton recorder regions (Richardson et al. 2006): B2 (Northern North Sea); C2 (Central North Sea); C3 (Irish Sea); C4 (West Scotland); D2 (Southern North Sea); D3 (English Chan­

num ber

nel); and D4 (Celtic Sea).

of

discrete

regim e

shifts

(R odionov

2004).

M arine Ecology 32 (Suppl. 1) (2011) 10-24 © 2010 Blackwell Verlag GmbH

-1 0 ° W

-5 ° W

0°

5° E

11

T em po ral c h a n g e in UK m arin e com m u nities

S p e n c e r, B irc h e n o u g h , M ie s z k o w s k a , R o b in so n , S im p s o n , Frid

et al.

Table 1. Summary of the num ber and length of time series, and the types of biological com ponent covered by those series In each of the seven marine regions (the continuous plankton recorder areas - see Fig. 1). The last year of data used for any of the series w as 2006. region

num ber of time series

length (years)

start year

biological com ponents

B2 C2 C3

35 65 37

30 28 19

1977 1979 1988

Marine m a m m a ls , f is h , Z o o p la n k t o n , p h y t o p la n k t o n Marine mammals, fish, Infaunal benthos, Zooplankton, phytoplankton Fish, Z o o p la n k t o n , p h y t o p la n k t o n

C4 D2

38 34

19 30

1988 1977

Marine Marine

D3 D4

68 47

19 25

1988 1982

Fish, rocky shore Invertebrates, Zooplankton, phytoplankton Fish, rocky shore Invertebrates, Zooplankton, phytoplankton

m o re often th a n annually. For these, w e calculated ann u al m eans. M ore detailed in fo rm a tio n o n th e variables for each co m p o n en t is given below.

Plankton Continuous plankton recorder data For every region, we obtain ed eight tim e series derived from m o n th ly c o n tin u o u s p la n k to n reco rd er (CPR) sam ­ ples collected b y th e Sir Alister H a rd y F o u n d atio n for O cean Sciences (SAHFOS). These w ere th e p h y to p lan k to n colour index (P C I), to tal abundances o f diatom s an d dinoflagellates, ech in o d erm an d d ecapod larvae, a n d euphausids, an d abundances o f th e im p o rta n t copepods Calanus finm archicus (boreal) a n d Calanus helgolandicus (tem perate). The PC I is based o n th e ‘greenness’ o f each sam ple, as referenced to stan d ard co lo u r charts, giving one o f fo u r category values p er sam ple. These values are based o n a ratio scale o f acetone extracts using sp ectro p h o to m etric m ethods, a n d give a n in d icatio n o f p h y to p la n k to n b io ­ m ass (R ichardson et al. 2006; section 5.1). For all o th er planktonic sam ples, th e u n its are th e n u m b e r o f organism s per sam ple w here each sam ple represents ap proxim ately 10 nautical m iles (18.5 km ) o f tow , w hich equates to 3 m 3 o f filtered seaw ater (B atten et al. 2003). For all these v ari­ ables, we calculated an n u al m eans fro m th e m o n th ly co n ­ tin u o u s p lan k to n reco rd er sam ples. For som e variables in som e years, th ere w ere n o individuals observed in th e m ajority o f m o n th s (R ichardson et al. 2006). English Channel Zooplankton data In region D3 (English C hannel), we also o b tain ed 22 Zoo­ p lan k to n variables fro m S tation L4, w hich is situ ated in the W estern English C hannel (50° 15.00' N , 4° 13.02' W ) and form s p a rt o f th e W estern C hannel O bservatory ru n b y the P lym ou th M arin e L aboratory w orking w ith th e M arine Biological A ssociation o f th e UK. T he w ater is 50 m deep an d is tidally influenced, w ith a 1.1-k n o t su r­ face stream at m ean spring tide. Typically stratification starts in early A pril, persists th ro u g h o u t th e su m m er an d is eroded by th e end o f O ctober. S tation L4 is strongly

12

m a m m a ls , f is h , Z o o p la n k t o n , p h y t o p la n k t o n m a m m a ls , f is h , Z o o p la n k t o n , p h y t o p la n k t o n

influenced b y th e T am ar E stuary, w ith increased n u trien ts a n d periodic incursions o f fresher surface w ater follow ing heavy ra in (Rees et al. 2009; Sm yth et al. in press). W eekly Z ooplankton sam ples have been collected a t L4 since 1988, using vertical n et hauls fro m th e sea floor to th e surface o f a W P2 n e t w ith a m esh-size o f 200 p m and a 0 .5 -m diam eter ap ertu re co rresp o n d in g to a m o u th area o f 0.25 m 2 (U N ESC O 1968; S outhw ard et al. 2005). The 22 species an d g roups used cover m o re th a n 99% o f th e to ta l Z ooplankton ab u n d an ce at this site. W e used the low est tax o n o m ic level available for each gro u p , an d no species c o n trib u ted to m o re th a n one variable. Originally, th e Z ooplankton tim e series co n tain ed th ree m issing data (Eloire e t al. in press). T he m issing d ata for Jan u ary and F ebruary 1988 w ere replaced b y th e average value o f the m o n th over th e entire tim e series. For A ugust 2000, th e m issing data w ere replaced b y th e average value o f th e m o n th ly averages o f th e previous an d follow ing m o n th s, an d th e average value for A ugust over th e entire tim e series. Finally, an n u al averages w ere calculated from th e m o n th ly averages.

Infaunal benthos For region C2 (C entral N o rth Sea), we o b tain ed infaunal m acro b en th ic data fro m th e D ove M l tim e series (B ucha­ n an & M oore 1986a). These d ata are based o n five 0.1 -m 2 grabs collected in Septem ber each year. T he D ove station M l (55°07' N , 01°20' W ) is 10.5 k m off th e NE English coast. It has p re d o m in a n tly sandy sedim ent, w ith a 20% silt-clay c o n ten t a n d lies in 55 m o f w ater (Frid et al. 1996, 2009). Sam pling com m enced in Septem ber 1972 a n d th e dataset analysed here covers sam ples taken in Septem ber o f each year betw een Septem ber 1979 and 2006. N o sam ples w ere taken, d u e to w eather o r o p era­ tio n al constraints, in Septem ber 1987, 1991 an d 2002. B uchanan & W arw ick (1974) a n d B uchanan & M oore (1986b) describe th e m eth o d s o f sam pling in detail. T he d ata used in this stu d y are to tal genera ab undance p er square m etre based o n at least five replicate sam ples (Frid et al. 2009). Analysis at th e genus level avoided any

Marine Ecology 32 (Suppl. 1) (2011) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

S p e n c e r, B irc h e n o u g h , M ie s z k o w s k a , R o b in so n , S im p s o n , Frid

et al.

problem s in identification at th e species level, o r changes in taxo n o m y leading to pro b lem s w ith hom o n y m s. The full dataset included 327 genera. To extract a sh o rter n u m b e r o f m acrob en th ic variables, genera w ere ranked separately based on to ta l ab u n d an ce across all years an d persistence (frequency o f occurrence). T he ranks were su m m ed an d th e com bined score used to select th e to p 30 species. For years w here th ere w ere m issing data, a n in te r­ polated value was obtain ed b y averaging th e densities of the 2 years before an d th e 2 years after th e m issing year.

Rocky shore invertebrates Q uantitative, replicated counts o f ab u n d an ce w ere m ade annually using replicate 50-cm 2 q u ad rats for th e boreal lim pet species Patella vulgata (Linneaus) an d th e lusitan ian Patella depressa (P en n an t) in th e m id sh o re region of sem i- to exposed rocky shores in regions D3 (W estern English C hannel: seven locations) an d D4 (Celtic Sea: eight locations for P. vulgata, b u t only seven for P. de­ pressa, w hose n u m b ers w ere n o t recorded at th e eighth site in som e years). T he cosm o p o litan Patella ulyssiponen­ sis was also counted , b u t was excluded fro m o u r analyses because m o st counts in m o st years w ere zero. These sites w ere p a rt o f a w ider U K survey (M ies­ zkow ska et a l 2006). T hree surveyors (S. H aw kins, M. B urrow s a n d N. M ieszkowska) w ere involved in data collection, a n d have u n d ertak en m u ltip le cross-calibration exercises to ensure co n tin u ity an d stan d ard isatio n in collection m ethodo lo g y across th e tim e series. N o t all sites w ere surveyed in every year an d th ere are gaps in the tim e series. A least-squares fit general linear regression m odel w ith sites a n d years as fixed factors was fitted to the log10(x + 10)-transform ed survey data to generate p redicted values for co m b in atio n s o f sites a n d years for w hich data was m issing. T he com plete d ata m atrix h ad 435 elem ents for each species. O f these, 227 elem ents (52% ) contained real data, a n d 208 m issing elem ents (48% ) w ere filled using m odel data. C alculated values of R 2 w ere P. depressa 0.84 an d P. vulgata 0.77. W e subse­ q uently excluded P. depressa at L y n m o u th because as a range edge location it was n o t recorded in all years, lead­ ing to several zero values. A lthough we are concerned a b o u t th e n u m b er o f m issing data in these tim e series, we th in k it im p o rta n t to consider th eir inclusion. W ith o u t them , th e rocky shore h ab itat, o n w hich m an y studies of the effects o f clim ate change have focused (H aw kins et al. 2009), w ould n o t be represented in o u r analyses.

Fish T he m o st extensive fish survey d ata used in this analysis w ere collected by th e C en tre for E n v iro n m en t Fisheries

Marine Ecology 32 (Suppl. 1) (2011 ) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

T em po ral c h a n g e in UK m a r in e co m m un ities

a n d A q u aculture Science (CEFAS) (Ellis et al. 2005) d u r­ ing five separate lo n g -term surveys. F our surveys used o tte r traw ls [B2, C2 an d D2 (N o rth ern , C entral an d S o u th ern N o rth Sea) a n d D 4 (Celtic Sea)], an d th ree used b eam traw ls [D3 (English C hannel), D 4 (Celtic Sea), an d C3 (Irish Sea)]. All surveys w ere co n d u cte d in a u tu m n (A u g u st-D ecem b er), fish w ere identified to species level, a n d catches w ere stan d ard ised to catch p er h o u r. For each o f th e seven SAHFOS CPR S tandard Areas, we calculated th e m ean catch p er traw l p er year for all 179 species, an d th e n identified th e d o m in a n t 30 species in each area in a w ay th a t com bines persistence a n d abundance. Species w ere ranked b y ab u n d an ce fro m highest (1) to low est (0), th e ranks w ere m u ltip lied b y th e p ro p o rtio n o f tim es the species ap peared in hauls, an d th e species w ith th e 30 highest scores w ere selected. Sim ilar m eth o d s w ere used b y G enner et al. (2004, 2010). Pelagic species [i.e. those w ith a n ad u lt pelagic phase) w ere subsequently rem oved because o f concerns th a t th e gear used in these surveys sam pled th e m incidentally. T hus, som e im p o rta n t aspects o f ecosystem change such as th e ratio o f pelagic to dem ersal fish (de Leiva M o ren o et al. 2000) cann ot be detected b y o u r analyses. In region D 4 (Celtic Sea) these d ata w ere su p p lem ented b y th e ‘S tan d ard H a u l’ series fro m th e M arin e Biological A ssociation’s L aboratory, P ly m o u th , as p a rt o f th e W es­ te rn C hannel O bservatory. O tte r traw ls w ere u n d ertak en a t 30 -5 0 m d ep th over a spatial scale o f 51 X 22 km off P ly m o u th (5 0 °0 8 '-5 0 °2 0 ' N , 0 3 °5 5 '-0 4 °3 9 ' W ) during 1911, 1913-1914, 1919-1922, 1950-1958, 1967-1979, 1983-1994 an d 2001-2007. T he ab u n d an ce o f dem ersal fish taxa was recorded. O ver th e series, seven vessels have been used for sam pling, ranging in overall length from 18.3 to 39.0 m . W here d ata are available, trawls were u n d e rta k e n a t th e sam e speeds a n d w ere com parable in dim ensions: h eadline length range, 16.2-19.8 m ; g ro undro p e length range, 19.8-27.4 m ; m ain n et stretched m esh diam eter, 75-270 m m , a n d all vessels used a fine-m esh cod end o r a cover (G enner et a l 2010). D ata inclu d ed in this analysis w ere stan d ard ised m ean catch p er h o u r, of all hauls d u rin g th e year, for 30 species, as an an n u al average o f all trawls collected, as previous analyses o f this d ata suggested in teran n u al v ariatio n is m u ch stronger th a n seasonal v ariatio n (G enner et a l 2010).

Marine mammals E stim ates o f to tal grey seal (Halichoerus grypus) p u p p ro ­ d u ctio n w ere o b tain ed at in d ividual b reeding colonies in regions B2 (N o rth e rn N o rth Sea: O rkney), C2 (C entral N o rth Sea: Isle o f M ay, Fast Castle, Farne Islands), D2 (S o u th ern N o rth Sea: L incolnshire, N orfolk), an d C4 (W est Scotland: In n er a n d O u ter H ebrides). All seal data

13

T em po ral c h a n g e in UK m arin e com m u nities

w ere derived fro m surveys either con d u cted o r rep o rted b y the Sea M am m al Research U n it (D uck & M ackey 2008; D uck et al. 2008). T here are n o reliable d ata o n total p o p u latio n size. P u p p ro d u c tio n at a fixed set of sites can be m easured reliably, alth o u g h its relationship to p o p u latio n size is com plicated b y density dependence in som e cases. P u p p ro d u c tio n in B2, C2 (ap art fro m th e Farne Islands), an d C4 was estim ated fro m repeated aerial surveys d u rin g th e breeding season using m ax im u m likeli­ h o o d m eth o d s (D u ck & M ackey 2008). C4 d ata were com bined estim ates o f p ro d u c tio n fro m 11 colonies in the In n er H ebrides a n d 15 in th e O u ter H ebrides from 1984 onw ards. P rio r to 1983, d ata are for colonies in the O u ter H ebrides only. B2 data are fro m u p to 26 colonies in O rkney. C2 d ata w ere fro m tw o colonies in th e Firth o f F orth, o f w hich only one (a new colony) was included in 1997. N o aerial survey data w ere available in 1983 for m o st colonies. W h ere necessary, we used th e m ean o f the values fro m 1982 a n d 1984 as an estim ate o f 1983 p u p p ro d u c tio n for B2 a n d C2 (we d id n o t need to interpolate for C4 because th e startin g year for this region was 1988). P up p ro d u c tio n for th e Farne Islands (C2) is th e cu m u la­ tive to tal from repeated g ro u n d co u n ts carried o u t by N ational T ru st staff. D ata for th e so u th e rn N o rth Sea (D2) are from th ree relatively recently established colonies th a t are sim ilarly g ro u n d -c o u n te d b y staff fro m L incoln­ shire W ildlife T ru st, th e N atio n al T ru st an d N atu ral England.

Statistical m ethods The RSD algorith m is designed to detect changes in u n i­ variate tim e series (R o d io n o v 2004). W e therefore used the first princip al co m p o n en t o f th e d ata for each region as a univariate su m m ary o f th e m ajo r p a ttern s o f co m ­ m u n ity change. D ata for each tim e series w ere n atu ra l log (x + 1)-tran sfo rm ed because we expect a positive rela­ tionship betw een level a n d variability (we ad d ed 1 to each observation because som e tim e series con tained zeros). W e th en centred an d scaled th e lo g -tran sfo rm ed d ata so th a t each series h ad m ean 0 an d stan d a rd d eviation 1. W e calculated princip al co m p o n en ts o f th e centred a n d scaled data for each region, treatin g each year as an observation and each tim e series as a variable. Because th e data are tim e series, observations in successive years are n o t in d e­ pendent. H ow ever, such dependencies are n o t a serious pro b lem w hen th e p rin cip al co m p o n en ts are used as descriptions o f data (Jolliffe 2002; section 12.1). M axi­ m u m au to co rrelatio n factor analysis (MAFA: Solow 1994) is an alternative tech n iq u e for extracting co m p o n en ts th a t describe changes in m u ltiv ariate tim e series w hich explic­ itly deals w ith au to co rrelatio n . It differs fro m principal c om ponents analysis in th a t it extracts orth o g o n al

14

S p e n c e r, B irc h e n o u g h , M ie s z k o w s k a , R o b in so n , S im p s o n , Frid

et al.

c o m p o n en ts w ith th e m ax im u m possible au to co rrelation, ra th e r th a n variance. This is useful for identifying sm o o th tren d s in tim e series. H ow ever, su d d en changes such as regim e shifts do n o t necessarily result in stro n g a u to c o r­ relations an d m ig h t n o t b e extracted b y MAFA. As we w an t to d eterm in e w heth er changes are su d d en or gradual, we th in k th a t p rin cip al c o m p o n en ts are m o re ap p ro p riate th a n MAFA for o u r purposes. T he tim e series in each region w ere g ro u p ed in to b io ­ logical co m p o n en ts (Table 1). W e are in terested in regim e shifts th a t affect m u ltip le categories. H ow ever, the unw eighted prin cip al co m p o n e n t analysis gives equal w eight to each tim e series. Categories for w hich m any tim e series are available m ay th erefore d o m in ate the first principal co m p o n en t. This m ay be undesirable because th e n u m b e r o f tim e series in a category reflects only the availability a n d tax o n o m ic reso lu tio n o f data. W e th ere­ fore also calculated w eighted p rincipal co m p o n ents, in w hich we gave equal w eight to each category rath er th a n each tim e series. To do this, we fo u n d th e principal co m ­ p o n en ts o f th e tran sfo rm ed variables

zm

x ij(k) — fij(k) = — ¡— r ~ \ J nkGm

w here x ^ is th e value o f th e ith observation fro m v ari­ able j, w hich is in category k, f t ^ i s th e sam ple m ean for th e jth variable, o j ^ i s th e sam ple variance for the jth variable, a n d n k is th e n u m b e r o f variables in th e /rth cat­ egory (Deville & M alinvaud 1983; Jolliffe 2002, section 14.2.1). T he RSD alg o rith m is designed to detect changes at discrete tim es in an otherw ise-stationary tim e series (R o­ d io n o v 2004). If th ere are tem p o ral tren d s in p o p ulations, th e original variables will n o t b e statio n ary in m ean, and it is unlikely th a t th e first p rin cip al co m p o n en t will be statio n ary in m ean. H ow ever, if th e p o p u la tio n is grow ing a t a c o n stan t average rate, th e first differences (th e differ­ ence betw een th e value in a given year an d th e value in th e previous year) o f th e lo g -tran sfo rm ed observations will b e statio n ary in m ean. W e therefore also analysed the first principal co m p o n en t o f th e first differences o f logtran sform ed data, using b o th th e unw eighted and w eighted ap proaches described above. W h en this is done, th e events th a t RSD is searching for will be changes in th e average rate o f change o f th e first prin cip al co m p o ­ n en t, rath er th a n changes in th e level o f th e first p rincipal co m p o n en t. Such changes are o f biological interest, and corresp o n d to changes in a w eighted su m o f p o p u latio n grow th rates, b u t they are n o t always inclu d ed in defini­ tions o f regim e shift (review ed b y Lees et al. 2006). W e used V ersion 2.1 o f th e MATLAB im p lem en ta­ tio n o f th e RSD softw are (dow nloaded 21 D ecem ber 2009

Marine Ecology 32 (Suppl. 1) (2011) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

et al.

T em po ral c h a n g e in UK m a r in e co m m un ities

fro m h ttp ://w w w .c lim a te lo g ic .c o m /s ta r s .h tm l). RSD (R odionov 2004) searches for shifts in th e level o f a sta­ tio n ary tim e series b y perfo rm in g t-tests o n individual observations, w ith th e null hypothesis th a t th e n th obser­ vatio n is draw n fro m th e sam e p o p u la tio n as th e preced­ ing sequence o f observations. If th e nu ll hypothesis o f no shift is initially rejected, follow -up tests are p erfo rm ed on a specified n u m b e r o f sub seq u en t observations. T he null hypothesis m ay n o t be finally rejected if these subsequent observations do n o t ap p ear consistent w ith th e pro p o sed shift. All analyses w ere d o n e w ith default param eters [I (cu to ff length) = 10, a (n o m in al size o f test) = 0.05, h (H u b er w eight param eter) = 1]. W e have n o t used any correction for m ultip le testing am o n g regions because we see RSD m ainly as an ex p loratory tool, an d its statistical properties are n o t well enough know n to u n d ertak e an ap p ro p riate correction. W ith in any single tim e series, tests at each tim e p o in t have n o m in al size a. H ow ever, th e sta­ tistical properties o f th e follow -up tests have n o t been exam ined in detail. T he null hypothesis is finally n o t rejected if any o f these follow -up tests does n o t provide stro n g enough evidence against it. The overall size o f the test a t any tim e p o in t is therefore n o t well defined b u t is certainly less th a n a. T here is n o co rrectio n in regim e shift detection for m u ltip le testing w ith in a single tim e series, w hich fu rth er com plicates th e issue. All analyses w ere d o n e using MATLAB R2009b for L inux (T he M athw orks, Inc., N atick, MA, USA). Because

o f concerns a b o u t gear changes an d o th er sam pling arte­ facts in th e fish data, w e repeated all th e analyses w ith o u t th e fish. Similarly, w e repeated all th e analyses w ith o u t th e lim pets, for w hich m an y observations w ere in te rp o ­ lated using a linear m odel.

R esults A fairly large n u m b e r o f p rincipal c o m p o n en ts are needed to acco u n t for m o st o f th e variability in th e data (Fig. 2: w eighted p rincipal co m p o n en ts gave sim ilar results, n o t show n). O ver all tran sfo rm atio n s, p rincipal co m p o n en t m eth o d s, a n d regions, th e first p rin cip al co m p o n en t explained betw een 16 a n d 47% o f th e variability in the d ata (Table 2). T hus, alth o u g h th e first p rin cip al c o m p o ­ n e n t is cap tu rin g a su bstantial a m o u n t o f variability, there are im p o rta n t features o f th e data th a t are n o t readily su m m arised in one dim ension. W h e n applied to th e first p rincipal c o m p o n en t (w hether u nw eighted o r w eighted) o f th e lo g -tran s­ fo rm ed data, regim e shift detectio n (Figs 3 -9 ) fo u n d one regim e shift in each o f th e regions C3 (Irish Sea, Fig. 5A,C), C4 (W est Scotland, Fig. 6A,C), an d D3 (English C hannel, Fig. 8A,C), an d tw o regim e shifts in each o f th e regions B2 (N o rth e rn N o rth Sea, Fig. 3A,C), C2 (C entral N o rth Sea, Fig. 4A,C) (th e last regim e shift here for th e unw eighted analysis was in 2006, th e final year o f th e series), D2 (S o u th ern N o rth

o 30


\ B2

10 20 C om ponent num ber

30

o

Eigen

§ 20 o

S p e n c e r, B irc h e n o u g h , M ie s z k o w s k a , R o b in so n , S im p s o n , Frid

I C2

L 20 40 C om ponent num ber

60

a> 15

10 20 30 C om ponent num ber

10 20 30 C om ponent num ber

a> 15

10

Fig. 2. Scree plots for unweighted principal com ponents analysis of the natural log (x + 1)-transformed data for each region.

20

C om ponent num ber

20 40 C om ponent num ber

a> 20

Com ponents are arranged on the horizontal axis in descending order of the am ount of variance they account for. The vertical axis (eigenvalue) is the variance of each com ponent.

Marine Ecology 32 (Suppl. 1) (2011 ) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

10

20 30 40 C om ponent num ber

15

T em po ral c h a n g e in UK m arin e com m u nities

S p e n c e r, B irc h e n o u g h , M ie s z k o w s k a , R o b in so n , S im p s o n , Frid

Table 2. Percentage variation explained by tw o different forms of first principal com ponent (unweighted and weighted) applied to two different transform ations [natural log (x + 1) and first differences of natural log (x + 1)] of the data for each region.

region

unweighted log

unweighted first difference

weighted log

weighted first difference

B2 C2

27 39

16 19

44 36

28 17

C3 C4 D2 D3 D4

32 31 37 21 36

24 17 16 20 18

23 47 45 24 29

30 38 33 26 18

Sea, Fig. 7A,C), a n d D4 (Celtic Sea, Fig. 9A,C). H o w ­ ever, in all regions o th er th a n C2 (C entral N o rth Sea), the log-transfo rm ed d ata do n o t ap p ear statio n ary in m ean except at th e shift points. T hus, except in C2, the ap p aren t regim e shifts fo u n d b y th e regim e shift detection algo rith m m ay be m o re ap p ro p riately described as trends. T he unw eighted first p rincipal co m p o n e n t o f th e logtransform ed data for C2 show s a stro n g step in 1995

B2 unweighted

1980

1985

et al.

betw een tw o ap p aren tly statio n ary regim es (Fig. 4A). Superficially, this is th e p a tte rn expected fro m a genuine regim e shift. H ow ever, th e step is absent from the w eighted first principal c o m p o n en t (Fig. 4C). Separate analyses o f th e unw eighted first prin cip al co m p o n en t o f th e log -tran sfo rm ed d ata for each category (Fig. 10) show th a t th e step is p resen t only in th e infaunal ben th o s (Fig. 10B). Because th e infaunal b en th o s m ake u p 30 o f 65 tim e series for C2, they d o m in ate th e overall p attern w hen equal w eight is given to each series, b u t n o t w hen equal w eight is given to each category. T he absence o f the step in o th er categories suggests th a t w hatever change occurred in th e seabed c o m m u n ity was n o t tran sm itted to th e o th er categories inclu d ed in this study, an d is therefore n o t a regim e shift in th e usual sense o f the term . Excluding either fish o r lim pets d id n o t change the overall qualitative p atte rn , except th a t w ith o u t fish there was n o evidence o f either tren d s o r step changes in C3 (Irish Sea, n eith er unw eighted n o r w eighted: results n o t show n). T hus, th e tre n d in C3 (Fig. 5A,C) is largely driven b y changes in th e fish data, w h eth er real o r artefactual.

B2 unweighted first difference

1990 1995 Y ear

2000

2005

weighted

1980

1985

1990 1995 Y ear

2000

2005

2000

2005

B2 w eighted first difference

O

CL

1980

1985

1990 1995 Y ear

2000

2005

1980

1985

1990 1995 Y ear

Fig. 3. Regime shift detection applied to region B2 (Northern North Sea), using tw o different forms of principal com ponent (unweighted and w eighted) and tw o different transform ations [natural log (x + 1) and first differences of natural log (x + 1)]. (A) Unweighted first principal com po­ nent of the natural log (x + 1[-transformed data. (B) Unweighted first principal com ponent of the first differences of natural log (x + 1[-trans­ formed data. (C) W eighted first principal com ponent of the natural log (x + 1[-transformed data. (D) W eighted first principal com ponent of the first differences of natural log (x + 1[-transformed data. In each panel, time in years is on the horizontal axis, the vertical axis is the value of the first principal com ponent, the solid lines are the observed values, and the dashed lines are the regime m eans found by regime shift detection with default param eters [/ (cut-off length) = 10, a (nominal size of test) = 0.05, h (Huber w eight parameter) = 1],

16

Marine Ecology 32 (Suppl. 1) (2011) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

S p e n c e r, B irc h e n o u g h , M ie s z k o w s k a , R o b in so n , S im p s o n , Frid

et al.

T em po ral c h a n g e in UK m a r in e co m m un ities

A C2 unweighted

C2 unweighted first difference

o

CL

"O 0 £O) 'o c5

0 -10

=> -5

-10

1980

1985

1990 1995 Year

2000

-2 0

2005

C

1985

1990 1995 Year

2000

2005

2000

2005

D C2 weighted

C2 weighted first difference

o

o

T03

T03

Q_

Fig. 4. Regime shift detection applied to regime C2 (Central North Sea). See Fig. 3 legend for explanation.

1980

Q_

-2

'1980

1985

1990 1995 Year

2000

2005

'1980

1985

1990 1995 Year

C3 unweighted first difference

C3 unweighted

1990

-2

1995

2000

2005

1990

Year

1995

2000

2005

Year C3 weighted first difference

C3 weighted

O Q_ g> '0 £ Fig. 5. Regime shift detection applied to regime C3 (Irish Sea). See Fig. 3 legend for

1990

1995

explanation.

T he first p rincipal co m p o n en ts o f th e first differences o f th e log-transform ed d ata (Figs 3-9B ,D ) are ap p ro x i­ m ately stationary in m ean. In all b u t three cases (C2 unw eighted, Fig. 4B; D3 unw eighted, Fig. 8B; D 4 w eighted, Fig. 9D ), n o regim e shifts w ere detected in the prin cip al co m p o n en ts o f first differences. In these three exceptional cases, th e detected shifts w ere trivial (very sm all a n d in th e final observation p o in t). T hus, overall, th ere is little evidence fo r consisten t changes in p o p u la ­ tio n grow th rates. In all b u t tw o cases (T able 2), th e first

Marine Ecology 32 (Suppl. 1) (2011) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

2000 Year

2005

1990

1995 Year

2000

2005

p rincipal co m p o n e n t explained m o re o f the variability in th e lo g -transform ed d ata th a n in th e first differences o f lo g -tran sfo rm ed data. T his is consisten t w ith the idea that th e d o m in an t p a tte rn in th e log data is a tem p o ral trend, w hich is relatively easy to c ap tu re in o n e dim ension.

D iscussion T h ere have b een m a n y rep o rts o f responses to clim ate change in m a rin e species fro m th e seas a ro u n d th e UK.

17

Spencer, B irchenough, M ieszkow ska, Robinson, Sim pson, Frid e t al.

T em po ral c h a n g e in UK m a r in e co m m u n ities

B

A

C4 unweighted first difference

C4 unweighted

oQ_

o Q_

T03

T3

0

JZ

g>

'0

'0

1

sc

-5

Z>

Z>

-10

1990

1995

2000

-5

2005

1990

1995 Year

Year

C

2000

2005

D C4 weighted

C4 weighted first difference

oQ_

oQ_

T03

T03

-2 -3

1990

1995

2000

-2

2005

1990

1995 Year

Year

2000

2005

Fig. 6. Regime shift detection applied to regime C4 (West Scotland). See Fig. 3 legend for explanation.

B

A D2 unweighted

D2 unweighted first difference

oQ_

■0a

O Q _ ■0a

.c

.c

Z>

Z)

g> 0 sc

g>

0 S C

-5

1980

1985

1990 1995 Year

2000

2005

-5

1980

1985

1990 1995 Year

2000

2005

2000

2005

C

oQ_

■0a .ro - 1

-2 D2 weighted -2

1980

1985

D2 weighted first difference 1990 1995 Year

2000

2005

-3

1980

1985

1990 1995 Year

O ver th e p ast few decades polew ard shifts in biogeo­ g raphic b o u n d aries have b een recorded for p lan k to n (B eaugrand & R eid 2003), in tertid al rocky b e n th o s (M ies­ zkow ska et a l 2006), subtidal b en th o s (H in z et a l in review) an d fish (P erry et a l 2005). C hanges in phenology are also w idespread an d im p o rta n t in m arin e systems. For exam ple, th e advan cem en t o f spring an d su m m er events has occurred m o re slowly in secondary consum ers th a n

18

Fig. 7. Regime shift detection applied to regime D2 (Southern North Sea). See Fig. 3 legend for explanation.

p rim ary p ro d u cers o r p rim a ry consum ers, and th is m is­ m atch has th e p o ten tial to d isru p t ecosystem fun ctio n (T hackeray et a l 2010). T ren d s in ab u n d an ce have also been d o cu m en ted , in cluding increases in p o p u latio n ab u n d an ces o f b en th ic a n d pelagic species w ith w arm w ater affinities close to n o rth e rn range lim its an d cold w ater species close to so u th e rn range lim its (B eaugrand 2003; B eaugrand & Ibanez 2004; M ieszkow ska et a l 2005,

Marine Ecology 32 (Suppl. 1) (2011) 1 0 -2 4 © 2 0 1 0 Blackwell Verlag GmbH

Spencer, B irchenough, M ieszkow ska, Robinson, Sim pson, Frid et al.

T em po ral c h a n g e in UK m a r in e co m m un ities

B

A D3 unweighted o

o

T3

T3

'0

'0

Q_

CL 0

I =§ -1 0

I =§ -1 0 D3 unweighted first difference

-15

1990

1995

2000

-15

2005

1990

Year

C

1995 Year

2000

2005

D D3 weighted

o Q_

o Q_ T03

T3 0

-2

Fig. 8. Regime shift detection applied to regime D3 (English Channel). See Fig. 3 legend for explanation.

-3

-2

1990

1995

2000

-3

2005

D3 weighted first difference 1990

Year

1995 Year

2000

2005

D4 unweighted

o

O

T3

T3

Q_

Q_

0

0

-C

g>

'0

'0

sc

3

I

-1 0

-5

=)

-5

1985

1990

1995

2000

-1 0

2005

D4 unweighted first difference 1985

1990

Year

D4 weighted

o

o

T3 0

T03

2005

2000

2005

Q_

-2

—2

Fig. 9. Regime shift detection applied to

2000

D4 weighted first difference

Q_

regime D4 (Celtic Sea). See Fig. 3 legend for

1995 Year

—3

1985

1990

explanation.

2007; V ance 2005; Rees et al. 2006; Callaway et al. 2007; H id d in k & ter H ofstede 2008; G enner et al. 2010; Eloire et al. in press; W id d ico m b e e t al. in press). H ow ever, lo n g -term assessm ents th a t cover a co m b in atio n o f tim e series observations represen tin g a w ider range o f ecosys­ tem s com ponents are lim ited in UK w aters (Southw ard et al. 2005). Overall, changes in U K m arin e co m m u n ities ap p ear to be d o m in ated by gradual tren d s over th e last tw o to three

Marine Ecology 32 (Suppl. 1) (2011 ) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

1995 Year

2000

2005

-4

1985

1990

1995 Year

decades, ra th e r th a n su d d e n shifts th a t affect m an y c o m p o ­ n en ts o f th e c o m m u n ity at th e sam e tim e. T rends instead o f su d d en shifts seem plausible ecologically for this area of th e w o rld given th a t physical con d itio n s are largely being driven b y th e gradual response to clim atic tren d s such as changing sea tem p e ra tu re (S outhw ard et al. 2005). T here is evidence o f m u ltip le equilibria in a w ide range o f m a th e­ m atical m odels for ecosystem s in clu d in g N o rth A frican vegetation (H iggins et al. 2002), coral reefs (M u m b y et al.

19

Spencer, B irchenough, M ieszkow ska, Robinson, Sim pson, Frid e t al.

T em po ral c h a n g e in UK m a r in e co m m u n ities

A m arine m am m als

oCL TQ)3

Infaunal benthos

o

CL

TQl3

-2

1980

1985

1990

1995

2000

-5

2005

1980

1985

1990

Year

1995

2000

2005

Year

D

C fish

o

phytoplankton

o

CL

CL

TQ)3

TQl3

-5

1980

1985

1990

1995

2000

2005

Fig. 10. Unweighted first principal com ponent of natural log (x + 1)-transformed data for region C2 (Central North Sea), -5

separated Into biological categories [A: marine 1980

1985

1990

Year

Year

E Z o o p la n k to n

o

1995

CL

Tai3

2000

2005

mammals (two time serles), B: Infaunal benthos (30 time series), C: fish (25 time series), D: phytoplankton (three time series), E: Zooplankton (five time series)]. In each panel, time In years Is on the horizontal axis, the vertical axis Is the value of the first principal com ponent, the solid lines are the

-5

1980

1985

1990

1995

2000

2005

Year

2007) an d lakes (C arp en ter 2005). In such m odels, gradual changes in physical conditio n s, or large en ough d istu r­ bances to state variables such as th e abundances o f o rg an ­ ism s, can lead to su d d e n changes in ecosystem state (Beisner et al. 2003). T here is n o d o u b t th a t regim e shifts can occur, an d have im p o rta n t socioeconom ic conse­ quences (Folke et al. 2004). H ow ever, we do n o t see co m ­ pelling evidence for such su d d e n changes in o u r data. T he sam e m ay be tru e o f o th er ecosystem s to w hich regim e shift detectio n has been applied. For exam ple, th e changes in six tim e series fro m th e Black Sea in terp re ted as regim e shifts b y D askalov et al. (2007, th e ir Figure 1) could be in terp re te d as n oisy tren d s ra th e r th a n discrete changes in level. The sam e is tru e o f th e changes in p h y ­ to p lan k to n and Z ooplankton in th e N o rth e rn A driatic (K am burska & F o n d a-U m an i 2009; th eir Figure 13) an d in th e first principal co m p o n en t o f a set o f 114 physico­ chem ical an d biological variables fro m th e N o rth Sea (K enny et al. 2009; th eir Figure 11). H ow ever, d istin­ guishing betw een these alternatives statistically requires m o re sophisticated tim e series m odels th a t are cu rrently in developm ent. In th e m ean tim e, we should n o t too readily accept th e idea o f step-like regim e shifts w hen trends appear plausible. This conclusion is consistent w ith som e other, sm aller-scale statistical analyses o f U K m arin e tim e series. For exam ple, Solow & Beet (2005) fo u n d th a t although there w ere su bstantial changes in th e a b u n ­ dances o f ph y to p lan k to n , copepods, cod, h ad d o ck an d h erring in the N o rth Sea betw een 1963 an d 1997, there

20

observed values, and the dashed lines are the regime m eans found by regime shift detection.

was little evidence for a discrete regim e shift betw een tw o locally stable states. In contrast, B eaugrand & R eid (2003) re p o rt m u ltip le tem p o ral d iscontinuities in N o rth Sea biological tim e series. H ow ever, th e events they are detecting are o f a different type, because th ey analysed one tax o n (e.g. euphausiids, copepods) a t a tim e, and looked at a sm all n u m b e r o f taxa over a longer tim e p e r­ io d th a n th a t o f o u r data. T hey calculated th e p rincipal c o m p o n en ts o f sp atio tem p o ral d ata for each taxon, and used a m eth o d w hich will detect adjacent 6-year blocks w ith significantly different m e a n values. T hus, th e events they detect are relatively sh o rt-te rm changes in th e a b u n ­ dances o f in dividual taxa. H ow ever, they n o te d th a t long­ te rm tren d s w ere th e d o m in a n t p a tte rn in th eir data, w hich is consistent w ith o u r results. O u r analyses do suggest th a t th ere was a p otential regim e shift in region C2 (C entral N o rth Sea) aro u n d 1995 driven p rim arily b y th e infaunal benthos. The in fau ­ nal b en th ic tim e series has been previously analysed in isolation in a m o re extensive form . A m ong th e 89 d o m i­ n a n t genera, th ere are a series o f su d d e n changes in species co m p o sitio n at 5-1 0 -y ear intervals betw een 1972 a n d 2005 (Frid et al. 2009). D espite these changes, higher-level p ro p erties such as to tal ab u n d an ce a n d gen­ era richness rem ain ed rou g h ly constant. T he m o st m arked changes in species co m p o sitio n identified in th e 33-year series w ere in th e early 1980s a n d early 1990s. In the sh o rter tim e series analysed using RSD here, th e 1980s shift m ay n o t have been detected because it was to o close

Marine Ecology 32 (Suppl. 1) (2011) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

Spencer, B irchenough, M ieszkow ska, Robinson, Sim pson, Frid et al.

to the start o f the dataset. T he 1995 shift we detected m ay correspond to th e early 1990s shift fo u n d b y Frid et al. (2009). T hus, th e RSD analysis is consistent w ith previous rep o rts o f rou g h ly decadal shifts in species co m ­ p o sitio n in th e C entral N o rth Sea. H ow ever, these shifts did n o t p ropagate to th e o th er c o m p o n en ts o f th e ecosys­ tem analysed here for this region (p lan k to n , fish, an d m arin e m am m als). T here are th ree possible (a n d n o t m u tu ally exclusive) explanations. First, th e replacem ent of one polychaete-do m in ated assem blage b y a n o th e r m ay have little im pact o n o th er tro p h ic levels. T his could occur if m an y o f th e polychaete species are sim ilarly su it­ able food item s for consum ers such as fish, an d consum e resources at sim ilar rates. Secondly, if stocks o f m an y fish species in the region w ere red u ced as a result o f exploita­ tio n (FAO 2009, p. 196), th ere m ay have been little scope for a response to changes in p rey abundance. T hirdly, the b enthic data w ere fro m a single location, a n d we do n o t know the geographical extent o f th e changes in species com position. Local changes m ay have h ad little effect on w ide-ranging consum ers, o r o n sam ples taken fro m o th er locations. D istinguishing gradual fro m su d d e n change is im p o rta n t for ecosystem -based m anagem ent. T h ru sh & D ayton (2010) discuss several exam ples o f ‘ecological ratch ets’, in w hich a sustained fishing im p act pushes an ecosystem into a new state from w hich recovery to th e original state is dif­ ficult. In such cases, rem oving th e im p act will n o t restore the system. In con trast, th e lack o f stro n g evidence for w idespread regim e shifts in o u r d ata suggests th a t m o st c om ponents o f U K m arin e ecosystem s m ig h t re tu rn to states observed in previous decades if b o th abiotic variables an d h u m a n im pacts w ere re tu rn e d to th e ir 1970s levels. T his does n o t im ply th a t irreversible changes d id n o t occur before the start o f o u r data, a n d m ay tell us little a b o u t the risk o f fu tu re regim e shifts (T h ru sh et al. 2009). In fo rm atio n on th e responses o f m u ltip le tro p h ic levels to clim ate change is req u ired to feed in to n atio n al an d in tern atio n al legislation (e.g. U K M arin e & C oastal Access Bill, UK C lim ate C hange A ct, EU H ab itats D irective an d EU M arine Strategy F ram ew ork D irective). F u rth erm o re, the C o m m o n Fisheries Policy review recognises th e need for anthro p o g en ic im pacts o n m arin e ecosystem s a n d spe­ cies to be view ed in th e context o f pervasive clim ate change (C om m ission o f th e E u ro p ean C o m m u n ities 2008a,b, 2009). The effects o f clim ate change o n m arin e ecosystems are im p o rta n t b o th econom ically an d ecologically, w hether they are gradual o r sudden. For exam ple, clim ate-driven changes in p lan k to n m ay be an im p o rta n t d e te rm in an t of cod recru itm en t in th e N o rth A tlantic (B eaugrand & K irby 2010), and declines in th e a b u n d an ce an d d istrib u tio n of kelps are likely to be decreasing available n u rsery g rounds for juvenile fish (M ieszkow ska et al. 2005). T hus, m an ag e­

Marine Ecology 32 (Suppl. 1) (2011) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

T em po ral c h a n g e in UK m a r in e co m m un ities

m e n t strategies need to consider th e entire ecosystem, in clu d in g abiotic co m p o n en ts, ra th e r th a n focusing only on one ecosystem co m p o n e n t alone. F u rth erm o re, th e in tegra­ tio n o f direct h u m a n effects o n exploited species w ith direct o r in d irect clim atic effects is n eeded for a realistic perspec­ tive o n ecosystem responses. O u r analyses have highlighted m ulti-d ecad al tren d s across a b ro a d range o f ecosystem co m p o n en ts, b u t fu rth e r analyses will be req u ired to exam ­ ine th e likely drivers o f th e tren d s observed. A lthough across a range o f ecosystem co m p o n en ts, o u r analysis has co n cen trated o n changes in species a b u n ­ dances. Ecosystem approaches to m an ag em en t also con­ sider ecosystem fu n ctio n s an d services. Biological traits analysis (B rem ner et al. 2006) assum es th a t ecosystem fu n ctio n s are linearly related to species abundances. If this is tru e, th e n o u r results im p ly gradual changes in ecosys­ tem fu n ctio n for m o st biological c o m p o n en ts o f m o st UK m arin e ecosystems. H ow ever, at least som e ecosystem ser­ vices (such as coastal p ro te ctio n pro v id ed b y m arshes, m angroves, seagrasses, an d coral reefs) are nonlinearly related to species abundances (K och et al. 2009). In such cases, th ere m ay be u tility thresholds (S am h o u ri et a l 2010), such th a t m an ag em en t actions p ro d u ce m u ch greater responses for som e ecosystem states th a n others, even in th e absence o f regim e shifts. This is a n o th e r area in w hich m odels w ith b ro ad e r scope are needed.

C onclu sions Overall, change in U K m arin e co m m u n ities m ay be b etter described as tem p o ral tren d s th a n as a b ru p t regim e shifts, alth o u g h a b ru p t shifts m ay have occurred in som e regions. F u tu re analyses o f change in U K m arin e c o m m u ­ nities should therefore be based o n statistical m odels th at explicitly include tren d s, b u t also allow th e possibility of a b ru p t shifts. O ne pro m isin g ap p ro ach is to use statespace m odels (D u rb in & K o o p m an 2001), w hich are m u c h m o re general an d flexible th a n m an y o ther approaches to tim e-series analysis, an d w hich can be applied easily to n o n -sta tio n a ry tim e series. L ooking at large n u m b ers o f tim e series across an entire region co m plem ents th e analysis o f in d ividual tim e series, an d b ro ad en s o u r ability to describe an d u n d e r­ stan d regim e shifts a n d o th er ecosystem changes. W e have show n th a t getting m eaningful results fro m such an a p p ro ach requires n o t only co llaboration betw een large n u m b ers o f d ata providers, b u t also th e critical evaluation o f statistical m ethods.

A c k n o w le d g e m e n ts T he a u th o rs w ould like to th a n k th e M arin e E n viron­ m en tal C hange N etw o rk (h ttp ://w w w .m b a.ac.u k /m ecn )

21

T em po ral c h a n g e in UK m arin e com m u nities

Spencer, B irchenough, M ieszkow ska, Robinson, Sim pson, Frid et al.

and D efra for fu n d in g an d organising th e d ata analysis w orkshop. D efra has also pro v id ed fu n d in g th ro u g h th e M EC N to su p p o rt a n u m b e r o f th e tim e series used in this analysis in cluding th e D ove, PM L, Liverpool Bay, MBA fish tim e series an d M arC lim benthic datasets, and th e Cefas fish data. T he N atu ral E n viro n m ent Research C ouncil (NERC) O ceans 2025 Strategic Research P ro g ram m e fu n d ed d ata collection b y th e W es­ te rn C hannel O bservatory, a research collaboration betw een PM L an d th e MBA. A d d itional funders acknow ledged for th eir c o n trib u tio n s to various tim e series are D efra, C o untryside C ouncil for W ales, Envi­ ro n m e n t Agency, JN CC, English N a tu re /N a tu ra l E ng­ land, NERC, Scottish G overnm ent, Scottish N atu ral Eleritage, States o f G uernsey, T he C row n Estates, an d W W F. W e are grateful to Sergei R o d io n o v for discus­ sion on the regim e shift detectio n alg o rith m , M artin G enner for his c o n trib u tio n s to th e 2009 M EC N w o rk ­ shop on w hich this p a p er was based, a n d C laire W iddicom be for assistance w ith p lan k to n data. W e w ould like to th a n k tw o a n o n y m o u s reviewers for th o ro u g h an d constructive criticism . H istorical d ata retrieval at th e MBA was also assisted b y fu n d in g fro m th e NAGISA H isto ry o f the N earshore P rogram m e.

using biological traits analysis (BTA). Ecological Indicators, 6, 609-622. B uchanan J.B., M oore J.J. (1986a) A bro ad review o f variability and persistence in the N orth u m b erlan d benthic fauna 1971-85. Journal o f the M arine Biological Association o f the United Kingdom, 66, 641-657. B uchanan J.B., M oore J.J. (1986b) Long-term studies at a Benthic Station o ff the coast o f N orthum berland. Hydrobiologia, 142, 121-127. B uchanan J.B., W arw ick R.M. (1974) An estim ate o f benthic m acrofaunal p ro d u c tio n in the offshore m u d o f the N o rth ­ um berland coast. Journal o f the M arine Biological Association o f the United Kingdom, 54, 197-222. Callaway R., E ngelhard G.H., D ann J., C otter J., R um ohr H. (2007)

A century o f N o rth Sea epibenthos a n d trawling:

com parison betw een 1902-1912, 1982-1985 a n d 2000. M arine Ecology Progress Series, 346, 27-43. C arpenter S.R. (2005) E utrophication o f aquatic ecosystems: bistability and soil phosphorus. Proceedings o f the N ational A cadem y o f Sciences o f the United States o f America, 102, 10002-10005. C arpenter S.R., L athrop R.C. (2008) Probabilistic estim ate o f a threshold for eutrophication. Ecosystems, 11, 601-613. Chavez F.P., Ryan J., Lluch-C ota S.E., N iquen M . (2003) From anchovies to sardines and back: m ultidecadal change in the Pacific Ocean. Science, 299, 217-221. C om m ission o f the E uropean C om m unities (2008a) Directive

R eferen ces

20 0 8 /5 6 /E C o f the E uropean Parliam ent a n d o f the C ouncil

Batten S.D., Clark R., Flinkm an J., Hays G.C., John E., John

o f 17 June 2008 - establishing a fram ew ork for com m unity

A.W.G., Jonas T., Lindley J.A., Stevens D.P., W alne A.

action in the field o f m arine environm ental policy (M arine

(2003) CPR sam pling: the technical background, m aterials

Strategy Fram ew ork Directive). Official Journal o f the European Union, L 164/19, 22.

and m ethods, consistency a n d com parability. Progress in Oceanography, 58, 193-215. B eaugrand G. (2003) Long-term changes in copepod a b u n ­ dance a n d diversity in the no rth -east A tlantic in relation to fluctuations in the hydroclim atic environm ent. Fisheries Oceanography, 12, 270-283. B eaugrand G., Ibanez F. (2004) M onitoring m arine plankton ecosystems. II: L ong-term changes in N o rth Sea calanoid copepods in relation to hydro-clim atic variability. Marine Ecology Progress Series, 284, 35-47. B eaugrand G., Kirby R.R. (2010) Clim ate, plankton and cod. Global Change Biology, 16, 1268-1280. B eaugrand G., Reid P.C. (2003) Long-term changes in phy to ­

pean Strategy for M arine and M aritim e Research. Brussels, COM : 534 pp. C om m ission o f the E uropean C om m unities (2009) Green Paper, Reform o f the Common Fisheries Policy. Brussels, COM : 28 pp. D askalov G.M., G rishin A.G., R odionov S., M ihneva V. (2007) T rophic cascades triggered by overfishing reveal possible m echanism s o f ecosystem regim e shifts. Proceedings o f the N ational A cadem y o f Sciences o f the United States o f America, 104, 10518-10523. Deville J.-C., M alinvaud E. (1983) D ata analysis in official

plankton, Z ooplankton and salm on related to clim ate. Global

socio-econom ic statistics. Journal o f the Royal Statistical

Change Biology, 9, 801-817.

Society Series A , 146, 335-361.

B eaugrand G., Edwards M., B rander K., Luczak C., Ibanez F. (2008) Causes a n d projections o f a b ru p t clim ate-driven

D uck C.D., M ackey B.L. (2008) Grey Seal Pup Production in Britain in 2007. Sea M am m al Research U nit, U niversity o f

ecosystem shifts in the N o rth A tlantic. Ecology Letters, 11,

St Andrews, Available at: http://w w w .sm ru.st-and.ac.uk/

1157-1168.

docum ents/SC O S_2008_vl.pdf.

Beisner B.E., H aydon D.T., C uddington K. (2003) Alternative

D uck C.D., T hom pson D., M ackey B.L. (2008) The Status o f

stable states in ecology. Frontiers in Ecology and the Environ­

British Common Seal Popidations in 2007. Sea M am m al

ment, 1, 376-382.

Research U nit, University o f St Andrews, Available at:

B rem ner J., Rogers S.I., Frid C.L.J. (2006) M ethods for describ­ ing ecological functioning o f m arine benthic assemblages

22

C om m ission o f the E uropean C om m unities (2008b) A Euro­

http://w w w .sm ru.st-and.ac.uk/docum ents/SC O S_2008_ v l.p d f.

Marine Ecology 32 (Suppl. 1) (2011) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

Spencer, B irchenough, M ieszkow ska, Robinson, Sim pson, Frid et ai

D u rb in J., K oopm an S.J. (2001) Tim e Series Analysis by State Space Methods. O xford U niversity Press, Oxford. Ellis J.R., D ulvy N.K., Jennings S., Parker-H um phreys M., Rogers S.I. (2005) Assessing the status o f dem ersal elasmo-

T em po ral c h a n g e in UK m a r in e co m m un ities

H eath M.R., Beare D.J. (2008) New prim ary pro d u ctio n in northw est E uropean shelf seas, 1960-2003. M arine Ecology Progress Series, 363, 183-203. H em ery G., D ’Am ico F., Castege I., D u p o n t B., D ’Elbee J.,

branchs in UK waters: a review. Journal o f the M arine

Lalanne Y., M ouches C. (2008) D etecting the im pact o f

Biological Association o f the United Kingdom, 85, 1025-1047.

oceano-clim atic changes o n m arine ecosystems using a

Eloire D., Som erfield P.J., Conway D.V.P., H alsband-L enk C., H arris R., B onnet D. (in press) T em poral variability and co m m unity com position o f Zooplankton at station L4 in the W estern Channel: 20 years o f sam pling. Journal o f Plankton Research. FAO (2009) The State o f World Fisheries and Aquaculture 2008. FAO, Rome: 196. Folke C., C arpenter S., W alker B., Scheffer M., Elm qvist T., G underson L., H olling C.S. (2004) Regime shifts, resilience,

m ultivariate index: the case o f the Bay o f Biscay (N orth A tlantic-E uropean O cean). Global Change Biology, 14, 27-38. H id d in k J.G., ter H ofstede R. (2008) Clim ate induced increases in species richness o f m arine fishes. Global Change Biology, 14, 453-460. Higgins P.A.T., M astrandrea M.D., Schneider S.H. (2002) Dynam ics o f clim ate and ecosystem coupling: abrupt changes a n d m ultiple equilibria. Philosophical Transactions o f

and biodiversity in ecosystem m anagem ent. A nnual Review

the Royal Society o f London Series B Biological Sciences, 357,

o f Ecology Evolution and Systematics, 35, 557-581.

647-655.

Frid C.L.J., Buchanan J.B., G arw ood P.R. ( 1996) Variability and

H inz H., Capasso E., Lilley M., Frost M., Jenkins S.R. (in

stability in benthos: tw enty-tw o years o f m on ito rin g off

review) Investigating tem poral changes o f sub-tidal benthic

N orthum berland. ICES Journal o f M arine Science, 53, 978-980.

com m unities across a bio-geographic boundary. Global

Frid C.L.J., G arw ood P.R., R obinson L.A. (2009) Observing change in a N o rth Sea benthic system: a 33 year tim e series. Journal o f M arine Systems, 77, 227-236. G enner M.J., Sims D.W ., W earm o u th V.J., Southall E.J., Southw ard A.J., H enderson P.A., H aw kins S.J. (2004) Regio­ nal clim atic w arm ing drives long-term co m m unity changes o f British m arine fish. Proceedings o f the Royal Society o f London Series B Biological Sciences, 271, 655-661. G enner M.J., Sims D.W ., B udd G.C., M asterson P., M chugh

Change Biology. IPCC (2007) Clim ate change 2007: Synthesis report. C o n trib u ­ tio n o f w orking groups I, II a n d III to the F ourth Assess­ m ent R eport o f the Intergovernm ental Panel o n Clim ate Change. In: Pachauri R.K., Reisinger A. (Eds), Core W riting Team. IPCC, Geneva. Jolliffe I.T. (2002) Principal Component Analysis. 2nd edn. Springer, New York. K am burska L., F onda-U m ani S. (2009) From seasonal to deca­

M., Rendle E., Southall E.J., W earm o u th V., H aw kins S.J.

dal inter-annual variability o f m esozooplankton biom ass in

(2010) Body size-dependent responses o f a m arine fish assemblage to clim ate change a n d fishing over a century-

the N o rth ern A driatic Sea (G ulf o f Trieste). Journal o f M ar­ ine Systems, 78, 490-504.

long scale. Global Change Biology, 16, 517-527.

K enny A.J., Skjoldal H.R., Engelhard G.H., Kershaw P.J., Reid

Greene C.H., Pershing A.J., C ronin T.M., Ceci N. (2008) Arctic

J.B. (2009) A n integrated approach for assessing the relative

clim ate change and its im pacts o n the ecology o f the N o rth

significance o f h u m an pressures a n d environm ental forcing

Atlantic. Ecology, 89, S24-S38.

o n the status o f Large M arine Ecosystems. Progress in

H agerthey S.E., N ew m an S., R utchey K., Sm ith E.P., G odin J. (2008)

M ultiple regim e shifts in a subtropical peatland:

Oceanography, 81, 132-148. K och E.W., Barbier E.B., Sillim an B.R., Reed D.J., Perillo

com m unity-specific thresholds to eutrophication. Ecological

G.M.E., H acker S.D., G ranek E.F., Prim avera J.H., M uthiga

Monographs, 78, 547-565.

N., Polasky S., H alpern B.S., Kennedy C.J., Kappel C.V.,

H a rd m an -M o u n tfo rd N.J., Allen J.I., Frost M .T., Haw kins S.J., Kendall M.A., M ieszkowska N., R ichardson K.A., Somerfield P.J. (2005) Diagnostic m on ito rin g o f a changing environ­ m ent: an alternative UK perspective. M arine Pollution Bulle­ tin, 50, 1463-1471. H are S.R., M antua N.J. (2000) E m pirical evidence for N orth Pacific [climatic] regim e shifts in 1977 and 1989. Progress in Oceanography, 47, 103-145. H aw kins S.J., Sugden H.E., M ieszkowska N., M oore P.J.,

W olanski E. (2009) N on-linearity in ecosystem services: tem poral and spatial variability in coastal protection. Fron­ tiers in Ecology and the Environm ent, 7, 29-37. Lees K., Pitois S., Scott C., Frid C., M ackinson S. (2006) C har­ acterizing regim e shifts in the m arine environm ent. Fish and Fisheries, 7, 104-127. de Leiva M oreno J.I., Agostini V.N., C addy J.F., Carocci F. (2000) Is the pelagic-dem ersal ratio from fishery landings a useful proxy for n u trie n t availability? A prelim inary data

Poloczanska E., Leaper R., H erbert R.J.H., G enner M.J.,

exploration for the sem i-enclosed seas a ro u n d Europe. ICES

M oschella P.S., T hom pson R.C., Jenkins S.R., Southw ard

Journal o f M arine Science, 57, 1091-1102.

A.J., Burrows M .T. (2009) Consequences o f clim ate-driven biodiversity changes for ecosystem functioning o f N o rth

Link J.S., Stockhausen W .T., Skaret G., O verholtz W ., M egrey B.A., Gjosæter H., Gaichas S., D om m asnes A., Falk-Petersen

E uropean rocky shores. M arine Ecology Progress Series, 396,

J., Kane J., M ueter F.J., Friedland K.D., H are J.A. (2009)

245-259.

A com parison o f biological trends from four m arine

Marine Ecology 32 (Suppl. 1) (2011 ) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

23

T em po ral c h a n g e in UK m arin e com m u nities

ecosystems: synchronies, differences, a n d com m onalities. Progress in Oceanography, 81, 29-46. M ieszkowska N., Leaper R., M oore P., Kendall M.A., Burrows M.T., Lear D., Poloczanska E., Hiscock K., M oschella P.S., T hom pson R.C., H erbert R.J., Laffoley D., Baxter J., South­ w ard A.J., H aw kins S.J. (2005) M arine biodiversity and climate change: assessing and predicting the influence o f climatic change using intertidal Rocky Shore Biota. O ccasional Publications, no. 20. M arine Biological Association o f the United Kingdom, 53 pp. M ieszkowska N., Kendall M.A., H aw kins S.J., Leaper R., W illiam son P., H a rd m an -M o u n tfo rd N.J., Southw ard A.J. (2006) Changes in the range o f som e co m m o n rocky shore species in B ritain - a response to clim ate change? Hydrobiologia, 555, 241-251. M ieszkowska N., H aw kins S.J., Burrows M .T., Kendall M.A. (2007) Long-term changes in the geographic distribution and p opulatio n structures o f Osilinus lineatus (G astropoda: T rochidae) in B ritain a n d Ireland. Journal o f the M arine Biological Association o f the United Kingdom, 87, 537-545. M um by P.J., H astings A., Edwards H.J. (2007) Thresholds and the resilience o f Caribbean coral reefs. N ature, 450, 98-101. Perry A., Low P.J., Ellis J.R., Reynolds J.D. (2005) Climate

tion Methods. UNESCO-ROSTE/BAS W orkshop o n Regime Shifts, Paris, 14-16 June 2005, V arna, Bulgaria: 17-24. R odionov S.N. (2006) Use o f prew hitening in clim ate regime shift detection. Geophysical Research Letters, 33, L12707. R udnick D.L., Davis R.E. (2003) Red noise and regim e shifts. Deep-Sea Research Part I, 50, 691-699. Sam houri J.F., Levin P.S., A insw orth C.H. (2010) Identifying thresholds for ecosystem -based m anagem ent. PLoS ONE, 5, e8907. Sm yth T.J., Fishwick J.R., Al M oosawi L., C um m ings D.G., H a r­ ris C., Kitidis V., Rees A., M artinez V incente V., W oodw ard E.M.S. (in press) A b ro a d spatio-tem poral view o f the western English C hannel observatory. Journal o f Plankton Research. Solow A.R. (1994) D etecting change in the com position o f a m ultispecies com m unity. Biometrics, 50, 556-565. Solow A.R., Beet A.R. (2005) A test for a regim e shift. Fisheries Oceanography, 14, 236-240. Southw ard A.J., Langm ead O., H a rd m an -M o u n tfo rd N.J., A iken J., Boalch G.T., D ando P.R., G enner M.J., Joint I., Kendall M.A., H alliday N.C., H arris R.P., Leaper R., M ies­ zkowska N., Pingree R.D., R ichardson A.J., Sims D.W ., Sm ith T., W alne A.W., H aw kins S.J. (2005) Long-term oceano­

1912-1915.

graphic and ecological research in the w estern English

sen J., Conley D.J. (2008) Regime shift in a coastal m arine ecosystem. Ecological Applications, 18, 497-510. Potts D.L., H ux n ian T.E., E nquist B.J., W eltzin J.F., W illiam s D.G. (2006) Resilience and resistance o f ecosystem func­ tional response to a precipitation pulse in a sem i-arid grassland. Journal o f Ecology, 94, 23-30. Rees H.L., Pendle M.A., Lim penny D.S., M ason C.E., Boyd S.E., Birchenough S., Vivian C.M.G. (2006) Benthic responses to organic enrichm ent a n d clim atic events in the

et a!.

R odionov S.N. (2005) A B rief Overview o f the Regime Shift Detec­

change and d istribution shifts in m arine fishes. Science, 308, Petersen J.K., H ansen J.W., Laursen M.B., Clausen P., Carsten-

C hannel. Advances in M arine Biology, 47, 1-105. Thackeray S.J., Sparks T.H., Frederiksen M., B urthe S., Bacon P.J., Bell J.R., B otham M.S., B rereton T.M ., Bright P.W ., Carvalho L., C lutton-B rock T., Dawson A., Edw ards M., Elliot J.M., H arrin g to n R., Johns D., Jones I.D., Jones J.T., Leech D.I., Roy D.B., Scott W.A., Sm ith M., Sm ithers R.J., W infield I.J., W anless S. (2010) T rophic level asynchrony in rates o f phenological change for m arine, freshw ater and te r­ restrial environm ents. Global Change Biology, in press. T hrush S.F., D ayton P.K. (2010) W hat can ecology contribute

w estern N o rth Sea. Journal o f the M arine Biological Associa­

to ecosystem -based m anagem ent? A nnual Review o f M arine

tion o f the United Kingdom, 86, 1-18.

Science, 2, 419-441.

Rees A.P., H ope S.B., W iddicom be C.E., D ixon J.L., W o o d ­

T hrush S.F., H ew itt J.E., D ayton P.K., Coco G., L ohrer A.M.,

w ard E.M.S., Fitzsim ons M.F. (2009) Alkaline phosphatase

N orkko A., N orkko J., C hiantore M . (2009) Forecasting the

activity in the w estern English Channel: elevations induced

lim its o f resilience: integrating em pirical research w ith the­

by high sum m ertim e rainfall. Estuariae Coastal and Shelf

ory. Proceedings o f the Royal Society B Biological Sciences,

Science, 81, 569-574. Reid P.C., Borges M.F., Svendsen E. (2001) A regim e shift in the N o rth Sea circa 1988 linked to changes in the N o rth Sea horse m ackerel fishery. Fisheries Research, 50, 163-171. Resilience Alliance, Santa Fe Institute (2004) Thresholds and Alternate States in Ecological and Social-Ecological Systems. Resilience Alliance, Available at: http://w w w .resalliance.org/ index.php?id=183 (accessed 27 February 2010). R ichardson A.J., W alne A.W ., John A.W.G., Jonas T.D., Lind-

276, 3209-3217. UNESCO (1968) Monographs on Oceanographic Methodology: Zooplankton Sampling. U nited N ations, Paris. U nited N ations (1992) Convention on Biological Diversity. UN, New York: 31 pp. Vance T. (2005) Loss o f the Northern Species Alaria Escidenta from Southw est B ritain a n d Im plications for M acroalgal Succession. U niversity o f Plym outh, Plym outh: 31. W eijerm an M., L indeboom H., Z u u r A.F. (2005) Regime shifts

ley J.A., Sims D .W ., Stevens D., W itt M. (2006) U sing con­

in m arine ecosystems o f the N o rth Sea and W adden Sea.

tin u o u s plankton recorder data. Progress in Oceanography,

M arine Ecology Progress Series, 298, 21-39.

68, 27-74. R odionov S.N. (2004) A sequential algorithm for testing cli­

24

Spencer, B irchenough, M ieszkow ska, Robinson, Sim pson, Frid

W iddicom be C.E., Eloire D., H arb o u r D., H arris R.P., Som er­ field P.J. (in press) L ong-term phytoplankton co m m unity

m ate regim e shifts. Geophysical Research Letters, 31, L09204,

dynam ics in the w estern English C hannel. Journal o f P lank­

doi: 10.1029/2004GL019448.

ton Research.

Marine Ecology 32 (Suppl. 1) (2011) 1 0 -2 4 © 2010 Blackwell Verlag GmbH

marine ecology

an evolutionary perspective

' »

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

Trends in population dynamics and fishery of Parapenaeus lon giro stris and Nephrops norvegicus in th e Tyrrhenian Sea (NW Mediterranean): th e relative importance of fishery and environmental variables A le ssa n d r o Ligas1, P a o lo S artor1 & F ran cesco C o llo c a 2 1 Centro Interuniversitario di Biología Marina ed Ecología Applicata 'G. Bacci', viale N. Sauro 4, Livorno, Italy 2 Dlpartlmento di Biología Animale e dell'Uomo, University of Rome 'La Saplenza', viale dell'UnlversItà 32, Rome, Italy

K eywords Environmental variables; fishing effort;

A bstract

landings; series analysis; trawl survey.

T em poral v ariatio n in th e p o p u latio n ab u n d an ce o f th e deep-w ater rose sh rim p , Parapenaeus longirostris (Lucas, 1846) (D ecapoda, Penaeidae), a n d the N orw ay lobster, Nephrops norvegicus (Linnaeus, 1758) (D ecapoda, N e p h ro p i­ dae), in th e T y rrh en ian Sea (N W M ed iterran ean ), w ere evaluated using tim e-series d ata (1994—2008) fro m experim ental traw l surveys a n d com m ercial landings. The influence o f several enviro n m en tal variables (sea surface tem p era­ tu re, w in d -m ix ing index a n d N A O index) an d fishing effort indices (n u m b er o f days at sea p e r m o n th a n d m ean engine pow er o f th e traw l fleet) w ere inves­ tigated. T he tim e series w ere analysed b y m eans o f m in /m a x a u to -co rrelatio n factor analysis (MAFA) an d dynam ic factor analysis (DFA). T he ab u n d an ce of P. longirostris show ed a clear increasing tren d , significantly correlated w ith the fishing effort index (n u m b e r o f days at sea p er m o n th ), th e sea surface te m p er­ a tu re an d th e w in d -m ix ing index. T he tem p o ral v ariations in th e stock of P. longirostris, w hich has a preference for w arm w aters, w ere positively corre­ lated w ith th e rise o f th e sea surface tem p e ra tu re an d th e decrease o f w in d cir­ culation. For N . norvegicus, an increasing tre n d o f landings p er u n it o f effort an d re c ru itm e n t index con trasted w ith a decreasing tre n d o f relative p o p u latio n ab u n d an ce (biom ass a n d density indices).

C orrespondence A. Ligas, Centro Interuniversitario di Biología Marina ed Ecología Applicata 'G. Bacci', viale N. Sauro 4, 1-57128 Livorno, Italy. E-mail: [email protected] Accepted: 1 February 2011 doi: 10.1111/j. 1439-0485.2011,00440.x

U n d erstan d in g th e causes an d m echanism s o f change in the abun d an ce o f species over tim e is a crucial issue in m arin e ecology. Fishing exploitation is considered to be one o f th e m ain factors determ in in g th e dynam ics of m arin e po p u latio n s an d ecosystem s (B aum et al. 2003; M o rato et al. 2006; C iannelli et al. 2008; Pauly 2009). These effects include: changes in p re d a to r-p re y relatio n ­ ships th a t lead to shifts in food-w eb stru ctu re (C artes

(e.g. higher grow th rate, earlier ag e-at-m atu rity ) (F ro m en ­ tin & F on ten eau 2001), effects o n th e p o p u latio n s of n o n -ta rg e t species (e.g. cetaceans, sea birds, sea turtles) resulting fro m by-catch (Kaiser & D e G ro o t 2000), sus­ p en sio n o f superficial sedim ents (S m ith et a í 2003), an d a re d u ctio n o f h a b ita t com plexity a n d alteratio n o f b e n ­ thic co m m u n ity stru c tu re (Kaiser et a í 2000). Large-scale changes in clim ate a n d oceanographic co n d i­ tio n s are also k n o w n to influence th e dynam ics o f m arine p o p u latio n s (G islason et a í 2000; L loret et a í 2001;

et al. 2001), effects o n ab u n d an ce a n d body-size d istrib u ­ tio ns th a t can result in fauna d o m in ated b y sm all-size individuals (Jennings et a í 2001), genetic selection for different physical characteristics a n d rep ro d u ctiv e traits

R othschild et a í 2005). For exam ple, th e influence of global w arm in g in th e 20th cen tury o n lo n g -term changes in p h y to p la n k to n co n cen tratio n in th e N o rth A tlantic has been d em o n strated (Reid et a í 2001). In the

Introduction

Marine Ecology 32 (Suppl. 1) (2011 ) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

25

T rends in P. congirostris a n d N. n o rveg icu s

Ligas, Sartor & Colloca

M ed iterranean Sea, en rich m en t o f n u trie n ts in surface w aters has been show n to affect pelagic food-w eb dynam ics and fishery p ro d u ctiv ity (M olinero et al. 2008). T his in tu rn can affect deep-sea n ecto -b en th ic co m m u n ities w hich are know n to dep en d o n th e dow nw ard flux o f organic m atter from th e surface layers (C o m p an y et a í 2008). A dditionally, changes in river discharge an d surface p ro d u c tio n can alter tro p h ic webs a n d assem blage co m p o ­ sitions in deep M ed iterran ean w aters (C artes et a í 2009). C o m pany et a í (2008) described how clim ate-driven cascading dense shelf w ater influences th e ecology o f deepsea p o p u latio n s o n a decadal tim escale. B artolino et a í (2008) linked th e w in d circulation to th e re c ru itm e n t of the E uropean hake, Merluccius merluccius, one o f th e m ost im p o rta n t dem ersal species in M ed iterran ean w aters. M any o th er studies have highlighted significant relationships betw een large-scale atm ospheric variables (such as the N o rth A tlantic O scillation index, N AO , w hich is tra d itio n ­ ally defined as th e n orm alised p ressure difference betw een Azores and Iceland) or local scale (surface tem p eratu re, w ind circulation, etc.) atm o sp h eric variables an d dem ersal po p u latio n s (Lloret et a í 2001; F ariña & G onzález H erraiz 2003; Z u u r et al. 2003a,b; Z u u r & Pierce 2004; Erzini 2005; M aynou 2008; C artes et al. 2009; G onzález H erraiz et a l 2009). Since the 1950s, a w arm in g process has occurred in th e W estern M ed iterran ean basin. This is d em o n strated by b o th environm en tal changes (e.g. surface tem p eratu re increase; see Vargas-Y ánez et al. 2009) an d biological changes (e.g. n o rth w a rd advance o f th erm o p h ilic species; see CIESM 2008). In a d d itio n to enviro nm en tal changes, Italian fishing g rounds, sim ilar to those o f o th er M ed iter­ ran ean countries, have been affected b y a decrease o f fish­ 117

H ‘p O

c

ing effort, m ainly due to th e EU C o m m o n Fishery Policy, w hich p ro m o tes th e red u c tio n o f fishing effort th ro u g h incentives to decom m ission. To analyse th e effects o f enviro n m en tal an d a n th ro p o ­ genic factors o n dem ersal com m unities, tw o species w hich display different life cycles an d b eh avioural strategies w ere selected: th e deep-w ater rose sh rim p , Parapenaeus longi­ rostris (Lucas, 1846) a n d th e N orw ay lobster Nephrops norvegicus (Linnaeus, 1758). Parapenaeus longirostris is a fast-grow ing, short-lived species w ith th erm o p h ilic prefer­ ence (Abellö et a l 2002), in h ab iting th e w ater colum n layers close to th e seabed. Nephrops norvegicus is a longlived decapod, typical o f tem p erate an d cold w aters, w hich dwells in b u rro w s a n d exerts territo rial behaviour (Aguzzi et al. 2003). It was hypothesised th at, d ue to these contrastin g characteristics, th e tw o species w ould show different behaviours in relatio n to changes in envi­ ro n m en tal a n d an th ro p o g en ic factors. F rom th e results, we suggest a m echanism an d cause-effect relationships linking th e atm o sp h eric a n d enviro n m en tal variables w ith changes in th e ab u nd an ce o f b o th species.

S tu dy area T he stu d y area covered p a rt o f th e co n tin en tal shelf an d the u p p er a n d m iddle slope off th e w estern coasts o f Italy (C en­ tra l-n o rth e rn T y rrh en ian Sea, Fig. 1). T he T y rrh enian Sea is sem i-enclosed betw een islands (C orsica, Sardinia and Elba) an d th e m ain lan d (Italy), an d is separated from the rest o f th e w estern basin b y a channel o f m o d erate depth. It can therefore be considered a d istinct en tity w ith in the C entral-w estern M ed iterran ean basin (A rtale et al. 1994; G asparini et al. 2005). T he circulation in th e T y rrhenian r ? fc

137

er

V J -----f(Y

y.

,

v í

*

P o r to S .S te f a n o

R om a

50 0

k vi a «ta

Vo

Fig. 1. Study area; the main isobaths are

V'

.i 26

■T, “ J

(T O

shown, as well as the sampling stations investigated during the experimental trawl survey Medits 2008. The black triangles show the three points at which satellite data were collected (42°30' N, 11°00' E; 42°00' N, 12°00' E; and 41°00' N, 13°00' E).

Marine Ecology 32 (Suppl. 1) (2011) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

Ligas, Sartor & Colloca

Sea is organised in a series o f cyclonic (anti-clockw ise) an d anticyclonic (clockwise) gyres d eterm in ed b y th e w in d (Artale et a í 1994). T hree m ain cold w ater gyres, tw o cyclonic an d one anticyclonic, have been detected. T hey u n d erg o significant seasonal change, particularly th e central anticy­ clonic gyre th a t spreads over m o st o f th e basin in spring an d su m m er an d alm o st disappears in a u tu m n an d w inter. T he interm ed iate (LIW ) an d deep w aters have a co n stan t tem p eratu re (12.8-13.0 °C). M ixing o f surface a n d deep layers by w ind-driv en tu rb u len ce enriches th e u p p e r layer w ith n u trien ts (N ezlin e t a í 2004), giving th e T y rrh en ian Sea a relatively high co n cen tratio n o f n u trie n ts w ith in the M ed iterranean basin.

M aterial and m eth o d s F rom 1994 to 2008, landing data w ere collected m o n th ly over 3 -5 days o f observation a t th e au c tio n o f P o rto Santo Stefano, one o f th e m o st im p o rta n t fishing h a r­ b o u rs o f the area. T he exploitation o f Parapenaeus longi­ rostris takes place in th e fishing g ro u n d s betw een 200 an d 400 m d epth, w hile catches o f Nephrops norvegicus are o btain ed from a greater d ep th range (200-600 m ) (Sbrana et al. 2003). T he n u m b e r o f traw lers h abitually targeting the tw o species decreased d u rin g th e investigated period: fro m 30 vessels in 1994 to 12 in 2008 (S brana et al. 2006). D ata o n specific co m p o sitio n o f th e lan d in g (total w eight by species o r com m ercial category) a n d fishing effort (n u m b er o f fishing days) w ere collected for each vessel. T he landing rates (landing p er u n it o f effort, LPUE) w ere calculated b y taking in to acco u n t th e fishing day as a u n it o f effort (kg p e r day p er vessel). In ad d itio n , tw o indices o f fishing activity a n d capacity w ere co m ­ puted: (i) the total n u m b e r o f days at sea p erfo rm ed by the fleet p er m o n th , an d (ii) th e m ean engine pow er (kW ) o f the fleet per m o n th . D u rin g th e investigated p erio d (1994-2008), tw o exper­ im ental traw l surveys p er year w ere carried o u t u n d e r the fram ew ork o f th e In tern atio n al b o tto m traw l survey in the M editerranean (M edits) an d th e Italian dem ersal resources p ro g ram (G ru n d ). A ccording to th e sam pling proto cols (see R elini 1998 an d B ertrand et al. 2002), the M edits survey was p erfo rm ed in sp rin g a n d th e G ru n d survey in a u tu m n . T he tw o surveys w ere carried o u t according to a depth-stratified sam pling design w ith ra n ­ dom ly allocated hauls w ith in each stratu m . In ad d itio n , the n u m b er o f hauls in each stra tu m was p ro p o rtio n a l to the surface o f the stra tu m itself. T he h aul p o sitio n o f the M edits traw l survey 2008 is show n in Fig. 1. M ean biom ass (kg-km -2 ) a n d ab u n d an ce (N -km -2 ) indices w ere calculated for b o th species to o b tain tim e series com posed o f tw o observations p er year, for a to tal o f 30 observations. A re c ru itm e n t index (n u m b e r of

Marine Ecology 32 (Suppl. 1) (2011 ) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

T rends in P. congirostrís a n d N. n o rveg icu s

recruits p e r square kilom etre, no. recru its-k m -2 ) was also co m p u ted . Follow ing M o ri et al. (2000) a n d O rsi Relini et al. (1998), specim ens u n d e r th e size o f 20 m m CL (car­ apace length) w ere considered recruits. T he indices of N . norvegicus w ere co m p u ted taking in to acco u n t only th e hauls carried o u t in th e 200-800 m d ep th stratu m . T o investigate th e effect o f hydrological conditions, m ean m o n th ly values o f satellite-derived (1994-2008) sea surface tem p e ra tu re (SST, °C) a n d w in d speed (W , m-s-1 ) w ere gathered fro m th e Physical O ceanography D istrib ­ u ted Active A rchive C entre (PO.DAAC: h ttp ://p o d aac.jpl.nasa.gov/index.htm l). D ata tak en fro m three locations (42°30/ N -1 1 °0 0 ' E; 42°00/ N -1 2 °0 0 / E an d 41°00' N -1 3 °0 0 / E; see Fig. 1) in th e T y rrh en ian Sea were used to co m p u te a m ean m o n th ly value. A w ind-m ixing in d ex was calculated as th e cube o f th e w in d speed according to B artolino et al. (2008). M o n th ly d ata o f the N A O fro m 1994 to 2008 w ere obtain ed fro m th e Pacific Fisheries E n vironm ental L ab o rato ry (PFEL: h ttp ://las. pfeg.noaa.gov/). T he tim e series w ere explored b y m eans o f a u to - an d cross-correlation functions. The au to -c o rre latio n fu n ctio n gives an in d icatio n o f th e a m o u n t o f association betw een variables Yt an d Yt_k, w here th e tim e lag k takes th e val­ ues 1, 2, 3, etc. (Z u u r et al. 2007). T hus it is used to h ighlight th e presence o f cyclic p attern s in tim e series. F o rm u lated differently, th e a u to -co rrelatio n w ith a tim e lag o f k years represents th e overall association betw een values th a t are separated b y k tim e points. T he cross-correlation fu n ctio n show s th e relationship betw een Yt an d Xt_k. T herefore this to o l can be used to explore w h eth er th ere is a (linear) relatio n sh ip betw een tw o variables (Z u u r et al. 2007, 2009). In tim e series anal­ ysis, th e use o f significantly cross-correlated variables sho uld be avoided. The confidence intervals o f th e a u to ­ co rrelatio n w ere o b tain ed fro m ±2/Vn, w here n is the length o f th e tim e series. T o analyse th e lo n g -term changes o f th e variables, cyclical p attern s w ere rem oved fro m th e data o btained by th e seasonal d eco m p o sitio n b y Loess sm o o th in g (Z u u r et al. 2007). T he d ata w ere th e n analysed b y m eans of m u ltiv ariate tim e series analysis techniques: m in /m a x a u to -c o rrela tio n factor analysis (MAFA) a n d dynam ic fac­ to r analysis (DFA) to estim ate c o m m o n trends. These tools w ere used to estim ate c o m m o n u nderlying trends fro m th e m u ltip le tim e series dataset, an d to evaluate the correlations w ith species a b u n d an ce an d enviro n m ental a n d fishery factors. For this p u rp o se, th e tim e series of LPUE an d o f biom ass an d density indices w ere used as response variables a n d th e enviro n m en tal an d fishing effort factors as explanatory variables. All analyses were p erfo rm ed using th e softw are BRODGAR 2.6.6 (h ttp :// w w w .brodgar.com ).

27

T rends in P. congirostris a n d N. n o rveg icu s

MAFA can be described in various ways: a type of principal co m p o n e n t analysis especially for (sh o rt) tim e series; a m e th o d for extracting tren d s fro m m u ltiple tim e series; a m e th o d for estim ating index fun ctio n s from tim e series; a sm o o th in g m eth o d ; or a signal extraction procedure. T he u nderlying idea is th a t a tre n d is associ­ ated w ith high a u to -co rrelatio n a t tim e lag 1. Therefore, the first MAFA axis represents th e tren d , or th e m ain underlying p attern in th e data. T his axis can also be seen as an index fu n ctio n or sm o o th in g curve. C ross-correla­ tions (canonical correlations) betw een th e variables (b o th response and ex planatory variables) an d th e tren d s were co m p u ted to evaluate th e significance o f th e relationship betw een th e variables a n d th e tren d s (Erzini et a í 2005; Z u u r et al. 2007). The m ath em atics b eh in d MAFA are described in Solow (1994). T he u n derlying fo rm u la is sim ilar to principal co m p o n e n t analysis. T he MAFA cal­ culations involve a p rincipal co m p o n e n t analysis o n cen­ tred data, follow ed b y a first-differencing o n th e principal com ponents, a n d a second p rin cip al co m p o n e n t analysis o n these differenced com ponents. As a result, th e MAFA axes are m u tually u n co rrelated w ith u n it variance, an d the MAFA axes have decreasing a u to -co rrelatio n w ith tim e lag 1 (Z u u r et al. 2007). T he DFA is a m eth o d to estim ate co m m o n trends, effects o f explanatory variables an d in teractio n s betw een the response variables in a m ultivariate tim e series d ata­ set. Statistical details a n d applications o f DFA are given in Z u u r et al. (2003a,b) an d Z u u r & Pierce (2004). DFA applies a d im en sio n re d u c tio n to th e N tim e series. The dynam ic factor m odel, in w ords, is given b y N Tim e series = linear co m b in atio n o f M c o m m o n tren d s + explanatory variables + noise. DFA m odels w ith one co m m o n tre n d an d a sym m etric, n o n -diagonal covariance m atrix w ere used to analyse th e datasets. A series o f m odels w ere fitted, ranging fro m th e sim plest, w ith only one explanatory variable, to th e m ost com plex, w ith all th e explanatory variables. A kaike’s in fo rm atio n criterio n (AIC) was used as a m easure of goodness-of-fit a n d to com pare m odels (Z u u r et al. 2003b), w ith th e b est m o d el having th e sm allest AIC. Fac­ to r loadings w ere used to m ake inferences regarding the im p o rtan ce o f p articu lar trends, represen tin g underlying c o m m o n p attern s over tim e, b o th to specific response variables and to different g roups o f response variables (Erzini 2005; Erzini e t a í 2005; Z u u r et al. 2007).

Ligas, S a rto r & C o llo ca

w ere significantly correlated. In th e case o f Parapenaeus longirostris, LPUE tim e series w ere positively correlated to experim ental traw l survey tim e series (biom ass and d en ­ sity indices) (Table la ), suggesting a good m atch betw een fishery-dependent a n d fish ery -in d ep en d en t data. The re c ru itm e n t index was significantly correlated to the biom ass a n d density indices, a n d th e m ax im u m cross­ correlations w ere at tim e lags 0 a n d 2, respectively (Table lb ). This m eans th a t a peak o f re c ru itm en t was directly reflected in a peak o f density, w hile th e peak o f biom ass follow ed w ith a tim e lag 2, w hich corresponds to 1 year. T he correlations betw een th e lan d in g a n d survey tim e series o f Nephrops norvegicus w ere significant, b u t negative, suggesting an inverse relationship betw een the tw o variables. H ow ever, th e re cru itm en t index was po si­ tively correlated to th e LPUE, w ith th e m ax im u m correla­ tio n corresp o n d in g to a tim e lag 3. This suggests th a t a peak in re c ru itm e n t was follow ed b y a peak in LPUE after a tim e lag o f m o re th a n 1 year. T he analysis o f cross-correlations am o n g th e explana­ to ry variables also pro v ided significant results (Table 2).

Table 1. Response variables, (a) Cross-correlations. L = landing per unit of effort (kg per day per vessel): B = biomass Index (kg-km-2); D = density Index (n-krrT2); R = recruitment Index (no. recruits-kirT2). (b) Maximum cross-correlations: the time lags corresponding to the maxi­ mum cross-correlations are shown In the grey part of the table.

Parapenaeus longirostris B

L

D

Nephrops norvegicus R

B

L

D

R

(a)

P. longirostris L

1.00

B D

0.54

1.00

0.49

0.95

1.00

R

0.12

0.46

0.69

1.00

N. norvegicus L

1.00

B D

-0 .5 5

1.00

-0 .5 4

0.94

1.00

R

0.42

0.38

0.52

0.66

0.66

0.54

0.94

-0 .4 7

1.00

(b)

P. longirostris L B

0.79

D R

0 2

1

0.82

0.54

0.95

0.53 0.69

0

N. norvegicus

R esults The analysis o f th e tim e series dataset b y m eans of cross-correlation fu n ctio n s allows us to identify significant relationships betw een th e response variables. For b o th species, tim e series o f landings a n d traw l surveys data

28

L B D R

3

0 1

-0 .5 5

-1

Significance level for correlations: ± 0.37: significant correlations are highlighted In bold.

Marine Ecology 32 (Suppl. 1) (2011) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

T rends in P. congirostris an d N. n o rv eg icu s

Ligas, Sartor & Colloca

T a b le 2. Explanatory variables: cross-correlations. 0 .8 -

SST SST

W3

NAO

Days

kW

1.00

W3 NAO Days kW

0.19 0.30

1.00 -0 .1 2 -0 .0 2

1.00 -0 .0 2

1.00

0.18

0.14

0.00

0.41

-0 .4 5

c o « 0

0.4-

o

0 .2

-

0 .2

-

O -

-0 .4

1.00

0

2

4

6

8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 T i m e l ag

SST = Sea Surface Tem perature (°C); W3 = wind-mixing index (m3-s~3); NAO = North Atlantic Oscillation index; Days = days a t sea per month; kW = m ean engine pow er (kW). Significance level for correlations: ± 0.37. Significant correlations are highlighted in bold.

Sea surface tem p e ra tu re (SST) an d w in d -m ix in g index (W 3) w ere negatively correlated. SST show ed an increas­ ing tren d , w hereas th e W 3 series follow ed a decreasing p attern . For the fishing efforts p aram eters, a positive co r­ relation was fo u n d betw een days at sea an d m ean engine pow er. A ccording to the results o b tain ed b y m eans o f cross­ correlations, it was decided to use th e LPUE o f P. longi­ rostris an d N . norvegicus only as response variables for the analyses o f tim e series. A m ong th e explanatory variables, the w ind-m ixing index, th e N A O in d ex an d th e days at sea per m o n th w ere used. The LPUE tim e series o f P. longirostris an d N . norvegi­ cus w ere characterized b y w ide fluctuations, m aking it im possible to identify an y clear tre n d (Fig. 2). B oth tim e series show ed peaks in late sp rin g (A p ril-Ju n e), w hen it is know n th a t the catch o f th e tw o species is higher. The presence o f a seasonal p a tte rn was confirm ed b y th e a u to ­ correlation function: significant correlations w ere id e n ti­ fied a t tim e lags o f 12 a n d 24 m o n th s (Fig. 3). Som e exam ples o f the tim e series o f th e explanatory variables are show n in Fig. 4. T he tim e series o f days at sea per m o n th was characterised b y a clear decreasing tre n d (Fig. 4A). Figure 4B a n d C show flu ctu ation s over tim e of sea surface tem p era tu re a n d w in d speed. Sea surface te m ­ p eratu re peaked in su m m er, w hen th e w in d speed was

Fig. 3. Auto-correlation plot of the landing per unit of effort (LPUE)

time series of Parapenaeus longirostris and Nephrops norvegicus (thick line). Dotted lines: confidence Interval limits (± 0.15).

600-, £

500-

! 400o 300 «

nj

200-

Q 100-

30-,

B

2622-

?

14-

12

C

10 8

0 6 £

4 2 0 -I---------------1----------- 1------------- 1------------- 1------------- 1------------- 1------------- 1-----

Jan-94

Jan-96 Jan-98

Jan-00 Jan-02 M onths

Jan-04

Jan-06

Jan-08

Fig. 4. Time series plot of monthly data of explanatory variables from January 1994 to December 2008. (A) Number of days a t sea per m onth (com puted from the Porto Santo Stefano trawl fleet). (B) Sea

surface tem perature (SST, °C). (C) Wind speed (m-s~1).

7°-i ® 600

0O 50_Ä o 40-

■g 2°ioJan-94

Jan-96

Jan-98

Jan-00 Jan-02 M onths

Jan-04

Jan-06

Fig. 2. Landing per unit of effort (LPUE) time series of

Jan-08

Parapenaeus

longirostris and Nephrops norvegicus (thick line) from th e Porto Santo Stefano trawl fleet.

Marine Ecology 32 (Suppl. 1) (2011 ) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

lower. These tren d s explain th e significant, b u t negative, cross-correlation betw een th e tw o variables. To rem ove th e seasonal p attern s, th e ex planatory variables w ere also sm o o th ed b y m eans o f th e seasonal d eco m p o sitio n by Loess sm o o th in g (see Fig. 5). T he results obtain ed b y m eans o f MAFA described a clear scenario in th e case o f P. longirostris. T he estim ated tre n d show ed an increasing p atte rn , alth o u g h ch aracter­ ized b y flu ctu atio n s (Fig. 6). H igh a n d positive correla­ tio n s betw een th e tren d a n d th e LPUE tim e series o f the tw o species w ere identified (Table 3). W hile for P. longi­ rostris all th e response variables considered (LPUE,

29

T rends in P. congirostris a n d N. n o rv eg icu s

Ligas, Sartor & Coi loca

A ccording to th e factor loadings, only P. longirostris

0.3

was correlated to th e tren d c o m p u ted b y m eans o f DFA (0.223 for P. longirostris, a n d 0.006 for N . norvegicus). T he estim ated tre n d (Fig. 7) was sim ilar to th a t obtained using MAFA, w ith a general increasing p a tte rn an d tw o m ain peaks in 2001 a n d 2006. Flowever, this m odel, w hich was characterized b y th e low est AIC value (Table 4), suggested n o significant relationship w ith fish­ ing effort, as it was correlated only to th e m o n th ly tim e series o f w in d -m ix in g in d ex (W 3) a n d th e N A O index. In fact, th e estim ated t-values for th e regressions for individual species w ith W 3 a n d N A O w ere relatively large

o.o cn -0 .1

-

0.2 1.0

X

d) 7? ■d Q)

0.5

.E w

CD CO

- 1.0

Jan-94

,---------------- ,---------------- ,----------------- ,-,

Jan-96

Jan-98

Jan-00

Jan-02 M onths

,

—

,------------------------

Jan-04 Jan-06

Jan-08

10-

Fig. 5. Sea surface tem perature (SST) and win d-m ixin g index time series obtained by m eans of seasonal decom position by Loess sm ooth­ ing.

o0.3-, 0 .2 -

Û) o o


50 -

100 Time

150

0.1

—0.2 -I--------------- 1----------- .------------- 1--------------.------------- 1------------- .------------- 1-----

Jan-94

Jan-96 Jan-98

Jan-00 Jan-02 M onths

Jan-04

Jan-06

Jan-08

Fig. 6. Common trend com puted by m eans of MAFA from the LPUE time series of Parapenaeus longirostris and Nephrops norvegicus.

T able 3. Canonical correlations betw een the com m on trend obtained through MAFA and, respectively, the response variables (landing per unit of effort time series of Parapenaeus longirostris and Nephrops

Fig. 7. Common trend com puted by m eans of DFA from the LPUE time series of Parapenaeus longirostris and Nephrops norvegicus.

T able 4. Values of Akalke's Information criterion (AIC) for DFA m od­ els with one com mon trend and different sets of explanatory variables (W3 = wind-mixing Index; NAO = North Atlantic Oscillation Index; Days = num ber of days at sea per month), based on diagonal and symmetric matrices. Model

Matrix

Explanatory variables

AIC

norvegicus), and the explanatory variables (W3 = wind-mixing Index; NAO = North Atlantic Oscillation index; Days = num ber of days at sea per m onth, days).

1 2

Diagonal Diagonal

W 3, NAO, Days W 3, NAO

319.7 298.4

Response variables

Explanatory variables

3 4

Diagonal Diagonal

W 3, Days NAO, Days

307.5 178.2

0.97

W3

-0 .4 5

0.35

NAO

-0 .0 9

5 6

Diagonal Diagonal

W3 NAO

291.5 388.3

Days

-0 .3 1

7 8 9

Diagonal Diagonal Symmetric

Days W 3, NAO, Days

248.5 258.0 296.3

10 11 12 13

Symmetric Symmetric Symmetric Symmetric

W 3, NAO W 3, Days NAO, Days W3

159.0 348.5 279.8 379.9

14

Symmetric

NAO

406.9

15 16

Symmetric Symmetric

Days

369.7 372.1

P. longirostris N. norvegicus

Significance level for correlations: ± 0.1 S. Significant values are high­ lighted in bold.

biom ass, density an d re c ru itm e n t indices) w ere correlated w ith the estim ated tren d , in th e case o f N . norvegicus, tw o contrasting scenarios em erged fro m th e results: an increase in term s o f LPUE an d rec ru itm e n t indices, a n d a decrease in term s o f density an d biom ass indices.

30

-

The lowest AIC value Is highlighted In bold.

Marine Ecology 32 (Suppl. 1) (2011) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

T rends in P. congirostrís a n d N. n o rveg icu s

Ligas, S a rto r & C o llo ca

for N. norvegicus, indicating stro n g relationships (Table 5). H ow ever, a large diagonal elem ent o f th e erro r covariance m atrix (R > 0.74) was o b tain ed for N . norvegi­ cus, confirm ing th a t these variables did n o t fit well to the m odel.

D iscussion T he present study aim ed to u n d e rstan d th e change over tim e o f tw o dem ersal stocks in relatio n to en v ironm ental an d anthropogenic factors, using analysis o f a relatively long an d com plete tim e series o f stock ab u n d an ce data. In the A tlantic O cean a n d N o rth Sea, d ata have been col­ lected since at least th e 1950s (e.g. for m an y fish stocks in the N o rth A tlantic; R ijnsdorp et a í 2006). In contrast, in the M editerranean Sea, tim e series o f fisheries data usually only cover th e last few decades. Therefore, th e availability o f 15 years o f fisheries d ata fro m tw o o f th e m o st a b u n ­ d a n t decapods o f th e dem ersal co m m u n ities o f M ed iterra­ nean w aters, b o th im p o rta n t targ et species (Aguzzi et a í 2004; Sobrino et al. 2005; G uijarro et al. 2009; M orello et al. 2009), should be regarded as an u n iq u e o p p o rtu ­ nity. The results clearly show ed a n increasing tre n d in the abun d an ce o f the stock o f P. longirostris a n d a m o re h e t­ erogeneous scenario for N . norvegicus in th e T y rrh en ian Sea d u rin g the investigated period. In ad d itio n , o u r results strongly suggest th a t tem p o ral variations in the abun d an ce o f th e tw o species w ere correlated w ith b o th environm ental and fishing activity variables.

Environm ental effects A tm ospheric an d surface w ater en v iro n m en tal variables w ere investigated in this study. A lthough these variables have been used in several studies w hich highlighted signi­ ficant correlations w ith dem ersal a n d deep-sea co m m u n i­ ties (Lloret et al. 2001; F ariña & G onzález H erraiz 2003; Z u u r et al. 2003a,b; Z u u r & Pierce 2004; Erzini 2005; M ay nou 2008; C artes et al. 2009; G onzález H erraiz et al. 2009), very few attem p ts to explain th e m echanism s

T able 5. Estimated t-values for regressions betw een the response variables (LPUE time series of Parapenaeus longirostris and Nephrops

norvegicus) and the explanatory variables (W3 = wind-mixing Index; NAO = North Atlantic Oscillation index). t-value

P. longirostris N. norvegicus

W3

NAO

1.26 -4 .8 2

1.23 -3 .1 1

Significant values are highlighted in bold.

Marine Ecology 32 (Suppl. 1) (2011 ) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

involved in linking u p p e r layers an d b en th ic h abitats have been m ad e (C o m p an y et al. 2008; C artes et al. 2009). M an y o th er en v iro n m en tal an d oceanographic variables, such as p rim ary p ro d u c tio n , chlorophyll a n d n u trie n t concentrations, salinity, upw elling, currents, a n d river dis­ charge, have been show n to b e influential in th e life cycles a n d dynam ics o f m arin e ecosystem s (B aham ón & C ru ­ zado 2003; Erzini 2005; Erzini et al. 2005; R othschild et al. 2005; C o m p an y et al. 2008; C ury et al. 2008; C artes et al. 2009; Sardà et al. 2009). In th e T y rrh en ian Sea, oceanographic param eters are p o o rly an d irregularly con­ sidered. T he value o f using SST, w in d circulation a n d the N A O index was th e availability o f an extensive a n d com ­ plete dataset covering th e tim e sp an o f th e available fish­ eries data. This enabled a th o ro u g h investigation to be m ad e in to th eir influence over th e course o f 15 years. A m ong th e enviro n m en tal variables used, only SST an d th e w in d -m ix in g index (W 3) w ere clearly related to the tre n d show ed b y P. longirostris an d N . norvegicus, w hereas th e N A O index was n o t significantly associated w ith either. Parapenaeus longirostris is considered to be a spe­ cies w ith a preference for w arm w aters, b eing m o re a b u n ­ d a n t in th e S outheastern M ed iterran ean th a n in the N o rth w estern basin (Abellô et al. 2002). T he cu rren t w arm in g o f th e u p p er a n d in term ed iate w ater layers of th e W estern M ed iterran ean (Vargas-Yánez et al. 2009), reflected in th e observed increase in SST an d decrease in w in d circulation (W 3), could have h ad a positive effect o n th e life cycle an d ab u n d an ce o f this species in th e T yr­ rh en ia n Sea. A possible explanation for this p h e n o m e n o n is provided b y C artes et al. (2009). T hey hypothesised an association betw een high tem p eratu res, low rainfall regim es an d river discharges a n d a red u c tio n in th e flux o f organic m a tte r th a t m a in ta in deep-w ater benthic com ­ m u n ities off th e C atalonian coasts. These enviro n m ental co nd ition s resulted in a h igher ab u n d an ce o f Z ooplankton a n d increased p ro d u c tio n o f su p rab en th o s (C artes et a í 2009). A lthough P. longirostris displays a w ide range of prey item s, its d iet is m ain ly based o n su p rab en th ic crus­ taceans, such as m ysids (especially Lophogaster typicus) (S obrino et al. 2005). Therefore, th e w arm in g phase observed in recent years could have favoured th e P. longi­ rostris p o p u latio n in th e T y rrh en ian Sea. In a d d itio n to this, B artolino et al. (2008) fo u n d a positive correlation betw een th e re c ru itm e n t o f th e E u ro p ean hake, Merluccius merluccius, a n d w ind circulation in th e T y rrh en ian Sea: high re cru itm en t rates w ere associated w ith stro n g w ater a n d w ind circulation. T he re c ru itm e n t o f th e tw o species, M . merluccius an d P. longirostris, takes place in th e sam e area, at a b o tto m d ep th o f 100-150 m (C olloca et a í 2004). E u ro p ean hake juveniles are k n o w n to p rey on crustaceans, such as th e juveniles o f P. longirostris (C arpentieri et al. 2005b). T he enviro n m en tal con d itio n s w hich

31

T rends in P. congirostris a n d N. n o rveg icu s

positively affect P. longirostris, such as high tem p eratu res and low w ind circulation, are th e sam e as those th a t neg­ atively affect th e re cru itm en t o f M . merluccius (B artolino et a í 2008). The resulting low er p re d a tio n pressure could have fu rth er enhanced th e recru itm en t success o f th e deep-w ater rose shrim p. In contrast, N . norvegicus, w hich show ed a negative tren d in term s o f density an d biom ass indices, was nega­ tively correlated w ith th e N A O an d th e w in d -m ix in g index. A gain this m ay be related to m echanism s linking the p ro d u ctiv ity in th e u p p e r layers w ith th e stru c tu re of dem ersal com m unities, as p ro p o sed b y C artes et al. (2009). W hile phases o f w arm er an d dryer atm ospheric conditions favour p la n k to n ic /su p rab e n th ic feeders, b e n ­ thic feeders an d p red ato rs such as N . norvegicus (Aguzzi et a í 2009) are disadvantaged b y th e re d u ctio n o f th e organic m atter flux resulting fro m th e decreased rainfall and river discharge. Sim ilar responses to atm ospheric w arm ing processes b y N . norvegicus have been observed in o th er areas. In th e context o f only m in o r changes in fishing pressure, F ariña & G onzález H erraiz (2003) an d G onzález H erraiz et al. (2009) show ed a decline in the p o p u latio n abu n d an ce o f N . norvegicus in th e A tlantic. This decline was associated w ith th e positive phase o f th e NAO index, w hich determ ines w arm er tem p eratu res in N o rth e rn E urop e (H alliday & P in h o rn 2009).

Fishing activity effects The fishing effort is a com plex variable th a t is difficult to quantify because it is influenced b y m an y different fac­ tors, such as increasing catch efficiency an d changes in fleet characteristics. Increasing catch efficiency o f th e fleet (also k now n as ‘technological creep’) is usually related positively to a n increase in skipper skills, investm ents in auxiliary equip m en t, m o re efficient gear an d m aterials, replacem ent o f old vessels w ith new ones and, to a lesser extent, u pgraded engines (R ijnsdorp et a í 2006). D u rin g the investigated perio d , a decrease in th e n u m b e r o f ves­ sels occurred: th e fleets o f P o rto Santo Stefano a n d ad ja­ cent p o rts decreased b y a b o u t 50%, p ro d u c in g a n alm ost p ro p o rtio n al decrease in fishing effort. In the case o f N . norvegicus th e d ata show ed tw o co n ­ trasting trends: an increase o f landings p er u n it o f effort and recru itm en t index, an d a decrease o f relative p o p u la ­ tio n abundance. T he daily activity o f N . norvegicus could help explain these divergent trends. Light in ten sity in flu ­ ences how organism s perceive th eir en v iro n m en t, m o d u ­ lating th eir in ter- a n d intra-specific interactions. D em ersal com m unities exposed to light in ten sity v ariations are expected to react to th em , p ro d u cin g changes in species com p o sitio n an d density. T herefore, th e d iu rn al activity cycles o f dem ersal species m ay consistently bias d e m o ­

32

Ligas, S a rto r & C o llo ca

graphic evaluation b y b o tto m traw l sam pling. C o m m er­ cial fishing often operates o n a 24-h basis, w hereas experim ental traw l surveys are usually carried o u t in the daytim e. Traw l fleets exploiting th e T yrrh en ian Sea often p erfo rm 2 -3 days o f fishing op eratio n s, carrying o u t hauls d u rin g b o th th e day a n d n ig h t (S brana et a í 2003). A lthough d iu rn al versus n o ctu rn al bias in sam pling has been fo u n d to be m o d erate w hen traw l catches are p e r­ fo rm ed o n fishing g ro u n d s o n th e contin en tal slope (A gu­ zzi & B ah am ó n 2009; B aham ón et al. 2009), th e fact th a t N. norvegicus is a p red o m in a n tly n o c tu rn a l species (A gu­ zzi & Sardá 2008) m ay help explain th e differences observed betw een com m ercial a n d experim ental survey data. Nephrops norvegicus spend m o st o f th e tim e w ith in or a t th e en trance o f th eir b u rro w s a n d are caught by traw ling only w hen they emerge. E m ergence varies w ith tim e o f day, season, anim al size, fo o d presence, h u n g er state, sex an d rep ro d u ctiv e status. T hus th e fisheries exploit th e p o p u latio n selectively an d in a different m a n ­ n er w ith respect to males an d fem ales (Aguzzi et a í 2003; Aguzzi & Sardá 2008; Aguzzi & B aham ón 2009). In p a r­ ticular, egg-bearing females sp en d m o st o f th e ir tim e in th eir b u rro w s d u rin g th e entire eg g-incubation period, w hich lasts for 4 -6 m o n th s in th e M ed iterran ean Sea (Ag­ uzzi e t a í 2003). F u rth erm o re, juveniles rarely leave th eir burrow s. These factors, related to th e biology o f the spe­ cies, therefore, strongly c o n trib u te to p ro te ctio n o f the N. norvegicus life-stages th a t are perceived as sensitive to traw ling exploitation. Parapenaeus longirostris also show s v ariations in density a n d d ep th d istrib u tio n according to daytim e rh y th m s and p h o to p e rio d length. C arp en tieri et a í (2005a) observed higher catch rates o f P. longirostris at n ig h t in th e shelfb reak in th e T y rrh enian Sea. In ad d itio n , th ey fo u n d the highest density index d u rin g late w in te r-sp rin g , w hich corresponds to th e spaw ning peak (A rdizzone et a í 1990). As m o st larvae occur a ro u n d th e 100-m isobath, adults could displace d u rin g th e spaw ning p erio d to shal­ low er depths (S obrino et al. 2005). It is w o rth highlighting th a t th e tre n d o f P. longirostris was characterized b y huge in teran n u al fluctuations. A part fro m enviro n m en tal co n d itio n s an d fishing activity, this in teran n u al variability was pro b ab ly related to the sh o rt life-span a n d fast grow th rates o f this species (Abellô et al. 2002). A sim ilar p atte rn , characterized b y a biom ass p eak in 2001, was observed in o th er areas o f th e W estern M editerranean, such as in th e Balearic su b -b asin (G uijar­ ro et al. 2009).

C onclu sions L o ng-term changes in th e ab un dan ce o f tw o im p o rta n t dem ersal species in th e T y rrh en ian Sea, th e deep-w ater

Marine Ecology 32 (Suppl. 1) (2011) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

T rends in P. congirostrís a n d N. n o rveg icu s

Ligas, S a rto r & C o llo ca

rose shrim p (Parapenaeus longirostris) an d th e N orw ay lobster (Nephrops norvegicus), w ere fo u n d to correlate sig­ nificantly w ith identified enviro n m en tal a n d a n th ro p o ­ genic factors. W hile th e increasing a b u n d an ce of P. longirostris was correlated to a rise o f sea surface te m ­ p eratu re, a corresp o n d in g decrease o f w in d circulation an d to the red u ctio n o f fishing effort, a co rresponding tre n d for N . norvegicus was n o t evident. O n one hand, the p o p u latio n abu n d an ce o f N . norvegicus was negatively correlated w ith en v iro n m en tal v ariations, w hile o n the o th er h and, it did n o t show any association w ith th e gen­ eral decrease o f fishing effort in th e area. H ow ever, the recru itm en t index, as calculated in th e study, could be used as a proxy for change in stock abundance. Som e m echanism s have been p ro p o sed to lin k a tm o ­ spheric co nditions (sea surface tem p eratu re, w ind circula­ tio n and th e N AO ) to th e tro p h ic webs an d c o m m u n ity stru ctu re in the deep-w ater b en th ic habitats. H ow ever, these m odels need to be im p ro v ed to achieve a deeper an d m o re accurate u n d e rsta n d in g o f th e m echanism s linking these ecosystems. F u rth er analyses are req u ired to b etter u n d erstan d th e relationships betw een v ariations in the abun d an ce o f dem ersal species an d en v ironm ental an d anthro p o g en ic factors. T he availability o f suitable in fo rm atio n o n enviro n m en tal characteristics, such as ap p ro p riate sea-floor top o g rap h y , sed im en t com position, hydrographical characteristics, an d tro p h ic webs (prey availability, presence a n d ab u n d an ce o f p re d a to r species) is necessary to b ette r u n d e rstan d th e tem p o ral change in species abundance, d istrib u tio n an d biology.

cean Nephrops norvegicus o n the activity rhythm s o f con tin en ­ tal m argin prey decapods. Marine Ecology, 30, 366-375. Aguzzi J., Sarda F. (2008) A history o f recent advancem ents on

Nephrops norvegicus behavioral and physiological rhythm s. Reviews in Fish Biology and Fisheries, 18, 235-248. Aguzzi J., Sarda F., Abello P., C om pany J.B., R otlant G. (2003) Diel a n d seasonal patterns o f Nephrops norvegicus (D eca­ poda: N ephropidae) catchability in the w estern M editerra­ nean. Marine Ecology Progress Series, 258, 201-211. Aguzzi J., Sarda F., Allué R. (2004) Seasonal dynam ics in

Nephrops norvegicus (Decapoda: N ephropidae) catches off the Catalan coast (W estern M editerranean). Fisheries Research, 69, 293-300. Ardizzone G.D., G ravina M.F., Belluscio A., Schintu P. ( 1990) D epth-size d istribution p attern o f Parapenaeus longirostris (Lucas, 1846) (D ecapoda) in the central M editerranean Sea.

Journal o f Crustacean Biology, 10, 139-147. Artale V., Astraldi M ., Buffoni C., G asparini G.P. (1994) Sea­ sonal variability o f gyre-scale circulation in the n o rth ern T yrrhenian Sea. Journal of Geophysical Research C, 99, 14127-14137. B aham ón N., C ruzado A. (2003) M odelling nitrogen fluxes in oligotrophic environm ents: N W M editerranean and NE Atlantic. Ecological Modelling, 163, 223-244. B aham ón N., Sarda F., Aguzzi J. (2009) Fuzzy diel patterns in catchability o f deep-w ater species o n the continental m argin.

ICES Journal o f Marine Science, 66, 2211-2218. B artolino V., Colloca F., Sartor P., Ardizzone G.D. (2008) M odelling recruitm ent dynam ics o f hake Merluccius merluc­

cius, in the central M editerranean in relation to key environ­ m ental variables. Fisheries Research, 93, 277-288. B aum J.K., Myers R.A., Kehler D.G., W orm B., H arley S.J., D oherty P.A. (2003) Collapse and conservation o f shark

A c k n o w le d g e m e n ts T he au th o rs w ould like to th a n k th e E d ito r an d th e Ref­ erees for useful com m en ts an d revisions th a t significantly im proved the stru ctu re a n d th e q uality o f this paper. W e acknow ledge also D r Jessica Craig, U niversity o f A ber­ deen, A nna D avies, A ndrew Silva a n d Letizia Sim eni for p ro of-reading and English revision.

populations in the N orthw est A tlantic. Science, 299, 389392. B ertrand J.A., Gil de Sola L., P apaconstantinou C., Relini G., Souplet A. (2002) The general specifications o f the MEDITS survey. Scientia Marina, 66, 9-17. C arpentieri P., Colloca F., Ardizzone G.D. (2005a) D ay -n ig h t variations in the dem ersal nekton assemblage o n the M edi­ terranean shelf-break. Estuariae and Coastal Shelf Science,

63, 577-588.

R eferen ces Abello P., Abella A., A dam idou A., Jukic-Peladic S., M aiorano P., Spedicato M .T. (2002) Geographical patterns in abundance and p opulation structure o f Nephrops norvegicus and Parape­

naeus longirostris (Crustacea: D ecapoda) along the E uropean M editerranean coasts. Scientia Marina, 66, 125-141. Aguzzi J., B aham ón N. (2009) M odeled d a y -n ig h t biases in decapod assessm ent by b o tto m traw ling survey. Fisheries

Research, 100, 274-280.

C arpentieri P., Colloca F., Cardinale M., Belluscio A., Ardizz­ one G.D. (2005b) Feeding habits o f E uropean hake (Merluc­

cius merluccius) in the central M editerranean Sea. Fishery Bulletin, 103, 411-416. Cartes J.E., Elizalde M ., Sorbe J.C. (2001) C ontrasting life his­ tories, secondary p roduction, and trophic structure o f Peracarid assemblages o f the bathyal suprabenthos from the Bay o f Biscay (NE Atlantic) and the Catalan Sea (N W M editer­ ranean). Deep-Sea Research I, 48, 2209-2232. Cartes J.E., M aynou F., Fanelli E., Papiol V., Lloris D. (2009)

Aguzzi J., B aham ón N., M arotta L. (2009) The influence o f light

Long-term changes in the com position a n d diversity o f

availability and predatory behaviour o f the decapod crusta­

deep-slope m egabenthos and trophic webs off C atalonia

Marine Ecology 32 (Suppl. 1) (2011 ) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

33

T rends in P. congirostris a n d N. n o rveg icu s

(w estern M editerranean): are trends related to clim atic oscil­

groundfish populations in the early 1990s. Fisheries Research,

lations? Progress in Oceanography, 82, 32-46.

97, 163-182.

Ciannelli L., Fauchald P., C han K.S., Agostini V.N., D ingsor G.E. (2008) Spatial fisheries ecology: recent progress and future prospects. Journal o f M arine Systems, 71, 223-236. CIESM (2008) Clim ate w arm ing a n d related changes in M edi­ terranean m arine biota. CIESM Workshop Monographs, 35, 152. Colloca F., C arpentieri P., Balestri E., Ardizzone G.D. (2004) A

Jennings S., D im ore T.A., D uplisea D.D., W arr K.J., Lancas­ ter J.E. (2001) Trawling disturbance can m odify benthic pro d u ctio n processes. Journal o f A nim al Ecology, 70, 4 59475. Kaiser M.J., De G root S.J. (2000) Effects o f Fishing on NonTarget Species and Habitats: Biological, Conservation, SocioEconomic Issues. Blackwell Science, Oxford: 399 pp.

critical habitat for M editerranean fish resources: shelf-break

Kaiser M.J., Ramsay K., R ichardson C.A., Spence F.E., Brand

areas w ith Leptometra phalangium (Echinoderm ata: C rinoi­

A.R. (2000) C hronic fishing disturbance has changed shelf

dea). M arine Biology, 145, 1129-1142. C om pany J.B., Puig P., Sarda F., Palanques A., Latasa M., Scharek R. (2008) Clim ate influence o n deep sea pop u la­

sea benthic c om m unity structure. Journal o f A nim al Ecolology, 69, 494-503. Lloret J., Lleonart J., Sole I., F rom entin J.M. (2001) Fluctua­

tions. PLoS ONE, 3, el431. doi:10.1371/journal.pone.

tions o f landings a n d environm ental conditions in the

0001431

north-w estern M editerranean Sea. Fisheries Oceanography,

C ury P.M ., Shin Y.J., Planque B., D u ra n t J.M., From entin J.M., K ram er-Schadt S., Stenseth N.C., Travers M., G rim m V. (2008) Ecosystem oceanography for global change in fish­ eries. Trends in Ecology and Evolution, 23, 338-346. Erzini K. (2005) T rends in NE Atlantic landings (southern

10, 33-50. M aynou F. (2008) E nvironm ental causes o f the fluctuations o f red shrim p (Aristeus antennatus) landings in the Catalan Sea. Journal o f M arine Systems, 71, 294-302. M olinero J.C., Casini M ., Buecher E. (2008) The influence o f

Portugal): identifying the relative im portance o f fisheries

the Atlantic and regional clim ate variability o n the long­

and environm ental variables. Fisheries Oceanography, 14,

term changes in gelatinous carnivore populations in the

195-209.

northw estern M editerranean. Limnology and Oceanography,

Erzini K., Inejih C.A.O., Stobberup K.A. (2005) A n application o f two techniques for the analysis o f short, m ultivariate non-stationary tim e-series o f M auritanian traw l survey data. ICES Journal o f M arine Science, 62, 353-359. Fariña A.C., González H erraiz I. (2003) T rends in catch-per-

53, 1456-1467. M orato T., W atson R., Pitcher T.J., Pauly D. (2006) Fishing dow n the deep. Fish and Fisheries, 7, 24-34. M orello E.B., A ntolini B., G ram itto M.E., A tkinson R.J.A., Froglia C. (2009) The fishery for Nephrops norvegicus

unit-effort, stock biom ass a n d recruitm ent in the N o rth and

(Linnaeus, 1758) in the central A driatic Sea (Italy): preli­

N orthw est Iberian A tlantic Nephrops stocks. Fisheries Research, 65, 351-360.

m inary observations com paring b o tto m traw l and baited creels. Fisheries Research, 95, 325-331.

F rom entin J.M., Fonteneau A. (2001) Fishing effects and life

M ori M., Sbrana M., De Ranieri S. (2000) Reproductive biol­

history traits: a case study com paring tropical versus tem ­

ogy o f female Parapenaeus longirostris (Crustacea, Decapoda,

perate tunas. Fisheries Research, 53, 133-150.

Penaeidae) o f the n o rth T yrrhenian Sea (western M editerra­

G asparini G.P., O rto n a A., B udillon G., Astraldi M., Sansone E. (2005) The effect o f the Eastern M editerranean T ransient o n the hydrographic characteristics in the Strait o f Sicily

nean). A tti della Societä Toscana di Scienze. N aturali M em o­ rie Serie B, 107, 1-6. Nezlin N.P., Lacroix G., K ostianoy A.G., D jenidi S. (2004)

and in the T yrrhenian Sea. Deep-Sea Research Part I, 52,

Rem otely sensed seasonal dynam ic o f phytoplankton in the

915-935.

Ligurian Sea in 1997-1999. Journal o f Geophysical Research,

Gislason H., Sinclair M., Sainsbury K., O ’Boyle R. (2000) Sym­ posium overview: in corporating ecosystem objectives w ithin

109, C07013, doi:10.1029/2000JC000628. Orsi Relini L., Z am boni A., Fiorentino F., M assi D.

fisheries m anagem ent. ICES Journal o f M arine Science, 57,

(1998) Reproductive patterns in N orw ay lobster Nephrops

468-475.

norvegicus (L.) (C rustacea D ecapoda N ephropidae) o f

Gonzalez H erraiz I., Torres M.A., Fariña A.C., Freire J., C ance­ lo J.R. (2009) The NAO index a n d the long-term variability o f Nephrops norvegicus p opulation and fishery off W est o f Ireland. Fisheries Research, 98, 1-7. G uijarro B., M assuti E., M o ran ta J., Cartes J.E. (2009) Short spatio-tem poral variations in the p opulation dynam ics and biology o f the deep-w ater rose shrim p Parapenaeus longiros­ tris (Decapoda: Crustacea) in the w estern M editerranean. Scientia M arina, 73, 183-197. H alliday R.G., P in h o rn A.T. (2009) The roles o f fishing and environm ental change in the decline o f N orthw est Atlantic

34

Ligas, S a rto r & C o llo ca

different M editerranean areas. Scientia M arina, 62, 25-41. Pauly D. (2009) Beyond duplicity and ignorance in global fisheries. Scientia M arina, 73, 215-224. Reid P.C., Borges M., Svendsen E. (2001) A regim e shift in the N o rth Sea circa 1988 linked to changes in the N o rth Sea horse m ackerel fishery. Fisheries Research, 50, 163-171. Relini G. ( 1998) D em ersal traw l surveys in Italian seas: a short review. IFREMER, Actes de Colloques, 26, 46-75. R ijnsdorp A.D., D aan N., Dekker W . (2006) Partial fishing m ortality per fishing trip: a useful indicator o f effective

Marine Ecology 32 (Suppl. 1) (2011) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

T rends in P. congirostrís a n d N. n o rveg icu s

Ligas, S a rto r & C o llo ca

fishing effort in m ixed dem ersal fisheries. ICES Journal o f

Parapenaeus longirostris, in E uropean Atlantic and M editer­

M arine Science, 63, 556-566.

ranean w aters (D ecapoda, D endrobranchiata, Penaeidae).

R othschild B.J., C hen C., Lough R.G. (2005) M anaging fish stocks u n d e r clim ate uncertainty. ICES Journal o f M arine Science, 62, 1531-1541. Sarda F., C om pany J.B., B aham ón N., R otllant G., Flexas M.M.,

Crustaceana, 78, 1153-1184. Solow A.R. ( 1994) D etecting changes in the com position o f a m ultispecies com m unity. Biometrics, 50, 556-565. Vargas-Yánez M., M oya F., Tel E., G arcía-M artínez M.C.,

Sánchez J.D., Zúfiiga D., C oenjaerts J., O rellana D., Jordà G.,

G uerber E., B ourgeon M . (2009) W arm ing a n d salting in

Puigdefábregas J., Sánchez-Vidal A., Calafat A., M artin D.,

the w estern M editerranean d uring the second h alf o f the

Espino M . (2009) R elationship betw een environm ent a n d the

20th century: inconsistencies, unknow ns a n d the effect o f

occurrence o f the deep-w ater rose shrim p Aristeus antennatus (Risso, 1816) in the Blanes subm arine canyon (N W M editer­ ranean). Progress in Oceanography, 82, 227-238. Sbrana M., Sartor P., Belcari P. (2003) Analysis o f the factors affecting catch rates o f crustacean traw l fishery o f the n o rth ­ ern T yrrhenian Sea (western M editerranean). Fisheries Research, 65, 271-284. Sbrana M., Viva C., Belcari P. (2006) O bservation o n the fish­ ery o f the deep w ater rose shrim p Parapenaeus longirostris (Lucas, 1846) (Crustacea: Decapoda) in the n o rth ern T yr­ rhenian Sea (w estern M editerranean). Hydrobiologia, 557, 135-144. Sm ith C.J., R u m o h r LL, Karakassis I., P apadopoulou K.N. (2003) Analysing the im pact o f b o tto m trawls o n sedim en­

data processing. Scientia M arina, 73, 7-28. Z u u r A.F., Pierce G.J. (2004) C om m on trends in N ortheast Atlantic squid tim e series. Journal o f Sea Research, 52, 57-72. Z u u r A.F., Fryer R., Jolliffe I., Dekker R., Beukem a J. (2003a) Estim ating c om m on trends in m ultivariate tim e series using dynam ic factor analysis. Environmetrics, 14, 665-685. Z u u r A.F., T uck I.D., Bailey N. (2003b) D ynam ic factor analy­ sis to estim ate com m on trends in fisheries tim e series. Cana­ dian Journal o f Fisheries and Aquatic Sciences, 60, 542-552. Z u u r A.F., leño E.N., Sm ith G.M. (2007) Analysing Ecological Data. Springer, London: 680 pp. Z u u r A.F., leño E.N., Elphick C.S. (2009) A p rotocol for data exploration to avoid co m m o n statistical problem s. Methods

tary seabeds w ith sedim ent profile imagery. Journal o f Exper­

in Ecology and Evolution,

imental M arine Biology and Ecology, 285-286, 479-496.

210X.2009.00001.x

1, 3-14. doi:

10.111 l/j.2041-

Sobrino I., Silva C., Sbrana M., Kapiris K. (2005) A review o f the biology and fisheries o f the deep w ater rose shrim p,

Marine Ecology 32 (Suppl. 1) (2011 ) 2 5 -3 5 © 2011 Blackwell Verlag GmbH

35

marine ecology

an evolutionary perspective

»

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

Biomass, commonly occurring and dom inant species of m acrobenthos in Onega Bay (White Sea, Russia): data from three different decades Katya S o ly a n k o 1, V assily S p ir id o n o v 2 & A n d r e w N a u m o v 3 1 Institute for Estuarine and Coastal Studies, University o f Hull, Hull, UK 2

P.P. Shirshov Institute o f Oceanology o f the Russian Academy o f Sciences, Moscow, Russia

3 Zoological Institute o f the Russian Academy o f Sciences, Unlversltetskaya Naberezhnaya, St. Petersburg, Russia

K eywords

A bstract

Anthropogenic impact; biomass; decadal variation; European seas; macrobenthos.

C orrespondence Katya Solyanko, Institute for Estuarine and Coastal Studies, University o f Hull, HU6 7RX Hull, UK.E-mail: [email protected] Accepted: 1 February 2011 doi : 10.1111/j.1439-0485.2011,00438.x

O nega Bay is th e largest b ay in th e W h ite Sea, characterised b y shallow depth, a range o f sed im en t types an d stro n g tidal currents. All these factors provide co n d itio n s for high species richness an d biom ass. This stu d y reviews d ata from th ree surveys o f su blittoral m acro b en th o s u n d erta k e n b y R ussian institutes: the b en th ic survey covering th e entire O nega Bay in 1952; th e survey p erfo rm ed in th e n o rth e rn p a rt o f th e area in 1981/90, a n d a stu d y carried o u t in 2006 in th e eastern p a rt o f th e bay. In total, d ata fro m 107 statio n s w ere analysed. The data in different surveys w ere collected b y different grab types. The datasets o f b o th 1981/90 an d 2006 overlap th e 1952 survey area. T he p a tte rn o f biom ass d istrib u tio n was consistent betw een th e years o f survey an d was characterised b y th e low biom ass at th e n o rth e rn p erip h ery o f th e bay a n d th e highest b io ­ m ass observed in th e coastal w aters o f th e Solovetsky Islands. Bivalves an d cirripeds (m ostly M odiolus modiolus, Arctica islandica, Balanus balanus and Verucca stroemia) d o m in ated in biom ass. N eith er th e biom ass share o f d o m i­ n a n t species n o r th e frequency o f occurrence o f several c o m m o n species in these g roups changed m arkedly betw een 1952 an d 1981/90. A lthough the results o f th e 2006 survey ap p ear som ew hat different fro m th e p attern s o f p re ­ vious years, this does n o t indicate m ajo r changes in th e b en th ic com m unities, because th e survey in 2006 was designed in a different w ay an d its overlap w ith th e 1952 survey was m inim al. H ow ever, th e d o m in a n t species (by biom ass) A . islandica, M . modiolus an d V. stroemia - held th e ir leading positions. Results o f th e m u ltid im en sio n al scaling analysis based o n th e biom ass data for all taxa en co u n te red in th e 1952 survey indicate considerable m ixing o f th e sam ples fro m all surveys. This m ay be in terp re te d as th e absence o f m ajo r shifts in the su b litto ral co m m u n ities o f th e m acro b en th o s o f O nega Bay at decadal scale. This kin d o f stability m ay be explained b y an oceanographical regim e resilient to clim ate v ariatio n a n d a relatively low an th ro p o g en ic en v iro n m en tal im pact w hen com pared to o th er shallow E u ro p ean seas.

Introduction Studies co nducted in m o st E u ro p ean seas have show n th a t the com p o sitio n o f m acro b en th ic com m unities,

36

species frequency o f occurrence, p o p u la tio n density and biom ass often show considerable changes over tim e. Som etim es su d d e n in te r-a n n u al changes are detected, b u t changes are m o re likely across decades. D rastic shifts in

Marine Ecology 32 (Suppl. 1) (2011) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

M a c ro b e n th o s o f O n eg a Bay (W hite Sea, Russia)

S o ly an k o , S p irid o n o v & N a u m o v

species com p o sitio n a n d stru c tu re o f com m unities detected in th e Black Sea w ere fo u n d to be due to e u tro ­ p hication, fishing an d th e in tro d u c tio n o f alien species (C hikina & K ucheru k 2005). R educed biom ass a n d n u m ­ b er o f species was fo u n d in th e K attegat an d Skagerrak due to d irect effects o f traw ling, lo n g -term tem p eratu re fluctuations a n d eu tro p h ica tio n o f th e area (P earson et a í 1985; R osenberg et a í 1987). C onsiderable changes in b enthic com m unities w ere detected in th e N o rth Sea an d the Irish Sea due to e u tro p h icatio n , b o tto m traw ling, dredging, oil drilling op eratio n s a n d clim ate variatio n (Frid et al. 1999, 2009; B radshaw et al. 2002; W ieking & K rönke 2003; K rönke et a í 2004). In th e B arents Sea, changes w ere associated w ith b o tto m traw ling pressure an d clim ate variatio n (G alkin 1998; B row n et al. 2005; D enisenko 2008; C arroll et al. 2008). These studies in d i­ cate th e role o f anth ro p o g en ic effects o n th e co m p o sitio n o f m acrobenthic com m unities. In th e W h ite Sea, th e ‘y oungest’ sea o f E u ro p e (existing only since the beginning o f th e H o locene), belonging to b o th the N o rth east A tlantic an d A rctic realm s a n d charac­ terised by a very peculiar oceanographical regim e (Berger & N au m o v 2001; Filatov et al. 2005a,b ), th ere has been n o a tte m p t to analyse historical datasets o n subtidal b e n ­ thic com m unities. T he em phasis o f previous studies has been o n identifying spatial p attern s (D erjugin 1928; Kudersky 1966; Beklem ishev et al. 1980; G olikov et al. 1985; L ukanin et al. 1995; Berger & N au m o v 2001); lo n g -term tem p o ral trends in b en th ic co m m u n ities have received relatively little atten tio n . N evertheless, th ere has been a long tra d itio n o f benthic research associated w ith m arin e

biological stations (K udersky 1966; Fokin et al. 2006; N a u m o v 2006). T he m ain objective o f th e p resen t study was to analyse data fro m th ree different decades w ith regard to th e com p o sitio n , occurrence a n d biom ass of d o m in a n t an d c o m m o n m acro b en th ic species a n d discuss if an y tem p o ral p a tte rn is revealed b y these historical datasets.

S tu d y area O nega Bay is th e largest bay in th e W h ite Sea, w ith an area o f 12,800 k m 2. T he d ep th o f th e bay is generally <50 m , w ith th e exception o f n o rth e rn parts, w here dep th s can reach 87 m . T he b o tto m relief is uneven, espe­ cially along th e coastline. P articularly com plex b ath y m etry is observed along th e bay’s w estern coast, w here n u m e r­ ous islands are co ncentrated. A b ro a d range o f sedim ent types characterises O nega Bay, b u t coarse a n d h a rd sedi­ m en ts w ith a sm all percentage o f silt are th e d o m in an t su b strata (Berger & N a u m o v 2001). O nega Bay is con­ nected to th e central p a rt o f th e sea b y th e W estern an d th e E astern Solovetsky Salm a, or stra it (Fig. 1). Deep w aters o f th e Salmas enable large volum es o f w ater to en ter th e bay, generating stro n g tidal cu rren ts exacerbated b y th e shallow dep th s in th e Bay. T he m ax im u m speed of a spring tid e is 1.5-2.0 m-s_1 in th e E astern Salma, an d 1.5-1.7 m-s_1 in th e W estern Salm a (B abkov 1998; Filatov et al. 2005a). S trong tidal currents increase th e tu rb id ity o f th e w ater, leading to vertical h o m o th e rm y a n d h o m o h alin ity in m an y p arts o f th e bay. A developed th erm o cline is largely ab sen t in m o st areas o f th e N o rth e rn an d

Solovetsky Islands

▲R/V "Professor M esy atsev", 1952 (0.1 m2 Petersen grab) • R/V "Kartesh", 1981/1990 (0.25 m2 "Ocean" grab) ♦ R/V "Professor V. K uznetsov", 2006 (0.1 m2 van Veen grab)

Boundary of overlapping stations

30

60

kilometres

Fig. 1. Location of benthic sampling stations of surveys of Onega Bay In 1952, 1 9 8 1 /9 0 and 2006 showing overlapping station boundaries.

Marine Ecology

32

(Suppl. 1) (2011) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

37

M a c ro b e n th o s o f O n e g a Bay (W hite Sea, Russia)

S o ly an k o , S p irid o n o v & N a u m o v

C entral O nega Bay (personal observations in July 2006 and June 2010). O nega Bay is th e m o st species-rich area o f the entire W h ite Sea, w ith aro u n d 500 species o f inver­ tebrates a n d a high b en th ic biom ass (G olikov et a í 1985; L ukanin et a í 1995). The area m ay be regarded as being exposed to low er an th ro p o g en ic im pacts th a n m an y o th er N o rth east A tlantic seas, as th e in d u strial activity in th e area has never been particu larly high an d has decreased recently (T erzhevik et al. 2005).

M eth o d s This stu d y is based o n th e data fro m th ree b en th ic surveys conducted respectively in 1952, 1981/90 a n d 2006 (Fig. 1, Table 1). T he d ata in th e different surveys w ere collected using a Petersen (0.1 m 2), a Petersen O cean-50 (0.25 m 2) and a V an V een (0.1 m 2) grab. Table 1 show s th e dates of the surveys, vessels, n u m b e r o f stations, sam ples at a sta­ tion , d ep th o f sam pling, a n d o n -d eck processing p rotocol. T he 1952 survey data p o oled w ith o th e r m aterial col­ lected in O nega Bay w ere described b y Ivanova (1957) and K udersky (1966), b u t o u r re-analysis o f these data is based on the original p ro to co ls o f sam ple exam ination. The 1952 survey was processed incom pletely: M ollusca, C irripedia, B rachiopoda, E ch in o d erm ata a n d o th er taxa w ere identified to species level b y S. S. Ivanova an d L. A. Kudersky. O th er g roups w ere recorded as higher taxa an d the to tal abun d an ce an d biom ass o f Porifera, H ydrozoa, Polychaeta, P a n to p o d a, Bryozoa, T u n icata a n d several orders o f C rustacea, i.e. A m p h ip o d a, C um acea an d M y­ sidacea, w ere calculated. T he original statio n d ata an d th e protocols for processing th e b en th ic collections b y the

W hite Sea Biological S tation o f th e K arelian -F innish Branch o f th e A cadem y o f Sciences o f USSR (WSBS KFB) are deposited in th e A rchive o f th e K arelian Science C en­ tre o f th e R ussian A cadem y o f Sciences (KSC RAS) in P etrozavodsk (A nonym ous 1952a,b). T hey w ere digitised in M icrosoft EXCEL fo rm at suitable for fu rth e r use in electronic databases. M aterial o n P orifera, H ydrozoa, Polychaeta, P a n to p o d a a n d B ryozoa fro m this survey was transferred to th e Zoological In stitu te o f th e th e n A cad­ em y o f Sciences o f USSR (n o w R ussian A cadem y o f Sci­ ences) in L eningrad, n o w St. P etersburg (Z IN RAN) (Ivanova 1957). T he fate o f th e m aterial o n o th er groups rem ains u n know n. M aterial fro m th e 1981/90 surveys was identified m ostly to species level, w ith th e exception o f N em ertini, O ligochaeta a n d som e fam ilies o f Porifera, H yd ro zoa and B ryozoa, w hich w ere identified b y A. D. N aum ov, V. V. Fedyakov a n d V. V. L ukanin in co n su ltatio n w ith special­ ists at ZISP o n som e faunal groups. T he d ata are m a in ­ tain ed in th e in fo rm atio n system ‘B enthos o f th e W hite Sea’ im p lem ented in CLIPPER 5.0 algorithm ic language (N au m o v 2006). B enthic collections fro m th e 2006 survey w ere p ro ­ cessed w ith m eth o d s an d tax o n o m ic reso lu tio n sim ilar to th e one used in 1981/90. M o st o f th e identification was done b y A. R ogacheva an d K. Solyanko in co n sultation w ith o th er specialists. The m aterial is stored in the Z o o ­ logical M u seu m o f th e M oscow U niversity. D ue to the unclear status o f th e tax o n usually identified as Hiatella arctica (L., 1867), nam ely, th e possible presence o f a n o th er, yet un id en tified species o f th e genus (N aum ov 2006), th e bivalve was listed as Hiatella sp. for all surveys.

Table 1. Basic data for surveys in Onega Bay used in the study. Survey Characteristics

KFB

ZIN RAS

IO RAS

Notes

Dates

10 August - 10 Septem ber 19S2

26 Septem ber 1981 - 2 Septem ber 1981; 2 July 1990

15 July -1 7 July 2006

Stations 113 and 114 were sampled in 1990

Vessel

Professor Mesyatsev

Kartesh

Professor Vladimir Kuznetsov

Gear

Petersen grab - 0.1-m2 sampling area

Petersen grab Ocean SO - 0.25-m 2

van Veen grab - 0.1 -m2 sampling area

No. of stations No. of casts per station

70 2

Total no. of grab samples Finest mesh size in process

134 0.7S

27

3-5 38

1

1

of rinsing samples, mm Depth range, m Mean depth, m

7-S3 26

5-70 24

6-36 19

sampling area 28 1

10

KFB = Karelian-Finnish Branch of the Academy of Sciences of USSR; ZIN RAS = Zoological Institute of the Russian Academy of Sciences, St. Peters­ burg; IO RAS = Institute of Oceanology of the Russian Academy of Sciences.

38

Marine Ecology 32 (Suppl. 1) (2011 ) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

M a c ro b e n th o s o f O n eg a Bay (W hite Sea, Russia)

S o ly an k o , S p irid o n o v & N a u m o v

To test for differences betw een surveys in th e biom ass o f 11 b io m ass-p red o m in an t an d co m m o n bivalve species in 1952 an d 2006, u n iv ariate techniques w ere applied such as A N O VA, th e M a n n -W h itn e y (7-test, m ed ian test an d K olm o g o ro v -S m irn o v test (H am m er et a í 2001). Species com p o sitio n a n d biom ass d ata for these areas w ere com pared using m ultivariate techniques (C larke & W arw ick 2001). The one-w ay A N O SIM test (PRIM ER v6) was used to determ in e th e differences in species co m ­ p o sitio n an d biom ass betw een th e stu d ied years (overlap­ ping stations), using 17 species o f bivalves a n d seven species o f echinoderm s. O nly species fro m th e 1952 (m ean values) an d th e 1981/90 surveys w ere com pared. A N O SIM is analogous to analysis o f variance (ANOVA) in univariate statistics. T he 1952 data w ere n o t com p ared to th e 2006 data because o f th e sm all n u m b e r o f overlap­ ping stations. In th e A N O SIM p ro ced u re, th e pro bab ility o f a priori groupings o f sam ples was estim ated by repeated p erm u tatio n s o f d ata {i.e. repeated ra n d o m rela­ belling o f sam ples in th e m atrix). Initially, a global R sta­ tistic was calculated to d eterm in e w hether significant differences exist betw een all g roups (analogous to th e glo­ bal F test in ANOVA). If differences w ere significant at a global level, th en pairw ise com parisons betw een sam ple groups w ere cond u cted to test for differences betw een pairs. In global tests, th e null hypothesis {i.e. ‘n o differ­ ence betw een g ro u p s’) was rejected a t a significance level o f P < 0.05. Possible changes in th e c o m m u n ity stru ctu re in term s o f abun d an ce and biom ass w ere m easured b y th e ABC (ab u n d an ce/b io m ass com parison, statistics W ) curves m eth o d . T his m eth o d was applied only for stations w here the biom ass an d a b u n d an ce h ad been recorded ad e­ quately. T he ab u n d an ce-b io m ass co m p ariso n (ABC) curves w ere co nducted using th e PRIM ER v.6.0 softw are package. N o n -m etric m u ltid im en sio n al scaling (nM D S) based o n B ray -C u rtis sim ilarity was carried o u t using loga­ rith m -tran sfo rm ed biom ass d ata (all replicates included). T he d ata o f different years w ere p o o led in to one dataset. T he list o f taxa con tain ed species fro m th e 1952 survey: 20 species o f bivalves w ere inclu d ed (o th er species o f biv­ alves appearing in later surveys w ere p o oled in to gro u p ‘O th er bivalves’), 13 species o f gastropods (plus ‘O th er g astropods’ g ro u p ), seven species o f echinoderm s (plus ‘O th er echinoderm s’ g ro u p ), th ree species o f cirripeds an d one species o f b rach io p o d . T he rest o f th e taxa were entered as higher tax o n o m ic g roups (Porifera, C nidaria, Polychaeta, A m phip o d a, C um acea, D ecapoda, P an to p o d a, B ryozoa an d Ascidiacea). A lthough th e list o f taxa did n o t include in fo rm a tio n a b o u t all species, th e taxa id e n ti­ fied to species level w ere th e m o st im p o rta n t in term s of biom ass.

Marine Ecology 32 (Suppl. 1) (2011 ) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

R esults Biomass an d abundance of m acrobenthos B iom ass d istrib u tio n in th e N o rth e rn O nega Bay show ed a consistent p a tte rn in 1952 an d 1981/90 (Fig. 2). This consistency was also fo u n d in th e eastern p a rt o f th e bay w hen th e 1952 an d 2006 data w ere com pared. In the n o rth e rn p erip h ery o f th e bay, an d generally in th e W es­ te rn a n d th e E astern Salm a, th e biom ass was relatively low an d this zone o f low biom ass extended to th e coastal areas in th e no rth w estern p a rt (Fig. 2). The low est b io ­ m ass (5.5 g 'tn -2 ) was recorded at S tation 4 n ear River Z olotitsa in 1952. In th e coastal zone o f th e Solovetsky Islands, biom ass varied greatly; how ever, m o st stations w ith biom ass exceeding 1000 g 'm -2 w ere co n cen trated in this area. T he highest biom ass reco rd ed was 9200 g 'm -2 a t S tation 237 in 1981/90 so u th o f Bolshoi Solovetsky Island. In th e central p a rt o f O nega Bay a n d off the O nega P eninsula coast th e biom ass was generally low er th a n a ro u n d th e islands (in m o st cases <500 g 'm -2 ) b u t greater th a n in th e n o rth o f th e bay (Fig. 2). In general, th e m acro b en th ic biom ass in O nega Bay can be consid­ ered significant: it exceeded 100 g 'm -2 at m o re th a n 60% o f all stations. A m ong large tax o n o m ic groups, bivalves m ad e a m ajor c o n trib u tio n to to tal b enth ic biom ass, co n stitu tin g a t least 40% o f th e biom ass o f each survey (Fig. 2). H orse m ussel M odiolus modiolus an d q u ahog Arctica islandica together w ith barnacles Balanus crenatus an d Verruca stroemia con­ stitu te d th e greatest biom ass w ith in all surveys. C irripeds w ere th e next m o st im p o rta n t c o n trib u to rs to th e total b enth ic biom ass (above 20% ) in 1952 a n d 1981/90, fol­ low ed b y polychaetes. H ow ever, this was n o t th e case in

Biomass, g-m

o 0-50 O 50-150 O 150-500 Q 500-1000 Q 1000-2000 ( J2000-10.000

1981 and I990#urvey# rtiivey

Fig. 2. Distribution of m acrozoobenthos biomass (g-m 2) In Onega Bay In the years 1952, 1 9 8 1 /9 0 and 2006.

39

M a cro b e n th o s o f O n eg a Bay (W hite Sea, Russia)

S o ly an k o , S p irid o n o v & N a u m o v

the S outheastern O nega Bay in 2006, w here th e positions o f these tw o groups were reversed (Fig. 3). Sponges, hydroids, brachiop o d s, bryozoans an d echinoderm s co n trib ­ u ted to sim ilar fractions o f th e to tal m acro b en th ic biom ass (averaging 3 -9 % ) in 1952 an d 1981/90 (Fig. 3). M edian biom ass values in th e surveys were in th e range 114-151 g 'm -2 an d rath er sim ilar (Table 2). H owever, com parison o f biom ass values (using a n o n -p aram etric M a n n -W h itn e y U-test) show ed statistically significant d if­ ferences betw een all stations in 1952 an d in 1981/90 (P < 0.05) and betw een th e 1981/90 an d th e 2006 sta­ tions (P < 0.01). This was due to som e exceptionally high values (>2000 g 'm -2 ) in 1981/90 (several stations a ro u n d the Solovetsky Islands). N o statistically significant differ­ ences in biom ass were fo u n d betw een th e 1952 a n d 2006 data (Table 2). N o significant difference was detected betw een the 1952 stations an d th e overlapping 1981/90 stations. Benthic abun d an ce varied considerably betw een surveys from 10 to 43,604 ind-m -2 (Table 2). A bundance in 1981/90 was n otably h igher (m ean o f 5182 ind-m -2 ) com pared to th e 1952 survey (m ean o f 2029 ind-m -2 ) and 2006 survey (m ean o f 2407 ind-m -2 ). The b io ­ m ass/ab u n d an c es ratio (B /A ), o r a m ean m ass o f a speci­ m en, was rem arkably sim ilar (Table 2) an d was n o t significantly different betw een th e 1952 an d th e 1981/90 surveys. The B /A ratio o f th e 2006 survey was low er th a n in the o th er tw o surveys (M a n n -W h itn e y U-test, P < 0.01 for the 1952 an d 2006 co m p ariso n an d P < 0.05 for the 1981/90 and 2006 com p ariso n ). H ow ever, there was no significant difference in th e B /A values for th e 1952 sta­ tions overlapping w ith th e 2006 survey (Table 2). In term s o f ab u n d an ce-b io m ass co m p ariso n (ABC curves)

1952 H 1981/1990

A 100

Bivalvia

Cirripedia

Frequency of occurrence and biom ass of particular taxa M ost o f th e bivalve species w hich w ere listed as d o m in an t a n d su b d o m in a n t in b en th ic co m m u n ities o f O nega Bay in 1952 (Ivanova 1957; K udersky 1966) an d th e 1980s (G olikov et al. 1985; L ukanin et a l 1995; N au m o v 2001) occu rred w ith sim ilar frequency in 1952 an d 1981/90 (Table 3). F u rth erm o re, H eteranom ia spp., Nicania m ontagui, N uculana sp., M odiolus modiolus an d M ytilus edulis show ed nearly th e sam e values. O nly Leionucula bellotii, Clinocardium ciliatum , M acom a calcarea occurred 1.6-2.1 tim es m o re frequently in 1981/90 co m p ared to 1952, w hereas Thyasira gouldi was a b o u t five tim es m ore c o m m o n in this year (Table 3). C orrelatio n betw een fre­ quencies o f occurrence o f th e bivalve species listed in Table 3 (w ith o u t T. gouldi, w hich was th e m o st dissim ilar in this respect) in th e 1952 an d th e 1981/90 surveys was h igh an d statistically significant (r = 0.73, P < 0.005, n - 13). In th e 2006 survey area som e o f th e bivalve species w ere fo u n d at a h igher frequency th a n at th e overlapping stations in 1952 (Table 3). In contrast, H eteranom ia spp. was m u ch rarer in 2006 th a n in 1952. M ytilus edulis and Chlamys islandica were fo u n d only in 1952. F u rth erm ore, b o th absolute biom ass an d th e biom ass shares o f p a rtic u ­ lar species in 1952 an d 1981/90 were also sim ilar in m any cases (Tables 3 an d 4). N o n -p aram etric tests indicate sta­ tistically significant differences in absolute biom ass only for Elliptica elliptica, H eteranom ia squam ula, M. calcarea

H2006

U

M i

Hydrozoa

Polychaeta Echinodermata Gastropoda

11952 H 1981/1990

40

th ere was n o significant difference betw een th e 1952 su r­ vey (taking all stations o r overlapped stations) and 1981/90 surveys.

il

U .

H2006

30-

* 20 V VI c« ¡ io

Fig. 3. Percentage of contribution to the

S

o Ascidia

40

Brachiopoda

Bryozoa

Porifera

Apyrae

total biomass (mean for stations + SD): for taxonomic groups with a high relative contribution (A) and other groups with lower relative contribution (B).

Marine Ecology 32 (Suppl. 1) (2011) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

M a c ro b e n th o s o f O n eg a Bay (W hite Sea, Russia)

S o ly an k o , S p irid o n o v & N a u m o v

Table 2. Comparison of the macrobenthic biomass and abundance. For mean biomass, mean abundance and mean biomass ratio, the standard deviation Is presented In brackets.

Parameters

19S2 - all stations

19 8 1 /9 0 - a ll stations

2006 - a ll stations

No. of stations Benthic biomass (B) range, g-m-2

70 6 - 2188

27 11-9210

Mean B, g-mT2 (SD) Median B, g-mT2 Benthic abundance (A) range, Ind-m-2 Mean A, Ind-m-2 (SD) Median A, Ind-m-2

273 (371) 1S1 10-22,310 2029 (368S) S9S

959 (2008) 142 60-43,604 B182 (9S28) 1332

5-1195 190 (254) 114 250-19,020 2407 (3540) 1170

B/A, range, g-m-2 Mean B/A, g-m-2 (SD) Median B/A, g-m-2

0.02-1.62 0.28 (0.32) 0.14

0.01-1.24 0.26 (0.3S) 0.11

0.01-0.58 0.1 (0.12) 0.06

10

1952 - stations In the area overlapping with 19 8 1 /9 0 survey

1952 - stations In the area overlapping with 2006 survey

41 2-2188

6 14-1706

332 (408) 188 10-22,310 2452 (4182) 890

374 (504) 68 230-8630 2928 (2956) 1985

0.02-1.62 0.26 (0.32) 0.13

0.02-0.53 0.13 (0.15) 0.07

Table 3. Frequency of occurrence and mean contribution to the total biomass of com mon bivalves, cirripeds, echinoderms, gastropods, and brachlopods (In descending order of frequency of occurrence for the 1952 survey). 1952 - stations overlapping with 2006 survey

BS ± SE

FO ± SE

BS ± SE

FO ± SE

BS ± SE

FO ± SE

BS ± SE

26 ± 8

30 ± 13

26 ± 7

62 ± 10

15 ± 74

38 ± 11

22 ± 8 52 ± 10

11 ± 5

11 ± 4 24 ± 6

17 ± 11 17 ± 11 8

30 ± 3

25 ± 6

15 ± 4 22 ± 5 49 ± 6 59 ± 5 33 ± 5 20 ± 4

12 4 1 2 5

3 1 1 1 2

58 ± 14 83 ± 11 33 ± 14 33 ± 14 25 ± 13

14 ± 7 9± 5 3± 1 1± 1 1± 1 35 ± 11

1952 - all stations FO ± SE

BS ± SE

FO ± SE

18 ± 3

■t*

Species

2006 - all stations

1952 - stations overlapping with 1 9 8 1 /9 0 survey

19 8 1 /9 0 - all stations

10 16 43 47 27 18 9

16 ± 6 24 ± 6 13 4 1 1 8

52 56 56 52 33

Arctica islandica Chlamys Islandica Clinocardium ciliatum Elliptica elliptica Heteranomia spp. Hiatella sp. Leionucula bellotii Macoma calcarea Modiolus modiolus Mytilus edulis Nicania montagui Nuculana sp. Thyasira gouldi

± ± ± ± ± ± ±

3 3 4 4 4

3 2

l+

Bivalvia

± ± ± ± ±

17

2 1 1 1

4

± ± ± ± ±

10 10 10 10 9

26 ± 8

11 5 1 1 1 7

± ± ± ± ± ±

4 3 1 1 1 4

24 ± 7 37 8 13 58 55

± ± ± ± ±

8 4 5 8 8

1 1 1 6

4 ± 2

12 ± 4 28 ± 5 6± 3

51 ± 6 18 ± 3

50 ± 14 8

1± 1 2 ± 1 1± 1

50 ± 8 42 ± 8 37 ± 8

4 ± 2 9 ± 4 1± 1

30 ± 5 56 ± 5 7± 3

3 ± 1 3± 1 1± 1

8 58 ± 14 8

6± 2

44 ± 5

21 ± 4 36 ± 7 15 ± 3

33 ± 14

10 ± 2

17 ± 4 72 ± 5

8 67 ± 14

6 19 ± 6

17 ± 11

1± 1

31 ± 4 52 ± 4 10 ± 3

5± 2 6± 1 2± 1

37 ± 4

22 ± 4

13 ± 3 55 ± 4

31 ± 6 15 ± 2

27 ± 4 4 ± 2

1± 1 2± 1

26 ± 8 22 ± 8

1± 1 2 ± 2

27 ± 4 12 ± 3

2± 1 4 ± 3

59 ± 9 26 ± 8

1± 1 3 ± 2

4 ± 2 4 ± 2

1± 1 1± 1

15 ± 7 7 ± 5

1± 1 1± 1

4 ± 2

6± 2

19 ± 7

1± 1

16 ± 6

33 ± 4

8 ± 2

37 ± 9

10 ± 3

5

7 10 9 9

± ± ± ±

1

53 ± 8

46 ± 5 18 ± 4

± ± ± ±

1 1 2 20

± ± ± ± ±

46 ± 10 12 ± 6

24 ± 4 8 ± 2

15 44 67 63

1

35

1 1

1

Cirripedia

Balanus balanus Balanus crenatus Verruca stroemia

4 56 ± 10 56 ± 10

5 21 ± 6 8 ± 2

3

2

37 ± 8

7 ± 3

21 ± 7

19 ± 8

Echinodermata

Henricia sp. Ophiopholis aculeata Ophiura robusta Stegophiura nodosa

3 5 18 ± 6

1± 1 5± 2

2 ± 1

23 ± 5 13 ± 4

1± 1 6± 5

7± 3 6± 3

2 ± 1 1± 1

9± 4

5± 2

6 ± 2

1± 1

43 ± 5

6± 1

1

1± 1

Gastropoda

Margarites g. groenlandicus Puncturella noachina Buccinum undatum

3

1

8

1

Brachiopoda

Hemithiris psittacea

58 ± 14

11 ± 5

FO = frequency of occurrence (%); BS = biomass share (%); SE = standard error.

Marine Ecology 32 (Suppl. 1) (2011 ) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

41

M a c ro b e n th o s o f O n e g a Bay (W hite Sea, Russia)

S o ly an k o , S p irid o n o v & N a u m o v

T able 4. Differences in biomass and statistical comparison of biomass data for dom inant bivalve species at the stations in the overlapping area betw een the surveys in 19S2 and 1 9 8 1 /9 0 in Onega Bay. Biomass, g-m 2 1952 (n = 36) Mean (SE)

Species

19 8 1 /9 0 (n = 27) Mean (SE)

M ann-W hitney (J-test (P)

Test of median (P)

Species which may be dom inant in the benthic communities (Kudersky 1966; Golikov e ta /. 1985; Lukanin e ta /. 1995) Arctica islandica 14.41 ± 7.98 39.34 ± 27.58 468.00 (0.56) 0.92

Chlamys Islandica Clinocardium ciliatum Elliptica elliptica Modiolus modiolus Nicania montagui Nuculana spp.

25.54 ± 14.09 15.97 ± 4.48 30.08 ± 7.20

95.91 ± 70.33 12.62 ± 5.49 12.71 ± 7.13

Kolmogorov-Smirnov test K (P)

0.70 (0.70)

461.50 (0.51) 470.50 (0.66) 242.50 (0.001)**

0.54 0.39 0.01*

0.55 (0.92) 0.63 (0.82) 1.91 (0.001)**

453.00 (0.45) 419.50 (0.25) 474.50 (0.73)

0.46 0.61 0.91

0.62 (0.84) 0.76 (0.60) 0.50 (0.97)

203.48 ± 70.89 1.85 ± 0.55 1.89 ± 0.83

466.97 ± 253.78 1.43 ± 0.44 1.43 ± 0.44

13.87 ± 3.18 1.94 ± 0.52 0.19 ± 0.15

3.42 ± 1.48 4.93 ± 2.32 2.29 ± 1.4

233.50 (0.001)** 469.00 (0.86) 381.00 (0.02)*

0.001** 0.51 0.06

1.97 (0.001)** 0.61 (0.85) 0.92 (0.37)

0.06 ± 0.03

0.45 ± 0.14

251.50 (0.001)**

0.001**

1.95 (0.001)**

Other com m on species

Heteranomia squamula Hiatella arctica Macoma calcarea Tyasira gouldi

*Different levels of statistical significance of differences. SE = standard error; P = probability of belonging to the sam e general set of variables.

and T. gouldi (Table 4). Biom ass data for these a n d o th er co m m o n bivalves (17 species) for 49 overlapping stations w ere also tested for differences using a one-w ay A NO SIM test. N o significant difference betw een th e stud ied years was fo u n d (Table 5). T he 2006 survey ind icated a greater c o n trib u tio n (aver­ aged to nearly 67% ) o f A. islandica. In 1952 th e co n trib u ­ tio n was low er b u t th e species still m ade th e greatest c o n trib u tio n to to tal b en th ic biom ass (Table 3). N o n e th e­ less, one sho uld bear in m in d th a t th e 1952 a n d 2006 data allow little d irect co m p ariso n d u e to th e sm all n u m ­ b er o f w idely scattered stations in th e earlier survey versus m u ch m o re closely set stations along th e shorew ard tr a n ­ sects in 2006. A m ongst co m m o n cirripeds Verucca stroemia occurred at a very sim ilar rate an d m ade sim ilar c o n trib u tio n s to biom ass in 1952 an d 1981/90, w hereas Balanus balanus, w hich occurred tw ice as frequently in 1952 com p ared to

B. crenatus, was n o t co m m o n in 1981/90 o r 2006. Ver­ ucca stroemia a n d B. crenatus occurred m u ch m o re fre­ q uently th a n B. balanus in th e 1981/90 a n d 2006 survey areas (Table 3). T he m o st c o m m o n echinoderm s in th e 1952 an d the 1981/90 surveys w ere (in descending o rder) Ophiura robusta, Stegophiura nodosa, Ophiopholis aculeata and Henricia sp. T he frequencies o f occurrence a n d average c o n trib u tio n s to biom ass w ere h igher in 1981/90 for all species, alth o ug h S. nodosa show ed h igher occurrence in 1952 in th e area w hich overlapped w ith th e 1981/90 su r­ vey. A gain, th e one-w ay A N O SIM test for seven species o f relatively c o m m o n echinoderm s for 34 overlapping sta­ tions d id n o t show a significant difference in biom ass betw een th e stu d ied years (Table 4). In th e overlapping area o f th e 2006 a n d 1952 surveys, O. aculeata did n o t occur in either year an d o th er th ree species w ere n o t fo u n d in 1952 (Table 3).

T able 5. Comparison of the biomasses of com m on bivalves (17 species) and echinoderms (seven species) for all overlapping stations betw een the 1952 and the 1 9 8 1 /9 0 surveys using a one-way ANOSIM test. Taxa

Species

No. of species

No. of stations

Global R

P-value

Bivalvia

Arctica islandica; Chlamys islandicus; Clinocardium ciliatum; Elliptica elliptica; Heteranomia squamula; Hiatella arctica; Leionucula bellotii; Macoma calcarea; Modiolus modiolus; Mya truncata; Mytilus edulis; Nicania montagui; Nuculana minuta; Nuculana pernula; Pandora glacialis; Serripes groenlandicus; Thyasira gouldi Asterias rubens; Henricia sanguinolenta; Ophiacantha bidentata; Ophiopholis aculeata; Ophiura robusta; Stegophiura nodosa; Strongylocentrotus pallidus

17

49

0.039

0.08

7

34

0.08

0.06

Echinodermata

42

Marine Ecology 32 (Suppl. 1) (2011 ) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

M a c ro b e n th o s o f O n eg a Bay (W hite Sea, Russia)

S o ly an k o , S p irid o n o v & N a u m o v

G astropods w ere n o t co m m o n ly fo u n d in th e 1952 su r­ vey; only three species occurred w ith a frequency above 5%: Margarites groenlandicus groenlandicus, Puncturella noachina an d B uccinum u n datum . In 1981/90 these three w ere also the m o st frequently o ccurring species, w ith P. noachina occurring w ith a sim ilar rate, w hereas in 1952 the tw o o th er species w ere fo u n d m o re frequently (Table 3). H em ithyris psittacea, th e only b rach io p o d species living in the W hite Sea, show ed a very sim ilar occurrence rate an d average co n trib u tio n to to tal b en th ic biom ass in 1952 an d 1981/90. In 2006 th e species was n o t as c o m m o n as in the 1952 survey area overlapping w ith th e 2006 survey (Table 3).

C om parison at the assemblage level R esults o f th e M DS analysis based o n th e biom ass data for all taxa accounted for in th e 1952 survey indicate co n ­ siderable m ixing o f th e sam ples o f all surveys: variatio n betw een sam ples o f th e 1981/90 a n d th e 2006 surveys is largely inside the v ariatio n o f th e 1952 survey p erform ed at a w ider spatial scale (Fig. 4). A pairw ise A N O SIM test revealed no statistically significant differences betw een the 1952 and th e 1981/90 data. H ow ever, differences at a sta­ tistically significant level (P < 0.05) w ere fo u n d betw een these surveys an d th e 2006 survey. To com pare the co m m u n ities at a sm aller scale, the stu d y area was divided in to sub-areas (Fig. 5). C o m p ari­ so n o f th e d o m in a n t p a tte rn in p articu lar sub-areas betw een the stations o f th e 1952 survey a n d th e 1981/91 survey also did n o t indicate m ajo r shifts (Table 6). Subarea F covered th e n o rth e rn stations o f th e 2006 survey. These stations w ere located n ear S tation 65 o f th e 1952 survey, w hich h ad a sim ilar species co m p o sitio n w ith

S17 8my CWtu mnùmùy

* A +J AA

Fig. 4. Results of multidimensional scaling (MDS) analysis of the sam­ ples of surveys In Onega Bay conducted In 19S2, 1 9 8 1 /9 0 and 2006. Explanations are given In the text.

Marine Ecology 32 (Suppl. 1) (2011) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

Stations 16-19 o f th e 2006 survey. H ow ever, th e biom ass o f M odiolus modiolus in 1952 was som ew hat h igher th an in 2006 (Fig. 5, su b -area F). In S outheastern O nega Bay (Fig. 5, su b -area G) th e co m m u n ity was also d o m in ated b y Arctica islandica in b o th 1952 a n d 2006.

D iscussion T he benthic surveys considered in th e presen t stu d y were n o t designed to stu d y in te r-a n n u a l variatio n in benthic com m unities. W h en p lan n in g th e 2006 survey th e stations w ere inten tio n ally set in th e area w hich was covered the least b y th e surveys in earlier years. F u rtherm o re, the m eth o d s o f sam pling an d gears differed betw een surveys. Bearing this in m in d , we expected to find greater differ­ ences betw een th e surveys fro m th ree different decades. M ed ian b enth ic biom ass was very sim ilar in all years of investigation a n d clearly different fro m o th er areas o f the W h ite Sea w ith sim ilar d ep th an d b o tto m to p ography. In particu lar, in th e G orlo (th e shallow strait separating the o u ter p a rt o f th e W h ite Sea fro m its deep basin) a n d in th e D vina Bay th e m ed ian biom ass was one o rd e r o f m ag­ n itu d e low er (N au m o v 2001). N eith er th e biom ass o f d o m in a n t bivalves a n d cirri­ peds n o r th e frequency o f occurrence o f th e m o st com ­ m o n species show ed any considerable changes betw een 1952 a n d 1981/90. T he c o n trib u tio n to th e to tal b io ­ m ass o f som e bivalves an d cirripeds (M odiolus modiolus, Arctica islandica, Chlamys islandica, M ytilus edulis, Ellip­ tica elliptica, Balanus balanus, Verucca stroemia an d , to lesser extent, Clinocardium ciliatum ) did n o t change betw een 1952 a n d 1981/90. All these species were described as d o m in a n t in various b en th ic com m unities identified using different m eth o d s in th e 1950s an d the 1980s (K udersky 1966; G olikov et a í 1985; L ukanin et al. 1995). N uculana pernula a n d N uculana m inuta m ay be added to this list b u t it is possible th a t these m orphologically sim ilar species w ere p o o rly distinguished (N au m o v 2006) in earlier surveys a n d so th eir presence c an n o t be confirm ed w ith certainty. F u rth erm o re, the frequency o f occurrence an d biom ass o f o th er co m m o n species (Heteranom ia squam ula, Hiatella sp., Nicania m ontagui, H em ithyris psittacea an d c o m m o n ech ino­ derm s) did n o t show m u ch variation. A t th e assemblage level, few differences w ere revealed using m u ltivariate statistics an d d irect co m p ariso n o f th e closely located statio n s fro m different surveys. The stability o f th e ABC curves a n d th e average m ass o f a specim en also indicate th e absence o f shifts in b en th ic co m m u n ities sim ilar to those observed in som e areas u n d e r th e influence of eu tro p h ic a tio n (R osenberg 1987). A lthough th e results of th e 2006 survey ap p ear som ew hat different fro m the p attern s o f previous years this does n o t ind icate m ajor

43

M a c ro b e n th o s o f O n e g a Bay (W hite Sea, Russia)

i

l'A 2 survey

•

1 ' IS 1 1 ' »'i n s u r v e y s

S o ly an k o , S p irid o n o v & N a u m o v

Fig. 5. Sub-areas of detailed comparison at

♦ 2()(in s u r v e y

the assem blage level. Explanations are given In the text.

T able 6. Benthic taxa composition (In term s of biomass) a t stations of the 19S2 and the 1 9 8 1 /9 0 surveys performed for sub-areas In Onega Bay.

Survey

Subarea (see Flg. S)

19S2

A

No. of samples 9

Dominant taxa

One-way ANOSIM test resul

Hemithyris psittacea, Cirripedia, Nuculana minuta, Elliptica elliptica

R = 0.176; P > 0.0S

and other bivalves 1 9 8 1 /9 0 19S2

B

7 7

Hemithyris psittacea, Cirripedia, Elliptica elliptica and other bivalves Modiolus modiolus, Cirripedia, Heteranomia squamula, Hydrozoa Modiolus modiolus, Cirripedia, Heteranomia squamula, Ascidia Clinocardium ciliatum, Elliptica elliptica, Cirripedia, Ascidia Arctica islandica, Clinocardium ciliatum, Serripes groenlandicus,

No significant differences R = 0.38S; P > 0.0S

1 9 8 1 /9 0 19S2 1 9 8 1 /9 0

C

3 10 3

19S2

D

7

Ascidia, Cirripedia Cirripedia, Modiolus modiolus, Chlamys islandicus, Hiatella sp.,

R = 0.138; P > 0.0S

4

Bryozoa, Hydrozoa Cirripedia, Hemithyris psittacea, Modiolus modiolus, Chlamys islandicus,

No significant differences

1 9 8 1 /9 0 19S2 1 9 8 1 /9 0

E

8 4

19S2 1 9 8 1 /9 0

G

9 2

Hiatella sp., Bryozoa, Hydrozoa Modiolus modiolus, Cirripedia, Ascidia, Hiatella sp., Hemithyris psittacea Ascidia, Cirripedia, Hemithyris psittacea, Nuculana minuta and other bivalves Arctica islandica, Nicania montagui, Nuculana spp., Elliptica elliptica Arctica islandica, Elliptica elliptica, Clinocardium ciliatum, Nuculana minuta

changes in the benthic co m m u n ities because th e survey in 2006 was designed in a different w ay an d its overlap w ith the 1952 survey was m inim al. H ow ever, even in this case, th e d o m in a n t species A . islandica, M . modiolus and V. stroemia held th eir positions. In spite o f a sim ilarity overall, th ere are a p p a re n t dif­ ferences betw een th e surveys w hich need to b e discussed. First, the m ax im u m an d th e average biom ass o f keystone species such as M . modiolus, C. islandica an d A. islandica w ere higher in 1981/90 th a n in 1952. This m ay reflect p o p u latio n dynam ics related to co h o rt grow th an d tu r n ­ over. In clam s an d m ussels, lo n g -term p o p u la tio n cycles have been know n since th e second h alf o f th e 20th cen­

44

No significant differences R = 0.634; P < 0.0S Significantly different

R = 0.323; P < 0.0S Significantly different ANOSIM test failed

tu ry (Stephen 1938; P arsons et a í 1977; L ukanin et a í 1989); these are n o t necessarily related to en v ironm ental v ariatio n (N au m o v 2006). In th e W h ite Sea, a patch o f benthic assem blages w ith a stro n g d o m in an ce o f A . islan­ dica (p o p u la tio n density o f a b o u t 15,000 ind-m -2 ) has been m o n ito re d in C h u p a In let for m o re th a n 25 years. T he stru ctu re an d q u an titativ e characteristics o f this clam p o p u la tio n at dep th s >10 m rem ain ed stable for 23 years, before th e fractio n o f large (3 0 -4 0 m m ) specim ens declined ow ing to a drastic n atu ra l elim ination. In subse­ q u en t years, resto ratio n o f th e p o p u la tio n stru c tu re was observed, pro b ab ly as a result o f th e re -d istrib u tio n o f the clam s (G uerassim ova et a í 2008).

Marine Ecology 32 (Suppl. 1) (2011 ) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

S o ly an k o , S p irid o n o v & N a u m o v

A low er biom ass o f d o m in a n t bivalves in 1952 m ay also be explained b y th e use o f different sam pling m e th ­ ods. T he O cean-50 grab used in 1981/90 has a slightly larger sam pling area (0.25 m 2) th a n tw o casts o f a P eter­ sen grab (0.2 m 2). It is possible th a t large sessile species w ith aggregated d istrib u tio n w ere u n d erestim ated b y tak ­ ing tw o replicate sam ples o f sm aller size versus th e one of larger size. F urtherm o re, an O cean-50 grab is m u ch h ea­ vier th a n a Petersen grab because th eir m ass is p ro p o r­ tio nal to L3, w here L is a linear dim en sio n o f th e o pen grab. A heavy grab is pro b ab ly m o re effective in p e n e tra t­ ing the dense coverage o f large bivalves th a n a lighter one. F u rth er studies using b o th theoretical m odels an d field experim ents are n eeded to check these hypotheses. Som e species w hich w ere n o t d o m in a n t in th eir b io ­ m ass b u t are relatively c o m m o n in O nega Bay show ed an a p p aren t increase in th e frequency o f occurrence an d b io ­ m ass betw een 1952 a n d 1981/90. These species include sm all clam Thyasira gouldi, echinoderm s Ophiura robusta an d Ophiopholis aculeata, an d w helk Buccinum undatum . In 2006, T. gouldi was also c o m m o n an d B. u ndatum occurred w ith m u ch h igher frequency th a n fo u n d in p re ­ vious surveys. In this case th e differences in sam pling m ethodology m ay also have biased estim ates for these species. For exam ple, one m ay suppose th a t such m obile an d probably aggregating species such as o p h iu ran an d whelks are u n d erestim ated b y taking only tw o replicate sam ples o f the Petersen grab. H ow ever, it is questionable w hether this explanation also holds for T. gouldi. A lterna­ tive explanations w ould be tren d s for extension a n d /o r increasing abun d an ce in th e a fo rem en tio n ed species. Regardless o f w heth er these changes or tren d s are real or artefacts o f sam pling design, th ey are n o t essential in com parison w ith th e ap p a re n t absence o f shift in the do m inance p attern in b en th ic co m m u n ities an d th e rela­ tive stability o f biom ass characteristics o f m o st co m m o n species at a decadal scale. T aking in to acco u n t high spa­ tial variability an d m ethodological constraints o f surveys, we m ay also speculate th a t such shifts could be p o tentially overlooked. H ow ever, th e consistency o f th e do m in an ce p a tte rn in b enthic assem blages in sm all sub-areas (Fig. 5) over decades suggests th a t this is n o t th e case. Indeed, in the dynam ics o f th e enviro n m en tal co n d itio n s in the W hite Sea region we see h ard ly an y m ajo r changes th at could drive shifts in th e d o m in an ce p a tte rn in benthic com m unities. The period from th e early 1940s u n til th e first h alf of the 1980s was characterised b y general cooling, b u t from the m id-1980s onw ards, tem p eratu res increased (Tolstikov et al. 2004; Filatov et a í 2005b). For w ater tem p e ra ­ tu re, the data from a p erm a n e n t statio n a t th e entrance o f the low -shore fjord in th e K andalaksha Bay, C hu p a Inlet, w hich has u n restricted w ater exchange w ith th e off­

Marine Ecology 32 (Suppl. 1) (2011 ) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

M a c ro b e n th o s o f O n eg a Bay (W hite Sea, Russia)

shore p a rt o f th e W h ite Sea (B abkov 1998; H ow lan d et a í 1999), show s n eith er stro n g positive n o r negative a n o m a­ lies since th e late 1950s. The average tem p e ra tu re for the 50 -65 m layer indicates particularly little in ter-a n n u al variation; th e anom alies do n o t significantly exceed 0.5 °C a n d show a w eak co rrelatio n w ith th e anom alies in th e u p p e r 15-m layer (Berger et al. 2003). As O nega Bay is o p en to th e influence o f th e deep p a rt o f th e W hite Sea, ow ing to tidal wave p ro p ag atio n an d an anti-clockwise system o f p e rm an e n t cu rren ts (Babkov 1998; Filatov et al. 2005a), th e p a tte rn o f in ter-a n n u a l v ariatio n o f th e r­ m al regim e is n o t expected to be very different fro m th at in th e entran ce o f C hu pa Inlet. River discharge, w hich can p o tentially strongly affect b en th ic co m m u n ities in the coastal zone, also show s n o well expressed tren d s or m ajo r changes (Filatov et a í 2005b). M odelling o f yearly average p rim ary p ro d u c tio n based o n satellite chlorophyll data indicates th a t O nega Bay is one o f th e m o st p ro d u ctiv e areas in th e W h ite Sea (Rom ankevich & V etrov 2004). A considerable p a rt o f the p h y to p la n k to n p ro d u c tio n a n d allo ch th o n o u s organic m a tte r supplied b y river ru n -o ff is co n su m ed b y sestonfeeding bivalves (Aí. m odiolus, A. islandica, C. islandica, a n d M . edulis) an d cirripeds, w hich co n stitu te th e m ajo r­ ity o f th e biom ass in O nega Bay. These bivalve species are long-living (N au m o v 2006) an d have few consum ers m ostly flatfish, w hich do n o t p red ate o n older age groups o f M . modiolus, large clam s an d scallops (Ivanova 1957), an d eiders, w hich are highly a b u n d a n t in th e area. Eiders use th e area for breeding, m o u ltin g an d w intering in the polynyas b u t m ostly concentrate for feeding close to the shore, in p articu lar o n blue m ussels, M . edulis (Bianki 1991; G alaktionov 2001; M akarevich & K rasnov 2005). It is therefore unlikely th a t p red ato rs have a stro n g im pact o n th e p o p u la tio n dynam ics o f d o m in a n t sessile benthic species a t th e scale o f th e entire O nega Bay. D ue to their role in filtratio n o f organic particles, influencing n e a r-b o t­ to m h ydrodynam ics an d p ro d u c in g shell m aterial as su b ­ strate for epibenthos (N au m o v 2006), th e d o m in an t bivalves a n d cirripeds m ay be considered keystone species-m odifiers (M ills et al. 1993) in seabed biotopes. T hus th e stability o r quasi-periodic changes in th eir p o p u la ­ tion s c o n trib u te to th e relative stability o f th e subtidal m acro b en th ic com m u n ities in O nega Bay. T he ch aracterisation o f O nega Bay w ould be in c o m ­ plete w ith o u t m en tio n in g th a t th e an th ro p o g en ic in flu ­ ence o n its m arin e ecosystem was low to m o d era te in the 20th century. A lthough th e tre n d for e u tro p h icatio n of th e m arin e w aters was seen in th e W h ite Sea in th e 1980s co m p ared to th e 1950s (M aksim ova 1991), th e W h ite Sea w atershed area was n o t an area o f intensive agriculture an d pu lp p ro d u c tio n in th e second h alf o f th e 20th cen­ tu ry (Terzhevik et al. 2005), an d n atu ral organic m atter

45

M a c ro b e n th o s o f O n e g a Bay (W hite Sea, Russia)

in p u t from river ru n -o ff was always considerable (Rom ankevich & V etrov 2004). A lthough th ere is p o llu ta n t tra n sp o rt w ith river ru n -o ff, m u c h o f th e p o llu tio n is en trap p ed b y so-called m arginal filters in estuaries (Iva­ n o v & Brizgalo 2005). In O nega Bay, b ack g ro u n d p o llu ­ tio n w ith hydro carb o n s an d organochlorides is low; th e trace m etal co n cen tratio n s in bivalve tissues m ay be som ew hat higher th a n in th e n eig h b o u rin g K andalaksha Bay b u t they are still n o t high com pared w ith seas su r­ ro u n d e d by areas o f high p o p u la tio n a n d in d u strial d e n ­ sity (Savinov et al. 2001). O nega Bay has always been an im p o rta n t area for h errin g a n d navaga fishing for local and regional m arkets, b u t fisherm en m ostly used passive gears an d there was practically n o im p act o f b o tto m traw ling an d dredging o n seabed habitats. A p art from p in k salm on, w hich was in tro d u c e d in th e late 1950s1960s, there are n o alien species established in th e region (Berger 2001). It is o f in terest to co m p are th e p resu m ed stability of benthic com m u n ities in O nega Bay to exam ples know n from the o th er shelf areas o f sim ilar scale. In th e n eig h ­ b o u rin g S outhw estern B arents Sea th e response o f zoob en th o s to lo n g -te rm fluctu atio n s o f tem p e ra tu re a n d th e inflow o f A tlantic w aters is relatively rap id an d m anifests itself in changes o f occurrence o f th e arctic an d th e boreal species (G alkin 1998; D enisenko 2008). H ow ever, th e principal factor influencing v ariatio n o f q u an titativ e char­ acteristics o f infaunal b en th ic co m m u n ities has been th e b o tto m traw l fishery (D enisenko 2001; C arroll et a í 2009). In the 20th century, Skagerrak, K attegat, th e N o rth and th e Irish Seas show exam ples o f significant changes in benthic (m ostly infaunal) co m m u n ities th a t are likely caused by eu tro p h icatio n (P earson et al. 1985; R osenberg et al. 1987), b o tto m traw ling, b ack g ro u n d p o llu tio n (K rönke 1990; W ieking & K rönke 2003; T ü rk ay & K rönke 2004) an d scallop dredging (B radshaw et a í 2002). Begin­ ning from the 1980s an increasing im p act o f clim atic trends on b enth ic co m m u n ities o f th e so u th e rn p a rt of the N o rth Sea can b e traced (B eukem a & D ekker 2003; Sonnew ald 2008). T he studies o n th e Black Sea b en th o s indicated th a t changes in th e stru ctu re o f b o tto m co m ­ m unities m anifesting in th e change o f d o m in a n t spe­ cies and th e high m ag n itu d e o f v ariatio n in abundance and biom ass o f co m m o n species m ay h ap p en w ith in a few years u n d e r th e cum ulative influence o f th e conse­ quences o f eu tro p h ic atio n an d in tro d u c tio n o f alien species. T he m isbalanced b en th ic co m m u n ities are c o n tin ­ uing to experience rap id changes in th eir q u an titativ e spe­ cies com positio n (C hikina & K ucheruk 2005; K ucheruk et al. 2009). A m ongst the seas a ro u n d E urope, th e W h ite Sea an d particularly O nega Bay m ay rep resen t a rare case o f a shallow -w ater b en th ic ecosystem w hich has n o t yet been

46

S o ly an k o , S p irid o n o v & N a u m o v

m odified b y h u m a n im pact. T he specific oceanographical regim e o f th e W h ite Sea has possibly also m ad e it resilient to clim ate v ariatio n in th e p ast decades. T aking this into account, O nega Bay w ith its largely boreal a n d in several respects sim ilar characteristics to th e N o rth Sea and the W estern Baltic b io ta (Zenkevich 1963; N a u m o v 2001) is a prospective area for studies o f n atu ra l v ariatio n in benthic com m u n ities an d possible fu tu re clim ate-forcing in this yet u n d istu rb ed ecosystem belonging to th e N ortheast A tlantic realm .

A c k n o w le d g e m e n ts W e th a n k C ap tain Jan Stelm akh a n d th e crews o f R.V. Kartesh an d Professor V ladim ir K uznetsov in 1981/90 and 2006. W e are very appreciative o f th e su p p o rt o f the directo r o f th e In stitu te o f Biology o f KSC RAS, Prof. N in a N. N em ova, in giving us access to th e archive m a te ­ rial o f th e 1952 survey, an d th e help o f L uydm ila B. C al­ a n in a a n d th e staff o f th e A rchive o f th e KSC RAS, P etrozavodsk in w orking w ith th e archive m aterial. V alu­ able critics an d com m ents o f th e a n o n y m o u s referees helped to im prove th e m a n u sc rip t an d m ade o u r state­ m ents clearer. T he field stu d y in 2006 was su p p o rted by th e INTAS project 51-5458 (P o p u latio n an d tro p h ic fu n c­ tio n in sh rim p species Crangon allm anni), a n d the visits to th e A rchive o f KSC RAS becam e possible d u e to the travel funds pro v id ed b y th e L ighthouse F o u n d atio n (H am b u rg an d Kiel) an d W W F Russia to V. Spiridonov. This stu d y is p a rt o f th e R ussian F o u n d atio n for Basic Research P roject 10-05-00813a.

R eferen ces A nonym ous (1952a) Log Book o f on Deck Works in the 1st Cruise o f R.V. ‘Professor M esyatsev’, 17.08-11.09.1952. Archive o f the Karelian Science Centre o f the Russian A cad­ em y o f Sciences, Petrozavodsk (In Russian). A nonym ous (1952b) Protocols o f Processing Benthic Samples Collected in the 1st Cruise o f R.V. ‘Professor M esyatsev’, 17.08-11.09.1952. Archive o f the Karelian Science Centre o f the Russian Academ y o f Sciences, Petrozavodsk (In R ussian). Babkov A.V. (1998). Hydrology o f the W hite Sea. Belom orskaya biostantsiya, St. Petersburg: 94 pp (In Russian). Beklemishev K.V., P antyulin A.N., Sem enova N.L. ( 1980) Bio­ logical com position o f the W hite Sea. II. New findings rela­ ting to vertical zoning o f the W hite Sea. Transactions o f the W hite Sea Biological Station o f the Moscow University, 5, 2 0 28 pp (In Russian). Berger V.Y. (2001) Fishes. In: Berger V., Dahle S. (Eds), W hite Sea. Ecology and Environm ent. D erzhavets Publisher, St. Petersburg a n d Trornso: 55-76.

Marine Ecology 32 (Suppl. 1) (2011 ) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

M a c ro b e n th o s o f O n eg a Bay (W hite Sea, Russia)

S o ly an k o , S p irid o n o v & N a u m o v

Berger V.Y., N aum ov A.D. (2001) G eneral features. In: Berger V., Dahle S. (Eds), W hite Sea. Ecology and Environment. Derzhavets Publisher, St. Petersburg a n d Trom so: 9-22. Berger V.J., N aum ov A.D., Usov N., Z ubaha V., Sm olyar M.A.,

Global Change. Springer-Praxis Publishing, Chichester: 73-154. Filatov N.N., N azarova L.E., Salo Ju A., Tolstikov A.V. (2005b) Clim ate o f the W hite Sea catchm ent scenarios o f clim ate

T atusko R., Levitus S. (2003). 36-Years Time-Series (1963-

and river ru n o ff changes. In: Filatov N.N., Pozdnyakov

1998) o f Zooplankton, Temperature and Salinity in the W hite

D.V., Johannessen O.M . (Eds), W hite Sea. Its M arine E nvi­

Sea. NOAA, St. Petersburg: 362 pp.

ronm ent and Ecosystem Dynamics Influenced by Global

Beukem a J.J., D ekker R. (2003) R edistribution o f spat-sized M acoma balthica in the W adden Sea in cold a n d m ild w in­ ters. M arine Ecology Progress Series, 265, 117-122. Bianki V.V. (1991) The birds. Oceanographic Conditions and Biological Productivity o f the W hite Sea. A nnotated atlas. PIN RO Publication, M urm ansk: 191-201. Bradshaw C., Veale L.O., B rand A.R. (2005) The role o f scallop-dredge disturbance in long-term changes in Irish Sea

Change. Springer-Praxis Publishing, Chichester: 53-72. Fokin S.I., Sm irnov A.V., Layus Yu.A. (2006). M arine Biologi­ cal Stations in the Russian North (1881-1938). KMK, M os­ cow: 130 pp. Frid C.L.J., Clark R.A., H aii J.A. ( 1999) Long-term changes in the benthos o n a heavily fished gro u n d off the NE coast o f England. M arine Ecology Progress Series, 188, 13-20. Frid C.L.J., G arw ood P.R., R obinson L.A. (2009) The N o rth

benthic com m unities: a re-analysis o f an historical dataset.

Sea benthic system: a 36 year tim e-series. Journal o f the

Journal o f Sea Research, 47, 161-184.

M arine Biological Association o f the United Kingdom, 89,

Brown E.J., Finney B., Hills S., D om m isse M. (2005) Effects o f com m ercial otter traw ling o n benthic com m unities in the south-eastern Bering Sea. In: Barnes B.W., T hom as J.P. (Eds), Symposium on Effects o f Fishing Activities on Benthic Habitats. A m erican Fisheries Society, Bethesda, M aryland: 439-460. Carroll M.L., Denisenko S.G., R enaud P.E., A m brose W .G. (2008) Benthic infauna o f the seasonally ice-covered western

1- 10 . G alaktionov K.V. (2001) M arine and coastal birds. In: Berger V., Dahle S. (Eds), W hite Sea. Ecology and Environm ent. D erzhavets Publisher, St. Petersburg a n d Trom so: 77-88. Galkin Y.I. ( 1998) Long term changes in the d istribution o f m olluscs in the Barents Sea related to the clim ate. Berichte zur Polaiforschung, 287, 100-143. Golikov A.N., Babkov A.I., Golikov A.A., N ovikov O.K., Shere-

Barents Sea: patterns a n d relationships to environm ental

m etevskiy A.M. ( 1985) Ecosystems o f the O nega Bay and

forcing. Deep-Sea Research Part I, 55, 2340-2351.

neighbouring areas o f the basin o f the W hite Sea. In: Scarla­

Carroll M.L., Johnson B.J., Henkes G.A., M cM ahon K.W.,

ta O.A. (Ed.), Ecosystems o f the Onega Bay o f the W hite Sea.

V oronkov A., A m brose W .C., Denisenko S.G. (2009)

Explorations o f the Fauna o f Seas. Zoological Institute o f the

Bivalves as indicators o f environm ental variation and potential anthropogenic im pacts in the sou th ern Barents Sea. M arine Pollution Bulletin, 59, 193-206. Chikina M.V., K ucheruk N.V. (2005) Long-term changes in

USSR, Leningrad: 20-87 (In Russian). Guerassim ova A.V., K uznetsova E.K., M axim ovich N.V. (2008) O n m u lti-annual dynam ics o f a local p opulation o f Arctica islandica (M ollusca, Bivalvia) and peculiarities o f m acroben­

the structure o f coastal benthic com m unities in the n o rth ­

thos d istribution in the area o f Keretsky Archipelago (W hite

eastern p art o f the Black Sea: influence o f alien species.

Sea). Presentations o f the Scientific Conference dedicated to

Oceanology, 45, 176-182.

the 70 years anniversary o f the W hite Sea Biological Station o f

Clarke K.R., W arw ick R.M. (2001). Change in M arine C om m u­ nities: A n Approach to Statistical Analysis and Interpretation, 2nd edn. Prim er-E , Plym outh, UK: 176 pp. D enisenko S.G. (2001) Long-term changes o f zoobenthos b io ­ mass in the Barents Sea. Zoological sessions (A nnual reports 2000). Proceedings o f the Zoological Institute R A S: 59-66 (In Russian). D enisenko S.G. (2008) M acrozoobenthos o f the Barents Sea in the conditions o f changing clim ate and anthropogenic

the Moscow University. G rif 8c Co. Publishers, Moscow: 5 5 58 (In Russian). H am m er 0 ., H arp er D.A.T., Ryan P.D. (2001) Paleontological statistical software package for education and analysis. Pale­ ontología Electrónica, 4, 1-9. H ow land R.J.M., P antyulin A.N., M illw ard G.E., Prego R. (1999) The hydrography o f the C hupa Estuary, W hite Sea, Russia. Estuarine Coastal and Shelf Science, 48, 1-12. Ivanov V.V., Brizgalo V.A. (2005) W hite Sea w atershed hydrol­

im pact. D issertation D r. Biol. Sei. Zoological Institute of

ogy and anthropogenic im pact. In: Filatov N.N., Pozdnya­

Russian Academ y o f Sciences, St. Petersburg (In Russian).

kov D.V., Johannessen O.M . (Eds), W hite Sea. Its M arine

D erjugin K.M. (1928) Fauna des W eissen M eeres u n d ihre Existenzbedignungen. Exploration des mers d ’URSS, 7-8 , 1-511 (In Russian w ith extended G erm an sum m ary). Filatov N.N., Pozdnyakov D.V., Ingebeikin Yu.I., Z dorovenov R.E., M elentyev V.V., T olstikov A.V., Pettersson L.H. (2005a) O ceanographical regim e. In: Filatov N.N., P ozdnya­

E nvironm ent and Ecosystem Dynamics Influenced by Global Change. Springer-Praxis Publishing, Chichester: 15-47. Ivanova S.S. (1957) Q ualitative a n d Q uantitative Characteristics o f B enthos in O nega Bay o f the W hite Sea. Materials on com­ plex studies o f the W hite Sea (Moscow): 355-380 (In Russian). K rönke I. ( 1990) M acrofauna standing stock o f the Dogger

kov D.V., Johannessen O.M . (Eds), W hite Sea. Its M arine

Bank. A com parison: II. 1951-1952 versus 1985-1987. Are

E nvironm ent and Ecosystem Dynamics Influenced by

changes in the c om m unity o f the n o rth-eastern p a rt o f the

Marine Ecology 32 (Suppl. 1) (2011 ) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

47

M a c ro b e n th o s o f O n e g a Bay (W hite Sea, Russia)

Dogger Bank due to environm ental changes? Netherlands Journal o f Sea Research, 25, 189-198. Krönke I., Stoeck T., W ieking G., Palojarvi A. (2004) Relation­ ship betw een structural and functional aspects o f m icrobial and m acrofaunal com m unities in different areas o f the N o rth Sea. M arine Ecology Progress Series, 282, 13-31. K ucheruk N.V., Flint M.V., M aksim ova O.V., C hikina M.V., Siniakova U.V. (2009) Contemporary Dynamics o f Benthic

S o ly an k o , S p irid o n o v & N a u m o v

Pearson T.H., Josefson A.B., Rosenberg R. (1985) Petersen benthic stations revisited. 1. Is the K attegatt becom ing eutrophic? Journal o f Experimental M arine Biology and Ecol­ ogy, 92, 157-206. R om ankevich E.A., V etrov A.A. (2004). Carbon Cycle in R us­ sian Arctic Seas. Springer, Berlin: 331 pp. Rosenberg R., Gray J.S., Josefson A.B., Pearson T.H. (1987) Petersen benthic stations revisited. 2. Is the O slofjord and

Com m unities in the N orth-East Shelf o f the Black Sea N atural

eastern Skagerrak enriched? Journal o f Experimental M arine

and Social Economic Factors o f Environm ent Changes in Rus­

Biology and Ecology, 105, 219-251.

sia. N auka, Moscow: 1-22 (In Russian). Kudersky L.A. (1966). Bottom Fauna o f the Onega Bay o f the W hite Sea. Karelian Book Publisher, Petrozavodsk: 204-371 (In Russian). L ukanin V.V., N aum ov A.D., Fedyakov V.V. ( 1989) M ultiyear structural changes in an estuarine p opulation o f blue m ussel

Savinov V., Savinova T., Dahle S. (2001) C ontam inants. In: Berger V., Dahle S. (Eds), W hite Sea. Ecology and Environ­ ment. D erzhavets Publisher, St. Petersburg a n d Trom so: 120-136. Sonnewald M. (2008) Langzeituntersuchung zur Biodiversität der decapoden Crustaceen und deren Begleitfauna in der D e­

in the W hite Sea. Journal o f General Biology, 50, 366-371 (In

utschen Bucht: 2007 versus 1986, 1987 und 1990. D iplom ar­

R ussian).

beit im Fachbereich Biologie Johann W olfgang Goethe,

L ukanin V.V., N aum ov A.D., Fedyakov V.V. ( 1995) Peculiari­ ties o f benthos d istribution in the Onega Bay. In: Berger N.J. (Eds), W hite Sea. Biological Resources and Problems o f Their Rational Exploitations. St. Petersburg: 232-236 (In R ussian). M akarevich P.R., K rasnov J.V. (2005) A quatic ecosystem p ro ­

U niversität, F rankfurt am M ain. Stephen A.C. (1938) P ro d u ctio n o f Large Broods in C ertain M arine Lam ellibranchs w ith a Possible R elation to W eather C onditions. Journal o f A nim al Ecology, 7, 130-143. Terzhevik A.Y., Litvinenko A.V., D ruzhinin P.V., Filatov N.N. (2005) E conom y o f the W hite Sea w atershed. In: Filatov

file. In: Filatov N.N., Pozdnyakov D.V., Johannessen O.M.

N.N., Pozdnyakov D.V., Johannessen O.M . (Eds), W hite Sea.

(Eds), W hite Sea. Its M arine E nvironm ent and Ecosystem

Its M arine E nvironm ent and Ecosystem Dynamics Influenced

Dynamics Influenced by Global Change. Springer-Praxis P u b ­

by Global Change. Springer-Praxis Publishing, Chichester:

lishing, Chichester: 155-177.

241-301.

M aksim ova M .P. (1991) H ydrochem istry o f the W hite Sea.

Tolstikov A.V., Petrov M.P., Filatov N .N . (2004) Influence o f

Hydrometeorology and H ydrochem istiy o f Seas o f the USSR.

clim ate change o n oceanographic characteristics. In: Filatov

H ydrom eteoizdat, Leningrad: 8-112 (In Russian). Mills L.S., Soulé M.E., D oak D.F. (1993) The Keystone-Species

N.N. (Ed.), The Climate o f Karelia: Variability and Influence on W ater Objects and Catchm ent Areas. Karelian Research

C oncept in Ecology a n d Conservation. BioScience, 43, 2 19224. N aum ov A.D. (2001) Benthos. Ch. 4. In: Berger V., Dahle S. (Eds), W hite Sea. Ecology and Environment. Derzhavets, St. Petersburg a n d T rom so: 41-53. N aum ov A.D. (2006) Clams o f the W hite Sea. Ecological and Fannistic Analysis. Explorations o f the fauna o f the seas. Zoological Institute o f the Russian Academ y o f Sciences, St. Petersburg: 1-367 (In Russian). Parsons T.R., T akahashi M., H argrave B. (1977). Biological

Centre, RAS, Petrozavodsk: 130-134. T ürkay M., Krönke I. (2004) Eine Insel u n ter W asser: die Doggerbank. N a tu r und M useum , 134, 261-276. W ieking G., Krönke I. (2003) M acrofauna com m unities o f the Dogger Bank (central N o rth Sea) in the late 1990s: spatial distribution, species com position a n d trophic structure. H el­ goland M arine Research, 57, 34-46. Z enkevich L.A. (1963) Biology o f the Seas o f the USSR. A cad­ em y o f Sciences o f USSR Publishing H ouse, Moscow: 740 pp (In Russian).

Oceanographic Processes. Pergam on Press, Oxford: 323 pp.

48

Marine Ecology 32 (Suppl. 1) (2011 ) 3 6 -4 8 © 2011 Blackwell Verlag GmbH

marine ecology

an evolutionary perspective

^

/

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

The effect of tem perature variability on ecological functioning of epifauna in th e German Bight H erm an n N e u m a n n & Ingrid K röncke Departm ent for Marine Research, Senckenberg Institute, Wilhelmshaven, Germany

K eywords Benthos; biological traits analysis; cold winter; ecosystem functioning; functional diversity; North Sea; tem perature anomalies. C orrespondence Hermann Neumann, Departm ent for Marine Research, Senckenberg Institute, Südstrand 40, 26382 Wilhelmshaven, Germany. E-mail: hneum ann@ senckenberg.de Accepted: 22 November 2010 doi: 10.1111/j. 1439-0485.2010.00420.x

A bstract Benthic epifauna was sam pled in an area o f 10 X 10 nautical m iles in th e G er­ m an Bight. Samples w ere tak en in January an d Ju ly /A u g u st fro m 1998 to 2009. The ecological fu n ctio n in g o f th e epifaunal c o m m u n ity was assessed using b io ­ logical traits analysis (BTA). Twelve ecological traits o f 26 epifaunal species were considered an d analysed using n o n -m e tric m u ltid im en sio n al scaling (nm M D S). A nom alies in th e sea surface tem p eratu re (SST) close to th e stu d y area were m ainly above th e lo n g -term m e an d u rin g th e stu d y p eriod. SST was exception­ ally high d u rin g th e a u tu m n m o n th s betw een 2002 a n d 2006. A dditionally, the cold w in ter o f 1995-96 was clearly reflected in stro n g negative SST anom alies. T rait co m p o sitio n changed in 2002, m ain ly due to a decreasing tre n d o f traits related to a n o p p o rtu n istic life m o d e fro m 1998-2002. T raits related to re p ro ­ d u ctio n show ed a m u ch clearer response to th e high a u tu m n SST anom alies fro m 2002 to 2006 th a n o th er traits. W e concluded th a t th e cold w in ter resulted in an increase in o p p o rtu n istic species in th e stu d y area follow ed b y characteris­ tic p o st-d istu rb an ce succession stages to th e p o in t o f an established c o m m u n ity in 2002. T his indicates a recovery tim e o f epifaunal co m m u n ities in th e G erm an Bight o f 7 -8 years. A dditionally, th e results give evidence th a t clim ate-induced variability o f SST in th e G erm an Bight affects m ainly th e re p ro d u c tio n o f epi­ faunal species ra th e r th a n o th e r traits such as feeding type.

Introduction In the N o rth Sea ecosystem , a regim e shift occurred in the late 1980s from a ‘cold dynam ic eq u ilib riu m ’ to a ‘w arm dynam ic eq u ilib riu m ’ (B eaugrand 2004). T his shift was linked to p ro n o u n c e d m o d ifications in large-scale hydro-m etrological forcing a n d ecosystem param eters, including a m arked increase in oceanic inflow a n d sea surface tem p eratu re (B eaugrand 2004). T he w arm te m ­ p eratu re perio d has co n tin u ed to th e presen t day (H ughes & H olliday 2006) an d th ere is stron g evidence to suggest th a t m an y different species an d co m m u n ities in th e N o rth Sea ecosystem are resp o n d in g to these tem p eratu re changes. For exam ple, th e pheno lo g y o f p h y to - a n d Zoo­ p lan k to n in the N o rth Sea has changed an d p lan k to n com m unities have shifted due to a n increasing prevalence

Marine Ecology 32 (Suppl. 1) (2011) 4 9 -5 7 © 2010 Blackwell Verlag GmbH

o f w arm -w ater species (Edw ards & R ichardson 2004; E dw ards et al. 2008; K irby et al. 2008; M artens & van B eusekom 2008). B iogeographical shifts o f fish species have been identified a n d in terp reted as reflecting a response to increasing w ater tem p eratu re (E hrich & Stransky 2001; B rander et al. 2003; P erry et al. 2005). M ig ratio n p attern s o f species have changed (Sims et al. 2001). Benthic com m u n ities in th e S ou thern an d N o rth ­ ern N o rth Sea have been affected b y tem p e ra tu re changes (K röncke et al. 1998; N e u m a n n et al. 2009a,b). H ow ever, th e tren d o f increasing tem p e ra tu re was in te rru p te d by extrem e cold w in ter co n d itio n s in th e N o rth Sea region d u rin g 1995-1996. C old w inters influence b en th ic fauna greatly, th ro u g h direct (enhanced m ortality) a n d indirect (reduced re p ro d u c tio n a n d p ro d u ctio n ) effects o n the species, especially in shallow areas (Reiss et a í 2006;

49

Effect o f te m p e r a tu re variability o n e p ifa u n a

N eu m an n et al. 2008a,b, 2009a,b). These effects are observed as a red u ced n u m b e r o f species, diversity an d biom ass (Ziegelm eier 1970; B uchanan & M o o re 1986; B eukem a 1992; K röncke et al. 1998). As th e effects o f cold w inters m ig h t influence th e ecosystem for several years, it is essential to u n d e rsta n d th e m m o re precisely in o rd er to in terp re t lo n g -term dynam ics in th e N o rth Sea ecosystem. L im ited atte n tio n has been p aid to th e questio n o f how these clim ate-induced changes affect th e fu n ctio n in g of the N o rth Sea ecosystem despite a grow ing d em an d for the functional aspects o f system s to be in co rp o rated into conservation an d m an ag e m en t efforts (B rem ner 2008; Frid et al. 2008). A ccording to Jax (2005), th e te rm ‘fu n c­ tio n ’ in ecology refers to (i) processes an d th e causal rela­ tions th a t give rise to th em , (ii) th e role o f organism s w ith in a n ecological system , (iii) th e overall processes th a t sustain an ecological system a n d finally (iv) to th e services a system provides for h u m a n or o th er organism s. Studies o n species com p o sitio n w ere often in ad eq u a te to address these issues as ecosystem processes are d eterm in ed b y th e functional characteristics o f th e organism s involved, rath er th a n by tax o n o m ic id en tity (O d u m 1969; G rim e 1997; H o o p er et a í 2002). The sam e conclusion was draw n by D iaz & C abido (2001), w ho stated th a t ecosys­ tem stability is strongly a ttrib u te d to th e fu n ctio n al traits o f species an d th e ir interactio n s ra th e r th a n to species com position per se. Biological traits analysis (BTA), w hich was developed in terrestrial an d freshw ater ecology, is a useful analytical app ro ach to describe different aspects o f fu n ctio n in g (B rem ner et a í 2003b). BTA has been applied successfully to assess fishing effects o n benthic fau n a (B rem ner et a í 2003a, 2005; Tillin et al. 2006), to assess th e fu nctional diversity in different species assem blages (Bell 2007; M ouillot et a í 2007; Schratzberger et al. 2007) as well as for m anagem en t an d conservation p urposes (B rem ner 2008; Frid et al. 2008). BTA uses a com prehensive set of functional traits (e.g. m obility, feeding type, size, longev­ ity, an d reprod u ctiv e tech n iq u e), w hich can be used as indicators for ecosystem functioning. T he w ide range of traits used b y BTA, th e stro n g lin k betw een th e m an d ecosystem processes (D iaz & C abido 2001), as well as th e so u n d theoretical fram ew ork (see B rem ner 2008) are a considerable advance over trad itio n al m eth o d s dealing w ith ecosystem functioning. T o u n d erstan d th e im p act o f tem p e ra tu re variability o n ecosystem fu n ctio n in g in th e G erm an Bight, this study focused on a single co m p o n en t o f th e ecosystem , the m obile epifauna. W e applied BTA o n an epifaunal tim e series in the G erm an Bight covering a p erio d o f 12 years w ith su m m er an d w in ter sam pling. P revious studies show ed th a t th e epifaunal co m m u n ities in this area were severely affected b y th e cold w in ter in 1995-96, b u t also

50

N e u m a n n & K rö n ck e

show ed an increase in diversity an d secondary p ro d u c tio n in co n ju n ctio n w ith increasing sea surface tem p eratu re (N eu m an n et a í 2008a; N e u m an n et al. 2009b). The objectives o f o u r stu d y w ere (i) to assess th e seasonal and a n n u al effects o f SST variability o n th e fu nctional co m p o ­ sitio n o f epifauna a n d (ii) to com pare these results w ith th e o u tco m e o f th e species co m p o sitio n analysis in the sam e area.

M aterial and M eth o d s Study site T he area o f investigation (Box A; 10 X 10 n autical miles) was situ ated a b o u t 25 nau tical m iles n o rth w est o f the Island o f H elgoland, in close p ro x im ity to th e old Elbe glacial valley 30 m d ep th c o n to u r (54° 17' N -5 4 °2 7 / N a n d 006°58/ E -007°15/ E) (Fig. 1). T he m ean d ep th o f this area was 40 m a n d th e w ater co lu m n was generally well m ixed th ro u g h o u t th e year. S edim ents in th e so u th ­ w est co rn er o f Box A w ere m o re th a n 20% m u d (<63 p m fraction). T his percentage gradually decreased tow ards the n o rth e a st (0 -5 % ). T he tim e series started in 1998 and w ere p a rt o f th e G erm an sm all scale b o tto m traw l survey (GSBTS) (E hrich et al. 2007 for fu rth er in fo rm ation). E pifauna was sam pled tw ice a year in Jan u ary (first q u a r­ ter) a n d in Ju ly /A u g u st (th ird q uarter) o n b o ard th e FRV W alther Herwig. Sam pling d id n o t take place in w inter 1998 an d 1999 due to ship tim e constraints.

Epifauna data E pifauna was sam pled w ith a stan d ard ized 2 m beam traw l m ade o f galvanized steel w ith a chain m a tt attached.

re

re

re

Fig. 1. Location and depth of Box A and tem perature station Helgo­ land (Hel) In the North Sea.

Marine Ecology 32 (Suppl. 1) (2011) 4 9 -5 7 © 2010 Blackwell Verlag GmbH

Effect o f te m p e r a tu re variability o n e p ifa u n a

N e u m a n n & K rö n ck e

T he b eam traw l was fitted w ith a 2 0 -m m n et an d a cod end o f 4 m m m esh size. A S canm ar d ep th -fin d in g sonar was attached to th e to p o f th e n e t ju s t b eh in d th e steel beam to determ ine th e exact tim e an d p o sitio n o f contact w ith the seabed. F rom th e m o m e n t o f con tact w ith the g ro u n d , the beam was tow ed at a speed o f a b o u t 1.5-2 kn o ts for 5 m in. A ltogether, 197 beam traw ls w ere taken betw een 1998 an d 2009. In general, n in e replicates were taken in each sam pling season b u t th e replicate n u m b e r varied betw een 3 (w in ter 2000) an d 13 (w inter 2004) according to w eather conditions. O n average, 8.9 rep li­ cates w ere taken. Samples w ere sieved th ro u g h 5 -m m m esh an d the epibenthic fau n a was separated fro m the rem ains. Species w ere identified o n b o a rd to th e lowest possible taxonom ic level a n d ab u n d an ce d ata w ere sta n ­ dardized to a to w length o f 250 m (area sam ­ pled = 500 m 2).

Tem perature data T he Federal M aritim e a n d H y d rographic Agency o f G er­ m an y (BSH) p rovided weekly sea surface tem p eratu re (SST) d ata at the H elgoland S tation (Hel; 54°9.6/ N,

7° 18.0' E) close to Box A. M o n th ly stan d ard ized tem p era­ tu re anom alies fro m 1998 to 2008 w ere calculated from th e H elgoland statio n based o n th e 1968-2008 m ean.

Biological tra it analysis (BTA) T he epifaunal dataset was reduced to th e 26 m o st d o m i­ n a n t species in term s o f ab u n d an ce an d occurrence in B ox A, previously described b y N eu m a n n et al. (2008a,b). These species w ere coded in a ‘species b y tra it table’ (Fig. 2) to th e extent they displayed th e categories o f 12 traits. C oding was done using a ‘fuzzy coding’ ap p roach w hich uses positive scores to describe th e affinity o f spe­ cies to tra it categories (C hevenet et al. 1994). In this study, a scoring range fro m 0 (n o affinity) to 4 (total affinity) was applied. For exam ple, th e sh rim p Crangon allm anni was coded 0 (p erm a n e n t attach ed ), 0 (tem p o ­ rally attach ed ), 1 (B urrow er), 2 (C raw ler) an d 1 (Sw im ­ m er) for th e tra it ‘ad u lt m ob ility ’. T en o f th e traits used (in clu d in g th e categories) w ere ad o p te d fro m Tillin et a í (2006) reflecting a w ide range o f ecological fu n ctio n an d life-history m odalities o f species. T he traits ‘fertilization ty p e’ (in tern al, external) a n d ‘rep ro d u ctiv e season’

S p e c ie s by trait table

S p e c ie s by station table 1998

1999

Aporrhais pespelecani

34

345

Asterias rubens

12

123

M obility

Perm attach

Temp. attach

Burrower

Craw|er

Swimmer

Aporrhais pespelecani

0

0

3

1

0

Asterias rubens

0

0

0

4

0

Trait

Categories

Mobility

Perm, attached; Temp, attached; Burrower; Crawler; Swimmer

Habitat

Infauna; Epifauna; Epizoic

Feeding type

Deposit; Filter/suspens.; Grazer; Scavenger; Predator

1. Multiply c a te g o ry s c o r e s with a b u n d a n c e d a ta 2. S u m c a te g o ry s c o r e s o v e r ta x a

Food type Size (cm)

Algae; Invertebr.A/ertebr.; Carrion; Detritus; Plankton; Suspend, org. matter; Microorg. small (1-2); small-medium (3-10); medium (11-20); medium-large (11-20); large (> 50)

Adult longevity (yr)

< 2 ; 2-5; 5-10; 10+

Age sexual maturity (yr)

< 2 ; 2-5; 5-10; 10+

Reprod. technique Reprod. frequency

Asexual; Sexual (spawner); Sexual (egg lay/brood mini adults); Sexual (egg lay/brood - plankt. larvae) Annual once; Annual (2 or more); Biennial; Semelparous

Reprod. season

Winter; Spring; Summer; Autumn

Dissemination

No pelagic life stage; Pelagic life stage; Low mobility adult; Highly mobile adult; Migratory

Fertilization type

Internal; External

Station by trait table 1998

1999

Perm. attach

23

0

Tem p. attach

0

587

Burrow er Craw ler Sw im m er

211

265

2395

115

0

135

Fig. 2. Stages of the biological trait analysis (BTA) including the trait variables with the corresponding num ber of categories used to describe eco­ logical functioning of the epifaunal community in Box A.

Marine Ecology 32 (Suppl. 1) (2011 ) 4 9 -5 7 © 2010 Blackwell Verlag GmbH

51

Effect o f te m p e r a tu re variability o n e p ifa u n a

N e u m a n n & K rö n ck e

2 .5 -

Fig. 3. Anomalies in SST (°) at the station Helgoland (Hel) close to Box A, based on the 1968-2008 mean.

(au tu m n , w inter, spring, su m m er) w ere ad d ed to focus o n the rep ro d u c tio n o f species, as tem p e ra tu re variability has a large im p act o n th e re p ro d u c tio n cycles o f species and o n b en thic-p elag ic coupling in th e N o rth Sea (e.g. Edw ards & R ichardson 2004; K irby et al. 2007, 2008). T rait category scores for each species presen t in a y ear/seaso n w ere th e n w eighted b y th eir ab u n d an ce in th a t year/seaso n b y m u ltiplying th e scores w ith a b u n ­ dance data an d th e n su m m in g th e resulting values over all species (Fig. 2). T he result is a ‘statio n b y tra it table’ w hich contains th e frequencies o f occurrence o f biological traits in each year an d season (Fig. 2). It is im p o rta n t to m e n tio n th a t th e BTA used here describes only a single aspect o f fu n ctio n in g as it does n o t include o th er co m p o n en ts o f th e ecosystem, n o r does it quantify processes o r properties. N o n -m etric m u ltid im en sio n al scaling (nm M D S) in th e PRIM ER v 6 package (P ly m o u th M arin e E aboratory) was applied to th e statio n -b y -tra it table based o n fo u rth ro o ttransform ed data. Sim ilarities w ere calculated using the B ray-C urtis coefficient. T his m e th o d describes th e sim i­ larities betw een th e years an d seasons in term s o f th eir tra it com p o sitio n an d is a p p ro p riate for p ro v id in g a gen­ eral p ictu re o f fu n ctio n in g in m arin e assem blages (B rem ­ ner et a í 2006). A n A N O SIM ran d o m iz atio n test was p erform ed to test th e differences in tra it co m p o sitio n betw een the years (H 0: n o differences in tra it co m p o si­ tion).

R esults SST temperature anomalies from 1995 to 2008 In general, th e tem p eratu re anom alies w ere m ainly above the lo n g -term m ean (1968-2008) at H elgoland S tation from 1995 to 2008 (Fig. 3). H ow ever, th e cold w in ter of 1995/96 was clearly reflected in stro n g negative SST anom alies fro m th e start o f 1996, w hich persisted u n til M ay 1997. Since 2002, th e positive SST anom alies have often persisted th ro u g h o u t th e year, an d w ere exception­ ally high d u rin g th e a u tu m n m o n th s in 2002-2006. For exam ple, th e highest yearly anom alies w ere fo u n d in Sep­ tem ber in 2002-2004 (2.1, 1.3 an d 0.9) an d in N ovem ber

52

a n d O ctober in 2005 an d 2006 (1.6 a n d 1.9). SST a n o m a ­ lies w ere exceptionally high at th e first h alf o f 2007 (Janu­ ary to June) ranging fro m 1.4 (June) to 2.1 (A pril), w hich (together w ith Septem ber 2002) is th e highest recorded anom aly at th a t statio n in 1995-2008.

Biological trait analysis (BTA) T he nm M D S analysis based o n fo u rth ro o t-tra n sfo rm ed tra it d ata revealed distinct changes in th e tra it c om posi­ tio n o f th e epifauna in Box A in 2002 (Fig. 4). T he A N O ­ SIM ran d o m iz a tio n test confirm ed significant differences in tra it co m p o sitio n betw een th e years 1998-2002 (w in­ ter) a n d 2002 (sum m er) to 2009 (R = 0.625, P < 0.001). T he dissim ilarity betw een these tw o p eriods was 21%. T he m o st im p o rta n t tra it categories co n trib u tin g to this dissim ilarity w ere categories w hich belonged to an o p p o r­ tunistic life m od e, such as sm all size, early onset o f sexual m a tu rity an d a sh o rt life span. T hus, th e relative a b u n ­ dance o f sm all species ( 1 - 2 cm ) w hich have a n age o f m a tu rity <2 years an d an a d u lt longevity o f 2 -5 years decreased co n tin u o u sly in th e first years an d seasons o f th e stu d y p erio d (Fig. 4). Shifts in tra it com position a ro u n d 2 0 0 2 w ere also evident in th e traits: ad u lt m o b il­ ity, feeding type, dissem ination, as well as reproductive type, -frequency an d -season (Fig. 5). For exam ple, the p ro p o rtio n o f deposit a n d filter-/su sp en sio n feeders was m u ch h igher before 2003 (5 2 -8 0 % ) w hereas grazers, scav­ engers a n d p articu larly p red ato rs w ere th e d o m in a n t feed­ ing m o d e after 2003 (7 3 -9 8 % ). A dditionally, the a b u n d an ce o f m ig rato ry species was h igher after 2003 (1 1-21% ) th a n in th e p erio d before 2003 (1 -7 % ). T raits such as a d u lt m obility, rep ro d u ctiv e type, reproductive frequency an d rep ro d u ctiv e season n o t only shifted betw een 2002 a n d 2003 b u t show ed th e highest p ercen t­ ages o r even a seasonality in th e p erio d o f th e w arm a u tu m n m o n th s (2002-2007). T he p ro p o rtio n o f sexual egg layers w ith a plank to n ic larvae peaked in w in ter 2005 (75% ) a n d 2006 (75% ) an d decreased slightly afterw ards. T he percentages o f species w hich h ad th eir reproductive season in a u tu m n an d rep ro d u ce tw ice (o r m ore) per year show ed a clear seasonality. T he highest ab u n d ance o f

Marine Ecology 32 (Suppl. 1) (2011) 4 9 -5 7 © 2010 Blackwell Verlag GmbH

Effect o f te m p e r a tu re variability o n e p ifa u n a

N e u m a n n & K rö n ck e

Small size (1-2 cm)

Age at sexual maturity <2 yrs

Adult longevity 2-5 yrs

Fig. 4. nmMDS plot o f biological tra it com position in Box A from 1998 to 2009 including summer and w in te r sampling (top left). nmMDS plot was overlaid w ith the relative occurrence o f the tra it categories 'small size (1 -2 cm)' (top right), 'age a t sexual m aturity <2 years' (bottom left) and adult longevity 2 -5 years (bottom right). Data were fou rth root-transformed.

F e e d in g typ e

A d u lt m o b ility

■Temp, attach. «Burrower

■Deposit feeder ■Filter/susp. feeder «Grazer

«Crawler «Swimmer

¡Scavenger «Predator

100%

80%

80%

60%

60%

40%

40%

20%

20% 0%

0% Cq

Cq ^

<0

<0

<0 ^

Cq ^

Cq ^

Co ^

Co ^

Co ^

Co ^

Co

s'

Cq Cq £.G q £.CO'£.Gq £.GQ'£.Gq £.OQ'£.Cq £.G q £.C q £.G q ?/# /e /$ /'S-/ '8 /< g>/8 /

R e p ro d u c tiv e ty p e

■Asexual budding

D is s e m in a tio n

No pelagic life stage High mobility

«Sexual spawner

■Sexual egg layer-planktonic larvae «Sexual egg layer-mini adults 100%

100%

80%

80%

60% 40%

■Pelagic life stage ■Migratory

Low mobility

MIII

40%

20%

I

0% co Co ^

Co ^

co ^

co £

co ^

cq

^

co

Co $

I

20% 0% co

o

Cq

Cq

Cq ^

Cq

Gq

« 0 ^

Cq £

Cq

Cq ^

Cq

• 's 'g 's 's 's '& '& 's 's 'g 'g 'ÿ '& 'y s '& 'è 'g 's 'g 's ' R e p r o d u c tiv e fre q u e n c y

3Annual once

«Annual (2 or more)

R e p r o d u c tiv e s e a s o n

«Biennial

■Semel parous

■Winter «Spring «Summer «Autumn

111111 111 1111

80% 60% 40%20% -

CO Cq ^

Co ^

Cq ^

Cq ^

Co ^

Cq ^

Oq ^

Co ^

Cq ^

Cq ^

Cq

# ' # ' s /S‘' s /S /3 '/3''/<3’'<3-'S/3 /g ' s /<3’' £ ' S /ê>'Sl'g /S ' Fig. 5. Percentages of trait categories of the trait variables adult mobility, feeding type, reproductive type, dissemination as well as reproductive frequency and -season in Box A from 1998 to 2009.

Marine Ecology 32 (Suppl. 1) (2011 ) 4 9 -5 7 © 2010 Blackwell Verlag GmbH

53

Effect o f te m p e r a tu re variability o n e p ifa u n a

these species was fo u n d in w in ter 2003 to w in ter 2007, correlating to th e w inters follow ing exceptional w arm a u tu m n m onths.

D iscussion The shift in tra it co m p o sitio n in 2002 largely coincided w ith shifts in th e epifaunal species co m p o sitio n in Box A (N eu m an n et al. 2008a,b), w hich was also observed in th e shallow W est a n d N o rth Frisian coasts (N e u m an n et a í 2009a,b). In all these areas, exceptionally high abundances o f th e b rittle star Ophiura albida w ere fo u n d in 1998, w hich decreased in sub seq u en t years parallel to an increase in diversity, secondary p ro d u c tio n as well as abun d an ce an d biom ass o f o th er epifaunal species. The BTA revealed a decrease in traits related to a n o p p o rtu ­ nistic life m ode after su m m er 1998 (Fig. 4). T he p attern s fo u n d follow th e th eo ry o n th e effects o f distu rb an ce o n com m unities going back to th e m odels o f O d u m (O d u m 1969) and P earso n -R o sen b erg (P earson & R osenberg 1978). In th e P earso n -R o sen b erg m odel, th e second stage in the faunal succession was characterized b y th e ap p ea r­ ance o f o p p o rtu n istic species, w hich w ere able to recolonize a d isturbed h a b itat faster th a n K-selective species. The o p p o rtu n istic life m o d e (r-strategy) involves increased rep rod u ctiv e effort th ro u g h early onset o f m a tu ­ rity, sh o rt life sp an a n d sm all b o d y size (H eip 1995) p ro ­ viding a selective advantage in d istu rb ed enviro n m en ts by utilizing free resources faster th a n others. T hus, th e decrease in sm all species ( 1 - 2 cm ) w ith an age o f m a tu ­ rity <2 years a n d an a d u lt longevity o f 2 -5 years co n ­ firm ed (according to th e BTA) th a t th e c o m m u n ity in Box A was at a succession stage betw een th e o p p o rtu n istic dom inance a n d th e established c o m m u n ity betw een 1998 and 2002. T he occurrence o f seasonal v ariatio n fo rm ed a decisive p a rt o f ‘persistence stability’ in b en th ic c o m m u ­ nities follow ing catastrophic events in tem p erate areas w ith a highly dynam ic physical regim e (A rntz & R u m o h r 1982). Seasonality was fo u n d for th e traits reproductive frequency an d rep ro d u ctiv e season since 2003, b u t o th er traits also show conspicuous changes betw een 2 0 0 2 an d 2003 (Fig. 5). For instance, th e p ro p o rtio n s o f p redators, scavengers an d grazers w ere m u ch higher after w in ter 2003, w hereas those o f deposit a n d filter/su sp en sio n feed­ ers decreased. In co n ju n ctio n w ith th e shift in overall tra it com p o sitio n in 2 0 0 2 , this indicated a shift in th e c o m m u ­ n ity fro m th e d isturbance stage after th e cold w in ter of 1995/96 to the recovery stage betw een 2002 a n d 2003. T hus, the variability o f tra it co m p o sitio n u n d erp in s th e hypothesis th a t th e cold w in ter resulted in th e o u tb reak o f o p p o rtu n ists, follow ed b y characteristic p o st-d istu rbance succession stages to th e p o in t o f an established c o m m u n ity in 2002/2003 (N e u m a n n et al. 2008a,b ). The

54

N e u m a n n & K rö n ck e

effect o f cold w inters o n ecosystem s was less clear in the later years d u e to th e clear response o f ecosystem co m p o ­ n en ts to th e w arm in g o f th e N o rth Sea. H ow ever, cold w inters are also p a rt o f clim ate variability an d th eir im pacts have been observed in lo n g -term records o f p lan k to n (M artens & van B eusekom 2008) a n d benthic in faun a (K röncke et al. 1998; S chröder 2005). T he cu rren t stu d y revealed th a t th e recovery tim e o f epifaunal co m ­ m u n ities after cold w inters was 7 -8 years, co m p ared to a m u ch faster recovery in p lan k to n co m m u n ities ( < 1 year) an d b en th ic in fau n a co m m u n ities (2 -5 years) in the G er­ m an Bight (S chröder 2003; M artens & van B eusekom 2008). T he pro lo n g ed recovery tim e o f epifauna in shal­ low, w ell-m ixed areas has im p o rta n t im plications for the assessm ent o f ecosystem health an d consequently for m an ag em en t a n d conservation strategies. Succession o f th e epifaunal c o m m u n ity in Box A was m ainly driven b y bio tic factors such as tro p h ic in terac­ tions (N eu m an n et al. 2008a,b ). D u rin g o u r study, SST anom alies at th e statio n close to Box A w ere m ainly above th e lo n g -term m ean o f 1968-2008, w ith ex ception­ ally high anom alies in th e a u tu m n m o n th s o f 2002-2006. It is obvious th a t traits related to th e re p ro d u c tio n o f spe­ cies such as rep ro d u ctiv e type, -frequency a n d -season have sh o w n a clear response to these high a u tu m n w ater tem peratures. T hus, a high p ro p o rtio n o f sexual egg layers w ith p lan k to n ic larvae w ere fo u n d d u rin g th e p erio d o f high a u tu m n anom alies. A dditionally, higher abundances o f species w hich rep ro d u ce in a u tu m n an d are able to rep ro d u ce tw ice a year w ere fo u n d in th e w inters after th e w arm a u tu m n m o n th s. D irect positive effects o f te m ­ p eratu re o n key stages o f re p ro d u ctio n are well know n for m an y species w hich w ere fo u n d in Box A. For exam ­ ple, th e larval developm ent o f th e sw im m ing crab Liocar­ cinus holsatus (fro m h atch in g to m etam o rp h o sis) is faster w ith increasing tem p e ra tu re (C hoy 1991). F u rth erm ore, th e d u ra tio n o f th e larval stage as well as th e frequency o f breeding o f Pandalus spp. is positively linked to tem p era­ tu re (B ergström 2000), as has also been observed in other caridean species (W ear 1974). H en d erso n et al. (2006) fo u n d th a t th e re cru itm en t o f th e sh rim p Crangon cran­ gon in a u tu m n was correlated to SST an d th e w inter index o f th e N o rth A tlantic O scillation. Sim ilar changes w ere also observed in p lan k to n co m m un ities w here, in particular, ech in o d erm an d decapod larvae w ere fo u n d in higher abundances a n d /o r earlier due to tem p eratu rein d u ced shifts in th e re p ro d u ctio n cycle o f benthic species (Lindley et al. 1993; Greve et al. 2001; Edw ards & R ich­ ard so n 2004; K irby et al. 2007; R ichardson 2008). In co ntrast to traits related to rep ro d u c tio n , traits such as feeding type an d dissem ination show ed n o obvious response to th e exceptional w arm SST in a u tu m n b u t a clear shift in w in ter 2003 (w hen th ere was a higher

Marine Ecology 32 (Suppl. 1) (2011) 4 9 -5 7 © 2 0 1 0 Blackwell Verlag GmbH

Effect o f te m p e r a tu re variability o n e p ifa u n a

N e u m a n n & K rö n ck e

p ro p o rtio n o f p red ato rs, scavengers, grazers an d m ig ra­ to ry species) in relatio n to overall positive anom alies of SST. H ow ever, it was difficult to d eterm in e w h eth er these changes could be a ttrib u te d to th e clim ate-induced v ari­ ability o f SST o r w heth er th e tra it com positions ju st reflect the stage o f th e c o m m o n c o m m u n ity follow ing the succession after th e cold w inter. As N eu m a n n et a í (2008a,b, 2009a,b) argued th a t th e epifauna in th e shallow S outheastern N o rth Sea w ere influenced b y increased food supply d ue to a m u ch longer p erio d o f p rim a ry p ro d u c ­ tio n in co n ju n ctio n w ith higher SSTs (H ughes & H olliday 2007), we expected higher p ro p o rtio n s o f organism s such as deposit feeders in this study, b u t th a t was n o t th e case. H ow ever, th e increased a b u n d an ce o f epifaunal p red ato rs m ig h t be a ttrib u ted to h igher abundances of, for exam ple, deposit feeders o f low er tro p h ic levels {i.e. benthic infauna, m eiofauna) w hich in tu rn benefited from increased foo d supply. T hus, a higher p ro p o rtio n o f p re ­ dators since 2003 in Box A m ig h t also be a ttrib u te d to clim ate-induced tem p e ra tu re increase, especially as H e n ­ derson et a í (2006) also suggested th a t th ere m u st also be an increase in food availability if an increase o f larval developm ent due to h igher tem p e ra tu re is to be translated in to higher recruitm en t. The results o f th e BTA p rim arily revealed a greater im p act o f tem p era tu re variability o n traits related to rep ro d u ctio n th a n o n feeding traits in Box A. T herefore, w e assum ed th a t th e clim ate-induced tem p eratu re v ari­ ability indeed h ad a greater influence o n th e rec ru itm e n t o f epifauna th a n o n th e fo o d availability in th e stu d y area. In contrast, fo o d supply was fo u n d to be an im p o r­ ta n t factor influencing epifaunal species in th e n o rth e rn , stratified N o rth Sea (N e u m a n n et al. 2009a,b ), w hich w ere regarded to be fo o d lim ited (Davies & Payne 1984). F u rth er analysis, in clu d in g o u r data fro m th e N o rth ern N o rth Sea, sho uld be used to test these hypothesized functional differences betw een th e N o rth e rn an d S ou th ern N o rth Sea. W e are aw are th a t we will have m issed som e aspects of fu n ctio n in g as we excluded rare species in th e BTA an d th u s th eir c o n trib u tio n to functionality. A dditionally, we do n o t cover all aspects o f fu n ctio n in g due to th e choice o f only 12 functio n al traits in th e BTA. Two expert w orkshops in P lym o u th a n d L o n d o n have identified 10 key aspects o f m arin e system fu n ctio n in g a n d 24 co rre­ sp o n d in g functional traits for th e BTA (Frid et a í 2008). W e excluded traits such as ‘Energy transfer efficiency’ or ‘Intra-specific sociability’ to reduce th e d em an d for fu n c­ tio nal data, w hich w ere m ostly im possible to get. H o w ­ ever, this does n o t greatly affect o u r conclusions. The definition o f fu nction in g b y Jax (2005) given in the in tro d u c tio n em phasizes b o th processes an d th e role of single com ponents. A lthough o u r stu d y only inco rp orates

Marine Ecology 32 (Suppl. 1) (2011 ) 4 9 -5 7 © 2010 Blackwell Verlag GmbH

fu n ctio n al aspects o f one single co m p o n en t (th e benthic epifauna), it provides useful in fo rm atio n o n h o w the fu n ctio n al co m p o sitio n o f epifauna was linked to envi­ ro n m e n ta l changes. B ut th ere is an obvious need for holistic studies th a t include m o re b iotic c o m p o n en ts as well as ecological processes.

A c k n o w le d g e m e n ts W e th a n k th e captains an d crews o f RV W alther Herwig II I for th eir assistance d u rin g sam pling. W e gratefully acknow ledge th e Federal Research In stitu te for R ural Areas, Forestry an d Fisheries for p ro v id in g ship tim e an d data. In particular, w e th a n k A chim Schulz (BSH) for p ro v id in g tem p e ra tu re data. T he p resen t stud y was p re­ p ared at th e B iodiversity an d C lim ate R esearch C entre (BiK-F), F rankfurt a.M ., an d financially su p p o rted b y the research fu n d in g p ro g ram m e ‘LOEW E -L andes-O ffensive z u r E ntw icklung W issenschaftlich-ökonom ischer Exzel­ lenz’ o f H esse’s M in istry o f H ig h er E ducation, Research, a n d th e Arts.

R eferen ces A rntz W .E., R um ohr H. ( 1982) A n experim ental study o f m acrobenthic colonization a n d succession, and the im portance o f seasonal variation in tem perate latitudes. Journal o f Exper­ imental M arine Biology and Ecology, 64, 17-45. B eaugrand G. (2004) The N o rth Sea regim e shift: evidence, causes, m echanism s and consequences. Progress in Oceanog­ raphy, 60, 245-262. Bell J.J. (2007) C ontrasting patterns o f species and functional com position o f coral reef sponge assemblages. M arine Ecol­ ogy Progress Series, 339, 73-81. B ergström B.I. (2000) The biology o f Pandalus. Advances in M arine Biology, 38, 55-245. Beukem a J.J. ( 1992) Expected changes in the W adden Sea b e n ­ thos in a w arm er world: lessons from periods w ith m ild w inters. Netherlands Journal o f Sea Research, 30, 73-79. Brander K., Blom G., Borges M.F., Erzini K., H enderson G., M acKenzie B.R., M endes H., Ribeiro J., Santos A.M.P., Toresen R. (2003) Changes in fish d istribution in the eastern N o rth Atlantic: are we seeing a coherent response to changing tem perature? ICES M arine Science Symposia, 219, 261-270. Brem ner J. (2008) Species’ traits and ecological functioning in m arine conservation and m anagem ent. Journal o f Experi­ mental M arine Biology and Ecology, 366, 37-47. B rem ner J., Frid C.L.J., Rogers S.I. (2003a) Assessing m arine ecosystem health: the long-term effects o f fishing o n func­ tional biodiversity in N o rth Sea benthos. Aquatic Ecosystem Health & M anagement, 6, 131-137. B rem ner J., Rogers S.I., Frid C.L.J. (2003b) Assessing func­ tional diversity in m arine benthic ecosystems: a com parison o f approaches. M arine Ecology Progress Series, 254, 11-25.

55

Effect o f te m p e r a tu re variability o n e p ifa u n a

B rem ner J., Frid C.L.J., Rogers S.I. (2005) Biological traits o f

H ooper D.U., Solan M., Symstad A., Diaz S., Gessner M .O.,

the N o rth Sea benthos: does fishing affect benthic ecosystem

B uchm ann N., Degrange V., Grim e P., H u lo t F., M erm illod-

function? American Fisheries Society Symposium, 41, 4 77-

B londin F., Roy J., Spehn E., van Peer L. (2002) Species

489.

diversity, functional diversity, and ecosystem functioning.

B rem ner J., Rogers S.I., Frid C.L.J. (2006) M ethods for describ­ ing ecological functioning o f m arine benthic assemblages using biological traits analysis (BTA). Ecological Indicators, 6, 609-622. Buchanan J.B., M oore D.C. (1986) L ong-term studies at a b e n ­ thic station off the coast o f N orthum berland. Hydrobiologia,

142, 121-127. Chevenet F., Doledec S., Chessel D. (1994) A fuzzy coding

In: Loreau M., N aeem S., Inchausti P. (Eds), Biodiversity

and Ecosystem Functioning: Synthesis and Perspectives. O xford U niversity Press, New York: 195-208. H ughes S.L., H olliday N.P. (2006) ICES Report on Ocean Cli­

mate 2005. ICES Cooperative Research Report. R eport No. 280, In ternational C ouncil for the E xploration o f the Sea, Copenhagen. H ughes S.L., H olliday N.P. (2007) ICES Report on Ocean Cli­

approach for the analysis o f long-term ecological data.

mate 2006. ICES Cooperative Research Report. R eport No.

Freshwater Biology, 31, 295-309.

289, In ternational C ouncil for the E xploration o f the Sea,

C hoy S.C. (1991) E m bryonic a n d larval biology o f Liocarcinus

holsatus a n d Necora puber (Crustacea: Brachyura: P o rtu n i­ dae). Journal o f Experimental Marine Biology and Ecology, 148, 77-92. Davies J.M., Payne R. (1984) Supply o f organic m atter to the

Copenhagen. Jax K.. (2005) F unction a n d “ functioning” in ecology: w hat does it mean? Oikos, 111, 641-648. Kirby R.R., B eaugrand C., Lindley J.A., R ichardson A.J., Edwards M ., Reid P.C. (2007) Clim ate effects a n d benthic-

sedim ent in the n o rth ern N o rth Sea during a spring phy to ­

pelagic coupling in the N o rth Sea. Marine Ecology Progress

plankton bloom . Marine Biology, 78, 315-324.

Series, 330, 31-38.

Diaz S., Cabido M. (2001) Vive la difference: p lant functional diversity m atters to ecosystem processes. Trends in Ecology

& Evolution, 16, 646-655. Edwards M., R ichardson A.J. (2004) Im pact o f clim ate change on m arine pelagic phenology and trophic m ism atch. Nature,

430, 881-884. Edwards M., Johns D.G., B eaugrand C., Licandro P., John A.W.G., Stevens D.P. (2008) Ecological Status Report: Results

from the CPR Survey 2006/2007., SAHFOS, Plym outh. E hrich S., Stransky C. (2001) Spatial a n d tem poral changes in the southern species co m p o n en t o f N o rth Sea fish assem ­ blages. Senckenbergiana Maritima, 31, 143-150. E hrich S., A dlerstein S., B rockm ann U., Floeter J., G arthe S.,

Kirby R.R., B eaugrand C., Lindley J.A. (2008) C lim ate-induced effects o n the m eroplankton and the benthic-pelagic cou­ pling ecology o f the N o rth Sea. Limnology and Oceanogra­

phy, 53, 1805-1815. Kröncke I., D ippner J.W., Heyen H., Zeiss B. (1998) Long­ term changes in m acrofaunal com m unities off N orderney (East Frisia, Germ any) in relation to clim ate variability.

Marine Ecology Progress Series, 167, 25-36. Lindley J.A., W illiam s R., H u n t H.G. (1993) A nom alous sea­ sonal cycles o f decapod crustacean larvae in the N o rth Sea plankton in an abnorm ally w arm year. Journal o f Experimen­

tal Marine Biology and Ecology, 172, 47-65. M artens P., van Beusekom J.E.E. (2008) Z ooplankton response

H inz H., Kröncke I., N eum ann H., Reiss H., Sell A.F., Stein

to a w arm er n o rth ern W adden Sea. Helgoland Marine

M., Stelzenm üller V., Stransky C., T em m ing A., W egner G.,

Research, 62, 67-75.

Zauke G.P. (2007) 20 years o f the G erm an Small-Scale B ot­ to m Trawl Survey (GSBTS): a review. Senckenbergiana Mari­

tima, 37, 13-82. Frid C.L.J., P aram or O.A.L., B rockington S., B rem ner J. (2008) Incorporating ecological functioning into the designation

M ouillot D., D um ay O., T om asini J.A. (2007) Lim iting sim i­ larity, niche filtering and functional diversity in coastal lagoon fish com m unities. Estuariae Coastal and Shelf Science, 4, 443-456. N eum ann H., E hrich S., Kröncke I. (2008a) The effects o f cold

and m anagem ent o f m arine protected areas. Hydrobiologia,

w inters and clim ate o n the tem poral variability o f an epi-

606, 69-79.

benthic c om m unity in the G erm an Bight. Climate Research,

Greve W ., Lange U., Reiners F., N ast J. (2001) Predicting the seasonality o f N o rth Sea Z ooplankton. Senckenbergiana

Maritima, 31, 263-268. G rim e J.P. (1997) Biodiversity and ecosystem functioning: the debate deepens. Science, 277, 1260-1261. H eip C. (1995) E utrophication a n d zoobenthos dynamics.

Ophelia, 41, 113-136. H enderson P.A., Seaby R.M., Somes J.R. (2006) A 25-year study o f clim atic a n d density-dependent p opulation regula­

56

N e u m a n n & K rö n ck e

37, 241-251. N eum ann H., E hrich S., Kröncke I. (2008b) Spatial variability o f epifaunal com m unities in the N o rth Sea in relation to sam pling effort. Helgoland Marine Research, 62, 215-225. N eum ann H., E hrich S., Kröncke I. (2009a) The effect o f increasing tem perature o n epibenthic com m unities and spe­ cies in the n o rth ern N o rth Sea. Marine Biology, 156, 1817— 1826. N eum ann H., Reiss H., Rakers S., Ehrich S., Kröncke I.

tio n o f co m m o n shrim p Crangon crangon (Crustacea: Cari­

(2009b) T em poral variability o f sou th ern N o rth Sea epi­

dea) in the Bristol Channel. Journal of the Marine Biological

fauna com m unities after the cold w inter 1995/1996. ICES

Association o f the United Kingdom, 86, 287-298.

Journal o f Marine Science, 66, 2233-2243.

Marine Ecology 32 (Suppl. 1) (2011) 4 9 -5 7 © 2010 Blackwell Verlag GmbH

Effect o f te m p e r a tu re variability o n e p ifa u n a

N e u m a n n & K rö n ck e

O dum E.P. ( 1969) The strategy o f ecosystem developm ent. Sci­

ence, 164, 262-270. Pearson T.H ., Rosenberg R. ( 1978) M acrobenthic succession in

Schröder A. (2005) C om m unity dynam ics and developm ent o f soft b o tto m m acrozoobenthos in the G erm an Bight (N orth Sea) 1969-2000. Report of Polar Research, 494, 1-181.

relation to organic enrichm ent and pollution o f the m arine

Sims D .W ., G enner M.J., Southw ard A.J., H aw kins S.J. (2001)

environm ent. Oceanography and Marine Biology. An Annual Review, 16, 229-311.

variability. Proceedings. Biological Sciences/The Royal Society,

Perry A.L., Low P.J., Ellis J.R., Reynolds J.D. (2005) Clim ate change a n d d istribution shifts in m arine fishes. Science, 308, 1912-1915. Reiss H., M eybohm K., Kröncke I. (2006) C old w inter effects on benthic m acrofauna com m unities in near- a n d offshore regions o f the N o rth Sea. Helgoland Marine Research, 60, 224-238.

T im ing o f squid m igration reflects N o rth Atlantic clim ate

268, 2607-2611. Tillin H.M ., H id d in k J.G., Jennings S., Kaiser M.J. (2006) C hronic b o tto m traw ling alters the functional com position o f benthic invertebrate com m unities o n a sea-basin scale.

Marine Ecology Progress Series, 318, 31-45. W ear R.G. (1974) Incubation in British decapod crustacea, and the effects o f tem perature on the rate and success o f

change. ICES Journal of Marine Science, 65, 279-295.

em bryonic developm ent. Journal o f the Marine Biological Association of the United Kingdom, 54, 745-762.

Schratzberger M ., W arr K., Rogers S.I. (2007) Functional

Ziegelm eier E. (1970) U ber M assenvorkom m en verschiedener

R ichardson A.J. (2008) In h o t water: Zooplankton a n d clim ate

diversity o f nem atode com m unities in the southw estern

m akrobenthaler W irbelloser w ährend der W iederbesied­

N o rth Sea. Marine Environmental Research, 63, 368-389.

lungsphase nach Schädigungen du rch ‘katastrophale1

Schröder A.. (2003) C om m unity dynam ics a n d developm ent o f soft b o tto m benthos in the G erm an Bight (N o rth Sea)

Um welteinflüsse. Helgoländer wissenschaftliche Meeresunter­

suchungen, 21, 9-20.

1969-2000. Ph.D . thesis, U niversity Brem en (G erm any).

Marine Ecology 32 (Suppl. 1) (2011 ) 4 9 -5 7 © 2010 Blackwell Verlag GmbH

57

marine ecology

an evolutionary perspective

<

M arine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

Zoobenthos as an environmental quality element: the ecological significance of sampling design and functional traits Katri A a rn io , J o h a n n a M attila , A n n a T ö r n r o o s & Erik B o n sd o r ff Departm ent of Biosciences, Environmental and Marine Biology & Huso Biological Station, Abo Akademl University, Turku, Finland

Keywords

Brackish w ater benthic Index; biological traits analysis; ecological status; sampling methodology; w ater frame directive; zoobenthos. Correspondence

Katri Aarnio, D epartm ent of Biosciences, Environmental and Marine Biology & Huso biological station, Abo Akademi University, FI-20S00 Turku, Finland. E-mail: [email protected] Accepted: 25 November 2010 doi:10.1111/j. 1439-0485.2010.00417.x

A bstract T he EC W a te r Fram e D irective (W FD ) states th a t all coastal w ater bodies m u st achieve ‘g o o d ecological sta tu s’ b y th e year 2015. A range o f different classifica­ tio n m eth o d s have been developed a n d used to define ecological status to su p ­ p o rt th e W FD . The aim o f this stu d y was to co m p are th e effects o f using tw o different m esh sizes o f sieve (1.0 a n d 0.5 m m ) o n zoobenthic assem blages and o n th e ecological status o f b en th ic m acro fau n a (using th e Brackish w ater b en th ic index, BBI) in th ree ecologically d istinct archipelago areas (In n er, M id ­ dle an d O u ter) in th e A land Islands, N o rth e rn Baltic Sea. W e p erfo rm ed a b io ­ logical tra it analysis (BTA) to evaluate differences in th e fun ctio n al (trait) diversity o f m acro fau n a collected using different m esh sizes an d estim ate the ecological relevance o f m esh size. The results show ed th a t sieve m esh size had significant effects o n th e recorded n u m b e r o f species, ab u n dan ce, a n d total b io ­ m ass o f th e zoobenthos. Sm all-bodied species an d juveniles (e.g. M acom a balth­ ica) w ere n o t observed w hen using a 1.0-m m m esh. T he ecological status (sensu W FD ) was only slightly affected b y th e m esh size, a n d all areas h ad good o r high ecological status. BTA show ed a difference in tra it co m p o sitio n w hen using 0.5- or 1.0-m m m esh, p articularly in th e O u te r area, w here th e p ro p o r­ tio n o f sm all-sized species was high. O u r results highlight how biological traits, in a d d itio n to species n u m b e r an d biom ass, can play a key role w hen analyzing ecosystem stru c tu re for assessm ent a n d classification o f coastal ecosystems. W e show th a t com b in in g trad itio n a l m o n ito rin g for th e EU W FD w ith a fu nctional analysis strengthens o u r ability to in te rp re t enviro n m en tal quality, a n d thus increases th e p recision o f o u r advice for m an ag em en t purposes.

Introduction E u tro p h icatio n is one o f th e m o st severe en v ironm ental issues in the N o rth e rn Baltic Sea, affecting b o th pelagic and b enthic environm ents, in shallow an d deep areas (E lm gren 1989; B o nsdorff et al. 1997; H EL C O M 2009). Z oobenthos is w idely used as an in d icato r o f change in environm ental conditions, as th e organism s are relatively statio n ary and several species live for m an y years. T hus changes in enviro n m en tal co n d itio n s are reflected in zoobenthos as altered c o m m u n ity p aram eters. Increased

58

d isturbance o f coastal areas leads to changes in species n u m b e r a n d th e co m p o sitio n o f assemblages, as well as in th eir ab u n d an ce an d biom ass (P earson & R osenberg 1978; C ederw all & Elm gren 1980; D iaz & R osenberg 1995; N orkko & B o nsdorff 1996; B o nsdorff & Pearson 1999; P erus & B o nsdorff 2004). In th e N o rth e rn Baltic Sea, th e n u m b e r o f benthic spe­ cies is low p rim arily d u e to brackish w ater conditions (salinities vary betw een 3 an d 7 psu). Species are either o f m arin e o r lim nic origin an d th ey live at th e lim its o f th eir physiological tolerance (B onsdorff 2006). D ue to the low

Marine Ecology 32 (Suppl. 1) (2011) 58-71 © 2 0 1 0 Blackwell Verlag GmbH

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

A arnio, M attila, T örnroos & B onsdorff

salinity, th e organism s are sm all in size com p ared w ith th eir relatives in fully m arin e areas. H ence, th e size-spectru m o f benthic organism s is narrow , an d m o st organism s have an a d u lt size sm aller th a n a few centim eters (although certain polychaetes m ay reach 1 0 cm in length). To fully illustrate a n d u n d e rsta n d co m m u n ity dynam ics, individuals’ size m u st be considered a priori w hen choos­ ing m eth o d s for th e study. Sieve m esh sizes o f 1 m m or m o re are w idely used for b en th ic surveys in m arin e areas (B orja et al. 2009 a n d references th erein ), w hile a 0 .5 -m m sieve m esh is m o re often used in local studies in the N o rth e rn Baltic Sea (Perus et al. 2007). A ssessm ents o f an th ro p o g en ic effects o n benthic sys­ tem s have m ostly been based o n taxo n o m ic co m p o sitio n an d relative abund an ce o f taxa, w hich are still valuable an d easy to com p reh en d , serving as a base for fu rth er assessm ents (B lom qvist & B o nsdorff 1986; B o nsdorff & B lom qvist 1993; P erus & B o nsdorff 2004). H ow ever, recent studies have q uestioned th e use o f only species n u m b e r an d o th er basic param eters as m easures o f eco­ system health an d functio n in g , especially as m arin e b e n ­ thic system s h a rb o u r great n u m b ers o f phyla for w hich the taxonom ic divisions are still u n c erta in (W arw ick & Som erfield 2008). The increasing need for b ro ad en in g of the quality concept for hab itats o r coastal areas an d accepting the im p o rtan ce o f ecosystem functioning, has p ro m o te d a scientific an d applied discussion a b o u t p res­ ent quality indices, w h at they describe an d h o w th ey fit m o d e rn m anagem en t approaches (Frid et al. 2008; Tillin et al. 2008; Borja et al. 2009). T he ability o f m an ag em en t directives (e.g. sam pling m eth o d s), ecological indices an d o th er m easures o f an th ro p o g en ic stress to encom pass dif­ ferent scales o f fu n ctio n in g a n d biodiversity d u rin g eco­ system change has been questioned. For exam ple, the c o n trib u tio n o f som e species to th e fu n ctio n in g o f the ecosystem m ay decrease a n d th a t o f o th er species increase d u rin g environm en tal change, an d to include this requires an ap p ro p riate tim e a n d spatial sam pling scale (T h ru sh et al. 1997, 2000; Yachi & L oreau 1999; Stachow icz et al. 2002). F urther, organism s th a t ap p ear to p erfo rm sim ilar roles m ay n o t always resp o n d to stress in th e sam e way (R am say et a í 1998). H ence, th e n ext step is to connect the changes in abiotic characteristics o f th e h a b ita t or environm ent, the n u m b e r an d ab u n d an ce (o r biom ass) of species (species diversity) an d th e fu n ctio n in g o f these species (fun ctional diversity) in o rd er to best identify and direct m anagem ent efforts (B rem ner et a í 2003; Jax 2005; B rem ner 2008). A ccording to th e EU W ate r Fram e D irec­ tive (2 000 /60/E G ; W FD ) all coastal w aters sh o u ld achieve a good ecological status b y 2015. For this purp o se, w ater areas are being classified using biological q uality elem ents (m acrophytes, ph y to p lan k to n , zoobenthos) an d divided in to five classes o f ecological status: high, good, m oderate,

Marine Ecology 32 (Suppl. 1) (2011) 58-71 © 2010 Blackwell Verlag GmbH

p o o r an d b ad (2 0 0 0 /6 0 /E G W FD ; Borja et a í 2000; R osenberg et a í 2004; P erus et al. 2007; Josefsson et a l 2009). As th e EU W FD classifies th e entire Baltic Sea as one eco-region, this im plies th a t th e sam e q uality ele­ m en ts a n d indicators should be valid across th e entire sea. As has been show n in n u m ero u s recen t studies, this is n o t th e case (Perus & B o nsdorff 2004; L eonardsson et al. 2009; R osenberg et al. 2009). N o t only m ust species-sensitivity values be set according to regional ecological baselines, b u t also indicato rs o th er th a n ju st p resence/absence, ab u n d an ce a n d biom ass m u st be included. O ne p o ten tial w ay forw ard is to include fu n ctio n in g (cf. B onsdorff & P earson 1999) an d specific biological traits (B rem ner 2008). In th e case o f th e N o rth ­ ern Baltic Sea species, size m u st also be considered. T he aim o f this stu d y was to investigate how different m esh sizes o f sieve affect th e results o f b en th ic studies b o th stru ctu rally an d functionally. W e stu d ied th e effects o f m acro fau n a assem blage observations, using tw o sieve m esh sizes: 1.0 o r 0.5 m m . T he effects w ere m easu red on basic c o m m u n ity p aram eters, as well as o n th e ecological status o f th e en v iro n m en t, along an enviro n m en tal gradi­ en t fro m in n e r to o u ter archipelago using a specially developed index, th e brackish w ater b en th ic index (BBI; P erus et al. 2007). In a d d itio n we p erfo rm ed a biological tra it analysis (BTA; B rem ner et a í 2003) to evaluate dif­ ferences in fu nctional (trait) diversity o f different m esh sizes an d estim ated th e ecological relevance o f m esh size choice in relatio n to th e selected m acro-habitats.

S tu d y A reas T he field sam pling for this stu d y was co n d u cted in three areas (m acro -h ab itats) o f different exposure a n d degree of organic in p u t to th e sedim ents in th e A land archipelago (N Baltic Sea): In n er, M iddle an d O u te r archipelago areas (Fig. 1). T he In n er area was sheltered fro m th e o p en sea a n d h ad lim ited w ater exchange. It was directly affected b y h u m a n activities, m ain ly agriculture a n d fo o d industry. T he M iddle area was sem i-exposed a n d m oderately affected b y local sources o f eu tro p h icatio n . T he O uter area was exposed to th e o p en sea w ith high w ater exchange rates. It was only slightly affected b y local h u m a n activities, an d h ad low n u trie n t levels in co m p ari­ so n w ith th e o th e r areas studied. T he sed im en t quality ranged fro m san d /g rav el in th e O u ter exposed areas, w ith low organic co n ten t (m ean 1 .8 %) to cla y /m u d w ith high organic co n ten t (m ean 5.6%) in th e In n er sheltered areas (Table 1). The entire region (Fig. 1) has been th o ro u g h ly stu d ied for b en th ic in fau n a since th e early 1970s an d th ere w ere com prehensive records o f th e benthic assem ­ blages in these areas (e.g. H elm in en 1975; B o n sd o rff et a í 1991, 2003; P erus et al. 2001; P erus & B o nsdorff 2004).

59

Z o o b e n th o s as an e n v iro n m e n ta l q u ality e le m e n t

A arnio, M attila, Törnroos & Bonsdorff

Riiiand

Fig. 1. Map of the study areas in the Aland archipelago, Northern Baltic Sea. I, Inner area; M, Middle area; 0 , Outer area.

T able 1. Site characteristics of the three archipelago areas. The four variables, Depth, Salinity, Oxygen (02%) in bottom w ater and Organic con­ ten t in sediment are presented as: mean (min-max), the variable Dominating sediment type with the following abbreviations; C, clay; M, mud; S, sand; G, gravel. Archipelago area Site characteristics

Inner

Middle

Outer

Depth m

10.7 (5-16)

11.2 (6-27)

14 (4-26)

Salinity, %0 0 2% in bottom w ater Dominating sediment type Organdie content in sediment (loi), %

5.6 (5.6-5.7) 86 (80-91)

5.6 (5.3-5.8) 93 (87-99)

6.0 (5.4-6.2) 94 (86-113)

C, MC 5.6 (2.7-8.6)

C, MC, CG 5.5 (0.9-9.2)

CS, S, SG 1.8 (0.4-10.7)

M aterial and M eth o d s Sam pling was co n d u cte d betw een 14 A ugust 2007 an d 7 Septem ber 2007 w hen th e anim al su m m er-recru itm en t h ad occurred. In all areas, zoobenthic sam ples were taken using an E km an-B irge grab sam pler (289 cm 2) from tw o d ep th zones: < 1 0 m (hereafter called ‘shallow ’) an d > 1 0 m (hereafter called ‘d eep ’). Five replicate sam ples were taken from six stations in each area; three o n shallow an d three o n deep b o ttom s. The sam ples were sieved th ro u g h b o th

60

1.0- an d 0.5-m m screens (rep o rted as 1.0 an d 0.5 m m pooled). Fauna were identified to th e low est possible tax o ­ n o m ic level, co u n ted an d w eighed (w et w eig h t). The length o f individual M acom a balthica was m easured to th e nearest m m for estim ates o f p o p u la tio n stru ctu re an d recru itm en t success. A p aired i-test was used to co m pare th e n u m b e r o f species, abu n d an ce an d biom ass betw een th e 0.5- an d 1.0m m m esh results in the different d ep th zones an d areas. An overall analysis o f m esh size effects was do n e using tw ow ay ANOVA, w ith sieves (0.5 an d 1.0 m m ) an d areas

Marine Ecology 32 (Suppl. 1) (2011) 58-71 © 2010 Blackwell Verlag GmbH

A arnio, M attila, T örnroos & B onsdorff

(Inner, M iddle, O u ter) as factors. P rio r to th e analyses, d ata w ere log (x + 1 ) tran sfo rm ed if th ey did n o t m eet the assum ptions o f n o rm a lity an d h o m o g en eity o f variances. All statistical analyses w ere p erfo rm ed using th e statistical an d graphical softw are GRAPH PAD PRISM , version 5.0.

Ecological status T he ecological statu s sensu W FD was m easured using the BBI eq u atio n 1 (Perus et al. 2007). It was a d o p ted from the b enthic quality index (BQI; R osenberg et al. 2004) an d adjusted for low -saline coastal areas, w ith low species n um bers, an d th e sensitivity values for th e species have been adjusted to th eir actual e n v iro n m en t (cf. R u m o h r et al. 1996). BBI follows th e a ssu m p tio n th a t biodiversity increases w ith increasing distance fro m a p o llu tio n source along a grad ient o f disturbance, an d can take values betw een 0 a n d rou g h ly 1 (P earson & R osenberg 1978; Perus et al. 2007).

w here BQI = b enth ic quality in d ex (sensu R osenberg et al. 2004); B Q Imax = m ax im u m B Q I-value reco rd ed w ith in each type after calculating all available data w ith in the n atio n al Finnish zo obenthos database ‘H e rtta ’ (h ttp :// w w w .ym paristo.fi); H ’ = S h an n o n -W ien er diversity index (log 2 -base); H ’max = m ax im u m H ’-value reco rd ed w ith in type after calculating all available d ata w ith in n ational zoo benthos database; AB = to tal ab u n d an ce at each station; an d S = n u m b e r o f sp ecies/taxa at each station.

Biological trait analysis (BTA) For the BTA we selected 10 specific traits representing the prin cipal aspects o f m o rphology, life-history, living-, feeding habit, an d m o v em en t o f th e stu d ied taxa (Table 2). These w ere chosen to m axim ize th e differences am o n g species o r taxa, an d th u s to elucidate representative tra it p attern s in sam pling design an d differences betw een areas. T he 10 traits w ere separated in to sub-categories, i.e. m odalities. Body design, for exam ple, was divided into v erm in ifo rm unsegm ented, v erm in ifo rm segm ented, bivalved, tu rb in ate an d articulate. T his resulted in a to tal o f 45 different tra it m odalities for th e species-pool selected (Table 2). T he division o f traits a n d categories was deduced from B o nsdorff & P earson (1999), P earson (2001), and B rem ner et a í (2003, 2006a,b ), an d revised an d applied to fit th e Baltic Sea b en th ic species (A. T ö rn ­ roos un p u b l. data).

Marine Ecology 32 (Suppl. 1) (2011 ) 58-71 © 2010 Blackwell Verlag GmbH

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

Individual taxa w ere th e n coded for th e extent to w hich th ey display th e m odalities in a scoring range betw een 0 a n d 3, w ith 0 being n o affinity to a m o d ality an d 3 being to tal affinity. T he category scores w ere th e n standardized to 1 w ith in a trait. T his ‘fuzzy co ding’ p ro ced u re (Cheven e t et a í 1994) allows taxa to exhibit th e m odalities o f a variable (trait) to different degrees. T he p ro ced u re was developed an d first applied to terrestrial plants a n d fresh­ w ater invertebrates (O lff et a í 1994; T ow nsend & H ildrew 1994) b u t has n o w also been in tro d u c ed for m arin e sys­ tem s (B rem ner et a í 2003, 2006a). For o u r purposes, data o n traits w ere obtain ed fro m th e p rim a ry a n d secondary literatu re an d b y consulting expert advice (A. T ö rn ro o s u n p u b l. data). T hus, relevant a n d reliable in fo rm a tio n on all traits was o b tain ed for all taxa sam pled. This p roce­ d u re resulted in a taxa b y tra it m atrix, one o f tw o tables included in th e BT analysis. T o lin k th e ab u n d an ce of taxa at each statio n a n d m esh size w ith th e traits dis­ played b y th e taxa, we con d u cted a co -in ertia analysis (C oi; D olédec & Chessel 1994). This analysis assesses the c o -stru ctu re betw een tw o data tables, in this case a ‘taxa b y sta tio n ’ table an d a ‘taxa b y tra it’ table, an d sim u lta­ neously ord in ates th e tw o tables, m axim izing b o th the variance fro m th e in d ividual tables a n d th e correlation betw een th e m (D olédec & Chessel 1994; D ray et a í 2003). As a first step, tw o separate o rd in atio n s w ere con­ ducted: a centered PCA (p rinciple co m p o n e n t analysis) o n th e “ taxa b y sta tio n ” table an d a FCA (fuzzy corre­ spon d en ce analysis) o n th e “taxa b y tra it” table (Cheven e t et a í 1994; C harvet et a í 1998). These w ere th e n used in th e C oi analysis, a n d th e significance o f th e resulting c o -stru ctu re was exam ined w ith th e RV coefficient (a m easure o f sim ilarity betw een squ ared sym m etric m atrices). T o evaluate if th e value o f RV significantly dif­ fered fro m zero, a M o n te-C arlo ra n d o m p e rm u la tio n test was p erfo rm ed (n rep etitio n s = 999) (D olédec & Chessel 1994). To investigate tra it p a ttern s in relatio n to m esh size along th e en v iro n m en tal gradient, we con d u cted tw o separate C oi analyses; one o n th e In n e r area stations, an d one o n th e O u te r area stations. T his was d o n e to best elucidate p a ttern s in th e tw o areas, a n d to prev en t the u nev en a b u n d an ce d istrib u tio n in th e in n er archipelago to m ask th e m o re even p a tte rn (low er variability) of th e o u ter archipelago. BTA was th u s n o t con d u cted o n th e M iddle area, as we w an ted to h ighlight the opp o site ends o f th e range o f enviro n m en tal an d faunal a bundance. P rio r to th e analysis, dow n w eighting of a b u n d a n t taxa was d o n e using sq u are -ro o t tran sfo rm a­ tio n . The scores w ere p lo tted o n o rd in a tio n m aps, w ith each p o in t representing th e ab u n dance-w eighted biologi­ cal tra it co m p o sitio n o f each station. All analyses were d o n e in th e R e n v iro n m en t (R D evelopm ent C ore Team 2009).

61

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

A arnio, M attlla, T örnroos & B onsdorff

T able 2. Biological traits (10) and modalities (45) ascribed to species and used In the BTA. Labels listed correspond to trait modalities In Fig. 5. Biological traits

Trait modalities

Labels

Explanations

Mean size

0.1-1 mm

VS

Very small

1-5 mm 5 mm-1 cm 1-3 cm

S SM M

Small Small-medium Medium

Vermiform unsegm ented Vermiform segm ented

VermLuns Verml-seg

Wormlike, lacking true segm ents Wormlike, sem l-lndependent units

Blvalved Turbinate Articulate

Blvalved Turbinate Articulate Planktotrophlc Lecltotrophlc

Shell with tw o valves jointed by a ligament Whorled shell Jointed, arthrous Feeding on materials captured from the plankton Nourished on Internal resources, yolk

Dlrect_dev A ttached Tube_dweller Burrow_dweller Free

Direct developm ent of mini adults A dherent to substratum (>95% of adult time)

Body design

Larval type

Living habit

Planktotrophlc Lecltotrophlc Direct development Attached Tube-dweller Burrow dweller Free-living

Environmental position

Infauna (>5 cm) Infauna middle (2-5 cm)

lnf_deep lnf_mlddle

Infauna (top 2 cm) Bentho-pelaglc

lnf_top Eplbenthlc Bent_pel

Detrltlvore

Detrltlvore

Living on the surface of substrate Living In the w ater column but (primarily/occasionally) feeds on the bottom Feeds on detritus

Omnivore Herbivore Carnivore

Omnivore Herbivore Carnivore

Feeds on mixed diet of plant and animal material Feeds on plants Feeds on animals (predator)

Scavenger Jawed

Scavenger Jawed

Feeds on dead organic material Jaws, mandibles

Siphon Tentaculate

Siphon Tentaculate

Pharynx Radula Sessile

Pharynx Radula Sessile

Seml-moblle Mobile

Seml_mobll Mobil

Byssus Swimmer Rafter/dri fter Crawler Burrower

Byssus Swimmer Raft_drlft Crawler Burrower

Occasional m ovem ent with byssus threads Fins, legs, appendages via undulatory m ovem ent Rafting on e.g. algal mats, drifting On substrate via muscles, legs or appendages Lives and or moves In a burrow

Tube-bullder No transport

Tube_bullder No_trans

Lives and moves In a tube No transport

Diffusive mixing Surface deposition

Dlff_mlxlng Surf_deposltlon

Random diffusive transport (e.g. reworking, excavatlor Surface deposition of particles, 'regeneration' (e.g. excavation, egestlon)

Conveyer belt transport

Conv_belt_trans

Translocation of sediment, depth to surface (e.g. egestlon, excavation, defecations)

Reverse conveyer belt transport

Rev_conv_belt_trans

Subduction of particles from surface to depth (e.g. egestlon, excavation)

Eplbenthlc

Feeding habit

Resource capture m ethod

Mobility

Movement m ethod

Sediment transportation

R esults Basic community parameters B enthic faunal assemblages in th e stu d ied areas o f the A land archipelago consisted o f 30 sp ecies/tax a (Table 3). In the In n e r area, th e zo obenthic assem blage was d o m i­

62

In or on sediment, In w ater column Living within substrate, deeper than 5 cm Living within substrate, betw een 2 and 5 cm Living within top 2 cm of substrate

Both with and w ithout jaws Rasping Temporary (e.g. Mytilus edulis)

n ated b y gastropods an d oligochaetes, typically occurring o n m u d d y b o tto m s. M acom a balthica was also a b u n d a n t a n d d o m in ated b y biom ass. In th e M iddle area, th e assem ­ blage was sim ilar b u t M . balthica d o m in ated b o th n u m e ri­ cally an d b y biom ass. T he invasive polychaete Marenzelleria sp. was relatively a b u n d a n t in this area. T he O u ter area was

Marine Ecology 32 (Suppl. 1) (2011) 58-71 © 2010 Blackwell Verlag GmbH

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

A a rn io , M a ttila , T ö rn ro o s & B o n s d o rff

Table 3. Species list of the soft-bottom communities in the three archipelago areas (Inner, Middle and Outer) from both shallow and deep samples. X indicates if a species w as present. Total num ber of species on shallow versus deep stations are given at the bottom of the table. Total # spp, total num ber of species in each area. Inner area Species/taxa

Middle area

Outer area

Shallow Deep Shallow Deep Shallow Deep

Nemertea

Cyanophthalma obscura

X

X

X

X

X

Priapulida

Halicryptus spinulosus

X

X

Annelida Oligochaeta

Harmothoe sarsi Manayunkia aestuarina Marenzelleria spp. Hediste diversicolor Pygospio elegans

X X

X

X

X

X

X

X

X

X

X

X

X

X X X

X

X

X X

X

X

X X X

Mollusca

Cerastoderma glaucum Macoma balthica Mya arenaria Mytilus edulis Hydrobia spp. Radix spp. Limapontia capitata Potamopyrgus antipodarum Theodoxus fluviatilis Arthropoda Acarina Ostracoda

Semibalanus Improvisus Idotea chelipes Jaera albifrons Gammarus sp. Leptocheirus pilosus Monoporeia affinis Corophium volutator Saduria entomon Neomysis Integer

X X X

X X

X X

X X

X X

X X

X X

X X

X

X X

X

X

X

X

X

X

X X

X

X

X

X

X X X X

X X

X X X

X

X

X

X X

Chironomidae

Chironomus plumosus Total shallow versus deep 16 Total # spp

X

18

X

X X

X X

X

X X X X X

X X

22

19

X X X

X X X

X X X X X

11

19

17

22

X

28

characterized by M . balthica a n d o th er bivalves (M ytilus ed­ ulis an d Cerastoderma glaucum ) to g eth er w ith M arenzelleria sp. T he a m p h ip o d Monoporeia affinis was also c o m m o n in this area. As b o th th e shallow a n d th e deep stations in all areas show ed identical p a ttern s regarding species n u m b er,

Marine Ecology 32 (Suppl. 1) (2011 ) 58-71 © 2010 Blackwell Verlag GmbH

a b u n d an ce an d biom ass (P > 0.05, u n p aired t-test), the tw o d ep th zones w ere p o oled in th e statistical analysis. T he n u m b e r o f species fo u n d in each area was signifi­ cantly low er using th e 1.0-m m m esh th a n th e 0 .5 -m m m esh. In th e In n e r area, 18 species w ere fo u n d using the 0 .5 -m m m esh a n d 14 using th e 1.0-m m m esh. In the M iddle area, 22 species w ere recorded (19 w ith th e larger m esh alone). T he O u te r area h ad th e highest to tal species n u m b er: 28 w ith th e 0 .5 -m m m esh a n d 27 w ith the 1.0-m m m esh (Table 3). The m ean n u m b e r o f species was significantly higher using th e 0 .5 -m m m esh com p ared w ith th e 1.0-m m m esh (P < 0.0001; p aired f-test) in all archipelago areas (Table 4). In th e overall analysis using a 2-w ay ANOVA th ere was a significant difference in spe­ cies n u m b e r b o th betw een th e sieves (P < 0.0001) an d betw een th e areas (P < 0.0001) (Table 5; Fig. 2A). T he to tal ab u n d an ce values w ere significantly higher w ith th e 0 .5 -m m m esh th a n w ith th e 1.0-m m m esh in all areas (P < 0.0001; p aired f-test) (Table 4). For b o th m esh sizes th e a b u n d an ce was low est in th e In n e r area an d highest in th e O u ter area. In th e overall analysis using a 2-w ay A NO VA th ere was a significant difference in a b u n ­ dance b o th betw een sieves (P < 0.0001) an d am o n g areas (P = 0.0162) (Table 5; Fig. 2B). B iom ass values w ere also low est in th e In n er area an d highest in th e O u ter area, an d they w ere significantly h igher in th e 0 .5 -m m m esh com p ared w ith th e 1.0-m m m esh fractio n in all areas (P < 0.0001; p aired f-test) (Table 4). In th e overall analysis using a 2-w ay ANOVA th ere was a significant difference in ab u n d an ce b o th betw een sieves (P < 0.0001) an d am o n g areas (P = 0.0043). T here was also a significant in teractio n (P = 0.0043) betw een m esh a n d area (Table 5; Fig. 2C). In all areas, b o th th e ab u n d an ce an d th e biom ass esti­ m ates o f th e n u m erically d o m in a n t species w ere reduced significantly w hen using only th e 1.0-m m m esh (Fig. 3). Table 4. Results of paired f-test analysis of mesh size effects on num ber of species, abundance and biomass In the Inner, Middle and Outer areas. df

f

P

Species Inner archipelago Middle archipelago Outer archipelago Abundance

29 29 34

9.497 1S.S6 11.29

<0.0001 <0.0001 <0.0001

Inner archipelago

29

6.S9S

<0.0001

Middle archipelago Outer archipelago Biomass Inner archipelago

29 34

7.236 8.2S3

<0.0001 <0.0001

29

S.373

<0.0001

Middle archipelago Outer archipelago

29 34

8.142 9.106

<0.0001 <0.0001

63

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

A a rn io , M a ttlla , T ö r n r o o s & B o n s d o rff

Table 5. Results of 2-way ANOVA analysis of mesh size effects on num ber of species, abundance and biomass In the Inner, Middle and Outer areas.

14

A

m 92 '8

12

I

I 0.5 mm

■

1.0 mm

T

10

Cl

Source of variation

df

SS

MS

F

« 0 o3

P

8 6

-Q

1 4

No. of species Mesh Area Interaction Subjects (matching) Residual A bundance Mesh Area Interaction Subjects (matching) Residual Biomass Mesh

2

83.44 172.9

83.44 86.45

149.2 25.50

<0.0001 <0.0001

2 16

0.8229 54.25

0.4115 3.390

0.7358 6.063

0.4947 0.0004

1

Z

0

B

10 000

T" 16

8.948

0.5592

1

2 2 16

60,830,000 55,890,000 6,332,000 82,930,000

60,830,000 27,950,000 3,166,000 5,183,000

16

27,540,000

1,721,000

I 7500-

C 35.34 5.392 1.840 3.012

<0.0001 0.0162 0.1909 0.0170

§ 5000-

(Ü O C

o 2500

i_U i J

1

18.00

18.00

33.67

<0.0001

Area Interaction Subjects (matching)

2 2 16

67,730 8.331 69,230

33,860 4.165 4327

7.827 7.793 8094

0.0043 0.0043 <0.0001

Residual

16

8.553

0.5345

C

2 0 0

1

-,

-1 5 0 -

"o) sCD’ 1 » -

£ O ûû

O ligochaetes, w hich w ere a b u n d a n t in th e In n e r a n d M id ­ dle area, w ere reduced b y 96 -9 9 % w hen using only a 1.0m m m esh size. O stracods w ere red u ced b y 97% in th e In n er area an d b y 100% in th e M iddle an d O u te r areas, and polychaetes, nam ely Marenzelleria sp, w ere reduced b y 75% in the O u ter area w hen using th e 1.0-m m m esh. The Baltic clam , M . balthica, d o m in ated in all areas by biom ass (5 8 -7 8 % ), b u t ab u n d an ce estim ates w ere reduced significantly, w hen th e 1 .0 -m m m esh was used. T he size d istrib u tio n o f M . balthica was affected by m esh size: w hen th e 1 .0 -m m m esh was used, th e n u m b e r o f individuals m easuring 1 an d 2 m m in size (i.e. the ann u al spat) was red u ced m arkedly. In th e In n er area, 96% o f 1-m m -sized M . balthica a n d 32% o f 2 -m m -sized individuals w ere lost using th e 1.0-m m m esh. In th e M id ­ dle area, th e corresp o n d in g values w ere 1 0 0 % ( 1 m m ) and 45% (2 m m ), an d in th e O u ter area 99% (1 m m ) and 47% (2 m m ). B oth sieves cap tu red equal n u m b ers of clam s o f size classes 3 m m an d larger. T hus th e m ain dif­ ference was th e loss (o r u n d erestim atio n ) o f recru itin g individuals, w hich m ay affect th e evaluation o f th e eco­ logical status o f a b en th ic habitat.

Ecological status This survey show ed th a t zo o b en th o s as an ecological quality elem ent resulted in evaluation o f a relatively good

64

2

50

QInner

Middle

Outer

Archipelago area Fig. 2. Number of species (A), abundance (B) and biomass (C) In 0.5-mm and 1.0-mm mesh In the three archipelago areas (Inner, Middle, Outer). Values Indicate mean ± SD.

overall status (Fig. 4). All b u t one sam pled statio n and all th ree areas w ere classified as ‘g o o d ’ ( 1 .0 -m m m esh) or ‘h ig h ’ (0 .5 -m m m esh) ecological status. T he BBI itself was highest in th e O u te r area, b u t as th e class b o u n d aries are different for th e different areas (an d d epths), th e ecologi­ cal status was sim ilar to th e o th er areas.

Biological traits T he C o i analyses for th e In n e r an d O u ter area stations illustrated th e relationship betw een tax o n com position a n d ab u n d an ce a t shallow an d deep stations w ith the tw o m esh sizes, a n d biological traits. A clear difference in the tra it co m p o sitio n was identified betw een th e tw o arch i­ pelago areas in term s o f n u m b er o f m odalities found. In th e In n e r area, n o scavengers (feeding type) or tube builders (m o v em en t type) m odalities com p ared w ith T he significance o f th e value in Table 6 ) betw een

w ere registered, resulting in 43 45 in th e O u te r area. resulting correlation (n o ted R th e tw o sets o f coordinates was

Marine Ecology 32 (Suppl. 1) (2011) 58-71 © 2010 Blackwell Verlag GmbH

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

A a rn io , M a ttila , T ö rn ro o s & B o n s d o rff

A bundance

A Inner area

Biomass

A bundance (Ind/m5) 500 1000 1500 2000

B iom ass (giri2) 2500

10

15

20

25

00

35

40

45

M. üattflts . fA. ansiTanö C. plbncsius HyrHoOia spp. P. antifxxSaru-m . N. On/srsicobr -

B

Abunda one (ind/m5)

Middle area

500

1000

B iom ass (g/m2)

1500

0

2000

10 2 0 0 0 40 5 0

00 7 0 80 00 100

M. úasfita Oligochaeta Hydrobia spp, P. aniipoaaruni MsranzelOnö spp Marenzelleria spp. -

Ostracoda

A bundance (indVm2)

Outer anea

500

1000

1500

2000

B iom ass (gVm2) 2500

3000

20

40

EO

80

100 120 140

160

fA. ¿aivica

Msrenzeti&riB spp. Ostracoda Hydratö spp Chironemidae -

C. stáucom Ifarsnzflferfispp. Hydrobia spp.

C. voyator Fig. 3. Abundance and biomass of the dom inant species In 0.5-mm and 1.0-mm mesh In the Inner (A), Middle (B) and Outer (C) areas. Values Indicate mean ± SD. Note the different scales on x-axes.

exam ined w ith the M o n te-C arlo test. T he test show ed th a t the O u ter area h ad a b o rd erlin e significance for a n o n -ra n d o m p a tte rn (RV = 0.254, P = 0.071). H ow ever, the opposite was tru e for th e In n e r area (RV = 0.268, P = 0.297). Still, we chose to p resen t b o th results to illus­

th e first axis o f th e o rd in atio n , th e tw o m esh sizes were separated for b o th shallow a n d deep stations, th e larger size b eing g ro u p ed m o re tow ards th e centre an d th e sm al­ ler m esh size sam ples m o re spread o u t, i.e. separated from th e o thers (Figs 5 an d 6 ). This m eans th a t th e m esh size

trate the tre n d and m o re evident p a tte rn in th e O u ter area com pared w ith th e In n e r one, considering th e higher

o f th e sieve influences th e fu n ctio n al analysis, a n d im plies th a t for a reliable analysis o f biological traits in these rela­

species diversity an d m o re equal a b u n d an ce o f species (Figs 5 an d 6 ). In the BTA o f th e O u te r area, axes 1 a n d 2 o f th e co­ in ertia analysis acco u n ted for 90% (65% an d 25%, respectively) o f th e variability in biological tra it co m p o si­ tio n betw een the stations. A clear sep aratio n betw een shallow and deep stations along th e second axis could be seen, especially for th e o u te r archipelago (Fig. 6 ). A long

tively species-poor assemblages, in fo rm a tio n is needed for all species th a t can be sam pled (Fig. 6 ). T he shallow areas w ere characterized b y sm all-sized detritivores (species ob tain in g food th ro u g h suspension, surface a n d /o r su b ­ surface feeding) w ith a diffusive sed im en t tra n sp o rt m ode (taxa such as M acom a balthica, Potamopyrgus antipoda­ rum an d C h iro n o m id ae). T he deeper areas show ed a c o m p ilatio n o f detritivores p erfo rm in g n o sedim ent

Marine Ecology 32 (Suppl. 1) (2011 ) 58-71 © 2010 Blackwell Verlag GmbH

65

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

A a rn io , M a ttlla , T ö r n r o o s & B o n s d o rff

0

0 .5 mm

A

1 .0

mm

0.8

Fig. 4. Ecological status, m easured using BBI, In shallow (S) and deep (D) bottom s In the three archipelago areas. Sampling stations are

0.6 0.4 0.2

r — r~- T '

0.0

F18F15 F6 F17 F9 F3 M13M20M7 M5 M15M18 E23 E26 E24

tra n sp o rt

(e.g.

M ytilus edulis)

and

o m n iv o ro u s

E18 E11 E15

Indicated on the x-axls. Background colours: blue = high, green = good, yellow = m oderate, orange = poor and red = bad ecological status. Note th at the class borders for different status Ile on different BBI-levels In different depths and different archipelago areas.

tu b e-

w idespread an d m o st ab u n d a n t species are stu d ied (El­

builders perfo rm in g reversed conveyer b elt tra n sp o rt (taxa such as Marenzelleria sp. an d Pygospio elegans).

lingsen et al. 2007). T he m esh size o f sieve also had a significant effect on th e registered p o p u la tio n stru ctu re o f th e bivalve M acom a balthica, w hich is a key species in th e N o rth e rn Baltic Sea (Segersträle 1962; O lafsson 1989). P o p u la tio n stru ctu re a n d re cru itm en t success o f th e species are often used as indicators o f th e enviro n m en tal conditions. A dult M . balthica are quite to le ra n t a n d can w ith stan d stressed enviro n m en tal con d itio n s for som e tim e, w hereas juve­ niles are sensitive even to sm all disturbances in the envi­ ro n m e n t (B onsdorff et al. 1995). W h en th e 1.0-m m m esh was used, m o st juveniles ( 1 - 2 m m in size) w ere lost, and th u s th e w hole an n u al re c ru itm e n t could be m issed from any analysis. It is th u s im possible to m ake estim ates on rec ru itm en t success an d p o p u la tio n stru ctu re if th e larger m esh size is used. T he estim ate o f th e ecological status according to the E U -W FD is d o n e using several different indices, and alm o st every co u n try has developed an index o f th eir ow n, suitable for th eir p articu lar en v iro n m en t (D iaz et al. 2004; Z ettler et a l 2007; Borja et al. 2009; Josefsson et al. 2009; L eonardsson et al. 2009). For th e N o rth e rn Baltic Sea, BBI has been developed to acco u n t for th e low salin­ ity an d low species n u m b ers in th e area (Perus et al. 2007). D ue to th e com plex to p o g rap h y a n d th e gradients

D iscussion The results fro m this stu d y show ed th a t th e choice of m esh size (1.0 o r 0.5 m m ) in th e sieve affected all basic co m m u n ity param eters, in all areas an d at b o th depths (shallow an d deep). The n u m b e r o f species, abundance and biom ass w ere all significantly red u ced w hen using th e larger m esh size alone. The n u m b e r o f species d ro p p ed by 42% in th e In n e r an d M iddle area, a n d b y 25% in th e O u ter area. Also, som e species, such as oligochaetes an d polychaetes, w ere sam pled in significantly red u ced n u m ­ bers w ith the 1.0-m m m esh. Sm all-sized species, such as ostracods and sm all polychaetes (e.g. M anayunkia aestua­ rina), as well as juveniles o f m an y species, w ere lost co m ­ pletely w hen th e larger m esh size was used. In o th er w ords, the b en th ic c o m m u n ity m ay look very different w hen using different m esh sizes. W h e n m an y species are seem ingly lost (d u e to large m esh size) fro m an area w ith naturally low biodiversity, th e ecological assessm ent an d rep resen tatio n o f th a t assem blage will b e w rong. It is im possible to o b tain a representative p ictu re o f th e overall biodiversity an d ecosystem fu n ctio n in g if only th e m ost T able 6. Main characteristics of co-lnertla analyses.

(a) Coi Inner archipelago (b) Coi Outer archipelago

Axis

Covar

Vari

Var2

Ineri

Iner2

R value

F1 F2 F1 F2

2.009 0.709 1.803 1.127

4.439 2.137 4.986 2.802

0.575 0.485 0.621 0.514

19.924 24.637 25.552 33.653

0.548 0.972 0.490 0.878

0.787 0.684 0.583 0.783

Covar, covariance betw een both sets of coordinates of co-lnertla analysis; V ari, Inertia of the abundance data projected onto co-lnertla axes; Var2, Inertia of the trait data projected onto co-lnertla axes; R value, correlation betw een both sets of coordinates resulting from the co-lnertla analysis; Ineri, maximum Inertia projected onto axes of the simple analysis of abundance data (eigenvalues of centered PCA); Iner2, maximum Inertia projected onto axes of the simple analysis of trait data (eigenvalues of FCA).

66

Marine Ecology 32 (Suppl. 1) (2011) 58-71 © 2010 Blackwell Verlag GmbH

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

A a rn io , M a ttila , T ö rn ro o s & B o n s d o rff

Inner area

F2

d = 1 .0

----------- d=0i

Conv belt trans

Rev con belt trans T e n ta c u lis |n;_ dç; p

lnf_middle

ri'SL

Siphon

V

Sh allow 1 . t i J

Lecitotrophic Bivalvei Plankta

M Vermi_uns Articulate Swimmer Uent_pel Byssus

Carnivore

Herbivore

*F* I \

Burrow dw eller

/tp lb e n th ic No trans i Omnivore ills free —------

D eeP \

1

F3L •

J —y

Radula

Turbinate

Jawed

Tube_dweller

Verml_seg

Pharynx

Fig. 5. Co-lnertla ordination of stations (both mesh sizes) and of biological traits for the Inner area. Position of the trait variables (43 modalities) and some representative taxa on the F1 x F2 co-inertia plain is presented In the large plot (cf. Table 2 for variable labels). Inset ordination plot at top right: position of sites, both 1.0- and 0.5-mm mesh sizes (bold) on the F1 x F2 plain.

o f salinity an d exposure in th e archipelago areas, th e BBI has different class b o u n d aries for different areas an d depth-zones (Perus et al. 2007). In th e In n e r an d O u ter archipelago areas, th e status was som ew hat b etter in the shallow th a n in the deeper areas. In o u r stu d y th e ecolog­ ical status was good o r even high in all areas a n d depths, except for one deep statio n in th e In n er area, w here the status was m o d erate (0.5 m m ) or b ad (1.0 m m ). Identify­ ing the b o rd e r betw een m o d erate an d good is critical, as all w ater areas should have a good ecological status by 2015. In o u r study, th e p ro p o rtio n o f sites w ith a good ecological status was th e sam e irrespective o f m esh size. H ow ever, the statu s was generally som ew hat b etter w hen a 0 .5 -m m m esh ra th e r th a n a 1.0-m m one was used. U sing a 1.0-m m m esh w o u ld certainly n o t overestim ate the ecological status, a n d som etim es a conservative esti­ m ate m ay be desired. As th e estim ated ecological status using the BBI was u n ifo rm ly a n d significantly higher using the 0 .5-m m m esh th a n th e 1.0-m m m esh, im p o r­ ta n t ecological in fo rm a tio n is lost using only th e larger m esh size. O n th e o th er h an d , th e m o re conservative esti­ m ate m ay be valid fro m a m an ag e m en t p o in t o f view

Marine Ecology 32 (Suppl. 1) (2011 ) 58-71 © 2010 Blackwell Verlag GmbH

(Fig. 4). For th e A land archipelago, sim ilar estim ates of ecological status have been obtain ed using m acrophytes as biological p aram eters (S ö d erströ m 2008). BTA was fo u n d to be a useful ap p ro ach in th e coastal areas o f th e N o rth e rn Baltic Sea. O u r analysis - one of th e first in this region (b u t see B oström et al. 2010) serves to highlight th e issue o f tim e c o n su m p tio n versus sam pling effort (e.g. m esh size choice) a n d reliability of com prehensible results in m anagem ent. W h en choosing a less tim e-co n su m in g a n d th ereby m o re econom ical sam ­ pling m e th o d (e.g. 1 .0 -m m m esh size), th e ecological p er­ cep tion o f a system is adversely affected. A lthough the larger m esh size did n o t overestim ate th e ecological sta­ tus, th e ecological fu n ction ality o f th e system in question could be w rongly in terp re te d if all species an d th eir func­ tio n al traits are n o t covered. H ow ever, th e applicatio n of fu n ctio n al m u lti-tra it analyses, such as BTA, to species level o r even m o re p ro p erly in d ividual level, is still tim econsum ing, taxonom ically difficult a n d needs fu rth er refin em en t (A lbert et a í 2010). T he difference in trait co m p o sitio n w hen using 0.5- o r 1.0-m m m esh show ed a significant tre n d , particularly in th e O u te r archipelago,

67

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

A a rn io , M a ttlla , T ö r n r o o s & B o n s d o rff

Outer area d = 2 .0

Dm_mixing lnf_top Semi mobi Burrower rbm ate Burrow_dweller Planktotrophi Bivalved Detrltlvore Radula Surt_depositfon inf m iddle V erm r.se Conv belt trans

Jawed Tube_dweller SM V Crawler Herbivore Raft drift ir e d .d e v Aftieulate f re e Mqfrile Carnivore Ep benthic . Scavenger Bent pel

Swimmer

No_t Pharynx Omnivore

Siphon

verm i uns

Lecitotrophic d = 0.2

Rev_con_belt_trans in# ¿ e e Tube builder T e n tjc u b te

: LSI Byssus Attached Sessile Fig. 6. Co-lnertla of ordination of stations (both mesh sizes) and of biological traits for the outer archipelago area. The position of the trait vari­ ables (45 modalities) and some representative taxa F1 x F2 co-lnertla plain are presented In the large plot (cf. Table 2 for variable labels). Inset ordination plot at bottom right: position of sites, both 1.0- and 0.5-mm mesh sizes (bold) on the F1 x F2 plain.

w here the p ro p o rtio n o f sm all-sized species is high. A functional ap p ro ach to classifying an d assessing h ab itat and ecosystem q uality is generally agreed u p o n to d ay an d m ay be th e m o st relevant for delivering ecosystem -based targets (B rem ner 2008; T illin e t al. 2008). D iscussion a b o u t draw backs a n d problem s still concerned w ith th e approach have focused m ain ly o n th e operatio n al m ea­ sures o f functio n in g , m eth o d s to best elucidate fu n c tio n ­ ing and th e extensive species-specific in fo rm atio n required in analysis (B rem ner et a í 2003, 2006a,b; Tillin et a í 2008). H ow ever, th e scale o n w hich fu n ctio n in g is studied is also significant (H ew itt et a í 2008). As show n in this study, it is particu larly essential to consider th e scale at w hich one sam ples, n o t only th e spatial scale th a t concerns th e design (e.g. betw een o r w ith in hab itats an d w ith in landscapes). T he choice o f m esh size, a n d thereby inclusion or exclusion o f b o th rare an d c o m m o n species in analysis, is essential to th e conclusions o f h ab ita t q u al­ ity, ecosystem stability an d functioning. T he function al consequences o f sam pling m e th o d o n the scale o f m esh size o f sieve, have n o t to o u r know ledge been th o ro u g h ly evaluated. O u r findings suggest this can

68

m arkedly affect th e m easu rem en t o f b en th ic fu n ctioning o f coastal areas. W e also show th a t it is im p o rta n t to dif­ ferentiate betw een th e shallow ( < 1 0 m ; p h o tic zone) and deeper ( > 1 0 m ; eu ph otic zone) areas in com plex archipel­ ago areas, w here th e shoreline is long a n d to p o g rap h y is com plex (G ranö et al. 1999).

C oncluding Remarks O u r results highlight h o w biological traits, in a d d itio n to species n u m b e r an d biom ass, can play a key role in a n a­ lyzing ecosystem stru c tu re an d in assessm ent an d classifi­ cation o f coastal systems, an d for o u r u n d e rstan d in g o f th e com plexity o f ecological fu n ctio n in g o f these systems (B rem ner 2008; H ew itt et al. 2008). In conclusion, th e ecological im plications o f using lar­ ger m esh sizes o f th e sieve ( 1 . 0 m m is reco m m en ded for th e Baltic Sea in th e W FD ) instead o f sm aller is th at, in shallow areas, individuals o f sm all species an d th eir p articu lar traits are n o t sufficiently sam pled, i.e. th ey m ay be lost in a fu n ctio n al perspective. In deeper areas, espe­ cially tra it m odalities linked to th e essential process o f

Marine Ecology 32 (Suppl. 1) (2011) 58-71 © 2 0 1 0 Blackwell Verlag GmbH

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

A a rn io , M a ttila , T ö rn ro o s & B o n s d o rff

b io tu rb a tio n are lost. F rom an ecological p o in t o f view, a b ro ad er tra it co m p o sitio n is o b tain ed w ith 0 .5 -m m m esh sizes, generating a m o re reliable an d com plete p ictu re of ecosystem functioning. W e also show th a t co m b in in g tra ­ ditional m o n ito rin g for th e EU W FD w ith a fu nctional analysis o f th e b enth ic assem blages strengthens o u r ability to in te rp re t environ m en tal quality, a n d th u s increases the precision o f o u r advice for m an ag e m en t purposes.

B onsdorff E., Laine A.O., H än n in en J., V uorinen I., N orkko A. (2003) Z oobenthos o f the o u ter archipelago w aters (N Baltic Sea) - the im portance o f local conditions for spatial distri­ b u tio n patterns. Boreal E nvironm ent Research, 8, 135-145. Borja A., Franco J., Pérez V. (2000) A m arine biotic index to establish the ecological quality o f soft-bottom benthos w ithin E uropean estuarine and coastal environm ents. M arine Pollution Bulletin, 40, 1100-1114. Borja A., Miles A., O cchipinti-A m brogi A., Berg T. (2009) C ur­ ren t status o f m acroinvertebrate m ethods used for assessing

A c k n o w le d g e m e n ts T his stu d y was fu n d ed b y A bo A kadem i U niversity, the G overnm ent o f A land an d th e M aj an d T o r Nessling fo u n d atio n . W e th a n k C am illa H eilm an for field sam pling an d sorting o f th e b en th ic sam ples.

the quality o f E uropean m arine waters: im plem enting the W ater Fram ew ork Directive. Hydrobiologia, 633, 181-196. B oström C., T örnroos A., B onsdorff E. (2010) Invertebrate dis­ persal a n d habitat heterogeneity: expression o f biological traits in a seagrass landscape. Journal o f Experimental M arine Biology and Ecology, 390, 106-117. B rem ner J. (2008) Species’ traits and ecological functioning in

R eferen ces A lbert H.C., T huiller W ., Yoccoz N.G., D ouzet R., A uberi S., Lavorel S. (2010) A m u lti-trait approach reveals the stru c ­ ture and the relative im portance o f intra- vs. interspecific variability in p lant traits. Functional Ecology, 24, 1192-1201. Blom qvist E.M., B onsdorff E. (1986) Spatial a n d tem poral

m arine conservation and m anagem ent. Journal o f Experi­ m ental M arine Biology and Ecology, 366, 37-47. B rem ner J., Rogers S.I., Frid C.L.J. (2003) Assessing functional diversity in m arine benthic ecosystems: a com parison o f approaches. M arine Ecology Progress Series, 254, 11-25. B rem ner J., Rogers S.I., Frid C.L.J. (2006a) M ethods for describing ecological functioning o f m arine benthic

variations o f benthic m acrofauna in a sand b o tto m area on

assemblages using biological traits analysis (BTA). Ecological

Aland, n o rth ern Baltic Sea. Ophelia, 4 (Suppl), 27-36.

Indicators, 6, 609-622.

B onsdorff E. (2006) Z oobenthic diversity-gradients in the Bal­

B rem ner J., P aram or O.A.L., Frid C.L.J. (2006b) Developing a

tic Sea: c ontinuous post-glacial succession in a stressed eco­

Methodology for Incorporating Ecological Structure and Func­

system. Journal o f Experimental M arine Biology and Ecology,

tioning into Designation o f Special Areas o f Conservation

333, 383-391. B onsdorff E., Blom qvist E.M. (1993) Biotic couplings o n shal­ low w ater soft b o tto m s - exam ples from the n o rth ern Baltic Sea. Oceanography and M arine Biology A nnual Review, 31, 153-176. B onsdorff E., Pearson T.H . (1999) V ariation in the sublittoral m acrozoobenthos o f the Baltic Sea along environm ental gra­

(SAC) in the 0-12 N autical M ile Zone. School o f Biological Sciences, U niversity o f Liverpool, Liverpool: 168 pp Cederwall H., Elm gren R. (1980) Biomass increase o f benthic m acrofauna dem onstrates e u trophication o f the Baltic Sea. Ophelia, 1 (Suppl.), 31-48. C harvet S., Kosmala A., Statzner B. ( 1998) B iom onitoring th ro u g h biological traits o f benthic m acroinvertebrates: p e r­

dients: a functional group analysis. Australian Journal o f

spectives for a general tool in stream m anagem ent. Archiv

Ecology, 24, 312-326.

fü r Hydrobiologie, 142, 415-432.

B onsdorff E., A arnio K., Sandberg E. (1991) T em poral and

Chevenet F., Doledec S., Chessel D. (1994) A fuzzy coding

spatial variability o f zoobenthic com m unities in archipelago

approach for the analysis o f long-term ecological data.

w aters o f the n o rth ern Baltic Sea - consequences o f e u tro ­

Freshwater Biology, 31, 295-309.

phication? Internationale Revue des Gesamten Hydrobiologie, 74, 433-449. B onsdorff E., N orkko A., B oström C. (1995) R ecruitm ent and p opulation m aintenance o f the bivalve M acoma balth­ ica (L.) - factors affecting settling success a n d early su r­

D iaz R.J., R osenberg R. (1995) M arine benthic hypoxia: a review o f its ecological effects and the behavioural responses o f benthic m acrofauna, Oceanography and M arine Biology A nnual Review, 33, 245-303. D iaz R.J., Solan M., V alente R.M. (2004) A review o f

vival o n shallow sandy bottom s. In: E leftheriou A., Ansell

approaches for classifying benthic habitat and evaluating

A.D., Sm ith C J. (Eds), Biology and Ecology o f Shallow Coastal Waters. Proceedings o f the 28th E uropean M arine

habitat quality. Journal o f Environm ental M anagement, 73,

Biology Sym posium . Olsen 8c Olsen, Fredensborg: 2 53260. B onsdorff E., Blom qvist E.M., M attila J., N orkko A. (1997) L ong-term changes and coastal E utrophication. Examples

165-181. Dolédec S., Chessel D. ( 1994) C o-inertia analysis: an alterna­ tive m eth o d for studying species-environm ent relationships. Freshwater Biology, 31, 277-294. D ray S., Chessel D., Thioulouse J. (2003) C o-inertia analysis

from the A land Islands and the Archipelago Sea, no rth ern

and the linking o f ecological data tables. Ecology, 84, 3078-

Baltic Sea. Oceanologica Acta, 20, 319-329.

3089.

Marine Ecology 32 (Suppl. 1) (2011 ) 58-71 © 2010 Blackwell Verlag GmbH

69

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

Ellingsen K.E., H ew itt J.E., T hrush S.F. (2007) Rare species, habitat diversity and functional redundancy in m arine benthos. Journal o f Sea Research, 58, 291-301. Elm gren R. ( 1989) M an ’s im pact on the ecosystem o f the Baltic Sea: energy flows today and at the tu rn o f the century. Am bio, 18, 326-332. Frid C.L.J., P aram or O.A.L., B rockington S., B rem ner J. (2008) Incorporating ecological functioning into the designation and m anagem ent o f m arine protected areas. Hydrobiologia, 606, 69-79. G ranö O., R oto M., Laurila L. (1999) E nvironm ent and land

Perus J., Liljeqvist J., B onsdorff E. (2001) A long-term study o f changes in the zoobenthos in the A land archipelago a com parison betw een 1973, 1989 and 2000. Forskningsrapporter frân Huso Biologiska Station, 103, 1-58 (In Swedish w ith English sum m ary). Perus J., B onsdorff E., Bäck S., Lax H.-G ., Villnäs A., W estberg V. (2007) Z oobenthos as indicators o f ecological status in coastal brackish waters: a com parative study from the Baltic Sea. Am bio, 36, 250-256. R D evelopm ent Core Team (2009) R: A Language and Environ­ m ent for Statistical Computing. R F oundation for Statistical

use in the shore zone o f the coast o f Finland. Pnblicationes

C om puting,

Institnti Geographici Universitatis Tnrknensis, 160, 1-76.

w w w .R -project.org.

HELCOM (2009) E utrophication in the Baltic Sea - an in te ­ grated them atic assessm ent o f the effects o f n u trie n t enrich­

V ienna.

ISBN

3-900051-07-0,

URL

http://

Ramsay K., Kaiser M.J., H ughes R.N. ( 1998) Responses o f b e n ­ thic scavengers to fishing disturbance by tow ed gears in dif­

m ent in the Baltic Sea region. Baltic Sea E nvironm ent

ferent habitats. Journal o f Experimental M arine Biology and

Proceedings, 115B, 1-148.

Ecology, 224, 73-89.

H elm inen O. (1975) B ottenfaunan i den äländska skärgarden. M eddelanden fràn Huso Biologiska Station, 17, 43-71. H ew itt J.E., T hrush S.F., D ayton P.D. (2008) H abitat variation,

Rosenberg R., Blom qvist M., N ilsson H.C., Cederwall H., D om m ig A. (2004) M arine quality assessm ent by use o f benthic species-abundance distributions: a proposed

species diversity and ecological functioning in a m arine

new p rotocol w ithin the E uropean U nion W ater

system. Journal o f Experimental M arine Biology and Ecology,

Fram ew ork Directive. M arine Pollution Bulletin, 49,

366, 116-122. Jax K.. (2005) F unction and ‘functioning’ in ecology: w hat does it mean? Oikos, 111, 641-648. Josefsson A.B., Blomqvist M., H ansen J.L.S., Rosenberg R.,

728-739. Rosenberg R., M agnusson M., Nilsson H.C. (2009) T em poral a n d spatial changes in m arine benthic habitats in relation to the EU W ater Fram ew ork Directive: The use o f sedim ent

Rygg B. (2009) Assessm ent o f m arine benthic quality change

profile imagery. M arine Pollution Bulletin, 58, 565-572.

in gradients o f disturbance: com parison o f different Scandi­

R um ohr H., B onsdorff E., Pearson T.H . (1996) Z oobenthic

navian m ulti-m etric indices. M arine Pollution Bulletin, 58, 1263-1277. Leonardsson K., Blom qvist M., Rosenberg R. (2009) T heoreti­ cal a n d practical aspects o n benthic quality assessment

succession in Baltic sedim entary habitats. Archive o f Fishery and M arine Research, 44, 179-214. Segerstrâle S.G. (1962) Investigations o n Baltic populations o f the bivalve M acoma balthica (L.) II. W hat are the reasons

according to the E U -W ater Fram ew ork Directive - exam ples

for periodic failure o f recruitm ent and the scarcity o f M aco­

from Swedish waters. M arine Pollution Bulletin, 58, 1286-

m a in deeper w aters o f the inner Baltic?. Societas Scientia-

1296. N orkko A., B onsdorff E. (1996) P opulation responses o f

rum Fennicae Commentationes Biologicae, 24, 1-26. Söderström S. (2008) T esting o f classification m ethods for

coastal zoobenthos to stress induced by drifting algal m ats.

coastal w aters at A land Islands according to the EU W ater

M arine Ecology Progress Series, 140, 141-151.

Fram ew ork Directive - Chlorophyll a and soft-bottom vege­

O lafsson E.B. (1989) C ontrasting influences o f suspensionfeeding a n d deposit-feeding populations o f M acoma balthica o n infaunal recruitm ent. M arine Ecology Progress Series, 55, 171-179. O lff H ., Pegtel D.M ., van G roenendael J.M., Bakker J.P. (1994) G erm ination strategies d u rin g grassland succession. Journal o f Ecology, 82, 69-77. Pearson T.H. (2001) Functional group ecology in soft-sedi-

tation. Forskningsrapporter frân Huso Biologiska Station, 121, 1-85 (In Swedish w ith English sum m ary). Stachowicz J.J., Fried H., O sm an R.W., W hitlatch R.B. (2002) Biodiversity, invasion resistance a n d m arine ecosystem func­ tion: reconciling p attern a n d process. Ecology, 83, 25752590. T hrush S.F., Schneider D.C., Legendre P., W hitlatch R.B., D ayton P.K., H ew itt J.E., H ines A.H., C um m ings V.J.,

m ent m arine benthos: the role o f biotu rb atio n . Oceanogra­

Lawrie S.M., G rant J., Pridm ore R.D., T u rn er S.J., McArdle

phy and M arine Biology, 39, 233-267.

B.H. (1997) Scaling-up from experim ents to com plex

Pearson T.H., Rosenberg R. (1978) M acrobenthic succession in relation to organic enrichm ent a n d pollution o f the m arine environm ent. Oceanography and M arine Biology, 16, 2 2 9 311. Perus J., B onsdorff E. (2004) L ong-term changes in m acrozoo-

70

A a rn io , M a ttlla , T ö r n r o o s & B o n s d o rff

ecological systems: w here to next? Journal o f Experimental M arine Biology and Ecology, 216, 243-254. T hrush S.F., H ew itt J.E., C um m ings V.J., G reen M .O., Funnell G.A., W ilkinson M.R. (2000) Im proving the generality of field experim ents: the interaction o f processes operating over

benthos in the A land archipelago, n o rth ern Baltic Sea. Jour­

different spatial scales o n intertidal sandflats. Ecology, 81,

nal o f Sea Research, 52, 45-56.

399-415.

Marine Ecology 32 (Suppl. 1) (2011) 58-71 © 2010 Blackwell Verlag GmbH

A a rn io , M a ttila , T ö rn ro o s & B o n s d o rff

Z o o b e n th o s as a n e n v iro n m e n ta l q u a lity e le m e n t

Tillin H.M ., Rogers S.I., Frid C.L.J. (2008) A pproaches to clas­

Yachi S., Loreau M . ( 1999) Biodiversity a n d ecosystem p ro d u c ­

sifying benthic h abitat quality. Marine Policy, 32, 455-464.

tivity in a fluctuating environm ent: the insurance hypothe­

Tow nsend C.R., H ildrew A.G. (1994) Species traits in relation to a habitat tem plet for river systems. Freshwater Biology, 31, 265-275. W arw ick R.M., Somerfield P.J. (2008) All anim als are equal

sis. Ecology, 96, 1463-1468. Z ettler M.L., Schiedek D., Bobertz B. (2007) Benthic biodiver­ sity indices versus salinity gradient in the southern Baltic Sea. Marine Pollution Bulletin, 55, 258-270.

b u t som e are m ore equal th an others. Journal o f Experimen­

tal Marine Biology and Ecology, 366, 184-186.

Marine Ecology 32 (Suppl. 1) (2011 ) 58-71 © 2010 Blackwell Verlag GmbH

71

marine ecology an evolutionary perspective

O »

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

Assessment of benthic ecosystem functioning through trophic w eb modelling: th e example of th e eastern basin of th e English Channel and th e Southern Bight of the North Sea C lé m e n t G arcia1,2,3, Pierre C hardy4, Jea n -M a rie D e w a r u m e z 1,2,3 & J ea n -C la u d e D a u v in 5 1 Université de Lille Nord de France, Lille, France 2 3 4 5

Université Lillei, LOG, Wimereux, France CNRS, UMR8187, Wimereux, France Station Marine d'Arcachon, Université de Bordeauxl, UMR S80S EPOC-OASU, Arcachon, France Université de Caen Basse Normandie, Laboratoire M orphodynamique Continentale e t Côtière, UMR CNRS 6143 M2C, Caen, France

K eywords English Channel; functional unit; North Sea; soft-bottom communities; trophic web. C orrespondence Clément Garcia, centre for Environment, Fisheries and Aquaculture Science, Lowestoft Laboratory, Pakefleld Road, Lowestoft, Suffolk, NR33 OHT, UK. E-mail: [email protected] Accepted: 15 December 2010 d o t 10.1111/j. 1439-0485.2011,00428.x

72

A bstract B enthic organism s ap p ear to be accurate proxies for assessing coastal ecosystem stru ctu res an d changes due to clim atic a n d an th ro p o g en ic stresses. F unctional studies o f b en th ic system s are relatively recent, m ain ly because o f th e difficul­ ties in o b tain in g th e basic param eters for each b en th ic co m p artm en t {i.e. d etri­ tus, bacteria, m eio fau n a an d m acro fau n a). O u r stu d y focuses o n th e eastern b asin o f th e English C hannel an d th e S o u th ern Bight o f th e N o rth Sea. T rophic web m odelling was used to assess th e fu n ctio n in g o f th e th ree m ain benthic c o m m u n ity assemblages. To test a n d assess th e relative im p o rtan ce o f factors assum ed to influence tro p h ic stru c tu re (geographical e n v iro n m en t and sedi­ m en tary particle size d istrib u tio n ), th e stu d y area was subdivided in to divisions defined a priori according to th e tw o m ain stru ctu ral factors o f c o m m u n ity dis­ trib u tio n ; geographic d istrib u tio n a n d sed im en tary pattern s. T hen, a steady state tro p h ic m odel utilising th e inverse m e th o d was applied to a diagram com posed o f eight co m p artm en ts, in clu d in g d etritu s, bacteria, m eiofauna, m ac­ ro b en th o s an d fish. For each co m p artm en t, six physiological param eters w ere assessed, based o n o u r ow n data, em pirical relationships an d literatu re data. This m eth o d allow ed estim atio n o f th e flux o f m a tte r a n d energy w ith in and betw een th e u n its o f th e benthic system an d assessm ent o f th e a m o u n t o f tr o ­ phic energy sto red in these u n its (available m ostly to fish). O u r results show ed th a t suspension-feeders co n tro l m o st o f th e m a tte r transfer th ro u g h th e m acrob en th ic food-w eb, except in th e fine sand co m m u n ity , w here deposit-feeders play a d o m in a n t role. T he results also show ed th at, w hatever th e geographic area, tro p h ic stru ctu re is strongly linked to th e sed im en tary conditions. As b e n ­ thic co m m u n ities are connected th ro u g h hydrodynam ics, a m odel o f th e entire eastern basin o f th e English C hannel w ould ap p ear to be acceptable. Elowever, th e m ain sed im en t types m u st be tak en in to a cco u n t w hen establishing rela­ tio n sh ip s betw een th e fu n ctio n al units.

Marine Ecology 32 (Suppl. 1) (2011) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

G arcia , C h a rd y , D e w a ru m e z & D auvin

Introduction Ecosystem fu n ctionin g has b ecom e one o f th e m ain fields o f interest in m arin e ecology (see H o o p e r et al. 2005 for a review). A ccording to C hristensen et al. (1996), ecosystem fu n ctio n in g includes th ree m ain ph en o m en a: ecosystem properties {i.e. th e different fu nctional c o m p artm en ts o f an ecosystem and th e rates o f th e processes th a t lin k th e co m ­ p artm en ts together), ecosystem goods {i.e. th e d irect m a r­ ket values o f an ecosystem ) an d ecosystem services {i.e. the d irect or indirect benefits th a t ecosystem s p rovide to h u m an s). M arine b en th ic co m m u n ities w ere initially assessed using qualitative m eth o d s th a t identify th e tax o ­ nom ic com p o sitio n o f th e com m unity. A lthough such m eth o d s highlight en v iro n m en tal stress (Bilyard 1987) such as resistance to an th ro p o g en ic disturbances (P earson & R osenberg 1978), it is quite difficult to o b tain in fo rm a tio n a b o u t the fu nctionin g o f th e ecosystem fro m these m eth o d s (W arw ick et al. 2002). H ow ever, o th er m eth o d s based on q uantitative exam in atio n have been developed to b etter investigate th e fu n ctio n o f b en th ic invertebrates in the ecosystem. These new tools include w o rk o n m esocosm s (Solan et al. 2003), biological traits analysis (B rem ner et al. 2006) or tro p h ic w eb m odelling (C h ard y & D auvin 1992). T he tro p h ic w eb m odelling to o l appears to be essential for synthesising data, developing theories a n d d iscrim inating betw een alternative com p etin g explanations o f how ecosystem s fu n ctio n (U n d erw o o d 1990, 1996). A m ong the different tro p h ic w eb m odels already developed, steadystate/dynam ic-process m odels p rovide th e m o st explicit rep resen tatio n o f tro p h ic in teractio n (W hipple et a í 2000), particularly th e steady-state inverse m odel (C h ard y 1987; V ézina & P latt 1988; V ézina 1989). The b en thic com m u nities in th e eastern English C h an ­ nel have been w idely stu d ied using b o th qualitative descriptive m ethod s (D auvin 1997a) a n d quantitativ e analyses (Kaiser et al. 1998; Ellien et al. 2000; Newell et al. 2001). H ow ever, few studies have addressed tro p h ic relationships in this area, w ith those th a t have, focusing o n local scales only (th e Bay o f Som m e, Rybarczyk et a í 2003, a n d the Bay o f Seine, Rybarczyk & Elkaim 2003). In this context, there is a need for large-scale assessm ent of energy flow an d tro p h ic stru ctu re o f th e system , w hich can be well ap p ro x im ated using tro p h ic w eb m odelling. The m ain objective o f this stu d y was to test w h eth er the tro p h ic stru ctu re o f benthic com m unities, th ro u g h th e rela­ tio nships am o n g b en th ic invertebrates, depends m ainly on geography o r o n sed im en t type. B oth o f these factors are considered to have a stro n g co rrelatio n w ith h y drodynam ic patterns, w hich influence th e org an isatio n o f th e benthic com m unities in th e area (D auvin 1997a). W e utilised the inverse m odel sim u latio n tech n iq u e for this purp o se, w hich estim ates carbon flows th ro u g h th e b en th ic ecosystem; this

Marine Ecology 32 (Suppl. 1) (2011 ) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

was d o n e using th e q u an titativ e dataset for a large spatial area in th e eastern basin o f th e English C hannel.

M aterial and m e th o d s Study site T he area stu d ied is th e eastern basin o f th e English C h an ­ nel an d th e so u th e rn p a rt o f th e N o rth Sea, called the S o u th ern Bight. T his epicontinental sea is a shallow w ater zone (m ax im u m 50 m ) th a t is subjected to a variety of h ydro d y n am ic forces. The tidal range in th e area is high, reaching a b o u t 9 m o n th e French coast o f th e Bay of S om m e (S alom on & B reton 1991). T he tid al cu rren t velocities are highly variable, usually b eing stro n g er near th e French coast th a n th e English coast (Salom on & Bre­ to n 1991). T he w ater generally m oves fro m th e English C hannel to th e N o rth Sea, alth o u g h a long p erio d of stro n g easterly w inds can reverse this tren d (Salom on & B reton 1991). These p attern s are also m odified b y coastal g eography a n d th e presence o f th ree estuaries (th e Seine estuary, th e S om m e estuary a n d th e S cheldt-R hine-M euse estuary com plex). Local h ydrodynam ics creates particular stru ctu res, such as th e gyres th a t retain th e w ater masses in a restricted zone n ear th e B arfleur C ape in th e n o rth ­ w estern p a rt o f th e Bay o f Seine a n d th e Isle o f W right. T he particle size o f th e sed im en t is strongly correlated w ith th e hydrodynam ics described above, w ith a sed im en­ tary g rad ien t (Fig. 1) ranging fro m coarse sedim ents in th e m iddle o f th e D over Strait to fine sedim ents in the area’s bays an d estuaries (L arsonneur et al. 1982). This differential sed im en tatio n leads to a b io -sed im en tary gra­ d ien t fro m pebbles an d gravel to fine san d in th e places w here five m ain co m m u n ities have been identified previ­ ously (C abioch & G laçon 1975, 1977; C abioch et a í 1978): (i) th e pebble an d gravel c o m m u n ity w ith sessile epifauna an d O phiothrix fragilis (E chinoderm ata); (ii) the coarse san d c o m m u n ity w ith Branchiostoma lanceolatum (C ep h alo ch o rd ata); (iii) th e fin e-to -m ed iu m clean sand co m m u n ity w ith Ophelia borealis (Polychaeta); (iv) the m u d d y fine san d c o m m u n ity w ith Abra alba (M ollusca); a n d (v) th e ‘m u d d y hetero g en eo u s’ c o m m u n ity w ith a m ix o f species fro m th e pebble an d gravel com m unity, th e coarse sand c o m m u n ity a n d th e m u d d y fine sand com m unity. A dditionally, th e offshore English C hannel is m ain ly com posed o f coarse sand to pebble substrates, w hereas th e fine san d is confined to bays a n d th e littoral fringe.

Sampling strategy M acrofaunal m aterial was collected betw een 2006 an d 2008 in a n area ranging fro m th e eastern basin o f the

73

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

G arcia , C h a rd y , D e w a r u m e z & D auvin

50

1 0 0 Km

Pebbles ESI Gravels (23 Medium sand £•£] Gravely sand I ® Muddy fine sand

Fig. 1. Distribution of superficial sediment in the English Channel (from Larsonneur et al. 1982). Representation of the six geographic and sediment divisions of the eastern part of the English Channel and the Southern Bight of the North Sea. NS, North Sea; DS, Dover

English Channel France ■ Gravei and P ebbles A C o arse san d O Fine san d

English C hannel to th e so u th ern b ig h t o f th e N o rth Sea (from 0° longitu d e to th e Franco-Belgian b o rd er). The m ain objective was to u p d ate th e b en th ic invertebrate know ledge 30 years after th e first extensive b en th ic sam ­ pling in the English C hannel (d u rin g the RCP M anche survey, C abioch 8 c G laçon 1975, 1977; C abioch et a l 1978). The secondary objective was to supply th e first quantitative description o f th e b en th ic co m m u n ities over the entire area, to allow assessm ent o f th e tro p h ic stru c­ tu re o f th e b en thic co m m u n ities a n d aid th e com plex p lanning and decision-m aking req u ired for m anaging anthropogenic pressure in this dynam ic area (M artin et a l 2009). Q uantitative sam ples were taken w ith a 0.25-m 2 H am o n grab (tw o sam ples for th e m acro b en th ic fauna and one sam ple for sedim ent). As o u r focus was o n the m acrobenthic co m p o n e n t o f th e to tal b en th ic biom ass, sam ples were sieved th ro u g h a 2 -m m m esh (w hich allows m ore th a n 95% o f m acro b en th ic biom ass to be retained, see G hertsos 2 0 0 2 ). The sam ples w ere th e n sorted, an d the organism s were identified to species level w here feasi­ ble. Biom ass was d eterm in ed w ith the ash-free-dry-m ass m eth o d to reduce th e variatio n w ith in an d betw een spe­ cies due to gut c o n ten t (van der M eer et a l 2005). To extend an d im prove th e spatial reso lu tio n o f the study area, tw o o th e r quantitativ e databases were also included in this study. The first one covers th e entire Bay

74

Strait; BS, Bay of Seine.

o f Seine (see G hertsos 2002 an d D auvin 8 c Ruellet 2008 for details). The second covers th e French coast from the P ointe d ’Ailly to the Belgium b o rd e r (see D esroy et a l 2003 for details). Thus, a to tal o f 403 quantitatively sam ­ pled sites fro m th e Bay o f Seine to the S ou th ern Bight w ere available for tro p h ic web analysis (Fig. 1). All m acro fau n a l/se d im en t m aterial was gathered an d processed using th e sam e basic m ethods.

Modelling strategy M any tro p h ic web m odels have been applied to very large spatial areas, such as the N o rth Sea (M ackinson 8 c Daskalov 2007), th e Irish Sea (Fees 8 c M ackinson 2007) and the Baltic Sea (H arvey et a l 2003). To test w h eth er such a large-scale m o d el w ou ld be ap p ro p riate for th e eastern basin o f th e English C hannel, we exam ined tro p h ic stru c­ tu re at different spatial scales. To accom plish this, an a priori division o f th e area was m ade based o n the tw o m ain factors assum ed to influence th e b en th ic c o m m u n i­ ties an d th eir o rganisation (taking in to acco u n t th a t the sedim ent factor is influenced by h ydrodynam ics w hich, in tu rn , is influenced by th e geographic factor). The area was split in to three geographic divisions (Bay o f Seine, D over Strait an d N o rth Sea) an d three m ain sedim ent divisions follow ing th e d o m in a n t sedim ent types in the area (i.e. gravel a n d pebbles, coarse sand an d fine sand)

Marine Ecology 32 (Suppl. 1) (2011) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

G arcia , C h a rd y , D e w a ru m e z & D auvin

(Fig. 1). Following K röncke et al. (2004) a n d K röncke (2006), th e expression ‘geography h ere refers to all envi­ ro n m en tal variables acting over a spatial area (e.g. h y d ro ­ dynam ism , freshw ater in p u ts, food supply an d quality). Sim ulations w ere th e n ru n for th e th ree geographic divi­ sions an d th e three sed im en t divisions, a n d th e o u tp u ts fro m these sim ulations w ere com pared. Sim ulations were also ru n for each sed im en t type w ith in th e th ree geo­ graphic divisions. T hus, th ere w ere th ree sub-divisions for each division, except for th e Bay o f Seine, w hich lacks fine sand com m unities, resulting in a to tal o f eight su b ­ divisions in th e stu d y area.

M odel form ulation and principles T rophic w eb stru ctu re was assessed using a tro p h ic inverse m odel originally in tro d u c e d b y V ézina & P latt (1988) for the pelagic food-w eb o f th e English C hannel an d th e Celtic Sea, w hich since th e n has been used b y a n u m b e r o f au th o rs in various m arin e ecosystem s (C hardy et al. 1993a,b; N iquil et al. 2001; L eguerrier et al. 2003). T he inverse m ethod -b ase d steady state m odel is a diag­ nostic m eth o d th at, alth o u g h it does n o t in co rp o rate a tem p o ral dim ension, can provide a com prehensive description o f th e general tro p h ic stru ctu re o f an ecosys­ tem . O u r m odel is com posed o f eight b iotic an d abiotic c o m p artm en ts and is used to estim ate th e carbon flows resulting fro m secondary b en th ic p ro d u c tio n (C h ard y & D auvin 1992). T he in fo rm atio n req u ired for d irect esti­ m atio n o f m o st o f th e flows in such a food-w eb m o d el is either n o t available o r is very difficult to obtain. T hus, it seem s m o re ap p ro p riate to use th e flow balance principle, as th e in p u ts are equal to th e su m o f th e o u tp u ts a n d the rate o f the biom ass stan d in g stock is u n d e r steady-state conditions (V ézina & P latt 1988). This k in d o f inverse p ro b lem can be en co u n te red in all research fields w here th e n u m b er o f observations is less th a n the n u m b e r o f p aram eters th a t need to be k n o w n in ord er to describe th e system (V ézina & P latt 1988). To solve this k in d o f inverse p roblem , T aran to la & V alette (1982) have p ro p o sed th ree fu n d am en tal conditions: • H aving a given state o f in fo rm atio n a b o u t th e values o f th e observed param eters. • H aving in fo rm atio n a b o u t th e u n k n o w n param eters (we assum e th a t a n a priori decision is m ade a b o u t th e u n k n o w n p aram eter values associated w ith an interval o f confidence). • H aving the necessary in fo rm a tio n a b o u t th e th e o reti­ cal relationships betw een k n o w n data an d u n k n o w n param eters. In tro p h ic web studies, th e know n data are estim ations o f th e biom ass stan d in g stock in each b en th ic c o m p a rt­ m e n t (i.e. the biom ass values o f each c o m p artm en t); the

Marlne Ecology 32 (Suppl. 1) (2011 ) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

u n k n o w n param eters are th e physiological p aram eters (e.g. ingestion rate, egestion rate). These p aram eter values are taken fro m d ata rep o rted in th e literatu re a n d /o r fro m em pirical relationships. F rom these data, a m ean value is calculated for each param eter, an d th e m odel allows this value to m ove betw een a n u p p e r an d a low er b o u n d , w hich are d eterm in ed b y th e confidence interval o f th e m ean. The relationships linking these b o u n d s are m ain ly th e tro p h ic preferences. This m eth o d yields the a n n u al average o f th e carbon flows co nnecting th e differ­ en t functional com p artm en ts. T he fu n ctio n al diagram (Fig. 2) o f th e b en th ic com ­ p a rtm e n t needs to be sim ple en ough to fit th e different b enth ic co m m u n ities b u t also accurate enough to express th e know ledge a b o u t th e b en th ic c o m p artm en ts in the eastern basin o f th e English C hannel an d th e S ou thern B ight o f th e N o rth Sea. W e define th e functional com ­ p artm en ts based o n th e available know ledge a b o u t the tro p h ic co m p a rtm e n t an d o n th e size o f th e benthic organism (this criterio n is m ainly used to divide th e b e n ­ thic organism s betw een m acro fau n a a n d m eio fau n a com ­ p artm en ts). This is a steady-state m odel, an an n u al average rep resen tatio n o f biom asses an d flows. T em poral biom ass variatio n s are n o t considered (d X /d t) = 0. The steady-state hypothesis is expressed b y th e general equa­ tion: dX i \ \ - ¿ f = J 2 Fp - J 2 Ftp = ° Fjú su m o f th e flows going fro m 'ƒ to ‘1’ (sum

w here

o f th e in p u ts, co n su m p tio n o f Y ); Fip> su m ° f the flows going fro m ‘1’ to th e o th er co m p artm en t ‘p ’ a n d to th e general o u tp u ts o f th e system (su m o f o u tputs: predito ry m o rtality, n o n -p re d ito ry m ortality , egestion an d resp iratio n ). A t th e scale o f co m p artm en ts, th e steady-state is expressed b y th e balance o f th e processes: cLXi m — = ^ 2 ( I i - X i. Cji. (1 - Ei)) - (M í + R i)X i dt

i=

i

n

x p■° p ï = 0

-

p=

i

where: j = 1 ...m , is tn n u m b e r o f p rey available for ‘1’; p = 1 ...n , is n n u m b er o f p red ato rs o f ‘1’; Ii is an n u al ingestion rate o f ‘1’; X i is th e biom ass o f th e c o m p artm en t ‘1’; Cji is th e feeding preference o f th e co m p artm en t ‘1’ for th e resource 'ƒ; Ei is th e a n n u a l egestion rate o f ‘1’; M i is th e an n u al n o n -p re d a to ry m o rta lity rate o f ‘1’; an d R i is th e an n u al resp iratio n rate o f ‘i\ T he a n n u al p ro d u c tio n /b io m a ss (P /B ) ratios for all seven co m p artm en ts, fro m w hich th e physiological p aram -

75

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

G arcia , C h a rd y , D e w a r u m e z & D auvin

P.O.M. Flow (pelagic inputs, phytobenthos...)

Detritus Suspension-feeder X4

XI

Deposit-feeder & mixed X5

Bacteria X2

Meiofauna X5

Omnivore X7

Carnivore X6 Fish X8

eters w ere derived, w ere fo u n d in th e literatu re o n either existing tro p h ic web m odels (A m éziane et al. 1996; Leguerrier et al. 2003; M ackinson & D askalov 2007) o r field stu d ­ ies (W arw ick et al. 1978; W arw ick 1980; W arw ick & G eorge 1980; V ranken & H eip 1986; V ran k en et al. 1986). N one o f the P /B values was obtain ed w ith em pirical data. As only the largest b en th ic organism s (2 -m m sieve) were considered in this study, juveniles a n d sm all species were ignored for the biom ass estim ation. All th e large species w ere assum ed to be adults a n d we therefore decided to take the sm allest P /B fo u n d for each co m p artm en t. For bacteria, we chose a value o f 3700, w hich is an in term ed iate value betw een th a t o f 9470 p ro p o sed b y M ackinson & D askalov (2007) and 167 p ro p o sed b y A m éziane et al. (1996). The P /B o f 0.95 for th e deposit-feeders a n d 0.8 for the suspension-feeders are th e m eans o f th e P /B for all th e deposit-feeder species an d th e P /B o f bivalves, as calculated by several au th o rs w orking in highly different en v iro n ­ m ents (W arw ick & Price 1975; W arw ick et al. 1978; W arw ick 1980; W arw ick & G eorge 1980; G eorge & W a r­ w ick 1985). The deposit-feeder value agrees w ith th e P /B of the co m p artm e n t ‘sm all in fau n a (polychaetes)’ p ro p o sed by M ackinson & D askalov (2007). T he low est m eiofauna P /B value (9) p ro p o sed in th e literatu re b y G erlach (1971), was chosen to illustrate th e a u to -p re d a tio n p h en o m e n o n

76

Fig. 2. Functional diagram of the benthic ecosystem in the eastern part of the English

Channel and the southern Bight of the North Sea. Trophic fluxes: faeces + non-predatory mortality: Respiration.

th a t occurs in this group. T he carnivore P /B value (0.65) was th e calculated m ean o f th e polychaete p re d ato r P /B value given b y G eorge & W arw ick (1985) for a h a rd -b o t­ to m com m unity. T he o m n iv o re c o m p a rtm e n t has a value close to carnivores (0.7). T his value was also chosen based o n th e m ean o m n iv o re values calculated fro m those given b y G eorge & W arw ick (1985) (betw een 0.2 a n d 0.4) and those used b y M ackinson & D askalov (2007) (0.55 for the ‘crab ’ c o m p a rtm en t a n d 3 for th e ‘sh rim p ’ c o m p artm en t). T he resp iratio n rate was derived fro m th e allom etric eq uatio n developed b y Schw ingham er et al. (1986): log 1 0 Ra = 0.367 + 0.993 lo g 1 0 Pa, w here Ra is th e a n n u al res­ p ira tio n rate (in kCal-year-1) a n d Pa is th e an n u al p ro ­ d u ctio n rate (in kC al year-1). T he egestion p aram eter was d eterm in ed fro m values fo u n d in th e literature. Ingestion rates w ere d educed fro m P /B values, assum ing th a t eges­ tio n a n d resp iratio n are know n. T he biom ass o f the fo u r m acro b en th ic c o m p artm en ts - deposit-feeder & m ixed, suspension-feeder, carnivore a n d o m n iv o re - was taken fro m th e p resen t w ork. The b acteria biom ass was consid­ ered to be sim ilar to values pro v id ed b y A m éziane et al. (1996) for th e Bay o f M orlaix in th e W estern English C hannel a n d th e m eio fau n a a n d fish biom asses w ere co n ­ sidered to b e sim ilar to those in th e N o rth Sea (M ackin­ son & D askalov 2007). These th ree co m p artm en ts

Marine Ecology 32 (Suppl. 1) (2011) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

Assessment o f benthic ecosystem functioning

Table 1. Main characteristics of the functional compartments of the different divisions and sub-divisions in the eastern part of the English Channel and the Southern Bight of the North Sea and values of biotic rates used in the simulations.

Garcia, Chardy, Dewarumez & Dauvin

fÛ

L fl N

CÛ

O

o

o

o

o

o

o

O

O

O

O

O

O

o

o

o

o

o

CsJ S—- S—-

d> d> d> d> d> d>

o

C MC MC MC M O

C T i O

C T i rsl

O

O

O

C

M

O

O

O

O

O

O

o

o

O

O

O

O

O

O

co rsi Ln Ln s— o

r-.

m

o

o

o

o

o

o

O

o Ln

cri

o

o

O

O

O

o

m

^ m

o

o

o

o

C MC MC M

O

O

cm lo lo 01 o

o

w

O

O

O

O

O

o r- Ln

C i

(MinNOOr-ooirM

rsi Ln m

o

o

C MC MC MC M

O

Ln C M

coco\r^mcooh o o ^ r o ^ - o ^ - o ö ö ö ^ ö ö ö ö ö

o

o

o

o

II

O O O O O LO

o

o>

dö

cr> u_

o

lo

Ln co

r-

'xi;

rn ^

cri

C UQ r-x m

r-x o

'xt

r-x o

O O O C T i O O O O O O C O O O O O O O C O O O O O O O C T i O O O O O O C r i O O O

cu C L . -C

>•> c

3

cu

CT

tí

II

C C û o

m

o

o

o

r-x. o

o

o

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ^ - 0 0 0 0 Q- I—

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

C MC MC MC M o

o

o

o

o

o

o

o

o

o

o

C MC MC MC M

o

o

o

o

o

o

o

o

o

o

o

o

o

C MC MC MC M

o

o

o

o

o

o

o

o

O l

O o

o

o

o

o

o

o

o

o^-^-oo^-mrvOmLnommoo

o

r-x r-* o (N I o o

o

o

o

o

o

o

C O C MO

rm co co L ei 'vt cri ^ lo r^i n

o lo

rsi N

Ö

ÖÖ Ö Ö Ö

c

II

o

1/1

rn

o

o

o

o

o

o

o

r--. r--. m

r-x o

^ tú

C MC MC MC M

o

i/i m m cû m C MC MO

in

o m

O o

o

o

o

o

m "x j-

•vt 'vt ö Lri -xt

^ co o

^

r-x. lo O

i/i m cu 1

Ln

C M 'xt

1/1

Il ^ Û É

^

O O O O l O O O O O O O O O O O O O O C O O O O O O O O O O O O O O O C T i O O O

o

o o

m o o o

o o

o o

O L Oo o o

o

o

o

o

o

O "si- O O O

o o

o

o

o

o

o

o

o

O 00 o o o

o

o

o

o

o

o o

o

o

o

o

o

o

o

u

o

II

o II

o r--. co co r-' o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

o

U

C MC MC MC M C MC MC MC M m C MC MC M C MC MC MC M o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o C MC MC MC M

II

- U

co o m m m m o c m m r- i—i—o o o o o o o o

cmO ï m o m o cmco Ln m -xt m mm r-x. m o o o o < —o cm o o o o o lo r-x. o o < — o o o o o o o o o o o o o o o o o o

CTiCTiO^oor^'xtcOLnLnLnocornLnLncx.criOcOLOO^LnLno

r--.

c m lo

o CD \

^ m

•xt m ö 'xt •xt

r ^ o o m o m r M L O O L n c x - L n r M r M m o O L n c x - ' x t m L n o O L n o c r i L o r ^

O O O C T i O O O O O O C T i O O O O O O C O O O O O O O C T i O O O O O O C r i O O O

o cm o o o o o o o o mo o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o

Marine Ecology 32 (Suppl. 1) (2011) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

B/1 tyi'i

L

Û

/1 Û o L

II

77

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

(bacteria, m eio fau n a a n d fish) h ad th e sam e biom ass in each o f th e m odels applied for each division a n d su b ­ division o f o u r stu d y area. T he physiological p aram eters are presented in Table 1. D iet preference values w ere d eterm in ed according to three different sources o f in fo rm atio n . D iet d ata were preferentially taken fro m experim ental studies o f g u t co n ­ tents for particu lar species (e.g. Fauchald & Jum ars 1979; L angdon & Newell 1990) or g roups o f species (Lopez et al. 1989). D ata fro m stable iso to p e studies w ere also used, w here available (e.g. Le Loc’h & H ily 2005; C arlier et al. 2007). Finally, som e rem ain in g m issing data were also taken from previous p ublished tro p h ic w eb m odels (e.g. C hardy & D auvin 1992; A m éziane et al. 1996; L eguerrier et al. 2003). T o assess a n d com pare th e fu n ctio n in g o f each sector o f the eastern basin o f th e English C hannel a n d th e S outhern Bight o f th e N o rth Sea, sim ulations w ere based o n the sam e initial m ean values for ingestion, egestion, P /B , n o n -p re d a to ry m o rtality a n d initial m a tte r in p u t. H ow ever, the m odel was allowed to select each p aram e­ te r’s value w ith in th e confidence interval o f th e m ean for each sim ulation. The values o f biom ass a n d resp iratio n w ere fixed for each sim u latio n (i.e. th e m o d el was n o t allowed to change th em ). T he sim u latio n o u tp u ts for each division an d su b-division w ere th e average an n u al carbon flows per square m etre th a t link all functional c o m p a rt­ m ents.

C om partm ent status W e sub-divided th e b en th ic ecosystem in to eight co m ­ p artm en ts defined b y feeding m o d e an d size. The general stru ctu re o f the diagram (Fig. 2) uses th e m a in co m p o ­ nents previously p ro p o sed b y C h ard y et al. (1993a,b), to w hich we add ed th e o m n iv o re an d th e dem ersal fish com partm ents. O m nivores have been separated fro m car­ nivores because, as scavengers th a t recycle organic m atter, they have a different fu n ctio n in th e ecosystem. The fish co m p artm en t was ad d ed to ‘close’ th e b en th ic tro p h ic web. • Fi. T he initial flow. T his is th e necessary a m o u n t of organic m a tte r for th e w hole ecosystem to function. It translates as th e n e t sed im en tatio n o f pelagic d etri­ tus (dead p h y to p la n k to n cells, faeces) th a t can be used by benthic organism s. • X L D etritus. T his is a n inactive c o m p artm en t. It appears to be a cross-road fro m w hich th e carb o n is passed to h igher levels, receiving m a tte r fro m outside the system (Fi) as well as fro m inside th e tro p h ic w eb itself (i.e. egestion, n o n -p re d a tio n m ortality). • X2. Bacteria. B enthic b acteria are associated w ith particles o f detritus.

78

G arcia , C h a rd y , D e w a r u m e z & D auvin

• X3. D eposit-feeders a n d M ixed. This gro u p includes strict deposit-feeders th a t feed only o r p red o m in an tly on d etritu s at th e sed im en t layer, b u t also organism s th a t are able to feed as either deposit-feeders or sus­ p en sio n feeders. N o d istin ctio n has been m ade betw een sub-surface an d surface deposit-feeders, as they all feed o n d etritu s an d bacteria. • X4. Suspension-feeders. This g ro u p is m ain ly co m ­ posed o f filter-feeding bivalves th a t feed in the w a te r-sed im en t interface. T hey feed m o re o n fresh m a tte r th a n th e deposit-feeder gro u p does (e.g. p h y ­ to p lan k to n , m ic ro p h y to b en th o s, fresh detritu s). T hey can also feed o n bacteria b o u n d to particles. L angdon & Newell (1990) have estim ated th a t th e bacteria could rep resen t 3.5 a n d 25.8% o f carbon needs in oysters a n d m ussels, respectively. As p h y to p lan k to n is n o t represented in o u r m odel, th e tro p h ic preference o f suspension-feeders was integrated b y in cluding a preference for b en th ic bacteria an d a lesser egestion. • X5. M eiofauna. N em atodes are often th e m o st a b u n ­ d a n t organism s in th e p e rm a n en t m eio fau n a (B oaden 2005). M o st o f th e m eiofaunal organism s feed on detritu s an d bacteria, b u t som e o f th em are also car­ nivores, in clu d in g cannibalism . • X 6 . C arnivores. T his gro u p is com posed o f p redators an d carnivores. T hey only feed o n living o r alm ost living organism s; m otile n em ertean a n d polychaete p red ato rs are th e m o st representative organism s in this group. • X7. O m nivores. This gro u p consists o f species th a t have an o p p o rtu n istic feeding m ode. These species will always prefer to feed o n fresh m aterial, b u t they can also feed as scavengers o n dead bodies a n d d etri­ tus. This gro u p is m ain ly com posed o f decapods and som e gastropods. • X 8 . Fish. T he only vertebrate co m p artm en t o f this tro p h ic w eb, this gro u p is com posed o f carnivorous dem ersal fish th a t feed o n every m acro b en th ic co m ­ p a rtm e n t in th e m odel.

R esults T he su m o f th e average biom ass values o f b en th ic inverte­ brates in th e w hole stu d y area is 5.253 g O m -2 , com posed m ostly o f suspension-feeders (77% ), th e n deposit-feeders an d m ixed ( 8 % ), w ith om nivores an d carnivores having sim ilar p ro p o rtio n s (7.5 a n d 6 % , respectively) an d m eio ­ fauna having th e sm allest p ro p o rtio n (1.5% ). To assess th e tro p h ic stru ctu re o f each division a n d su b ­ division o f o u r stu d y area, th e first step was to identify the p referred tro p h ic pathw ay (i.e. th e m ain co m p artm en ts th ro u g h w hich m o st o f th e carb o n will tran sit). The fish co m p a rtm e n t (X 8 ) is always th e m o st im p o rta n t p red ato r

Marine Ecology 32 (Suppl. 1) (2011) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

Garcia, C hardy, D ew aru m ez & Dauvin

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

P.O.M. flow

Fig. 3. Results from the simulation of annual carbon flows (g G rrr2-y~1) showing a representation of (A) TP1, the trophic path­

Suspension-feeder

way In the total area; (B) TP2, the trophic pathway in the Coarse sand division; and (C) TP3, the trophic pathway In the Fine sand division. Trophic fluxes: faeces + non-predatory mortality; main pathway in the carbon transfer betw een a prey com partm ent and all of its predator com partm ents; R, respiration.

Deposit-feeder

in each o f th e m acro b en th ic com p artm en ts. T o o b tain a m o re accurate p ictu re o f th e carb o n flow th ro u g h the m acro b en th ic co m p artm en ts, we did n o t take th e fish c o m p a rtm e n t in to acco u n t w hen d eterm in in g th e tro p h ic pathw ays; fish w ere only considered as th e to p p redators, w hich cam e in to play follow ing one o f th e tw o last m a cro ­ b enth ic co m p artm en ts {i.e. carnivore a n d om nivore).

P.O.M. flow

Suspension-feeder

Deposit-feeder

T he preferential tro p h ic pathw ay for th e w hole study area begins in th e d etritu s c o m p artm en t. M o st o f th e car­ b o n in this first c o m p a rtm en t is absorbed b y th e bacteria in th e second co m p a rtm e n t (87.1% o f th e u ptake); the suspension-feeders feed m ain ly o n b acteria (72.4% ). The m a in p red ato rs o f th e suspension-feeder co m p artm en t are th e fish (59.4% ), alth o u g h th e m ain benthic in v erteb rate’s p red ato rs are th e om nivores (21.8% ). T hus, th e to tal area was considered to have a ‘su sp en sio n -feed er/o m n iv o re’ tro p h ic pathw ay (Fig. 3A).

C om parison o f the divisions

P.O.M. flow

Suspension-feeder

D ep o sit te e d e i

Marine Ecology 32 (Suppl. 1) (2011 ) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

T he su m o f th e average biom ass values o f b en th ic in verte­ brates fro m each tro p h ic co m p a rtm e n t in th e different divisions o f o u r stu d y area reached values o f 0.462, 0.794 a n d 0.508 gC-m - 2 for th e th ree geographical divisions (N o rth Sea, th e D over S trait an d th e Bay o f Seine, respec­ tively) an d 0.419, 0.917 an d 0.761 gC-m - 2 for th e three m a in sedim en t divisions (gravel an d pebbles, coarse sand a n d fine sand, respectively). In th e geographic divisions, suspension-feeders were always d o m in an t in term s o f biom ass p ro p o rtio n s, ran g ­ ing fro m 33.3% in th e N o rth Sea to 73.7% in th e D over Strait. T his p a tte rn was also observed in th e sedim ent divisions, w here th e biom ass p ro p o rtio n s o f th e su spen­ sion-feeders w ere always betw een 59.2% in th e gravel an d pebbles a n d 69.1% in th e fine sand. The highest biom ass p ro p o rtio n for th e deposit-feeders an d m ixed was fo u n d in th e N o rth Sea geographic division, w ith 18.6%, a n d in th e fine sand sed im en t division, w ith 10.9%. C arnivores a n d om nivores have q u ite sim ilar p ro p o rtio n s in the D over Strait (4.4 an d 5%, respectively) an d in th e N o rth Sea (16.5 a n d 13.6%, respectively), b u t th e carnivores clearly d o m in a te (20.6% ) th e om nivores (9.8% ) in the Bay o f Seine. H ow ever, all th e sed im en t divisions have q u ite sim ilar p ro p o rtio n s for these tw o co m p artm ents ( 8 . 1 % for th e carnivores a n d 8 .6 % for th e om nivores in

79

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

G arcia, C hardy, D ew arum ez & Dauvin

Table 2. (a) Com partm ents for each of the three preferential trophic pathways identified, (b) Preferential trophic pathw ay for each division and sub-division of the Eastern English Channel and the Southern Bight of the North Sea. (a) N°

preferential trophic pathway

TP1

Detritus-Bacteria-Suspension-feeder-Omnivore-

TP2

Fish Detritus-Bacteria-Suspension-feeder-Carnivore-

TP3

Fish Detritus-Bacteria-Deposit-feeder and Mixed-Carnivore-Fish

(b) sedimenftsite

Bay of Seine

Dover Strait

North Sea

whole

gravel and pebbles coarse sand fine sand

TP1 TP1

-

TP2 TP1 TP3

TP3 TP1 TP3

TP2 TP1 TP3

whole

TP1

TP2

TP2

TP1

the gravel a n d pebbles, 1.9 an d 4.4% in th e coarse sand and 4.7 an d 4.7% in th e fine sand). Like the tro p h ic pathw ay for th e w hole stu d y area, the Bay o f Seine h ad a ‘su sp en sio n -feed er/o m n iv o re’ p a th ­ way. H ow ever, th e D over Strait a n d th e N o rth Sea sites h ad a different type o f tro p h ic pathw ay, w ith b o th of th em having a ‘su sp en sio n -feed er/carn iv o re’ pathw ay. Each o f th e sed im en t divisions h ad a different type of tro p h ic pathw ay (Table 2a). T he gravel a n d pebbles divi­ sion h ad the sam e ‘su sp en sio n -feed er/carn iv o re’ tro p h ic pathw ay as the w hole stu d y area, th e D over Strait a n d th e N o rth Sea, d en o ted in this p a p er as TP1. T he coarse sand division h ad th e sam e ‘su sp en sio n -feed er/o m n iv ore’(Fig. 3B) tro p h ic path w ay as th e Bay o f Seine, d enoted TP2. Finally, th e fine san d division h ad th e p a th ­ w ay th a t differed th e m ost, m ainly because th e principal p rim ary consum ers sw itch fro m being suspension-feeders to being deposit-feeders an d m ixed. This sw itch gives this division a ‘deposit-feeder a n d m ix e d /ca rn iv o re ’ (Fig. 3C) tro p h ic pathw ay, den o ted TP3.

C om parison of the sub-divisions This p a tte rn o f suspension-feeder biom ass d o m in an ce was observed in alm ost all th e sub-divisions, except in the gravel an d pebbles sub-d iv isio n o f th e N o rth Sea, w here deposit-feeders an d m ixed d o m in ate w ith 32.2%. The deposit-feeder an d m ixed biom ass in one sed im en t type for one geographic area has a sim ilar value in th e sam e sedim ent type for th e o th er tw o areas, 13.2% (Bay of Seine), 13% (D over Strait) a n d 13.9% (N o rth Sea) in fine sand, an d 7.1% (Bay o f Seine), 4.9% (D over Strait) an d 7.3% (N o rth Sea) in coarse sand. The exception is for the gravel a n d pebbles, w here th e deposit-feeder a n d m ixed

80

biom ass in N o rth Sea is m u ch h igher (32.2% ) th a n in the D over Strait an d th e Bay o f Seine (5.2 an d 4.5% , respec­ tively). H ow ever, th e carnivore a n d om nivore c o m p art­ m ents d o n ’t seem to follow a p articu lar p attern , except for th e th ree N o rth Sea sub-divisions, w here th e biom ass p ro p o rtio n s in b o th co m p artm en ts are system atically higher th a n in th e o th e r five sub-divisions. T he d o m in a n t tro p h ic path w ay for all eight sub-divi­ sions is one o f th e th ree previously identified tro p h ic pathw ays for th e divisions. T he tro p h ic path w ay identified for th e geographic sub-divisions o f th e gravel an d pebbles sed im en t type changes fro m one area to an o th er. In the Bay o f Seine, th e tro p h ic p athw ay is TP2, w hich is the sam e path w ay as th e w hole Bay o f Seine; in th e D over Strait, th e tro p h ic pathw ay is TP1, w hich is the sam e p athw ay as th e w hole D over Strait; an d in th e N o rth Sea, th e tro p h ic path w ay is TP3, w hich is th e sam e pathw ay as th e w hole fine sand (Table 2b). T he tro p h ic pathw ays in th e geographic sub-divisions o f coarse sand sed im en t an d fine sand sed im en t are m uch m o re stable. T he geographic sub-divisions o f th e coarse sand follow th e TP2 pathw ay, w hatever th e geographic site considered; in o th er w ords, th e tro p h ic pathw ay is th e sam e for th e entire coarse sand division. Similarly, the tro p h ic pathw ays in all th e geographic sub-divisions o f th e fine sand sed im en t are th e sam e - TP3 - w hich is also th e tro p h ic pathw ay for th e entire fine sand division (Table 2b).

D iscussion Food-w eb studies a n d tro p h ic n etw o rk analysis provide pow erful tools for identifying th e global fu nctional p ro p ­ erties o f benthic co m m u n ities (C h ard y et al. 1993a,b). N ew techniques for describing a n d quantifying th e flows o f organic m a tte r betw een c o m p artm en ts have been developed at th e sam e tim e as num erical m eth o d s such as tro p h ic m odels. O ne o f these num erical m eth o d s for flow n etw o rk assessm ent in tro p h ic w eb is th e tro p h ic inverse m odel used in this study. T his m o d el is based o n an underlying inverse m e th o d (C h ard y 1987), w hich states th a t th e su m o f in p u ts is equal to th e su m o f o u tp u ts (V ézina & P latt 1988). Since this m odel arrived in th e late 1980s (V ézina & Platt 1988; V ézina 1989; C hardy et al. 1993a,b) it has been w idely used in m an y different enviro n m ents and b iotic com p artm en ts, such as th e French coast o f B rittany in th e W estern English C hannel (C h ard y 1987; C hardy & D auvin 1992; C hardy et al. 1993a,b; A m éziane et al. 1996), th e in tertid al m u d flat o n th e French A tlantic coast (Leguerrier et al. 2003, 2004), A rcachon Bay (Blanchet 2004), th e Baltic Sea (H arvey et al. 2003), th e coast o f N orw ay (Salvanes et al. 1992), th e M ed iterran ean (Coli

Marine Ecology 32 (Suppl. 1) (2011) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

Garcia, C hardy, D ew aru m ez & Dauvin

et a l 2006), lagoons o n th e coast o f th e Pacific O cean (N iquil et al. 2001) an d th e coast o f th e USA (Eldridge & Jackson 1993; Breed et al. 2004). Inverse m ethods (i.e. ones in w hich th e values o f the u n k n o w n param eters are d educed fro m a set o f observa­ tio ns an d a system m odel) (T aran to la & V alette 1982) seem to be totally a p p ro p ria te for food-w eb research, as researchers in this field face th e fu n d am en tal lim itatio n th a t the n u m b er o f in d ep en d e n t observations o f physio­ logical rates th a t can be m ade is far less th a n th e n u m b e r o f param eters needed to describe th e w hole system (Véz­ ina & P latt 1988). T he m ain lim ita tio n o f these m eth o d s is th a t they all assum e th e system is m ass-balanced, w hich perm its only a static rep resen tatio n o f th e food-w eb for a particular tem p o ral scale (P asquaud et al. 2007). In this study, we chose a n an n u al rep resen tatio n o f th e foodw eb, m ainly because field surveys w ere co n d u cted over 2Vi years in different seasons, m aking it im possible to take the effect o f re cru itm en t in to account. The ecological credibility o f such inverse m eth o d s depends on th e functio n al u n it, w hich needs to be h o m o g e­ neous in term s o f th e tro p h ic types, physiological rates an d life cycles o f its co m p o n en t p arts (C h ard y et a l 1993a,b). W hatever the precision level reached, determ in in g the b o u n d aries o f the fu n ctio n al u n it is based o n varied crite­ ria, w hich are always som ew hat a rb itra ry (W arw ick & R ad­ ford 1989). A n alternative ap p ro ach w ould be to base the m odels o n the individual criteria, w hich w o u ld lead to an increase in the n u m b e r o f u n k n o w n param eters. It is th u s necessary to accept th a t th e food-w eb m u st be aggregated in functional units, w hich are inevitably heterogeneous (C hardy et al. 1993a,d). F urther field studies are necessary to investigate w hether a c o m p artm en t can be described m o re accurately. For exam ple, the deposit-feeders a n d m ixed co m p artm en t seem s to be the m o st active in th e fine san d com m unity; sub-dividing this co m p artm en t in to sub-surface depositfeeder, surface deposit-feeder sensus stricto an d half d ep o sit-feed er/h alf suspension-feeder w ould p rovide m o re in fo rm atio n on th e tro p h ic stru ctu re. T here is also a need for m o re in fo rm atio n a b o u t th e m eio fau n a c o m p artm en t, w hich is the least well k n o w n co m p a rtm e n t in benthic tro p h ic w eb studies. Flowever, even if m o re detailed an d n u m ero u s co m p artm en ts w ould increase th e accuracy of o u r know ledge a b o u t th e tro p h ic system , th e difficulties o f finding physiological p aram eters w o u ld m u ltip ly w ith the increase in th e n u m b ers o f th e com p artm en ts. B enthic co m m u n ity stru ctu re is th e result o f the com plex in teg ratio n o f m an y different factors, including abiotic, biotic and an th ro p o g en ic factors (D auvin 1993, 1997b). A m ong these factors, h ydrodynam ics seem s to be the m o st im p o rta n t factor in th e o rganization o f the b enthic invertebrates in a m egatidal sea such as th e Eng­

Marine Ecology 32 (Suppl. 1) (2011 ) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

lish C hannel. T hanks to a large tid al range, th e hy d rog­ raphical influence o f large rivers a n d th e m o rp h o lo g y of th e E astern English C h annel coast, h ydrodynam ics in the C hannel vary greatly a n d have a com plex p a tte rn (Salo­ m o n & B reton 1991). These hydrodynam ics lead to differ­ ential particle-size sed im en tatio n , w ith a g rad ien t ranging fro m pebbles an d gravel to fine sand (L arso n n eu r et a l 1982). D ep en d in g o n th e sed im en t type, different b en th ic spe­ cies are able to settle an d to u n d erg o a successful m eta­ m o rp h o sis (G ray 1974). P revious au th o rs have identified five m ain b io -sed im en tary stru ctu res, w hich have been stu d ied since th e late 1970s (see D auvin 1997a). For this study, we chose th ree sed im en t divisions; coarse sedim ent - gravel an d pebbles; in term ed iate sed im en t - coarse sand; a n d fine sed im en t - fine sand. These sed im en t divi­ sions w ere associated w ith th ree geographic divisions; the Bay o f Seine, th e D over Strait an d th e N o rth Sea (Fig. 1). T his first quan titativ e ap p ro ach at such a large spatial scale as th e E astern English C hannel allowed us to com ­ p are th e tro p h ic stru ctu re in th e various sed im en t an d geographic divisions th ro u g h tro p h ic w eb m odelling. Flowever, inverse m eth o d s are based o n th e p arsim ony p rin cip le (V ézina & P latt 1988). T hus, m an y flows can be u n d erestim ated or overestim ated (L eguerrier et a l 2003). W e used sim ilar in p u t param eters to ensure an identical estim atio n error, so th a t com parisons o f th e divisions an d sub-divisions w ould rem a in possible. W e also tested each o f th e m odel o u tp u ts b y ran d o m ly selecting different val­ ues o f p articu lar organic m a tte r (P .O .M .). flow entering th e system inside a confidence interval. W e then co m p ared th e different o u tp u ts o f each division a n d su b ­ division, to m ake sure th a t th ey w ere consistent. M oreover, sensitivity analyses show ed th a t o u tp u ts from inverse m eth o d s w ere ro b u st (M arquis et a l 2007). U sing th e p referred tro p h ic path w ay identified for each division (Table 2a), we fo u n d only slight differences am o n g geo­ g raphic divisions; th e tro p h ic pathw ays in th e D over Strait a n d th e N o rth Sea w ere sim ilar an d w ere th e m ­ selves sim ilar to th e p referred pathw ay for w hole area (TP1) (Table 2b). O nly th e Bay o f Seine was fo u n d to be different (TP2). Flowever, th e tro p h ic pathw ays in th e sed im en t divi­ sions w ere very different fro m each o th er (Table 2b). For exam ple, in th e gravel a n d pebbles an d coarse sand sedi­ m e n t divisions, th e suspension-feeders w ere d o m in an t. O f th e 1 0 suspension-feeder species th a t co n trib u te m o st to th e biom ass, five species w ere observed in b o th o f the com m unities. T he presence o f these five species could be seen as en hancing th e efficiency o f th e suspension-feeder c o m p a rtm e n t in term s o f tro p h ic w eb m atter transfer. In th e h igher levels o f th e tro p h ic w eb o f these divisions, the sw itch fro m carnivore in th e gravel a n d pebbles sedim ent

81

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

Garcia, C hardy, D ew arum ez & Dauvin

Table 3. Ten main contributive species to the mean biomass of sedim ent divisions for each trophic com partm ent. deposit-feeder and mixed

B

suspension-feeder

GP Arcopagia crassa

B

carnivore

3.725 Laevicardium crassum 6.316 Psammechinus miliaris Cirriformia tentaculata 1.250 Glycymeris glycymeris 5.963 Cerebratulus spp. Chaetopterus variopedatus 0.443 Lutraria spp. 5.093 Pelogenia arenosa Golfingia (Golfingia) elongata 0.273 Mytilus edulis 3.926 Asterias rubens Upogebia deltaura 0.271 Ophiothrix fragilis 3.129 Glycinde nordmanni Echinocardium cordatum 0.195 Paphia rhomboides 2.611 Tubulanus polymorphus Callianassa tyrrhena 0.191 Aequipecten opercularis 2.286 Lepidonotus squamatus Euclymene lumbricoides 0.179 Mya arenaria 2.080 Notophyllum foliosum Golfingia (Golfingia) margaritacea 0.159 Crepidula fornicata 2.052 Harmothoe impar Cs Echinocardium cordatum 6.848 Ensis directus 42.358 Marphysa sanguinea Arcopagia crassa 6.197 Laevicardium crassum 20.484 Nephtys caeca Amphitrite johnstoni 4.110 Spisula solida 3.116 Pelogenia arenosa Cirriformia tentaculata 1.250 Solecurtus scopula 2.912 Nephtys assimilis Tellina fabula 1.014 Glycymeris glycymeris 2.580 Lumbrineris latreilli Callianassa tyrrhena 0.703 Ensis arcuatus 2.306 Nephtys hombergii Tellina tenuis 0.673 Mya arenaria 2.080 Sigalion mathildae Callianassa tyrrhena 0.703 Aequipecten opercularis 1.793 Lumbrineris fragilis Echiurus echiurus 0.395 Ophiothrix fragilis 1.622 Nephtys longosetosa Callianassa subterranea 0.382 Solen marginatus 1.493 Gattyana cirrhosa Fs Echinocardium cordatum 12.955 Ensis directus 11.750 Nemertina Cirriformia tentaculata 1.250 Spisula solida 4.446 Nephtys hombergii Corbula gibba 0.675 Acanthocardia 3.897 Sthenelais boa (.Rudicardium) tuberculata Tellina fabula 0.352 Venerupis senegalensis 2.225 Lumbrineris fragilis Owenia fusiformis 0.284 Mya arenaria 2.080 Nephtys assimilis Tellina tenuis 0.262 Donax vittatus 1.927 Nephtys caeca Macoma balthica 0.248 Ensis arcuatus 1.921 Sigalion mathildae Callianassa subterranea 0.244 Lutraria angustior 1.827 Nephtys longosetosa Acrocnida brachiata 0.179 Spisula elliptica 1.245 Cerebratulus spp. Upogebia deltaura 0.174 Lutraria lutraria 1.168 Nephtys cirrosa

B

omnivore

B

0.145 Buccinum undatum

1.881

0.136 Necora puber 0.077 Sagartia troglodytes 0.059 Urticina felina

1.394 1.263 0.837

0.045 Atelecyclus rotundatus 0.635 0.011 Nassarius reticulatus 0.325 0.008 0.007 0.006 1.037 0.660 0.352 0.339 0.283 0.245 0.193 0.188 0.174 0.114 1.017 0.400 0.353

Ophiura ophiura Liocarcinus depurator Ophiura spp. Buccinum undatum Urticina felina Nassarius reticulatus Sagartia troglodytes Liocarcinus holsatus Diogenes pugilator Nassarius reticulatus Ophiura ophiura Cereus pedunculatus Atelecyclus rotundatus Nassarius reticulatus Diogenes pugilator Sagartia troglodytes

0.229 0.173 0.135 2.153 1.025 1.019 0.753 0.634 0.584 0.533 0.515 0.464 0.346 0.986 0.642 0.573

0.322 Ophiura ophiura 0.318 Pagurus bernhardus 0.288 Thia scutellata

0.456 0.263 0.151

0.266 Liocarcinus holsatus 0.107 Trivia monacha

0.145 0.074

0.094 Liocarcinus marmoreus 0.065 0.068 Liocarcinus depurator 0.054

B = mean annual biomass of the species in g-m 2-year 1 (ash-free dry weight); GP = Gravel and pebbles; Cs = Coarse sand; Fs = Fine sand.

division to om n iv o re in th e coarse sand sed im en t is m o re difficult to explain. T his could be because th e om nivores in coarse sand have a m o re regular biom ass d istrib u tio n am ong th e 1 0 species th a t d o m in ate th e biom ass (Table 3). T he tro p h ic pathw ay also sw itches fro m suspension-fee­ der d o m inance to deposit-feeder an d m ixed d o m inance betw een coarse san d a n d fine sand, despite th e fact th a t b o th these divisions have q uite sim ilar species. This sw itch can be explained b y th e increase in biom ass o f one deposit-feeder species, th e sea u rc h in Echinocardium cord­ atum , associated w ith th e decrease in biom ass o f th e d o m in an t suspension-feeder species, Ensis directus, w hich has its biom ass value divided b y fo u r in th e fine san d sed­ im en t division. Finally, th e sw itch betw een carnivore dom inance in fine san d to om nivore do m in an ce in coarse sand, seem s to be due m ostly to th e absence o f a signifi­ cant decrease in th e large o m n iv o ro u s cn id arian Urticina felina an d m olluscs B uccinum u n d a tu m a n d Nassarius reticulatus, w hich co n trib u te m o st to th e biom ass of the coarse sand sed im en t division.

82

In his tro p h ic m odel o f th e b en th ic tro p h ic web in A rcachon Bay, B lanchet (2004) fo u n d th e sam e depositfeeder d o m in an ce in a sim ilar fine sed im en t type, b u t w ith a large difference in th e m ean deposit-feeder biom ass (0.08 g O m - 2 in o u r stu d y com p ared w ith 0.52 g O m - 2 in A rcachon Bay), pro b ab ly due to the presence o f th e seagrass Zostera noltii. U nfortunately, fu r­ th er com parisons o f o u r results w ith those o f adjacent m arin e areas are q u ite difficult to carry out. T he m odels o f M ackinson & D askalov (2007) for th e N o rth Sea, and Lees & M ackinson (2007) for th e Irish Sea, m ainly deal w ith fisheries m anagem ent. In ad d itio n , these au th o rs did n o t investigate tro p h ic stru c tu re at th e b en th ic level and th e fu n ctio n al c o m p artm en ts utilised w ere very different. In th e M arennes-O lérons, L eguerrier et a l (2003) sought to highlight th e differences betw een th e carb o n flows o f cultivated oysters an d those o f n o n -cu ltiv ated benthos, a n d th e m odels m ad e for th e W estern English C hannel (C h ard y & D auvin 1992; A m éziane et al. 1996) w ere used m ainly to investigate b en th ic-p elag ic relationships, and used different com p artm en ts.

Marine Ecology 32 (Suppl. 1) (2011) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

Garcia, C hardy, D ew aru m ez & Dauvin

C om parison am o n g sub-divisions ten d s to show th at the im p o rtan ce o f th e geographic factor is low. In fact, for the geographic coarse san d an d th e fine san d su b -d iv i­ sions, no m a tte r w h at geographic lo catio n is considered, the tro p h ic stru ctu re always follows th e tro p h ic p athw ay o f th e sedim ent type to w hich it belongs (Table 2b). H ow ever, no clear p a tte rn ap p eared for th e gravel an d pebbles sedim ent. T his lack o f a clear p a tte rn can be explained b y th e sam pling m eth o d ; all th e sites w ere sam ­ pled w ith the quantitativ e H a m o n grab sam pling gear w hich reaches its fu nctional lim its in pebbles an d stony b o tto m s. T hus, it appears th a t th e gravel a n d pebbles sed­ im en t was u nder-sam p led . In a d d itio n , am o n g th e three sedim en t types, gravel an d pebbles appear to be th e least accurate in term s o f representing b en th ic o rganisation an d functioning, w hich could explain th e lack o f a clear p a tte rn observed in this division. It is unclear even for the coarse sand an d fine san d sed im en t types w h eth er the observed features are n a tu ra l o r directly d ep en d en t o n the sam pling strategy. In th e ir stu d y o f th e effects o f sam pling effort o n food-w eb stru ctu re, M artin ez et al. (1999) show ed th a t m ajo r tro p h ic w eb p ro p erties like fo o d chain length app ear to be ro b u st to v ariatio n in sam pling reso­ lution. H ow ever, fu rth e r investigations are req u ired to confirm this conclusion, p articularly assessm ent o f the o th er b io -sedim entary co m m u n ities o f th e E astern English C hannel an d the S ou th ern N o rth Sea {i.e. m u d d y -fin e sand an d m u d ). T he use o f a 2 -m m sieve is ap p ro p riate for sam pling large-sized species, b u t can u n d erestim ate sm all species, including som e deposit-feeders an d m ixed. H ow ever, m o re th a n 95% o f m acro b en th ic biom ass is retained o n 2 -m m sieve m esh (G hertsos 2002) a n d the p red o m in an tly pebbles to coarse san d co m m u n ities o f the E astern English C hannel are d o m in ated b y large-sized suspension-feeder species (D auvin & R uellet 2008), so this bias is m ainly restricted to th e less c o m m o n fine sedi­ m ents. A ccording to V ézina & P latt (1988), th e inverse m e th ­ ods provide a stro n g fo u n d a tio n for a n effective co m p ara­ tive analysis o f food-w eb dynam ics. T his stu d y allowed us to determ ine th a t th ere is v ariatio n in tro p h ic organisa­ tio n in th e E astern English C hannel an d th e S ou thern N o rth Sea, dependin g o n th e scale o f observation. In this respect, th e sedim en t division (th u s th e b io -sed im en tary division) appears to be th e m o st im p o rta n t factor co n ­ trolling b enthic ecosystem fu n ctio n in g in th e area, w ith the possible exception o f th e Bay o f Seine d u e to its very particular features {i.e. an enclosed b ay in close p ro x im ity to a river). T he tro p h ic org an isatio n o f th e overall area is an in teg ratio n o f th e specific p ro p erties o f each individual functional unit. T hus, views o f th e tro p h ic stru ctu re of the system can differ dep en d in g o n th e scales an d factors considered. F u rth er investigations are needed to identify

Marine Ecology 32 (Suppl. 1) (2011 ) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

a n d d eterm in e th e spatial lim its o f th e in d ividual func­ tio n al u n its, as well as th e ir intrinsic properties.

Lim itations and P ersp ectives A m o d el is a conceptual rep resen tatio n o f a particular ecosystem , w hich has th e p rim a ry advantage o f gathering a n d su m m arising th e cu rre n t know ledge o f ecosystem fu n ctio n in g (B arnsley 2007). T his stu d y show s th at inverse m odels are extrem ely useful for investigating the tro p h ic stru ctu re o f b en th ic ecosystems. O u r tro p h ic inverse m odel allow ed us to d eterm in e th e specific co n d i­ tio n s u n d e r w hich th e d etritic co m p artm en t is utilised a n d to identify w hich flows are th e m o st im p o rta n t for overall fu n ction in g o f th e system. The com parisons o f the different sed im en t a n d geographic divisions w ere also use­ ful for u n d e rsta n d in g th e v ariations in ecosystem func­ tions, for identifying general in fo rm a tio n a b o u t benthic fun ction in g , a n d th u s for p ro v id in g a basis for co m p ari­ so n w ith o th er b en th ic ecosystems. H ow ever, using this k in d o f m odel is only possible w hen q u an titativ e d ata are available, w hich leads to th e m ain p ro b lem w ith a stu d y such as ours; as far as th e benthic c o m p a rtm e n t is concerned, inverse m odels can only be used for sed im en t types in w hich a quan titativ e sam pling gear can operate. Pebbles an d sto n y sed im en t are excluded, unless SCUBA divers are em ployed, w hich involves m u ch m o re w o rk com p ared w ith th e so ft-b o tto m com m unities. A n o th er inconvenience o f inverse m odels is th a t they req u ire access to m an y physiological param eters th a t are h a rd to obtain. O ne so lu tio n to overcom e this difficulty is to derive all necessary physiological param eters {e.g. resp iratio n , ingestion) fro m th e P /B value for each com ­ p a rtm en t. T he P /B values for m an y species a n d /o r com ­ p a rtm e n ts are w idely available in th e literature, b u t they vary greatly dep en d in g o n th e authors. T his v ariatio n can be explained b y th e different m eth o d s used for th e assess­ m en t, b u t also b y th e intrinsic p ro p erties o f P /B . The an n u al P /B o f a co h o rt usually decreases w ith age; it fol­ lows th a t p o p u latio n s d o m in ated b y older year classes will have a low er P /B th a n those com posed o f yo u n g er in d i­ viduals (W arw ick 1980). A n o th er so lu tio n w ould be the coupling o f this k in d o f w o rk w ith o th er m odelling m e th ­ ods such as th e m o d el o f size spectra developed b y Jen­ n ings et al. (2002) for th e b en th ic system. This m e th o d assum es th a t organism s w ith h igher b o d y m ass feed at h igher tro p h ic levels, m ean in g th a t it requires fewer p aram eters to assess th e m ain energy flow th ro u g h the food-w eb. T o th e p ro b lem o f v ariatio n in this well know n co m p artm en t, it is necessary to a d d th e p ro b lem o f the c o m p artm en ts a b o u t w hich little is k n o w n - th e black boxes such as b en th ic bacteria or m eiofauna. As few studies

83

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

o f these co m p artm en ts are available, it is extrem ely difficult to gather th e necessary param eters w hich, b y v irtu e o f th eir lack o f atten tio n , are plagued b y in certitude. A n o th er p ro b lem is th a t m acro b en th ic co m m un ities are well know n for having large flu ctu atio n s in biom ass and abundance fro m year to year, m ainly due to p red a­ tio n o n larvae in th e p lan k to n (T h o rso n 1946) o r newly settled juveniles. In ad d itio n , high ad u lt m o rtality can also occur (W arw ick 1980). For these reasons, th e tro p h ic rep resen tatio n for 1 year m ay n o t be valid th e follow ing year. This is particu larly evident in p o p u latio n s th a t are do m in ated by species w ith long-lived plan k to n ic larvae, w hich are considered to have highly u nstable dynam ics (T h o rso n 1946). O u r stu d y has show n th at, as far as th e b en th ic co m ­ p a rtm e n t is concerned, a large-scale spatial m odel seems to be acceptable for o u r stu d y area, as th e b en th ic co m ­ m unities are all influenced b y hydrodynam ics. N o n e th e ­ less, as b enthic tro p h ic fu n ctio n in g is variable an d strongly d ep en d en t o n sed im en t type, this m odel w ould have to take in to acco u n t at least th e th ree m ain sed im en t types {i.e. gravel an d pebbles, coarse san d an d fine sand).

G arcia, C hardy, D ew arum ez & Dauvin

Boaden P.J.S. (2005) Irish intertidal m eiofauna: a m odicum o f progress. In: W ilson J.G. (Ed.), The Intertidal Ecosystem: The Value o f Ireland’s Shores. Royal Irish Academy, Dublin: 81-99. Breed G.A., Jackson G.A., R ichardson T.L. (2004) Sedim enta­ tion, carbon export a n d food web structure in the Missis­ sippi River plum e described by inverse analysis. M arine Ecology Progress Series, 278, 35-51. B rem ner J., Rogers S.I., Frid C.L.J. (2006) M ethods for describ­ ing ecological functioning o f m arine benthic assemblages using biological traits analysis (BTA). Ecological Indicators, 6, 609-622. C abioch L., Glaçon R. (1975) D istribution des peuplem ents benthiques en M anche orientale, de la baie de Som m e au Pas-de-Calais. Comptes Rendus de YAcademie des Sciences (Paris), 280, 491-494. C abioch L., Glaçon R. (1977) D istribution des peuplem ents benthiques en M anche orientale d u cap d ’A ntifer à la baie de Som m e. Comptes Rendus de YAcademie des Sciences (Paris), 285, 209-212. C abioch L., Gentil F., Glaçon R., Retières C. (1978) Le bassin oriental de la M anche, m odèle de d istribution de peuple­ m ents benthiques dans une m er à fortes marées. Journal de Recherche Océanographique, 3, 249-254.

A c k n o w le d g e m e n ts The au th o rs w ish to th a n k D r A urélie Foveau, A urore Savina, Em ilie H ouillez an d A m élie C h arn o z for th eir help in the so rting a n d identification o f th e species, Eric Lecuyer, D r N icolas D esroy, D r N icolas S pilm o n t and th e offi­ cers an d crew o f th e RV Cotes de la M anche for th eir effort at sea, Lisa Spencer a n d D r Julie B rem ner for correcting the English syntax a n d g ram m ar, an d tw o a n o n y m o u s ref­ erees for th eir helpful suggestions a n d com m ents. This w ork was carried o u t w ith financial c o n trib u tio n o f th e E uropean U n io n ’s In terreg Illa schem e (E u ro p ean R egio­ nal D evelopm ent Funds) CE1ARM 2 p ro ject co o rd in ated by A. C arpentier, Ifrem er, B oulogne-sur-m er.

Carlier A., Riera P., A m ouroux J.-M., B odiou J.-Y., Grém are A. (2007) Benthic trophic netw ork in the Bay o f Banyulssur-M er (northw est M editerranean, France): an assessment based o n stable carbon a n d nitrogen isotopes analysis. Estuariae, Coastal and S helf Science, 72, 1-15. C hardy P. (1987) M odèle de sim ulation d u système benthique des sédim ents grossiers d u golfe n o rm an d -b re to n (M anche). Oceanologica Acta, 10, 421-434. C hardy P., D auvin J.-C. (1992) C arbon flows in a subtidal fine sand c om m unity from the w estern English Channel: a sim ulation analysis. M arine Ecology Progress Series, 81, 147-161. C hardy P., D auvin J.-C., Lasserre P. sity and

(1993a)

Biodiver­

functional units in a coastal benthic

web. W orkshop

Biodiversity, P oint-á-P itre,

food

G uadeloupe:

1- 8 .

R eferen ces Am éziane N., C hardy P., D auvin J.-C. (1996) M odelling carbon flows in soft-bottom com m unities from the bay o f M orlaix, w estern English C hannel. In: Eleftheriou A.d. (Ed.), Biology

C hardy P., Gros P., M ercier H., M onbet Y. (1993b) Benthic carbon budget for the Bay o f Saint Brieuc (W estern C han­ nel). A pplication o f the inverse m ethod. Oceanologica Acta, 16, 687-694. C hristensen N.L., B artuska A.M., Brown J.H., C arpenter

and Ecology o f Shallow Coastal Waters, 28 EMBS Sym posium .

S.R., D ’A ntonio C., Francis R., Franklin J.F., M acM ahon

Olsen & Olsen, Fredenstourg, D enm ark: 215-224.

J.A., Noss R.F., Parsons D.J., Peterson C.H., T urner

Barnsley M.J. (2007) Environm ental Modeling: A Practical Intro­

M.G., W oodm ansee R.G. (1996) The re p o rt o f the

duction. Taylor & Francis G roup, Boca R aton, FL: 406 pp. Bilyard G.R. (1987) The value o f benthic infauna in m arine

Ecological Society o f A m erica C om m ittee o n the Scien­

pollution m on ito rin g studies. M arine Pollution Bulletin, 18, 581-585. Blanchet H . (2004) Structure et fonctionnem ent des

84

tific Basis for Ecosystem M anagem ent. Ecological Applica­ tion, 6, 665-691. Coli M., Palom era I., T udela S., Sarda F. (2006) T rophic flows, ecosystem structure and fishing im pacts in the South

peuplem ents benthiques d u Bassin d ’A rcachon. Ph.D . thesis,

C atalan Sea, N orthw estern M editerranean. Journal o f M arine

U niversité de B ordeauxl, Bordeaux: 331 pp.

Systems, 59, 63-96.

Marine Ecology 32 (Suppl. 1) (2011) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

Garcia, C hardy, D ew aru m ez & Dauvin

D auvin J.C. (1993) Le benthos: tém oin des variations de l’envi­ ronnem ent. Oceanis, 19, 25-53. D auvin J.C. (1997a) Les biocénoses marines et littorales français­ es des côtes Atlantique, M anche et M er dn Nord, syntheses, menaces et perspectives. M N H N , Paris: 359 pp.

K röncke I. (2006) Structure a n d function o f m acrofaunal com ­ m unities influenced by hydrodynam ically controlled food availability in the W adden Sea, the open N o rth Sea and the dees-sea. Senckenbergiana m aritim a, 36, 1-18. K röncke I., Stoeck T., W ieking G., Palojaervi A. (2004) Rela­

D auvin J.C. (1997b) E volution à long term e des peuplem ents

tionship betw een structure a n d function o f m icrobial and

de sédim ents fins sablo-vaseux de la M anche et de la m er

m acrofaunal com m unities in different areas o f the N orth

deu N ord. Oceanis, 23, 113-144. D auvin J.-C., Ruellet T. (2008) M acrozoobenthic biom ass in

Sea. M arine Ecology Progress Series, 282, 13-31. L angdon C.J., Newell R.I.E. ( 1990) C om parative utilization o f

the Bay o f Seine (eastern English C hannel). Journal o f Sea

detritus a n d bacteria as food sources by two bivalve suspen­

Research, 59, 320-326.

sion-feeders, the oyster Crassostrea virginica and the mussel,

D esroy N., W arem bourg C., D ew arum ez J.-M., D auvin J.-C. (2003) M acrobenthic resources o f the shallow soft-bottom sedim ents in the eastern English C hannel and southern N o rth Sea. ICES Journal o f M arine Science, 60, 120-131. Eldridge P.M ., Jackson G.A. (1993) Benthic trophic dynam ics in C alifornia coastal basin a n d continental slope c o m m u n i­

Geukensia demissa. M arine Ecology Progress Series, 58, 2 9 9 310. L arsonneur C., Bouysse P., Auffret J.P. (1982) The superficial sedim ents o f the English C hannel and its W estern Approaches. Sedimentology, 29, 851-864. Le Loc’h F., H ily C. (2005) Stable carbon and nitrogen isotope

ties inferred using inverse analysis. M arine Ecology Progress

analysis o f Nephrops norvegicus/Merluccius merluccius fishing

Series, 99, 115-135.

grounds in the Bay o f Biscay (NE A tlantic). Canadian Jour­

Ellien C., T hiébaut E., Barnay A.-S., D auvin J.-C., Gentil F., Salom on J.-C. (2000) The influence o f variability in larval

nal o f Fisheries and Aquatic Sciences, 62, 123-132. Lees K., M ackinson S. (2007) An E copath m odel o f the Irish

dispersal o n the dynam ics o f a m arine m etapopulation in

Sea: ecosystems properties and sensitivity analysis. Science

the eastern Channel. Oceanologica Acta, 23, 423-442.

Series Technical Report. Cefas, Lowestoft: 49 pp.

Fauchald K., Jum ars P.A. (1979) The diet o f w orm s: a study o f

Leguerrier D., N iquil N., Boileau N., Rzeznik J., Sauriau P.-G.,

polychaete feeding guilds. Oceanography and M arine Biology

Le M oine O., Bacher C. (2003) N um erical analysis o f the

an A nnual Review, 17, 193-284.

food web o f an intertidal m udflat ecosystem o n the Atlantic

George C.L., W arw ick R.M. (1985) A nnual m acrofauna p ro ­ d uction in a h a rd -b o tto m reef com m unity. Journal o f the

coast o f France. M arine Ecology Progress Series, 246, 17-37. Leguerrier D., N iquil N., Petiau A., Bodoy A. (2004) M odeling

M arine Biological Association o f the United Kingdom, 65,

the im pact o f oyster culture o n a m udflat food web in

713-735.

M arennes-O léron Bay (France). M arine Ecology Progress

Gerlach S.A. (1971) O n the im portance o f m arine m eiofauna for benthos com m unities. Oecologia, 6, 176-190. Ghertsos K. (2002) Structure spatio-tem porelle des peuple­ m ents m acrobenthiques de la baie de Seine à plusieurs

Series, 273, 147-162. Lopez G., T aghon G.L., L evinton J. (1989) Ecology o f M arine Deposit Feeders. Springer-Verlag, New York. M ackinson S., Daskalov G. (2007) A n ecosystem m odel o f the

échelles d ’observation. Ph.D. thesis, Université des Sciences

N o rth Sea to su p p o rt an ecosystem approach to fisheries

et Technologies de Lille: 181 pp.

m anagem ent: description a n d param eterisation. Science

Gray J.S. ( 1974) A nim al-sedim ent relationship. Oceanography and M arine Biology: A n A nnual Review, 12, 223-261. H arvey C.J., Cox S.P., Essington E., H ansson S., Kitchell J.F.

Series Technical Report. Cefas, Lowestoft: 142 pp. M arquis E., N iquil N., Delmas D., H a rtm a n n H.J., B onnet D., C arlotti F., H erbland A., Labry C., Sautour B., Laborde P.,

(2003) A n ecosystem m odel o f food web and fisheries in te r­

D upuy C. (2007) Planktonic food web dynam ics related to

actions in the Baltic Sea. ICES Journal o f M arine Science, 60,

phytoplankton bloom developm ent on the continental shelf

939-950. H ooper D.U., C hapin F.S., Ewel J.J., H ector A., Inchausti P., Lavorel S., Law ton J.H., Lodge D.M ., Loreau M., N aeem S., Schm id B., Setälä H., Sym stad A.J., V anderm eer J., W ardle

o f the Bay o f Biscay, French coast. Estuariae Coastal and Shelf Science, 73, 223-225. M artin C.S., C arpentier A., Vaz S., C oppin F., C uret L., D auvin J.-C., Delavenne J., D ew arum ez J.-M ., D upuis L., Engelhard

D.A. (2005) Effects o f biodiversity o n ecosystem functioning:

G., E rnande B., Foveau A., Garcia C., Gardei L., H arro p S.,

a consensus o f cu rren t knowledge. Ecological Monographs,

Just R., K oubbi P., Lauria V., M eaden G.J., M orin J., O ta Y.,

75, 3-35. Jennings S., Pinnegar J.K., P olunin N.V.C., W arr K.J. (2002)

Rostiaux E., Sm ith R., Spilm ont N., V erin Y., Villanueva C., W arem bourg C. (2009) The C hannel habitat atlas for m arine

Linking size-based and trophic analyses o f benthic c o m m u ­

resource m anagem ent (CHARM ): an aid for planning and

nity structure. M arine Ecology Progress Series, 226, 77-85.

decision-m aking in an area u n d e r strong anthropogenic pres­

Kaiser M.J., A rm strong P.J., D are P.J., Flatt R.P. (1998) Ben­ thic com m uniies associated w ith heavily fished scallop

sure. A quatic Living Resources, 22, 499-508. M artinez N.D., H aw kins B.A., D aw ah H.A., Feifarek B.P.

gro u n d in the English C hannel. Journal o f the M arine Biolog­

(1999) Effects o f sam pling effort o n characterization o f

ical Association o f the United Kingdom, 78, 1045-1059.

food-w eb structure. Ecology, 80, 1044-1055.

Marine Ecology 32 (Suppl. 1) (2011 ) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

85

A ssessm ent o f b e n th ic ecosystem fu n c tio n in g

van der M eer J., H eip C.H., H erm an

G arcia, C hardy, D ew arum ez & Dauvin

M oens T., van

Oevelen D. (2005) M easuring the flow o f energy a n d m atter in m arine benthic anim al population. In: Eleftheriou A., M cIntyre A. (Eds), M ethods for the Study o f M arine Benthos. Blackwell Science, Oxford: 326-407. Newell R.C., Seiderer L.J., R obinson J.E. (2001) Anim al: sedi­ m ent relationships in coastal deposits o f the eastern English Channel. Journal o f the M arine Biological Association o f the United Kingdom, 81, 1-9. N iquil N., Pouvreau S., Sakka A., Legendre L., Addessi L., Le Borgne R., C harpy L., Delesalle B. (2001) T rophic web

to the planktonic larvae in the sou n d (O resund). Meddelelser Fra Kommissionen fo r Danm arks fisheri- Og Havundersogelser, Serie: Plankton, 4, 1-523. U nderw ood A.J. (1990) Experim ents in ecology and m anage­ m ent: thei logics, functions and interpretations. Australian Journal o f Ecology, 15, 365-389. U nderw ood A.J. (1996) D etection, interpretation, prediction a n d m anagem ent o f environm ental disturbances: som e roles for experim ental m arine ecology. Journal o f Experimental M arine Biology and Ecology, 200, 1-27. Vézina A.F. ( 1989) C onstruction o f flow netw orks using

and carrying capacity in a pearl oyster farm ing lagoon

inverse m ethods. In: W ulff F., Field J.G., M ann K.H. (Eds),

(T akapoto, French Polynesia). Aquatic Living Resources, 14,

N etwork Analysis in M arine Ecology: M ethods and Applica­

165-174. P asquaud S., Lobry J., Elie P. (2007) Facing the necessity o f

tions. Springer-Verlag, Berlin: 62-81. Vézina A.F., Platt T. (1988) Food web dynam ics in the ocean.

describing estuarine ecosystems: a review o f food web ecol­

I. Best-estim ates o f flow netw orks using inverse m ethods.

ogy study techniques. Hydrobiologia, 588, 159-172.

M arine Ecology Progress Series, 42, 269-287.

Pearson T.H., Rosenberg R. (1978) M acrobenthique succession in relation to organic enrichm ent a n d pollution o f the m arine environm ent. Oceanography and M arine Biology: A n A nnual Review, 16, 229-311. Rybarczyk H., Elkaim B. (2003) A n analysis o f the trophic netw ork o f a m acrotidal estuary: the Seine E stuary (Eastern

V ranken G., H eip C. (1986) The productivity o f m arine n em a­ todes. Ophelia, 26, 429-442. V ranken G., H erm an P.M.J., V incx M ., H eip C. ( 1986) A reevaluation o f m arine nem atode productivity. Hydrobiologia, 135, 193-196. W arw ick R.M. (1980) P opulation dynam ics and secondary

Channel, N orm andy, France). Estuarine, Coastal and Shelf

pro d u ctio n o f benthos. In: T enore K.R., C oull B.C. (Eds),

Science, 58, 775-791.

M arine Benthic Dynamics. The Belle W . B aruch Library in

Rybarczyk H., Elkaim B., Ochs L., L oquet N. (2003) Analysis o f the trophic netw ork o f a m acrotidal ecosystem: the Bay

M arine Science, Colum bia: 1-24. W arw ick R.M., George C.L. (1980) A nnual m acrofauna

o f Som m e (Eastern Channel). Estuarine, Coastal and Shelf

pro d u ctio n in an Abra com m unity. In: Collins M.B. (Ed.),

Science, 58, 405-421.

Industrialized Embayments and Their Environm ental Prob­

Salom on J.-C., B reton M. (1991) C ourants résiduels de m arée dans la M anche. Oceanologica Acta, 11, 47-53. Salvanes A.G.V., Aksnes D.L., Giske J. ( 1992) Ecosystem m odel for evaluating potential cod pro d u ctio n in a west Norw egian fjord. M arine Ecology Progress Series, 90, 9-22. Schwingham er P., Hargrave B., Peer D., H aw kins C.M. (1986) P artitioning o f p ro d u c tio n and respiration am ong size groups o f organism s in an intertidal benthic com m unity. M arine Ecology Progress Series, 31, 131-142. Solan M., G erm ano J.D., R hoads D.C., Sm ith C., M ichaud E., P arry D., W enzhöfer F., K ennedy B., H enriques C., Battle E., Carey D., Iocco L., Valente R., W atson J., Rosenberg R.

lems. Pergam on, Oxford: 517-538. W arw ick R.M., Price R. (1975) M acrofauna p ro d u c tio n in an estuarine m ud-flat. Journal o f the M arine Biological Associa­ tion o f the United Kingdom, 55, 1-8. W arw ick R.M., R adford P.J. ( 1989) Analysis o f the flow netw ork in an estuarine benthic com m unity. In: W ulff F., Field J.G., M ann K.H. (Eds), N etwork Analysis in M arine Ecology: M eth­ ods and Applications. Springer-Verlag, New York: 220-231. W arw ick R.M., George C.L., Davies J.R. (1978) A nnual m acro­ fauna pro d u ctio n in a V enus com m unity. Estuarine and Coastal M arine Science, 7, 215-241. W arw ick R.M., A shm an C.M., Brown A.R., Clarke K.R., Dowell

(2003) Tow ards a greater u nderstanding o f p attern, scale

B., H a rt B., Lewis R.E., Shillabeer N., Som erfield P.J., T app

and process in m arine benthic systems: a picture is w orth

J.F. (2002) Inter-an n u al changes in the biodiversity and com ­

th an a th o u san d w orm s. Journal o f Experimental M arine

m u n ity structure o f the m acrobenthos in Tees Bay a n d the

Biology and Ecology, 285-286, 313-338.

Tees estuary, UK, associated w ith local a n d regional environ­

T arantola A., Valette B. (1982) Generalized nonlinear inverse problem s solved using the least squares criterion. Reviews o f Geophysics and Space Physics, 20, 219-232. T horson G. (1946) R eproduction and larval developm ent of

m ental events. M arine Ecology Progress Series, 234, 1-13. W hipple S.J., Link J.S., G arrison L.P., Fogarty M.J. (2000) M odels o f predation a n d fishing m ortality in aquatic ecosys­ tem s. Fish Fisher, 1, 22-40.

danish m arine b o tto m invertebrates, w ith special reference

86

Marine Ecology 32 (Suppl. 1) (2011) 7 2 -8 6 © 2011 Blackwell Verlag GmbH

marine ecology

an evolutionary perspective

»

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

Epiphytes and associated fauna on th e brown alga Fucus vesiculosus in the Baltic and th e North Seas in relation to different abiotic and biotic variables Priit K ersen 1,2, J o n n e K o tta 1, M artyn as B u cas3, N atalja K o le so v a 4 & Z a n e D é f é r é 5 1 Estonian Marine Institute, University of Tartu, Tallinn, Estonia 2 Institute of M athematics and Natural Sciences, Tallinn University, Tallinn, Estonia 3 Coastal Research and Planning Institute, University of Klaipeda, Klaipeda, Lithuania 4 Marine Systems Institute, Tallinn University of Technology, Tallinn, Estonia 5 Laboratory of Marine Ecology, Institute of Biology, University of Latvia, Salasplls, Latvia

K eywords Community composition; dominance structure; eplblonts; fucolds; host frond; marine benthos; mobile invertebrates; seaweeds; spatial variability; wave exposure. C orrespondence Priit Kersen, Estonian Marine Institute, University of Tartu, Mäealuse 14, 12618 Tallinn, Estonia. E-mail: pkersen@ ut.ee Accepted: 16 November 2010 doi: 10.1111/j. 1439-0485.2010.00418.x

A bstract Fucus vesiculosus L. is an im p o rta n t h a b itat-fo rm in g m acroalga b o th in the saline an d high diverse N o rth Sea an d th e d iluted a n d low diversity Baltic Sea. D espite its im p o rtan ce, com parisons o f th e spatial p attern s o f its epiphytes have rarely been rep o rted . In this stu d y we exam ined th e species co m p o sition an d density o f m acro-epiphytes an d m obile fauna o n th e canopy-form ing m ac­ roalga F. vesiculosus in h ab iting different regim es o f wave exposure in th e N o rth an d Baltic Seas. The N o rth an d Baltic Seas h ad d istinct epiphyte a n d m obile faunal com m unities. W ave exposure an d segm ents o f h o st fro n d s significantly co n trib u ted to th e variability in species co m p o sitio n a n d d o m in an ce stru ctu re o f epiphytes o n F. vesiculosus in th e N o rth Sea a n d Baltic Sea. T he stu d y in d i­ cated th a t th ere is n o clear spatial scale w here enviro n m en tal variables best p re­ dicted epiphytic an d m obile faunal com m unities, a n d th e fo rm atio n of epiphytic a n d faunal co m m u n ities is an in terp lay o f factors op eratin g th ro u g h m icro - to regional scales.

Introduction E piphytism an d co m p etitio n for a su b strate is a w ide­ spread p h en o m e n o n in m arin e com m u n ities, especially in the rocky in tertidal zone (Paine 1990; K raberg & N o rto n 2007). M an y algal species can grow o n som e h o st species o r even are obligatory epiphytes (Pavia & A berg 1999) p ro viding p o ten tial for m utu alistic interspecific associa­ tio ns (Stachow icz & W h itlatch 2005). Fucoids are w idely d istrib u ted peren n ial b ro w n m a cro ­ algae in the in tertid al N o rth eastern A tlantic w ith an im p o rta n t role in stru ctu rin g in tertid al com m unities (L üning 1990). T hey can also extend to brackish n o n tidal Baltic w aters. Fucus vesiculosus L. is an im p o rta n t h ab itat-fo rm in g m acroalga b o th in th e saline an d high diverse N o rth Sea an d th e d iluted a n d low diversity n o n -

Marine Ecology 32 (Suppl. 1) (2011) 8 7 -9 5 © 2011 Blackwell Verlag GmbH

tidal Baltic Sea (K iirikki 1996a; Berger et al. 2004; T orn et al. 2006; R ohde et al. 2008). Fucus vesiculosus hosts a large variety o f m acroalgal species (R indi & G uiry 2004), w hich pro v ide suitable h ab itat for sessile invertebrates (Jo h n so n & Scheibling 1987) a n d associated invertebrates, m ain ly grazers (O rav -K o tta & K otta 2004; R äberg & Kau tsky 2007). D espite its im p o rtan ce, com parisons o f the spatial p a ttern s o f its epiphytes have rarely been re p o rted (R indi & G uiry 2004; Fraschetti et al. 2005). E piphytic organism s, such as m icro - an d m acroalgae, invertebrates an d bacteria, are often p resen t o n th e thallus o f perennial m acroalgae. T heir a b u n d an ce is largely d eter­ m in ed b y abiotic factors, e.g. w ater m o tio n an d n u trie n t availability. T he ability o f epiphytes to tolerate regular desiccation d u rin g low tides determ ines th eir spatial d istrib u tio n (M o lin a-M o n ten eg ro et al. 2005). Elevated

87

E piphytes a n d asso ciated fa u n a o n b ro w n alg a

n u trie n t loading is expected to increase b o th th e n u m b er o f epiphytic algae an d invertebrates. H ow ever, th e rela­ tionship varies am o n g regions an d is m o d u lated b y a n u m b er o f o th e r enviro n m en tal variables, e.g. wave expo­ sure, regional species pool, characteristics o f th e h o st p lan t an d herbiv o ry (K otta et al. 2000; W o rm et al. 2002; K otta & W itm a n 2009). A m ong b iotic interactions, in tra ­ specific co m p etitio n for space an d light an d th e presence o f adequate food resources for invertebrates are im p o rta n t (L obban & H arriso n 2000). T he ability o f h o st algae to resist an d avoid epibionts has great im p o rtan ce (H o n k an en & Jorm alainen 2005), affecting the pho to sy n th etic rate an d grow th o f h o st algae (K orpinen et al. 2007). T he p o sitio n w ith in th e thallus of seaweeds is im p o rta n t factor stru ctu rin g epiphyte co m ­ m unities (L obban & Baxter 1983; C ardinal & Lesage 1992; L ongtin et al. 2009). Large epiphytes are associated w ith the basal disk; ephem eral epiphytes app earin g on th e tips o f th e h o st fucoid fro n d s (A rrontes 1990). T he cover o f epiphytes often increases w ith th e age o f algae. T he objective o f this stu d y was to exam ine th e species com p o sitio n an d density o f epiphytes an d m obile fauna o n the canopy-form ing m acroalga F. vesiculosus in h a b it­ ing a t different regim es o f wave exposure in th e N o rth and Baltic Seas. W e considered epiphytes hereafter as o rg an ism -o n -a-p lan t co ncept (sensu W ahl 2009; Steel & W ilson 2003, references therein ). T hus, epiphytes in this re p o rt com prise an y m acroalgae a n d sessile in verte­ brates on th e h o st algae. M obile fauna is defined here as m otile m acroinvertebrates associated w ith th e h o st m ac­ roalgae.

K ersen, K otta, Bucas, Kolesova & Deljere

W e tested th e follow ing hypotheses: 1 T he occurrence an d cover o f epiphytes are specific to th e fro n d segm ent o f h o st m acroalgae. 2 T he occurrence an d cover o f epiphytes are related to th e wave exposure o f th e site. 3 T he relatio n sh ip betw een abiotic (exposure), b iotic fac­ to rs (fro n d segm ent) an d epiphytes (species c om posi­ tio n , cover) varies am o n g different m arin e regions (N o rth versus Baltic Seas).

M aterial and M eth o d s Study area T he stu d y was p erfo rm ed in th e N o rth Sea an d th e Baltic Sea. In each region we selected th ree sites differing in exposure level. T he used exposure levels according to the EUNIS classification w ere as follows: sheltered, m o d e r­ ately exposed an d exposed. In th e N o rth Sea th e sam pling was d o n e o n th e southw est coast o f N orw ay in Raunefjo rd an d K orsfjord in su m m e r 2007 (Fig. 1). The N o rth Sea stu d y area contains n u m ero u s sm all an d large islands separated b y w ide or n arro w sounds. The b o tto m relief o f th e area is steep a n d very uneven. E spegrend M arine B io­ logical Station (N l; 60.273°N , 5.218°E) represented shel­ tered, L oholm en (N2; 60.266°N , 5.211°E) m o derately exposed an d Store Kalsoy (M3; 60.113°N, 5.069°E) exposed areas. D u rin g sam pling, salinity ranged betw een 30 a n d 33 p su a n d tidal range was c. 1 m in th e sam pling area. In th e Baltic Sea, sam ples w ere collected fro m the G ulf o f Riga an d th e Baltic P ro p er in su m m er 2008 (Fig. 1).

Fig. 1. Map of the sampling regions and sites. Different stations are Indicated by N1, N2, N3 In the North Sea and B1, B2, B3 In the Baltic Sea.

88

Marine Ecology 32 (Suppl. 1) (2011) 8 7 -9 5 © 2011 Blackwell Verlag GmbH

E piphytes a n d asso ciated fa u n a o n b ro w n alg a

K ersen, K otta, Bucas, Kolesova & Deljere

T he G ulf o f Riga is a w ide, shallow , sem i-enclosed b rack ­ ish w ater ecosystem. In general, th e b o tto m relief o f the area is q uite flat, w ith gentle slopes tow ards deeps. The n o rth e rn p a rt o f th e G ulf is characterized b y a w ide coastal zone w ith diverse b o tto m to p o g rap h y a n d exten­ sive reaches o f boulders. The coasts o f th e Baltic P ro p er are very exposed, hydrodynam ically active a n d ch aracter­ ized by a steep coastline. The in n e r p a rt o f K öigute Bay, the G ulf o f Riga (BÍ; 58.374°N , 22.972°E) represented a sheltered area, the o u ter p a rt o f K öiguste Bay (B2; 58.370°N , 22.982°E) a m oderately exposed area, and K iidem a Bay, the Baltic P ro p e r (B3; 58.568°N, 22.302°E) an exposed area. D u rin g sam pling, salinity ranged betw een 4 an d 7 psu. T he Baltic Sea is n early tideless, w ith an average daily tidal c o m p o n en t o f 15 cm (Schiewer 2008). T he w ater level flu ctu atio n s in th e area are m ainly caused by the m eteorological forcing w ith a seasonal sea level m ean range o f 30 cm (e.g. S uursaar & Sooäär 2007).

Sampling

Distal segment Middle segment

Basal segment

Fig. 2. Examined frond segm ents of the host

Fucus vesiculosus.

considered an im p o rta n t factor for m obile or associated fauna. Therefore, 2-factor PERM ANOVA was used to d eterm in e th e abundances o f m obile invertebrates. P rio r to analysis, a B ray -C u rtis sim ilarity m atrix was

In the N o rth Sea, sam ples w ere taken at low tid e o n the u p p e r litto ral zone in th e m id d le o f F. vesiculosus belt. In the Baltic Sea sam ples w ere collected b y a diver fro m a Fucus vesiculosus belt at 0.5-1 m d epth. F our replicates of h o st algae w ere collected ran d o m ly w ith th e aid o f a ro p e th a t was placed along th e shore an d m ark ed at every m etre. F our m arks w ere ran d o m ly selected an d h ost plants w ere collected n earest to th e respective m arks on the rope. Sam ples w ere tra n sp o rte d in plastic bags to the lab o rato ry for the fu rth e r analyses w ith in 24 h. M obile fauna w ere rem oved fro m h o st thalli, co u n ted a n d id e n ti­ fied to th e low est tax o n o m ic level possible using a dissect­ ing m icroscope (m agnification 4 -1 0 x ). T he cover of epiphytes w ere estim ated o n a six-grade scale ( 0 absence, 1 - from 1 to 20% , 2 - fro m 21 to 40% , 3 fro m 41 to 60% , 4 - fro m 61 to 80% an d 5 - fro m 81 to 1 0 0 % o f cover on h o st plant) separately o n basal, m iddle an d distal segm ents o f each h o st fro n d (R indi & G uiry 2004) (Fig. 2).

calculated using raw data (u n tran sfo rm ed ) a n d pres­ ence/ab sen ce tra n sfo rm atio n to detect w h eth er th e p o te n ­ tial differences betw een th e assemblages o f th e epibiota w ere due to differences in relative abundances o r species co m p o sitio n (C larke & W arw ick 2001). W h en a factor w ith m o re th a n tw o levels (i.e. wave exposure a n d h o st fro n d segm ent) was identified as sig­ n ificant (P < 0.05), post-hoc PERM ANOVA pair-w ise tests w ere co n d u cted to detect w hich levels w ere responsible for significant interactions. Taxa responsible for observed differences w ere identified b y sim ilarity percentages (SIM ­ PER), w here th e c u t-o ff percentage was set to 90. N o n ­ m etric m u ltid im en sio n al scaling (nM D S) was used to p resen t visual im ages o f th e differences in co m p o sitio n of epiphytic a n d m obile faunal assemblages in d istinct m a r­ ine regions, exposure levels an d fro n d segm ent o f the host.

Data analysis

R esults

All m ultivariate analyses w ere con d u cted using PRIM ER 6 softw are (C larke & G orley 2006). H ierarchical p erm u tatio nal m ultivariate analysis o f variance (PERM ANOVA) (A nderson et al. 2008) was used separately for epiphytes an d m obile fau na to exam ine differences in th e p attern s o f v ariation in com p o sitio n , cover a n d ab u n d an ce betw een regions (fixed factor), wave exposure (nested in region, fixed factor) a n d fro n d segm ent o f h o st m acro al­ gae (nested in region an d wave exposure, fixed factor). D ue to th e m obility o f organism s, fro n d segm ent was n o t

A total o f 27 epiphytic a n d m obile faunal taxa were reco rd ed o n th e fronds o f Fucus vesiculosus in th e stu died areas: 8 taxa o f m acroalgae, 5 taxa o f sessile invertebrates (i.e. suspension-feeders) an d 14 taxa o f m obile in verte­

Marine Ecology 32 (Suppl. 1) (2011) 8 7 -9 5 © 2011 Blackwell Verlag GmbH

brates (m ainly herbivores) (Table 1). All investigated factors significantly co n trib u ted to the variability in species co m p o sitio n a n d coverage o f epi­ phytic an d m obile faunal co m m u n ities o n F. vesiculosus (PERM ANOVA, Table 2). E piphytic a n d m obile fauna co m m u n ities w ere clearly differentiated in species

89

E piphytes a n d asso ciated fa u n a o n b ro w n alg a

K ersen, K otta, Bucas, Kolesova & Delyere

com p o sitio n an d d o m in an ce stru ctu re betw een th e N o rth and Baltic Seas (Table 2, PERM ANOVA: P = 0.001). The epiphytes an d m obile fauna taxa co n trib u tin g m o st to th e regional variability w ere th e b ro w n algae Pylaiella littoral­ is, Elachista fucicola, th e tu b e-b u ild in g polychaete Spiror­ bis spirorbis, a n d th e h erbivorous snail Theodoxus fluviatilis (S u p p o rtin g In fo rm a tio n Tables S1-S4). T he species co m p o sitio n o f epiphytic c o m m u n ity (p res­ ence/absence tran sfo rm ed data) o n th eir h o st was signifi­ cantly different betw een every level o f wave exposure in b o th the N o rth an d Baltic Seas (P < 0.05), except for m oderately exposed versus sheltered sites in th e N o rth Sea (PERM ANOVA pair-w ise test: P = 0.092). D issim ilarities betw een different exposure levels w ere m ostly due to Elac­ hista fucicola an d Pylaiella littoralis (S u p p ortin g In fo rm a ­ tio n Table S5).

Sim ilarly, th e d o m in an ce stru ctu re o f epiphytic co m ­ m u n ity (u n tran sfo rm ed data) o n th eir h o st was signifi­ cantly different betw een every level o f wave exposure in b o th th e N o rth a n d Baltic Seas (P < 0.05), except for m oderately exposed versus sheltered sites in th e N o rth Sea (PERM A NO VA pair-w ise test: P = 0.078). D issim ilarities betw een different exposure levels w ere m ostly due to E. fucicola an d P. littoralis (S u p p o rtin g In fo rm atio n Table S6 ). T he species co m p o sitio n (presence/absence data) and do m in an ce stru c tu re (u n tran sfo rm ed data) o f m obile fau­ nal c o m m u n ity differed significantly for every exposure level in th e N o rth an d Baltic Seas (PERM ANOVA pair-w ise test: P < 0.05). D issim ilarities betw een different exposure levels w ere m ainly d u e to G am m arus spp.,

T able 1. Recorded epiphytes and mobile fauna on the host Fucus vesiculosus at three study sites in the North (NS) and Baltic Sea (BS).

No.

Taxon

Region

Wave exposure

Frond segm ent of host

NS: Mean cover/abun ± SE

BS: Mean cover/abun ± SE

Bryozoa 1

Electra crustulenta (Pallas, 1766)

BS

S, ME

B, M, D

0

0.25 ± 0.07

2 Electra pilosa (L.) Polychaetae

NS

S, ME

B, M, D

0.47 ± 0.14

0

3 Spirorbis spirorbis (Linnaeus, 1758) Crustaceans 4 Balanus Improvisus Darwin, 1854

NS

S, ME

B, M, D

1.03 ± 0.18

0

BS

E

0.03 ± 0.03

S, ME, E S, ME, E

M -

0

BS, NS BS, NS

-

0.33 ± 0.26 1.5 ± 0.4

6.5 ± 2.21 6.17 ± 1.60

BS, NS BS

S, ME, E ME

-

0

0.25 ± 0.25

BS

E

-

0

0.08 ± 0.08

NS BS

ME S, ME, E

-

0.08 ± 0.08 0

0 14.92 ± 6.24

Lacuna vincta (Montagu) Littorina littorea (L.) Littorina obtusata (L.) Lymnaea peregra (Müller) Mytilus edulis L. Mytilus trossulus Gould Theodoxus fluviatilis (L.)

NS NS

E S, ME, E

0.17 ± 0.11 7.17 ± 1.62

0 0

NS BS NS

S, ME, E ME, E S

-

BS BS

E S, ME, E

-

0 0.17 ± 0.17 0 0

Ceramium tenuicorne (Kützing) Waern Ceramium virgatum Roth Chaetomorpha sp. Chordaria flagelliformis (Müller) Agarth Cladophora glomerata (L.) Kützing Elachista fucicola (Velley) Arenschoug Pylaiella littoralis (L.) Kjellman Ulva intestinalis L.

BS, NS BS, NS NS NS

ME, E ME, E S ME

B, M, D B, M, D M, D M

0.08 ± 0.06

BS, NS NS BS, NS

S, ME S, ME, E S, ME

B, M, D B, M, D B, M, D

0.03 ± 0.03 0.72 ± 0.17 0.06 ± 0.04

NS

S, ME

B, M, D

0.14 ± 0.06

0

NS

ME

B, M, D

0.11 ± 0.07

0

S 6

Gammarus spp. Idotea balthica (Pallas, 1772) Idotea chelipes (Pallas, 1766) Jaera albifrons Leach, 1814

7 8 Nemertina 9 Cyanophthalma obscura (Schultzei Mollusca 10 Gibbula cineraria (L.) 11 Elydrobia spp. 12 13 14 15 16

17 18 Macroalgae 19 20 21 22 23 24 25

26 Hydrozoa 27 Dynamena pumila (L.)

-

0.06 ± 0.04 0.06 ± 0.06

0.42 ± 0.26 0 0.42 ± 0.29 39.17 ± 6.47 0.28 ± 0.09 0 0 0.36 ± 0.09 0.19 ± 0.08 1.14 ± 0.26

S, Sheltered: ME, moderately exposed; E, exposed site. B, basal; M, middle; D, distal segment o f host alga. Means and standard errors were calculated from untransformed coverage and abundance data.

90

Marine Ecology 32 (Suppl. 1) (2011) 8 7 -9 5 © 2011 Blackwell Verlag GmbH

E piphytes a n d asso ciated fa u n a o n b ro w n alg a

K ersen, K otta, Bucas, Kolesova & Deljere

Littorina spp. an d Theodoxus fluviatilis (S u p p o rtin g In fo r­ m atio n Tables S7 a n d S8 ). D ifferent segm ents o f h o st fronds h ad significantly dif­ ferent species com p o sitio n o f epiphytic co m m u n ities at the m oderately exposed site in th e N o rth Sea (betw een m iddle an d distal segm ents; P = 0.033) an d a t exposed (betw een m iddle an d distal segm ents; P = 0.03) an d shel­ tered sites in th e Baltic Sea (betw een basal a n d distal seg­ m ents; P = 0.031). D ifferent segm ents o f h o st fro n d s h ad significantly different d o m in an ce stru ctu re o f epiphytic com m unities (u n tran sfo rm ed data) at th e sheltered site in the N o rth Sea (betw een basal an d m id d le segm ents; P = 0.026) and at exposed (betw een m id d le an d distal segm ents; P = 0.023) an d sheltered sites in th e Baltic Sea (betw een basal an d distal segm ents; P = 0.03). T he differ­ ences in species co m p o sitio n an d d o m in an ce stru ctu re w ere m ainly caused b y E. fucicola an d P. littoralis (S up­ p o rtin g In fo rm atio n Tables S9 an d SIO). A ccording to nM D S o rd in atio n , th e epiphytic c o m m u ­ n ity com p o sitio n a n d stru ctu re o n h o st m acroalgae clearly differed betw een sea regions in epiphyte coverage an d also in m obile fauna abundance. It is also possible to detect a separate effect o f wave exposure o n epiphytic an d m obile faunal co m m u n ity co m p o sitio n a n d stru ctu re w ith in the tw o sea regions. H ow ever, th e d istinctions are larger for

regions th a n for exposure levels. N evertheless, in som e instances th e differences w ere very clear, e.g. epiphytes w ere totally absent at th e exposed site o f th e N o rth Sea (Fig. 3).

D iscussion W e p red icted th a t th e occurrence an d cover o f epiphytes w o u ld be specific to th e fro n d segm ents o f h o st m a cro ­ algae. T he results agreed w ith th e hypothesis as different parts o f h o st seaweeds h ad different epiphytic an d m obile fau n a species co m p o sitio n a n d d o m in an ce stru ctu re. The distal segm ent o f h o st fro n d h a d th e low est coverage an d th e low est species richness o f epiphytes. This p a tte rn is d u e to th e high m etabolic activity o f apical (new ) p arts of Fucus vesiculosus thallus w here th e h o st alga p ro d u ces allelopathic c o m p o u n d s such as p h lo ro ta n n in s (W ik strö m & Pavia 2003). Also, th e to p m o st parts o f fucoid algae have a n anti-fo u lin g strategy o f periodically shed d in g surface cell layers (K iirikki 1996b), w hich reduces th e pro b ab ility o f epibionts settling an d b ecom ing established o n th e host p lant. A sim ilar strategy o f m echanical defence has been observed in red algal hosts (N ylund & Pavia 2005). W e also predicted th a t th e occurrence an d cover o f epi­ phytes w ould be related to th e wave exposure o f th e site.

T able 2. Main results of PERMANOVA analyses on the effect of region, wave exposure, and frond segm ent to species composition and domi­ nance structure of epiphytic and mobile faunal assem blages on Fucus vesiculosus. Source Epiphytic coverage P resence/absence transformed Region Wave exposure (Region) Frond segm ent (Wave exposure (Region) Res Total Untransformed Region Wave exposure (Region) Frond segm ent (Wave exposure (Region)) Res Total Mobile faunal abundance P resence/absence transformed Region

d.f.

SS

1 4

MS

15,498 36,967

15,498 9241.6

12

13,869

1155.7

54 71

20,403 86,736

377.84

1 4 12

18,220 50,430 19,143

18,220 12,607 1595.2

54

29,410

544.63

71

117,200

1

42,429

4

Res Total Untransformed Region Wave exposure (Region)

66 71

22,601 74,553

342.45

1 4

109,390 35,212

109,390 8803

66 71

55,825 200,430

845.83

Res Total

9522.1

42,429

Wave exposure (Region)

2380.5

Pseudo-F

41.016 24.459 3.0588

33.454 23.149 2.929

123.9 6.9515

12.33 10.408

P(perm)

Unique perms

0.001 0.001

998 997

0.001

999

0.001 0.001 0.001

998 997 996

0.001

999

0.001

999

0.001 0.001

997 996

Res, Residual.

Marine Ecology 32 (Suppl. 1) (2011 ) 8 7 -9 5 © 2011 Blackwell Verlag GmbH

91

E piphytes a n d asso ciated fa u n a o n b ro w n alg a

K ersen, K otta, Bucas, Kolesova & Deljere

Som e epiphytic (e.g. Spirorbis spirorbis, Bryozoa, Clado­ phora glomerata, Pylaiella littoralis) a n d m obile faunal species (e.g. Jaera albifrons) w ere n o t observed at exposed study sites, suggesting th a t occurrence a n d co v er/a b u n dance are related to th e exposure level o f a site. T his p a t­ te rn is explained b y th e high hydro d y n am ic pressure o n the thallus o f F. vesiculosus at highly exposed sites, w h i­ ch rem oves epiphytic algae a n d prevents b en th ic su sp en­ sion feeders fro m settling o n th e algae. W e also pred icted th a t th e relationship betw een abiotic (exposure), bio tic factors (h o st fro n d segm ent) an d epi­ phytes (species com p o sitio n , cover) w ould vary am o n g different m arin e regions (N o rth versus Baltic Seas). Indeed, o u r stu d y show ed th a t th e N o rth an d Baltic Seas h ad different epiphytic a n d m obile faunal species co m p o ­ sitions and d o m in an ce structures. T he epiphytic an d m obile faunal taxa co n trib u tin g m o st to th e dissim ilarity betw een N o rth an d Baltic Sea com m u n ities w ere th e bro w n alga P. littoralis an d th e h erbivore Theodoxus flu ­ viatilis, respectively. B oth species have a stro n g degree of tolerance to low ered salinity w hich consequently enables

th e m to thriv e in th e low salinity env iro n m en t. This sug­ gests th a t solinity determ ines interregional differences in epiphyte co m m u n ities betw een N o rth an d Baltic Seas (Kangas & Skoog 1978; Russell 1994; Snoeijs 1999). The­ odoxus fluviatilis was consistently absent in th e N o rth Sea stu d y sites, causing high dissim ilarities in ab undance a m o n g regions. This stu d y also show ed a h igher variability o f epiphytes a n d m obile faunal co m m u n ity stru c tu re in th e Baltic Sea th a n in th e N o rth Sea. It has been p ro p o sed th a t p ro ­ cesses affect ecosystem s sim ultaneously at v arious spatial a n d tem p o ral scales (D en n y et a l 2004; Fraschetti et al. 2005; K otta e t al. 2008). T he relative im p o rtan ce o f sm alla n d large-scale processes o n th e fo rm atio n o f m arine com m u n ities is little know n a n d it is likely th e patterns vary am o n g regions (e.g. H ew itt et al. 2007; K otta & W it­ m an 2009). O u r stu d y indicates th a t large-scale factors m ostly d eterm in e th e d istrib u tio n p attern s o f epiphytes in th e N o rth Sea a n d w ith in these p attern s, processes o p erat­ ing at m icroscale (e.g. due to fro n d segm ent) fu rth er m o d ify th e epiphyte com m unities. O n th e o th er h an d,

S p ecies composition

Dominance structure .11

R e g io n ▲ North se a • Baltic se a

R e g io n ▲ North se a • Baltic se a

• • ▲▲ Cfl o % xz Q. Q.

M

LU

AS

M0

.06

CC C

*

E•

fi cu

■Q O MAM

R e g io n ▲ North se a • Baltic se a

R e g io n ▲ North se a • Baltic se a

Fig 3. Non-metric multidimensional scaling (nMDS) plots showing the effect of sea region and wave exposure (E = exposed; M = moderately exposed and S = sheltered sites) on epiphytic (coverage) and mobile faunal (abundance) community composition and structure. Lefthand plots are com posed from presence/absence transform ed data, righthand plots from untransform ed data. Some marks are overlapped on the figure because epiphytes and mobile fauna w ere absent in these samples, thus representing 100% similarity.

92

Marine Ecology 32 (Suppl. 1) (2011) 8 7 -9 5 © 2011 Blackwell Verlag GmbH

E piphytes a n d asso ciated fa u n a o n b ro w n alg a

K ersen, K otta, Bucas, Kolesova & Deljere

large-, m eso- a n d m icroscale processes are all equally im p o rta n t in determ in in g th e d istrib u tio n p attern s o f epi­ phytes in the Baltic Sea. In general, associated faunal c o m m u n ity co m p o sitio n was different betw een all levels o f wave exposure in b o th m arin e regions, w hereas epiphytic co m p o sitio n a n d stru c­ tu re did n o t significantly differ betw een m oderately exposed an d sheltered sites in th e N o rth Sea. This indicates th a t epiphytic algae in h ab itin g th e N o rth Sea tolerate a larger range o f exposure th a n those in h ab itin g the Baltic Sea. The effect o f ho st fro n d segm ents o n th e p attern s of epiphytes varied am o n g N o rth an d Baltic Seas, su p p o rtin g the hypothesis th a t th ere are different factors (levels) form ing different epiphytic co m m u n ities o n F. vesiculosus in the Baltic and N o rth Sea. It seem s likely th a t a t sm aller spatial scales, biotic factors [i.e. fro n d segm ent) play a m o re im p o rta n t role in epiphytic co m m u n ities in the Baltic Sea, w hereas abiotic factors [i.e. wave exposure) are m o re im p o rta n t in th e N o rth Sea. O u r u n d erstan d in g o f th e causes o f local species diver­ sity in m arin e hab itats m ostly originates fro m observa­ tio ns p erform ed at sm all spatial scales. C o m p arin g local an d regional variability o f epiphyte com m unities, o u r stu d y clearly dem o n strated th a t regional differences define b ro ad p attern s o f species diversity an d are am o n g the m o st significant factors explaining p o p u la tio n variability in these m arin e environm ents. H ow ever, o u r stu d y was lim ited to tw o-regio n cases an d fu rth er studies fro m m u l­ tiple regions m ay pro v id e us w ith a generic know ledge of the processes shaping epiphyte com m unities. Besides the spatial aspect, epiphytes are k n o w n to have a stro n g co m ­ p o n e n t o f seasonal variability (B o ru m 1985; V airap p an 2007; T o rn et al. 2010). This was n o t considered in the cu rren t stu d y b u t m ay be highly relevant, as different regions are characterized b y different types an d inten sity o f seasonality. To conclude, all investigated factors c o n trib u ted sig­ nificantly to the variability in species co m p o sitio n an d coverage o f epiphytes an d m obile faunal com m unities o n F. vesiculosus. The N o rth a n d Baltic Seas each h ad d istinct epiphyte a n d m obile faunal com m unities. W ith in th e studied regions, wave exposure an d fro n d segm ent co n trib u ted significantly to th e variability in species com p o sitio n an d d o m in an ce stru ctu re o f epi­ phytes o n F. vesiculosus in th e N o rth Sea an d Baltic Sea. Large-scale factors greatly d eterm in e th e d istrib u tio n p attern s o f epiphytes in th e N o rth Sea, w hereas large-, m eso- an d m icroscale processes w ere all equally im p o r­ ta n t in determ in in g th e d istrib u tio n p a ttern s of epiphytes in the Baltic Sea. T he stu d y ind icated th a t there is no clear spatial scale w here en v ironm ental variables best predicted epiphyte an d m obile faunal

Marine Ecology 32 (Suppl. 1) (2011 ) 8 7 -9 5 © 2011 Blackwell Verlag GmbH

com m unities. The fo rm atio n o f epiphytic an d m obile faunal com m u n ities is an in terp lay o f factors operating th ro u g h m icro - to regional scales.

A c k n o w le d g e m e n ts W e are especially than k fu l to Lena K autsky for h er valu­ able advice o n sam pling a n d species identification. W e th a n k Stein Fredriksen, K jersti Sjotun a n d Jan Rueness for th eir k in d su p p o rt w ith lab o rato ry species identifica­ tio n . T his research was su p p o rte d b y th e E u ro p ean Social F u n d ’s D o cto ral Studies an d In tern atio n alisatio n P ro ­ g ram m e DoRa. F un din g for this research was pro v id ed by targ et-financed projects SF0180013s08 o f th e E stonian M in istry o f E d u catio n a n d b y th e E stonian Science F o u n ­ d a tio n grants 7813 a n d 8254. T he stu d y was partly carried o u t in th e fram e o f a n advanced course b y th e N ordic M arin e A cadem y ‘B iodiversity o f n o rth ea st A tlantic m ac­ roalgae’ at th e E speland M arin e Biological Station.

R eferen ces A nderson M.J., Gorley R.N., Clarke K.R. (2008) PERMANOVA

+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plym outh: 214 pp. A rrontes J. (1990) C om position, d istribution o n host, and seasonality o f epiphytes o n tree intertidal algae. Botanica

Marina, 33, 205-211. Berger R., Bergström L., Graneli E., Kautsky L. (2004) H ow does the eutrophication affect different life stages o f Fucus

vesicidosus in the Baltic Sea? - a conceptual m odel. Hydro­ biologia, 514, 243-248. B orum J. ( 1985) D evelopm ent o f epiphytic com m unities on eelgrass (Zostera marina ) along a n u trie n t gradient in a D anish estuary. Marine Biology, 87, 211-218. C ardinal A., Lesage V. (1992) D istribution o f the epiphytes

Pilayella littoralis a n d Polysiphonia lanosa on Ascophyllum nodosum in the Bay o f Fundy. Cahiers de Biologie Marine, 33, 125-135. Clarke K.R., Gorley R.N. (2006) PRIMER v6: User M an­

ual/Tutorial. PRIM ER-E, Plym outh: 192 pp. Clarke K.R., W arw ick R.M. (2001) Change in Marine Commu­

nities: A n Approach to Statistical Analysis and Interpretation, 2nd edn. PRIM ER-E, Plym outh: 172 pp. D enny M .W ., H elm uth B., L eonard G.H., H arley C.D.G., H u n t L.J.H., N elson E.K. (2004) Q uantifying scale in ecology: lessons from a wave-swept shore. Ecological Monographs, 74, 513-532. Fraschetti S., Terlizzi A., Benetti-Cecchi L. (2005) P attern o f d istribution o f m arine assemblages from rocky shore: evidence o f relevant scales o f variation. Marine Ecology

Progress Series, 296, 13-29. H ew itt J.E., T hrush S.F., D ayton P.K., B onsdorff E. (2007) The effect o f spatial and tem poral heterogeneity o n the design

93

E piphytes a n d asso ciated fa u n a o n b ro w n alg a

and analysis o f em pirical studies o f scale-dependent systems.

American Naturalist, 169, 398-408. H onkanen T., Jorm alainen V. (2005) Genotypic variation in tolerance and resistance to fouling in the brow n alga Fucus

vesiculosus. Oecologia, 144, 196-205. Johnson S.C., Scheibling R.E. (1987) Structure and dynam ics o f epifaunal assemblages o n intertidal m acroalgae Ascophyl­

lum nodosum a n d Fucus vesiculosus in N ova Scotia, Canada. Marine Ecology Progress Series, 37, 209-227. Kangas P., Skoog G. (1978) Salinity tolerance o f Theodoxus fluviatilis (M ollusca, G astropoda) from freshw ater and from different salinity regim es in the Baltic Sea. Estuarine, Coastal and Shelf Science, 79, 533-540.

K ersen, K otta, Bucas, Kolesova & Deljere

N ylund G.M., Pavia H . (2005) Chem ical versus m echanical in hibition o f fouling in the red alga Dilsea carnosa. Marine Ecology Progress Series, 299, 111-121. O rav-K otta H., K otta J. (2004) Food a n d h abitat choice o f the isopod Idotea baltica in the northeastern Baltic Sea. Hydro­

biologia, 514, 79-85. Paine R.T. (1990) Benthic m acroalgal com petition: com plica­ tions and consequences. Journal o f Phycology, 26, 12-17. Pavia H., C arr H., Äberg H.C. ( 1999) H abitat a n d feeding preferences o f crustacean m esoherbivores inhabiting the brow n seaweed Ascophyllum nodosum (L.) Le Joi. and its epiphytic m acroalgae. Journal o f Experimental Marine Biology and Ecology, 236, 15-32.

Kiirikki M. ( 1996a) M echanism s affecting m acroalgal zonation

Ráberg S., Kautsky L. (2007) A com parative biodiversity study

in the n o rth ern Baltic Sea. European Journal o f Phycology,

o f associated fauna o f perennial fucoids a n d filam entous

31, 225-232.

algae. Estuarine, Coastal and Shelf Science, 73, 249-258.

Kiirikki M. ( 1996b) E xperim ental evidence th a t Fucus vesicidosns

R indi F., G uiry M.D. (2004) C om position and spatio tem poral

(Phaeophyta) controls filam entous algae by the m eans o f the

variability o f the epiphytic m acroalgal assemblage o f Fucus

w hiplash effect. European Journal o f Phycology, 31, 61-66.

vesiculosus Linnaeus at Clare Island, Mayo, w estern Ireland. Journal o f Experimental Marine Biology and Ecology, 311,

K orpinen S., Jorm alainen V., H onkanen T. (2007) Effects o f nutrients, herbivory, a n d d e p th o n the m acroalgal c o m m u ­ nity in the rocky sublittoral. Ecology, 88, 839-852. K otta J., W itm an J. (2009) Regional-scale patterns. In: W ahl

233-252. R ohde S., H iebenthal C., W ahl M., Karez R., Bischof K. (2008) Decreased dep th d istribution o f Fucus vesiculosus in the

M.. (ed), Marine Hard Bottom Communities. Ecological

W estern Baltic: effects o f light deficiency and epibionts on

Studies, 206. Springer, Heidelberg: 89-99.

grow th a n d photosynthesis. European Journal Phycology, 43,

K otta J., Paalm e T., M artin C., M akinen A. (2000) M ajor

143-150.

changes in m acroalgae co m m unity com position affect the

Russell G. (1994) A Baltic variant o f Pilayella littoralis (Algae,

food and habitat preference o f Idotea baltica. International Review of Hydrobiologia, 85, 693-701.

Schiewer U. (2008) The Baltic Sea. In: Schiewer U.. (Ed). Ecol-

K otta J., Paalm e T., Püss T., H erkül K., K otta I. (2008) C o n tri­ b u tio n o f scale-dependent environm ental variability o n the biom ass patterns o f drift algae a n d associated invertebrates in the G ulf o f Riga, n o rth ern Baltic Sea. Journal o f Marine

Systems, 74(Suppl. 1), S116-S123. Kraberg A.C., N o rto n T.A. (2007) Effect o f epiphytism on reproductive and vegetative lateral form ation in the brow n, intertidal seaweed Ascophyllum nodosum (Phaephyceae).

Phycological Research, 55, 17-24. L obban C.S., Baxter D.M . (1983) D istribution o f the red algal

Fucophyceae). Annales Botanici Fennici, 31, 127-138.

ogy o f Baltic Coastal Waters. Ecological Studies 197. Springer, Berlin: 1-22. Snoeijs P. ( 1999) M arine and brackish waters. Acta Phytogeo-

graphica Suecica, 84, 187-212. Stachowicz J.J., W hitlatch R.B. (2005) M ultiple m utualists p ro ­ vide com plem entary benefits to th eir seaweed host. Ecology, 86, 2418-2427. Steel J.B., W ilson J.B. (2003) W hich is the phyte in epiphyte?

Folia Geobotánica, 38, 97-99. Suursaar Ü., Sooäär J. (2007) D ecadal variations in m ean and

epiphyte Polysiphonia lanosa on its brow n algal host Asco­ phyllum nodosum in the Bay o f Fundy, Canada. Botanica Marina, 26, 533-538. L obban C.S., H arrison P.J. (2000) Seaweed Ecology and Physiol­ ogy. C am bridge U niversity Press, Cam bridge: 366 pp.

T orn K., K rause-Jensen D., M artin G. (2006) Present a n d past

L ongtin C.M., Scrosati R.A., W halen G.B., G arbary D.J. (2009)

T orn K., M artin G., K otta J., K upp M. (2010) Effects o f differ­

extrem e sea level values along the Estonian coast o f the Bal­ tic Sea. Tellus, 59A, 249-260. dep th d istribution o f bladderw rack (Fucus vesicidosus) in the Baltic Sea. Aquatic Botany, 84, 53-62.

D istribution o f algal epiphytes across environm ental gradi­

ent types o f m echanical disturbances on a charophyte d o m i­

ents at different scales: intertidal elevation, h o st canopies,

nated m acrophyte com m unity. Estuarine Coastal and Shelf

and host fronds. Journal o f Phycology, 45, 820-827.

Science, 87, 27-32.

L üning K.. (1990) Seaweeds: Their Environment, Biogeography,

V airappan C.S. (2007) Seasonal occurrences o f epiphytic algae

and Ecophysiology. W iley-Interscience, New York: 527 pp.

o n the com m ercially cultivated red alga Kappaphycus al­

M olina-M ontenegro M.A., M unoz A.A., Badano E.I., M orales B.W., Fuentes K.M., Cavieres L.A. (2005) Positive interac­

varezii (Solieriaceae, Gigartinales, R hodophyta). Develop­ ments in Applied Phycology, 1, 385-391.

tions betw een m acroalgal species in a rocky intertidal zone

W ahl M. (2009) Epibiosis: Ecology, Effects and Defences. In:

94

and their effects o n the physiological perform ance o f Ulva

W ahl M. (ed), Marine Hard Bottom Communities. Ecological

lactuca. Marine Ecology Progress Series, 292, 173-180.

Studies, 206. Springer, Heidelberg: 61-72.

Marine Ecology 32 (Suppl. 1) (2011) 8 7 -9 5 © 2011 Blackwell Verlag GmbH

K ersen , K o tta , B ucas, K o leso v a & D eljere

W ikström S.A., Pavia H . (2003) Chem ical settlem ent inhibition versus post-settlem ent m ortality as an explanation for differ­ ential fouling o f two congeneric seaweeds. Oecologia, 138, 223-230. W o rm B., Lotze H.K., H illebard H., Som m er U. (2002) C onsum er versus resource control o f species diversity and ecosystem functioning. Nature, 417, 848-851.

S u p p ortin g Inform ation A dditional S u p p o rtin g In fo rm atio n m ay be fo u n d in the online version o f this article: Table SI. Results o f SIM PER analyses testing for differ­ ences in the species co m p o sitio n o f epiphytic co m m u n i­ ties o n Fucus vesiculosus betw een th e N o rth an d Baltic Seas (presence/absence tran sfo rm ed data, coverage o f epi­ phytes o n host).

Table S2. Results o f SIM PER analyses testing for differ­ ences in the d o m in an ce stru c tu re o f epiphytic co m m u n i­ ties o n Fucus vesiculosus betw een th e N o rth an d Baltic Seas (u n tran sfo rm ed data, coverage o f epiphytes o n host). Table S3. Results o f SIM PER analyses testing for differ­ ences in th e species co m p o sitio n o f m obile faunal co m ­ m unities on Fucus vesiculosus betw een th e N o rth an d Baltic Seas (presence/absence tran sfo rm ed data, a b u n ­ dance o f fauna on host). Table S4. Results o f SIM PER analyses testing for differ­ ences in the d o m inan ce stru ctu re o f m obile faunal c o m m u ­ nities o n Fucus vesiculosus betw een th e N o rth an d Baltic Seas (u n tran sfo rm ed data, ab u n d an ce o f fauna o n host). Table S5. Results o f SIM PER analyses testing for differ­ ences in the species co m p o sitio n o f epiphytic co m m u n i­ ties on F. vesiculosus betw een different wave exposure

Marine Ecology 32 (Suppl. 1) (2011 ) 8 7 -9 5 © 2011 Blackwell Verlag GmbH

E piphytes a n d asso ciated fa u n a o n b ro w n alg a

levels (presence/absence tran sfo rm ed data, coverage of epiphytes o n host). Table S6. R esults o f SIM PER analyses testing for differ­ ences in th e d o m in ance stru ctu re o f epiphytic co m m u n i­ ties o n Fucus vesiculosus betw een different wave exposure levels (u n tran sfo rm ed data, coverage o f epiphytes on h ost). Table S7. R esults o f SIM PER analyses testing for differ­ ences in th e species co m p o sitio n o f m obile faunal com ­ m u n ities o n Fucus vesiculosus betw een different wave exposure levels (presence/absence tran sfo rm ed data, a b u n d ance o f fau n a o n host). Table S8. R esults o f SIM PER analyses testing for differ­ ences in th e d o m in an ce stru ctu re o f m obile faunal com ­ m u n ities o n Fucus vesiculosus betw een different wave exposure levels (u n tran sfo rm ed , a b u n d an ce o f fauna on h ost). Table S9. R esults o f SIM PER analyses testing for differ­ ences in th e species co m p o sitio n o f epiphytic co m m u n i­ ties o n Fucus vesiculosus betw een different fro n d segm ents (presence/absence tran sfo rm ed data, coverage o f epi­ phytes o n host). Table SIO. R esults o f SIM PER analyses testing for dif­ ferences in th e d o m in an ce stru ctu re o f epiphytic c o m m u ­ nities o n Fucus vesiculosus betw een different frond segm ents (u n tran sfo rm ed data, coverage o f epiphytes on host). Please note: W iley-Blackwell are n o t responsible for the c o n te n t o r fu n ctio n ality o f any su p p o rtin g m aterials su p ­ plied b y th e au th o rs. A ny queries (o th er th a n m issing m aterial) sh o u ld be directed to th e co rresp o n d in g a u th o r for th e article.

95

marine ecology

an evolutionary perspective

»

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

Food resource use in sympatric juvenile plaice and flounder in estuarine habitats S te fa n o M ariani, Ciara B o g g a n & D avid B alata Marine Biodiversity, Ecology & Evolution, UCD School of Biology & Environmental Science, University College Dublin, Belfield, Dublin, Ireland

K eywords A daptation; coastal habitats; flatfish; Irish Sea; Platichthys flesus; Pleuronectes platessa; trophic niche. C orrespondence Stefano Mariani, Marine Biodiversity, Ecology & Evolution, UCD School of Biology & Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland. E-mail: [email protected] Accepted: 17 November 2010

A bstract E nv iro n m ental con d itio n s in estuarine h ab itats can vary greatly an d influence th e com p o sitio n o f fish assem blages a n d th e ir tro p h ic in terrelationships. W e investigated feeding habits a n d p attern s o f diet overlap in juvenile plaice (Pleu­ ronectes platessa) a n d flo u n d er (Platichthys flesus) fro m tw o estuarine habitats in th e Irish Sea. Plaice was fo u n d to vary its diet significantly across env iro n ­ m ents, w hereas flo u n d er exhibited a m o re consistent an d hom o g en eo u s feeding p attern . Im p o rtan tly , sym patric fish sam pled at th e sam e statio n w ere show n to reduce diet overlap. The results su p p o rt th e view th a t enviro n m en tal h etero ­ geneity in estuaries m ain tain s a w ide range o f selective forces, th e n et o u tcom e o f w hich can p ro d u ce a diverse array o f feeding a d ap ta tio n s am o n g interacting species.

doi:10.1111/j.1439-0485.2010.00419.x

Introduction D espite extensive h a b ita t d estru ctio n , p o llu tio n a n d long­ term irresponsible exploitation regim es (Lotze et al. 2006), estuarine an d coastal areas still retain a pivotal role in aquatic p ro d u c tio n processes, conservation, resource use, econom y an d com m erce. M o st o f such ‘tra n sitio n a l’ habitats represen t vital ‘n urseries’ for th e juvenile stages o f several com m ercially im p o rta n t fish (Beck et al. 2001; K raus & Secor 2005), p ro v id in g ab u n d a n t food resources, shelter an d favourable co n d itio n s for rap id grow th (H aedrich 1983). Yet, estuaries, lagoons a n d tidal flats are also characterised b y an unparalleled spatial a n d tem p o ral environm ental heterogeneity (E lliott & Q u in tin o 2007), w hich necessarily poses severe adaptive challenges to th e organism s th a t sp en d at least p a rt o f th eir life cycle therein. O ne m ain ecological challenge is to be able to p a rti­ tio n resources in a densely p o p u lated an d variable envi­ ro n m en t. Sim ilar species th a t occupy th e sam e h a b itat at the sam e tim e will likely consum e slightly different prey to m inim ise niche overlap (Schoener 1974), an d a n u m ­ b er o f studies have show n this to be th e case for fish

96

in h ab itin g coastal ecosystem s (Beyst et al. 1999; D arnau d e et al. 2001; M arian i et al. 2002; Platell et al. 2006; R usso et al. 2008). Juveniles o f flatfish species (O rd er P leuronectiform es) are fo u n d in ab u n d an ce in estuarine a n d coastal fish assem blages w orldw ide, m aking th em good candidates for studies o f resource p artitio n in g . In p articular, E u ro p ean flo u n d er (Platichthys flesus L.) and plaice (Pleuronectes platessa L.) rep resen t key species in cold tem p erate areas in th e N o rth east A tlantic an d the latter especially sustains a very valuable com m ercial fish­ ery. A fter h atching, juvenile flo u n d er an d plaice use shallow n u rsery g ro u n d s d u rin g th e first m o n th s o f life, betw een M arch a n d O cto b er (Russell 1976; G ibson 1994; Raffaelli & H aw kins 1996), exhibiting at this tim e a high degree o f spatial overlap. D espite th e re p o rted sim ilarity in diet (G ibson 1994; P iet et al. 1998), m o st studies suggest th a t sym patric pla­ ice an d flo u n d er segregate tro p h ic niches (A arnio et al. 1996; Beyst et al. 1999; A m ezcua et al. 2003; A ndersen et al. 2005; R usso et al. 2008). M ost com parative studies em phasise inter-specific v ariatio n a n d co m p etitio n in a specific spatial con tex t - som etim es going as far as p ro ­ viding m echanistic explanations for th e observed variation

M arine Ecology 32 (Suppl. 1) (2011 ) 96-101 © 2011 Blackwell Verlag GmbH

Food reso u rce use in plaice an d flo u n d e r

M aria n i, B o g g a n & B alata

in diet (Bels & D av en p o rt 1996; G ronkjaer et al. 2007; Russo et al. 2008) - b u t te n d to overlook th e overall role o f coastal environm en tal heterogeneity in influencing the adaptive responses o f species. H ere we com pare th e feeding habits o f sym patric flo under an d plaice in tw o different estuarine e n v iro n ­ m ents in the Irish Sea an d we test the hypothesis th a t local conditions will affect th e dietary p attern s in these species, resulting in spatial v ariations in th e ir tro p h ic inter-relationships.

M aterial and M eth o d s Study area The study was carried o u t in tw o inshore tidal inlets in the Irish Sea: N o rth Bull Island (53°22' N, 6°07' W ), in D ublin Bay, and W exford H a rb o u r (52°20' N , 6°27' W ), at the so u th ern m o st end o f th e Irish Sea basin (Fig. 1). N o rth Bull Island has previously been show n to have higher average salinity (37 psu) an d low er average te m ­ p eratu re (17 °C) th a n W exford H a rb o u r (27 psu an d 19 °C) th ro u g h o u t th e year (C raig et al. 2008). B oth localities are characterized by sa n d y /m u d d y b o tto m s, w hich rem ain com pletely exposed d u rin g low tide. W ith in each location, tw o stations ~ 5 0 0 m ap a rt were chosen for sam pling.

Sampling Juveniles o f plaice a n d flo u n d er were collected using a 10-m long, 4 -m high, h an d -d rag g ed seine (2 -m m m esh), betw een June an d July 2008, w hich corresponds to the p erio d o f m ax im u m ab u n d an ce an d activity o f 0 -group flatfishes in inshore tid al areas in th e N o rth east A tlantic (G ibson 1994; Raffaelli 8 c H aw kins 1996). In each locality, specim ens were collected once a week, over 4 weeks, d u r­ ing daytim e, at high an d low tide, to m axim ize the rep re­ sen tatio n o f th e sam ple for b o th species. Specim ens were co u n ted each tim e, an d a ra n d o m subsam ple was sacri­ ficed using an overdose o f p h en oxyethanol an d later placed in a 5% form alin solu tio n for preservation and identification.

D ata processing and analysis All preserved individuals were m easured w ith a calliper (fork length, LF, to th e nearest m m ) an d th e ir stom ach contents em p tied in to a P etri dish an d observed u n d er a stereom icroscope. Prey item s were classified to th e low est tax o n o m ic level possible an d recorded as present or absent. The m u ltivariate dataset was explored an d represented using a tw o -d im en sio n al u n co n strain e d prin cip al c o o rd i­

¿*£7

r/

C

North Bull Island

IRELAND

Dublin

N. Bull Island

Plaice S1

Plaice S2

Flounder S1 Flounder S2

Wexford H

Fig. 1. Map of study areas with bar plots representing the recorded numbers of plaice and flounder (annotations S1 and S2 refer to the tw o stations within each location).

Wexford Harbour

M arine Ecology 32 (Suppl. 1) (2011) 96-101 © 2011 Blackwell Verlag GmbH

Plaice S1

Plaice S2

Flounder S1 Flounder S2

97

Food reso u rce use in plaice a n d flo u n d e r

M aria n i, B o g g a n & B alata

n ate o rd in a tio n (PC O ) based o n G ow er’s dissim ilarity m easure (G ow er 1966). P erm u tatio n al m ultivariate analy­ sis o f variance (PERM ANOVA; A n d erso n 2001) was th en used to analyse th e v ariatio n in feeding habits o f plaice and flo und er betw een an d w ith in th e tw o different estuarine habitats. T he ex perim ent consisted o f a three-w ay design w ith ‘Species’ (‘Spe’, tw o levels) as a fixed factor, ‘Locality’ (‘Loc’, tw o levels) as a ra n d o m an d crossed fac­ to r, an d ‘Statio n ’ (‘Sta’, tw o levels) as a ra n d o m factor nested in ‘Locality’. Pairw ise tests w ere also co n d u cted to p in p o in t the levels responsible for significant interactions. Leeding was also exam ined b y co m p arin g th e v ariation o f m o st ab u n d a n t taxa, w hich w ere ‘p o o led ’ in to taxonom ical/ecological guilds as follows: ‘C o p ep od s’ (c o m ­ prising H arpactico id a, C yclopoida an d C alanoida), ‘W o rm s’ (com prising Polychaeta, O ligochaeta an d N em a­ to d a), ‘A m p h ip o d a + Iso p o d a’, a n d ‘O th er M alacostraca’ (com prising M ysidacea, B rachyura an d C aridea). These data w ere analysed b y u nivariate A N O VA, applying the sam e design described for PERM ANOVA, a n d after test­ ing for h o m og en eity o f variance using th e C o ch ran ’s C -test (U nderw o o d 1997). S tu d en t-N ew m an -K eu ls (SNK) tests w ere used for post hoc m ultip le pairwise com parisons.

R esults A to ta l o f 1144 flo u n d er an d 810 plaice w ere collected. L lounder w ere d o m in a n t in W exford H a rb o u r (975 versus 184) a n d plaice in N o rth Bull Island (626 versus 169) (Fig- !)• A to tal o f 202 fish w ere exam ined for sto m ach co n ­ tents: 50 flo u n d er (31 + 19) an d 50 plaice (30 + 20) from tw o stations in N o rth Bull Island, 50 flo u n d er (30 + 20) an d 52 plaice (36 + 16) fro m th e tw o statio n s in W exford H arb o u r. Pish size ranged betw een 22 an d 127 m m and no differences w ere observed betw een species an d loca­ tions (ANOVA: F = 1.42, d f = 3, P = 0.24) an d n o n e o f th em h ad a n em p ty stom ach. T w enty-one different prey item s w ere identified, w ith m ysids being generally the p ri­ m ary resource for flo u n d er an d polychaetes being the m o st a b u n d a n t p rey in plaice (Table 1). PC O o rd in a tio n o f sam ple centroids show ed a m o re clum ped d istrib u tio n for flo u n d er an d a greater scattering o f th e plaice data p o in ts (Pig. 2). PERM AN OV A detected significant differences for b o th th e interactions: Spe*Loc a n d Spe>fSta(Loc), as well as for th e effect ‘S tatio n(L oc)’, revealing th e dependence o f locality-specific v ariation in governing feeding in teractio n s betw een these species

Table 1. Frequency of occurrence of all prey Items found In the stom ach contents of plaice (P) and flounder (F) from Bull Island (B) and Wexford Harbour (W) at stations 1 and 2. FB1 (19)

FB2 (31)

FW1 (30)

FW2 (20)

PB1 (30)

PB2 (20)

PW1 (16)

PW2 (36)

Harpacticoida Cyclopoida

0.11 0

0.19 0.1

0.2 0

0.65 0

0.9 01

0.2 0.2

0 0

0.06 0

Calanoida Polychaeta Err.

0 0.05

0 0.1

0 0

0 0.15

0.03 0.47

0 0.55

0 0.75

0 0.56

Polychaeta Sed. Amphipoda Isopoda Bivalvia

0.21 0.53 0.1 0

0.03 0.48 0.1 0.6

0.2 0.07 0.03 0.03

0.25 0.2 0 0

0.03 0.27 0.03 0.2

0.35 0.25 0.1 0.4

0.18 0.19 0 0

0 0.31 0.08 0

Ostracoda

0

0.3

0.13

0

0.03

0

0

0.17

eggs Nematoda Brachyura Caridea

0 0 0.16 0

0.3 0 0.03 0

0.03 0 0.03 0.03

0.5 0 0.25 0

0.07 0 0 0.50

0.1 0 0 0

0 0 0 0

0.06 0.06 0 0

Mysidacea

0.63

0.23

0.57

0.6

0.1

0

0

0

Oligochaeta Holoturldae algae Hydrozoa Cirripedia fish

0 0 0.1 0.05 0 0

0 0 0.13 0 0 0.03

0 0 0.03 0 0 0

0 0 0 0 0 0

0.03 0 0.27 0 0 0

0.05 0 0.2 0 0 0

0 0.06 0.12 0 0.06 0

0 0 0 0.06 0 0

Tunicata

0

0

0.03

0

0

0

0

0

unidentified

0

0

0.03

0

0

0

0

0

Numbers In brackets In the column headers refer to sample size. Values In bold represent 'Im portant' (>25%) or 'dom inant' (>50%) prey Items, according to Albertlne-Berhaut (1973).

98

M arine Ecology 32 (Suppl. 1) (2011 ) 96-101 © 2011 Blackwell Verlag GmbH

Food reso u rce use in plaice a n d flo u n d e r

M aria n i, B o g g a n & B a la ta

40

1.2

Copepods

Amphipoda + Isopoda

T

1.0

0.8

PW1 O

A FB1

0.6

FW 1

0.4

•

O PW2

0.2

FB2

0

FW2 0.0

1 B-1

i

B-2

W-1 W-2

PB2 û- -2 0

A -40 -40

PB1

0

-2 0

20

40

PC01 (51.3% of total variation) Fig. 2. Ordination plot of sample centroids Inferred with Principal coordinate analysis. F is for flounder (black), P is for plaice (grey), B is

B-1

1,2 1 O th e r m a la c o s tra c a

1 .2 -

1.0

1 .0 -

0.8

0 .8 -

0.6

0 .6 -

0.4

0.4-

0.2

0 .2 -

0.0

0 .0 B-1

B-2

W-1 W-2

W-1 W-2

“W o rm s”

ii i B-1

Flounder

for 'North Bull Island' (triangles) and W is for 'Wexford Harbour'

B-2

B-2

I

W-1 W-2

= i Plaice

(circles).

T able 2. Results summary table for PERMANOVA procedure con­ ducted on presence/absence stomach content data. Values in bold are significant with a = 0.05. source Spe Loc Sta (Loc) Spe*Loc Spe*Sta(Loc) residual total

df

MS

pseudo-F

P-value

1 1 2 1 2

68,768 20,513 9171.8 31,029 11,756

2.215 2.073 3.400 2.612 4.358

0.114 0.081 0.001 0.041 0.001

191 198

2697.5

(Table 2). Pairw ise tests co n d u cte d o n b o th interactions show ed consistent significant differences betw een species w ith in stations b u t only plaice was sh o w n to vary its diet significantly betw een locations. U nivariate analyses w ere also inform ative in describing diet variatio n betw een an d w ith in species (Fig. 3). Signifi­ cant differences betw een species w ere detected in th e cate­ gory ‘W o rm s’ (F = 32.5, P = 0.01). The interactions Spe*Loc for ‘O th er M alacostraca’ (F = 42.9, P = 0.02) an d Spe*Sta (Loc) for ‘C o p ep o d s’ (F = 4.3, P = 0.01) w ere also significant, an d th e Spe*Loc in terac tio n for b o th ‘C ope­ p o d s’ (F = 10.7, P = 0.08) an d ‘A m p h ip o d a + Isopoda (F = 14.4, P = 0.06) w ere only m arginally above th e p ro b a ­ bility threshold. SNK tests confirm ed significant differences betw een plaice a n d flo u n d er across all stations in term s of ‘C opepods’, b u t only in W exford for ‘O th er M alacostraca’.

Marine Ecology 32 (Suppl. 1) (2011 ) 96-101 © 2011 Blackwell Verlag GmbH

Fig. 3. Frequencies of four main food categories In plaice and floun­ der from tw o estuaries. Results of univariate ANOVA tests are In the text.

D iscussion T he stu d y o f th e feeding habits a n d resource p artitio n in g in closely related fish can be very useful to u n d erstan d th e flows o f energy across th e food web (D arn au d e, 2005) a n d pro v id e im p o rta n t insights in to th e tro p h ic flexibility o f in teractin g species (M ariani et a í 2002; Platell et a í 2006; Russo et al. 2008). Yet, th e qu an tificatio n o f diet overlap o r niche segregation - even w hen su p p o rte d by ro b u st explanations o f th e processes underlying th e p a t­ tern s - m ay still only p rovide a very n arro w p ictu re of th e tru e flexibility o f a species’ tro p h ic ecology. This stu d y expands th e analysis o f resource p artitio n in g betw een tw o c o m m o n flatfish, plaice a n d flounder, by taking in to co n sid eratio n th e n atu rally high e n v iro n m en ­ tal heterogeneity o f estuarine habitats, an d p erform ing diet com parisons in tw o different estuarine habitats. W exford H a rb o u r was fo u n d to be d o m in ated by flo u n d er, w hereas N o rth Bull Island show ed a p re d o m i­ n an ce o f plaice. This is pro b ab ly linked to th e low er salin­ ities observed y e a r-ro u n d in W exford (C raig et a í 2008) an d th e w ell-know n p ro n o u n c e d preference o f flo u nder for brackish environm ents. This species ap p eared to exhi­ b it a m o re spatially h o m o g en eo u s food sp ectrum (clu m p ed scatter o f d ata in Fig. 2) relative to plaice,

99

Food reso u rce use in plaice a n d flo u n d e r

w hich exhibits rem arkable diet changes betw een th e tw o study locations (w ider d istrib u tio n o f data in Fig. 2). U nivariate tests o n th e m o st a b u n d a n t p rey item s (Fig. 3) illustrate well th e extent an d n a tu re o f diet v aria­ tio n betw een an d w ith in plaice an d flounder. Plaice seems to be the m ost efficient forager o f polychaetes a n d o th er w orm -like prey, w hereas flo u n d er consistently consum es a greater a m o u n t o f m alacostraca, p articu larly m ysids (Table 1). The frequency o f different preys across flo u n ­ der sam ples is m u ch m o re even th a n in plaice: for instance, considerable frequencies o f copepods, decapods and bivalves are fo u n d in th e stom achs o f plaice from N o rth Bull Island, w hereas virtually only polychaetes an d am p h ip o d s are consum ed in W exford. O ne explanation m ay reside in th e fact th a t W exford is a flo u n d e r-d o m i­ nated h abitat, w hich m ig h t drive th e less n u m ero u s plaice to select only preys, such as polychaetes an d am p h ip o d s, th a t are n o t ‘p referred ’ b y flounder, as indeed appears to be the case in W exford H arb o u r. Intra-specific co m p eti­ tio n m ay also play a role, p ro m p tin g plaice to select a w ider range o f prey in th e location w here it is m o re fre­ q u en t an d d o m in a n t {i.e. N o rth Bull Island). O n the o th er h an d , flo u n d er does n o t seem to go th ro u g h the sam e ‘diet sw itch’, w hen th e tw o estuaries are com pared. T he only p rey categories affected are a m ­ p h ip o d s and isopods, w hich show a low frequency in W exford (Fig. 3), alth o u g h this is counterbalanced by the intense co n su m p tio n o f o th er m alacostraca (espe­ cially m ysids). W ith o u t a parallel investigation o n th e abun d an ce o f p o ten tial p rey (W o u ters & C abral 2009), it rem ains difficult to assess to w h at extent th e results m ay be influenced b y differential availabilities of resources; how ever, th e presen t data unam b ig u o u sly show th a t estuarine en v iro n m en tal heterogeneity d eter­ m ines changes in resource use in plaice a n d flo u n d er and th a t th e responses are different for each species, resulting in th e v ariatio n o f p attern s o f tro p h ic in te r­ relationships betw een species. T he feeding habits o f plaice an d flo u n d er vary betw een and w ith in localities (Table 2), resulting in very interesting p attern s at finer scales: plaice in W exford consum ed significantly different p rey th a n plaice in Bull Island, and in each statio n w ith in estuary, plaice an d flounder consistently preyed u p o n different item s, effec­ tively reducing niche overlap. T his view o f tro p h ic niches an d resource use m akes th e fluctuating, unstable, seem ingly chaotic estuarine h ab ita t a m u ch m o re finetu n ed , sophisticated, elegantly fu n ctio n in g system th a n generally believed. F u rth er studies in clu d in g a greater n u m b er o f estuaries, an d possibly a greater n u m b e r of species, m ay ad d operatio n al com plexity, b u t w ould cer­ tainly help to characterise these m echanism s w ith greater confidence.

100

M aria n i, B o g g a n & B alata

C onclu sions W e have show n th a t th e p a ttern s o f niche overlap and resource p artitio n in g betw een plaice a n d flo u n d er in estu­ arine hab itats vary dep en d in g o n th e specific system stu d ­ ied. This strengthens th e view th a t estuaries, lagoons and o th er tran sitio n al h abitats m ay rep resen t a heterogeneous ‘m o saic’ o f selective forces (W einig & Schm it 2004), w hich is crucial to th e ev olution o f th e life-histories o f coastal m arin e fish (M ariani 2006) an d p erh ap s influences th e fu n ctio n in g o f m o re ‘extended’ phen o ty p ic traits (sensu D aw kins 1982), such as tro p h ic in teractions and c o m m u n ity structure. Fu tu re studies sh o u ld a tte m p t to evaluate w h ether the observed tro p h ic flexibility results entirely fro m p h e n o ­ typic plasticity (G ronkjaer et a í 2007) o r also to som e extent fro m genom ic ad ap ta tio n .

A c k n o w le d g e m e n ts T he stu d y was based o n d ata collected as p a rt o f CB’s final year project, internally fu n d ed b y th e U C D School o f Biology a n d E n v ironm ental Science. W e w ould like to th an k D ebbi Pedreschi for help d u rin g sam pling an d the editors an d tw o an o n y m o u s reviewers for th e ir valuable suggestions.

R eferen ces A arnio K., B onsodorff E., Rosenback N. (1996) Food a n d feed­ ing habits o f juvenile flounder Platichthys flesus (L.) and tu rb o t Scophthalmus maximus (L.) in the A land archipelago, n o rth ern Baltic Sea. Journal of Sea Research, 36, 311— 320. A lbertine-B erhaut J. (1973) Biologie des stades juveniles de teleosteens, M ugilidae, Mugil auratus Risso 1810, Mugil capito Cuvier 1829 et Mugil saliens Risso 1810. Regime alim entaire.. Station M arine d ’E ndoum e, Marseille: 2 pp 251-266. Am ezcua F., N ash R.D.M ., Veale L. (2003) Feeding habits o f the O rder Pleuronectiform es a n d its relation to the sedim ent type in the n o rth Irish Sea. Journal o f the Marine Biological Association o f the United Kingdom, 83, 593-601. A ndersen B.S., Cari I.D., G ronkjæ r P., S tottrup J.C. (2005) Feeding ecology and grow th o f age 0 year Platichthys flesus (L.) in a vegetated and a bare sand habitat in a n u trie n t rich fjord. Journal o f Fish Biology, 66, 531-552. A nderson M.J. (2001) A new m eth o d for n on-param etric m u l­ tivariate analysis o f variance. Austral Ecology, 26, 32-46. Beck M.V., K enneth L., H eck J.R., K enneth W .A., Childers D.L., Eggleston D.B., Gillanders B.M., H alpern B., Hays C.G., H oshino K., M inello T.J., O rth R.J., Sheridan P.F., W einstein M .P. (2001) The identification, conservation, and m anagem ent o f estuarine and m arine nurseries for fish and invertebrates. BioScience, 51, 633-641.

M arine Ecology 32 (Suppl. 1) (2011 ) 96-101 © 2011 Blackwell Verlag GmbH

F ood reso u rce use in plaice a n d flo u n d e r

M aria n i, B o g g a n & B alata

Bels V.L., D avenport J. ( 1996) A com parison o f food capture

Lotze H.K., Lenihan H.S., B ourque B.J., B radbury R.H., Cooke

and ingestion in juveniles o f two flatfish species, Pleuronectes

R.G., Kay M .C., Kidwell S.M., Kirby M.X., Peterson C.H.,

platessa a n d Lim anda lim anda (Teleostei: P leuronectifor­

Jackson J.B.C. (2006) D epletion, degradation a n d recovery

m es). Journal o f Fish Biology, 49, 390-401.

potential o f estuaries and coastal seas. Science, 312, 1806-

Beyst C., Cattrijsse A., Mees J. (1999) Feeding ecology o f juve­ nile flatfishes o f the su rf zone o f a sandy beach. Journal o f Fish Biology, 55, 1171-1186. Craig G., Paynter D., Coscia I., M ariani S. (2008) Settlem ent o f gilthead sea bream Sparus aurata L. in a southern Irish Sea coastal habitat. Journal o f Fish Biology, 72, 287-291. D arnaude A.M. (2005) Fish ecology and terrestrial carbon use

1809. M ariani S. (2006) Life-history- and ecosystem -driven variation in com position a n d residence p attern o f seabream species (Perciform es: Sparidae) in two M editerranean coastal lagoons. M arine Pollution Bidletin, 53, 121-127. M ariani S., M accaroni A., M assa F., Ram pacci M., T ancioni L. (2002) Lack o f consistency betw een the trophic interrela­

in coastal areas: im plications for m arine fish production.

tionships o f five sparid species in two adjacent central

Journal o f A nim al Ecology, 74, 864-876.

M editerranean coastal lagoons. Journal o f Fish Biology, 61,

D arnaude A.M., H arm elin-V ivien M.L., Salen-Picard C. (2001) Food partitio n in g am ong flatfish (Pisces: Pleuronectiform s) juveniles in a M editerranean coastal shallow sandy area. Journal o f the M arine Biological Association o f the United Kingdom, 81, 119-127. Dawkins R. ( 1982) The Extended Phenotype. O xford U niversity Press, Oxford, 307 pp. Elliott M., Q uintino V.M . (2007) The estuarine quality para­ dox, environm ental hom eostasis and the difficulty o f detect­ ing anthropogenic stress in naturally stressed areas. M arine Pollution Bidletin, 54, 640-645. G ibson R.N. (1994) Im pact o f h abitat quality and q uantity on the recruitm ent o f juvenile flatfishes. Journal o f Sea Research, 32, 191-206. Gower J.C. ( 1966) Some distance properties o f latent ro o t and vector m ethods used in m ultivariate analysis. Biometrika, 53, 325-338. Gronkjaer P., Cari J.D., Rasm ussen T.H., H ansen K.W. (2007) Effect o f h abitat shifts o n feeding behaviour and grow th o f 0 year-group flounder Platichthys flesus (L.) transferred betw een m acroalgae a n d bare sand habitats. Journal o f Fish Biology, 70, 1587-1605. H aedrich R.L. (1983) E stuarine fishes. In: K etchum B.H. (Ed), Estuaries and Enclosed Seas. Elsevier Publishing C om pany, Am sterdam : pp. 183-207. K raus R.T., Secor D .H . (2005) A pplication o f the nursery-role hypothesis to an estuarine fish. M arine Ecology Progress Ser­

138-147. Piet G.J., P iste re r A.B., Rijnsdorp A.D. ( 1998) O n factors structuring the flatfish assemblage in the sou th ern N o rth Sea. Journal o f Sea Research, 40, 143-152. Platell M.E., O rr P.A., P o tter I.C. (2006) Inter- and intraspe­ cific partitio n in g o f food resources by six large a n d a b u n ­ d a n t fish species in a seasonally open estuary. Journal o f Fish Biology, 69, 243-262. Raffaelli D.G., H aw kins S. (1996) Intertidal Ecology. C hapm an 8c Haii, L ondon: 356 pp. Russell S.F. ( 1976) The Eggs and Planktonic Stages o f British M arine Fishes. Academ ic Press , L ondon: 524 pp. Russo T., Pulcini D., O ’Leary A., C ataudella S., M ariani S. (2008) R elationship betw een body shape a n d trophic niche segregation in two closely related sym patric fishes. Journal o f Fish Biology, 73, 809-828. Schoener T.W . (1974) Resource p a rtitioning in natu ral com ­ m unities. Science, 185, 27-39. U nderw ood A.J. (1997) Experiments in Ecology. Their Logical Design and Interpretation Using Analysis o f Variance. C am ­ bridge U niversity Press, Cam bridge: 504 pp. W einig C., Schm it J. (2004) E nvironm ental effects o n the expression o f quantitative trait loci and im plications for phenotypic evolution. BioScience, 54, 627-635. W outers N., Cabral H .N . (2009) Are flatfish nursery grounds richer in benthic prey? Estuarine Coastal and S helf Science, 83, 613-620.

ies, 291, 301-305.

Marine Ecology 32 (Suppl. 1) (2011 ) 96-101 © 2011 Blackwell Verlag GmbH

101

marine ecology

an evolutionary perspective

»

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

mtDNA differentiation in th e mussel M y tilu s gallo pro vin cialis Lmk. on th e Iberian Peninsula coast: first results Javier R. Luis, A n g e l S. C o m e sa ñ a & A n d r é s S anjuan Xenética Evolutiva Molecular, Facultade de Bloloxia, Unlversldade de Vigo, Vigo, Spain

K eywords Atlantic Ocean; genetic differentiation; M editerranean Sea; mitochondrial DNA;

Mytilus galloprovincialis. C orrespondence Javier Rodríguez Luis, Xenética Evolutiva Molecular, Facultade de Bloloxia, Edit, de Ciencias, Unlversldade de Vigo, E-36310Vlgo, Spain. E-mail: [email protected] Accepted: 2 February 2011 doi : 10.1111/j.1439-0485.2011,00430.x

A bstract T he nucleo tid e sequence o f th e VD1 d o m a in o f th e Long U nassigned R egion in th e F m ito ch o n d rial D N A genom e was stu d ied for 135 Ib erian m ussels, 78 fro m the A tlantic a n d 57 from th e M editerranean. Significant genetic differenti­ a tio n betw een A tlantic an d M ed iterran ean M ytilus galloprovincialis sam ples was fo u n d (FSt = 0.262, P < 0 .0 0 0 0 1 ). T he fo u r m ain clusters observed in the n eig h b o r-jo inin g tree o f haplotypes w ere n o t exclusive for a specific region, b u t a clear geographic p attern could be observed. O ne o f th e clusters contained 8 6 % o f th e A tlantic individuals a n d th e rem ain in g th ree clusters w ere p re d o m i­ n an tly M editerranean. T he A tla n tic-M ed iterran ean d ifferentiation o f th e m ito ­ chondrial D N A haplotypes was in ag reem ent w ith previous d ata describing the sam e p a rtitio n in g in M . galloprovincialis a n d in m an y o th er m arin e organism s, using different kinds o f genetic m arkers. In all cases th e A lm eria O ran O ceano­ graphic fro n t has been associated to this genetic discontinuity.

Introduction In E urope, the m ussel M ytilus galloprovincialis Lmk. is distributed in th e Black Sea, th e M ed iterran ean an d o n the A tlantic coast fro m th e Ib erian P eninsula as far n o rth as the B ritish Isles (G osling 1992). T he Ib erian P eninsula occupies an in term ed iate lo catio n in this d istrib u tio n , betw een th e A tlantic an d M ed iterran ean regions. Extensive genetic studies o f M . galloprovincialis p o p u la ­ tions in th e Ib erian P eninsula have been carried o u t using allozym e poly m o rp h ism s (Sanjuan et a í 1994, 1997; Q uesada et al. 1995a), m tD N A RFLPs (Q uesada et a í 1995b; S anjuan et a í 1996) a n d m icrosatellites (D iz & Presa 2008). In all cases, results agree o n th e existence of a stro n g genetic d isco n tin u ity betw een A tlantic a n d M ed i­ terran ean p o p u latio n s associated to th e A lm eria O ran O ceanographic fro n t (A O O F). H ow ever, th e d irect analy­ sis o f nucleotid e v ariatio n w o u ld pro v id e a deeper insight in to th e p o p u la tio n dynam ics o f th e species, o n b o th sides o f the G ibraltar Strait, th a n is offered b y allozymes, restriction enzym e analyses or m icrosatellites.

102

C urrently, analysis o f m ito ch o n d rial D N A (m tD N A ) sequences is one o f th e m o st w idely used tools in m olecu­ lar phylogenetics studies due to u n ip aren tal inheritance, abu nd an ce o f selectively n eu tral m u tatio n s, low rate o f reco m b in atio n an d technical sim plicity. Skibinski et a í (1994) a n d Z o u ro s et a í (1994) described th e existence o f d oubly u n ip aren tal in h eritan ce (D U I) o f th e m tD N A in th e M ytilidae family. D U I involves th e existence o f heteroplasm ic m ales carrying a m atern al (F) an d a paternal (M ) m ito ch o n d rial genom e, an d ho m o p lasm ic females b earing only th e F genom e. T hus, th e F genom e is m a te r­ nally tra n sm itte d to offspring, w hereas th e M genom e is paternally tra n sm itte d to m ale p rogeny only. In species w ith D U I, m atern al lineages pro v id e m o re reliable in fo r­ m a tio n for p o p u la tio n a n d phylogenetic studies, as M lin ­ eages are n o t a p p ro p riate for phylogeographic studies due to th eir very fast evolution an d liability to invasion from th e F lineage (Ladoukakis et a í 2002). T he m ito ch o n d rial genom e o f M ytilus is divided in to tw o parts: th e core th a t contains all p ro tein , rRN A an d tRN A coding genes an d a few n o n co d in g regions o f <500 b p , an d th e LUR (large

M arine Ecology 32 (Suppl. 1) (2011 ) 1 02 -10 6 © 2011 Blackwell Verlag GmbH

mtDNA d iffe re n tia tio n in Iberian M. galloprovincialis Lmk.

Luis, C o m e s a ñ a & S a n ju a n

unassigned region). C ao et al. (2004) have divided the LUR into three parts: th e first variable d o m ain (VD1), the conserved d o m ain (C D ), an d th e second variable d o m ain (VD2). These do m ain s seem to be equivalent to those fo u n d in h u m a n m tD N A an d co n tain sequence m otifs w hich are k n ow n to be involved in th e replication an d tran scrip tio n o f th e m olecule. These observations suggest th a t the LUR is th e m ain co n tro l region o f the m ito ch o n d rial genom e (Cao et a l 2004). The h igh degree o f nucleotide variability m akes VD1 d o m ain an excellent to o l in o rd er to analyse genetic variatio n in th e m ussel M . galloprovincialis.

p rim e r (UNFOR1 an d UNREV1; C ao et al. 2004); 1.5 U o f T aq D NA polym erase (EcoTaq, Ecogen) an d 3 pL o f th e extracted DNA. A n initial d én a tu ra tio n at 94 °C for 3 m in, 40 PCR cycles (94 °C: 1 m in, 55 °C: 1.5 m in, 72 °C: 1 m in) an d a final extension at 72 °C for 6 m in were carried o u t in a G eneA m p PCR System 9700 th e r­ m al cycler (A pplied Biosystem s). The PCR p ro d u cts were visualized by UV tran sillu m i­ n atio n after electrophoresis in 1.5% SeaKem LE agarose gels (FM C B ioProducts) con tain in g eth id iu m brom ide. D o u b le-stran d ed D NA fro m PCR reactions was cleaned using th e Q iaquick PC R purificatio n kit (Q iagen G m bH ),

Thus, the aim o f this w o rk was to assess th e degree o f variation and differentiation, an d to infer the p o p u la tio n

follow ing th e m an u fac tu rer’s instructions. F rom purified PCR p ro d u cts, b o th strands o f a frag­ m e n t o f 575 bp, belonging to th e VD1 d o m ain o f the fem ale m tD N A LUR, was sequenced in tw o separated sequencing reactions using th e CEQ Dye T e rm in ato r

dynam ics processes leading to th e cu rre n t p attern s o f genetic variation in th e M . galloprovincialis p o p u latio n s living on the Iberian coast using th e n u cleotide sequence o f the VD1 do m ain o f th e large unassigned region (LUR) o f the F m tD N A genom es.

M aterial and M eth o d s A to tal o f 135 individuals o f M . galloprovincialis were col­ lected in tw o A tlantic an d tw o M ed iterran ean locations on the Iberian Peninsula coast (Fig. 1). A fter dissection, to tal D NA was extracted fro m gonadal tissue using the p rocedure o f DeSalle et al. (1993). A m plification o f th e large unassigned region (LUR) o f the m ito ch o n d rial genom e was carried o u t in a final v o l­ um e o f 50 pL co ntain in g 10 mM T ris-H C l, p H 9.0, 2 mM M gCl2, 50 mM KC1, 0 . 1 % T rito n X - 1 0 0 ; 0 . 2 mM o f each dN T P (A m ersham P harm acia B iotech); 0.06 pM o f each

T45

GSU GBA

GCQ GCA ^

--40'

J- 35 10°

-5°

D NA sequencer (Beckm an In stru m en ts) at th e Facultade de Bioloxia, U niversidade de Vigo. Sequences were read an d edited using th e softw are pro v id ed w ith th e seq uen­ cer an d aligned w ith CLUSTAL X version 2.0.9 (Larkin et al. 2007). N ucleotide diversity (T ajim a 1983; N ei 1987) for each sam ple was estim ated in the M EGA softw are v4.0.2. Gene diversity estim ated fro m haplotype frequencies (N ei 1987) as well as p o p u latio n pairw ise FSt distances (Reynolds et al. 1983; Slatkin 1995) betw een all pairs o f po p u latio n s, were co m p u ted using the A RLEQU IN soft­ w are package v3.1 (Excoffier et al. 2005). In th e case o f pairw ise FST distances we have applied th e B onferroni m eth o d , a m u ltip le-co m p ariso n correctio n used w hen several statistical tests are being p erfo rm ed sim u lta­ neously. To avoid spu rio u s positives, th e alpha value was low ered to acco u n t for th e n u m b e r o f com parisons being perform ed. H aplotype phylogenetic relationships were estim ated w ith a n eigh b or-jo in in g (NJ) m e th o d (Saitou 8 c N ei 1987) co n d u cte d by th e M EGA softw are v4.0.2 (T am ura et al. 2007), using th e g am m a-corrected T a m u ra -N e i dis­ tance (T am u ra 8 c N ei 1993). S u p p o rt for th e tree was o b tain ed by 1000 b o o tstra p replicates (Felsenstein 1985).

R esults

150 km

-

Cycle Sequencing Kit (B eckm an In stru m en ts) an d tw o different prim ers specific for th e fem ale m tD N A m olecule. Finally, fragm ents were m ig rated in a B eckm an CEQ2000

0°

Fig. 1. Sampling locations of M. galloprovincialis on the Iberian Pen­ insula coast: Suances (GSU), Baiona (GBA), Cambrils (GCA) and Cadaque (GCQ). Also shown is the Almería Oran Oceanographic front (AOOF).

M arine Ecology 32 (Suppl. 1) (2011) 102-106 © 2011 Blackwell Verlag GmbH

A to tal o f 135 individuals were sequenced for 575 b p o f th e VD1 d o m ain o f th e fem ale m tD N A . Seventy-six v ari­ able sites w ere observed, defining 40 different haplotypes w hose frequencies in each o f the fo u r sam ples are detailed in Table 1 . The sequence o f h aplotype h i 2 was deposited in G enB ank (accession no. H Q 675011). F our o f these

103

mtDNA d iffe re n tia tio n in Iberian M. galloprovincialis Lmk.

Table 1. Relative frequencies of the 40 haplotypes found in this study. Numbers in parentheses are sample sizes. Sample codes are indicated in Fig. 1. Atlantic

Mediterranean

haplotypes GSLK33) GBA(45) total(78) GCA(32) GCQ(25) total(57) h01 h02

0.36 0.06

0.31 0.02

0.34 0.04

0.09 0

0 0

0.05 0

h03 h04 h05 h06 h07 h08 h09

0 0.03 0.09

0 0.02 0.18

0 0.03 0.13

0.06 0 0

0.12 0.04 0.04

0.09 0.02 0.02

0 0.03 0 0

0.04 0.02 0.02 0.02

0.02 0.03 0.01 0.01

0 0 0.25 0.19

0 0 0.08 0.20

0 0 0.17 0.19

h 10 hi 1 h 12

0.03 0 0

0.02 0.04 0.04

0.03 0.02 0.02

0.12 0.03 0.06

0.16 0.12 0.04

0.14 0.08 0.05

h 13 h 14

0 0

0.02 0

0.01 0

0.06 0.12

0.04 0.04

0.05 0.08

GSU02 GSU03 GSU04 GSU05 GSU07

0.03 0.03 0.03 0.03 0.03

0 0 0 0 0

0.01 0.01 0.01 0.01 0.01

0 0 0 0 0

0 0 0 0 0

0 0 0 0 0

GSU14 GSU17

0.03 0.03

0 0

0.01 0.01

0 0

0 0

0 0

GSU20 GSU21 GSU25 GSU28 GSU29

0.03 0.03 0.03 0.03 0.03

0 0 0 0 0

0.01 0.01 0.01 0.01 0.01

0 0 0 0 0

0 0 0 0 0

0 0 0 0 0

GSU34

0.03

0

0.01

0

0

0

GBA03 GBA04 GBA17 GBA18

0 0 0 0

0.02 0.02 0.02 0.02

0.01 0.01 0.01 0.01

0 0 0 0

0 0 0 0

0 0 0 0

GBA22

0

0.02

0.01

0

0

0

GBA27 GBA29 GBA37 GBA40

0 0 0 0

0.02 0.02 0.02 0.02

0.01 0.01 0.01 0.01

0 0 0 0

0 0 0 0

0 0 0 0

GBA46 GCQ104

0 0

0.02 0

0.01 0

0 0

0 0.04

0 0.02

GCQ122 GCQ126

0 0

0 0

0 0

0 0

0.04 0.04

0.02 0.02

haplotypes ( h l l , h l2 , GBA04 an d G CQ 126) show ed a previously described d u p licatio n (C ao et al. 2004; Sm ietanka et al. 2004) o f 36 b p , sp an n in g fro m nucleotides 262 to 297 o f th e sequence o f haplotype h l2 . H aplotypes appearing m o re th a n once are n am ed w ith n u m b ers (h 0 1 -h l4 ) an d th e ‘singletons’ are n am ed b y th e code of the individual carrying th e haplotype. T here was only one h aplotype (hlO) presen t in all th e sam ples. H aplotypes h o i a n d h05 w ere th e com m o n est am ong the A tlantic sam ples (frequencies o f 34 an d 14%,

104

Luis, C o m e s a ñ a & S a n ju a n

respectively), w hereas haplotypes h08, h09 an d hlO w ere th e m o st a b u n d a n t in th e M ed iterran ean, w here they reach frequencies o f 14—19%. It is n o tew o rth y th a t th e percentage o f singleton haplotypes, calculated over the to tal n u m b e r o f individuals, was m u ch h igher in the A tlantic (30% ) th a n in th e M ed iterran ean (5% ). W h en calculated over th e n u m b er o f haplotypes, th e value was also distinctly higher in th e A tlantic ( 6 6 %) th a n in the M ed iterran ean (21% ). All th e p o p u latio n s show ed sim ilar degrees o f diversity at th e h aplotype level. H aplotype diversity (h) averaged 0.87 in th e A tlantic sam ples and 0.9 in th e M ed iterran ean sam ples. Conversely, th e average o f nucleo tid e diversity (n) in th e M ed iterran ean (0.025) was alm o st d o uble th e value in th e A tlantic (0.013), alth o u g h an u n p aired t-te st resulted in a prob ability o f 0.0815. M ore extensive sam pling will be necessary to clar­ ify this ap p a re n t difference in nucleo tid e diversity. T he p o p u la tio n pairw ise FST distances (d ata n o t show n) yielded highly significant values for th e A tlan ticM ed iterran ean pairs (P < 0.00001) an d nonsignificant values for th e M ed iterran ean pairs (P = 0.748). W h en the A tlantic p o p u latio n s w ere com pared, th e FST distance was fo u n d significant a t th e 5% level, alth o u g h it becam e nonsignificant after applicatio n o f B onferroni correction for th e six pairw ise com p ariso n s (alpha level was low ered fro m 0.05 to 0.0083). T he FSt value betw een th e A tlantic a n d th e M ed iterran ean p o o led sam ples (0.262) was highly significant (P < 0.00001). T he NJ tree (Fig. 2) show ed fo u r m ain clusters su p ­ p o rted for b o o tstra p values h igher th a n 70%. The largest cluster, su p p o rte d b y a b o o tstra p value o f 97% , included 8 6 % o f th e A tlantic individuals, an d 29 different h a p lo ­ types (24 exclusively A tlantic). T he rem ain in g th ree clus­ ters w ere p red o m in a n tly M editerranean, encom passing 81% o f th e individuals o f this geographic region.

D iscussion T he results o f th e analyses applied in this stu d y w ere consistent w ith th e existence o f a significant genetic dis­ co n tin u ity betw een th e A tlantic an d M ed iterran ean p o p u ­ lations o f M ytilus galloprovincialis o n th e Ib erian coasts. O n th e one h an d , th e p o p u latio n pairw ise F St distances show ed high d ifferentiation betw een th e A tlantic and the M ed iterran ean p o p u latio n s, b u t n onsignificant differences w ith in each group. O n th e o th e r h an d , th e NJ tree dis­ played fo u r highly differentiated clusters rep resen ting fo u r g roups o f haplotypes separated, one fro m each other, by a m in im u m o f 10 m u ta tio n a l steps. A lthough n o cluster is exclusive for a specific region, a clear geographic p a t­ te rn differentiates th e largest cluster, w hich includes 8 6 % o f th e A tlantic individuals, an d th e rem ain in g th ree clus­ ters, p red o m in an tly M editerranean.

M arine Ecology 32 (Suppl. 1) (2011 ) 1 02 -10 6 © 2011 Blackwell Verlag GmbH

Luis, C o m e s a ñ a & S a n ju a n

h02 (3A) — GSU07 h01 (26A/3M) — GCQ104 1-GSU25 ÍjG B A 0 3 T — GBA40 .GSU04 I— GSU20 I—GSU29 — h03 (5M) GSU03 GBA22 GSU17 — GSU21 GBA46 46 — GSU34 -------------GBA29 ■h04 (2A/1M) 97 ^ GSU02 — GBA27 h05 (1JA/1M) 75 — GSU14 h06 (2A) 71 I— GBA18 — GSU05 — GBA17 h07 (2A) GBA37 ----------- h08 (1A/10M) |h09 (1 A/11M) ---------------h 10 9 6T-----------------111 ^ (2A/8M) . h 11 (2A/4M) lGCQ126 100 ■h12 (2A/3M) GBA04" GCQ 122 61 -h13 (1A/3M) 99 - GSU28 — h 14 (5M) Fig. 2. Evolutionary relationships of the 40 haplotypes Inferred using the neighbor-joining m ethod. Evolutionary distances w ere com puted using the Tamura-Nei m ethod and the rate variation am ong nucleo­ tide sites w as modeled with a gam m a distribution (shape param e­ ter = 0.6673). Bootstrap percentages from 1000 replications are indicated on branches. Numbers In brackets correspond to haplotype absolute frequencies in the Atlantic (A) and the Mediterranean (M).

W e have defined as A tlantic haplotypes those belonging to th e first cluster as th eir frequency in th e A tlantic is m u ch higher th a n in th e M editerran ean , a n d th e m u ta ­ tio nal co n nection w ith th e rest o f th e haplotypes requires at least 10 nucleotid e changes. U sing th e sam e reasoning, the rem aining haplotypes w ere defined as M editerranean. A t the nucleotide diversity level, th e A tlantic haplotypes show ed a higher degree o f hom ogeneity, as all o f th e m belonged to th e sam e cluster, an d th e largest difference betw een tw o haplotypes was th ree m u tatio n a l steps. In contrast, M ed iterran ean haplotypes are m u ch m o re diverse, belonging to th ree clearly differentiated clusters. T his scenario explains th e high n value in th e M ed iterra­ nean. T he ap p aren t c o n trad ictio n betw een th e difference in th e n value and th e sim ilarity o f h aplotype diversities (0.87 an d 0.90) is explained b y th e high frequency o f sin ­

Marine Ecology 32 (Suppl. 1) (2011) 1 02 -10 6 © 2011 Blackwell Verlag GmbH

mtDNA d iffe re n tia tio n in Iberian M. galloprovincialis Lmk.

gletons in th e A tlantic cluster, typical o f p o p u latio n s th at have gone th ro u g h episodes o f recen t expansion. T he low n u m b e r o f haplotypes in th e M ed iterran ean clusters could be explained b y recen t bottlen eck effects th a t reduced genetic diversity. These results w ere in agreem ent w ith previous findings describing an A tla n tic-M ed iterran ean p a rtitio n in g in M . galloprovincialis (S anjuan e t al. 1994, 1996, 1997; Q uesada et al. 1995a,b, 1998; L adoukakis et al. 2002; S m ietanka et al. 2004; D iz & Presa 2008) using different k inds o f genetic m arkers (allozym e polym orphism s, m tD N A restrictio n fragm ent length polym orphism s, m tD N A sequences an d nuclear m icrosatellites). In all cases this genetic d isco n tin u ity has been associated w ith th e A lm eria O ran O ceanographic fro n t (Fig. 1; T in tore et a í 1988), a stro n g m arin e surface cu rre n t betw een Al­ m eria (Spain) an d O ran (Algeria). T he stro n g c u rren t an d a sharp change in oceanographic co n d itio n s (higher salin­ ity a n d te m p e ra tu re in th e eastern p a rt o f th e front) could rep resen t a n im p o rta n t obstacle to th e dispersal of m ussel larvae. A process o f vicariance d u e to isolation o f b o th p o p u ­ lations is consistent w ith th e clear genetic d ifferentiation observed betw een th e A tlantic an d M editerranean. The n arro w in g o f th e G ibraltar Strait in th e Pleistocene (Pielo u 1979) could acco u n t for th e isolatio n o f th e M ed iter­ ra n ean basin. Subsequently, after th e o p en in g o f the G ibraltar Strait, th e A O O F w ould have acted as a p artial b arrier for genetic flow, m ain tain in g som e degree o f the differentiation previously established. In spite o f this b arrier to gene flow th ere are significant p ro p o rtio n s o f typically A tlantic haplotypes presen t in the M ed iterran ean a n d vice versa. Specifically, we have observed th a t 14% o f th e A tlantic individuals carry M edi­ terran ea n haplotypes a n d 19% o f th e M ed iterran ean m u s­ sels carry A tlantic haplotypes. T his asym m etric gene flow explains th e m ixing o f A tlantic a n d M ed iterran ean in d i­ viduals in all th e m ain clusters o f th e tree. It is co n g ruent w ith th e p red o m in a n tly eastw ard directio n o f th e surface w ater circulation th ro u g h th e Straits o f G ibraltar (Perkins et al. 1990) a n d has been described previously in M . gal­ loprovincialis using m tD N A RFLPs (Q uesada et a í 1998). H ow ever, this difference is n o t statistically significant an d m o re sam ples should be analyzed to pro v id e m o re su p ­ p o rt for th e asym m etry o f th e gene flow.

Sum m ary All th e results in this stu d y are consistent w ith a process o f isolation, follow ed b y restricted secondary contact, gen­ erating th e cu rren t p attern s o f genetic d ifferentiation betw een th e A tlantic an d M ed iterran ean p o p u latio n s of M ytilus galloprovincialis in th e Ib erian P eninsula. The

105

mtDNA d iffe re n tia tio n in Iberian M. galloprovincialis Lmk.

tem p o rary closing o f th e M ed iterran ean Sea, follow ed by the opening o f th e Strait o f G ibraltar an d subsequent gene flow restricted b y th e A O O F, w o u ld be a plausible geological scenario explaining this situ atio n . N evertheless, a m o re exhaustive sam pling w ould be necessary to p ro ­ vide b etter evidence o f th e recen t dynam ics o f A tlantic and M ed iterran ean p o p u latio n s, a n d th e in teractio n s betw een them .

R eferences Cao L., Kenchington E., Zouros E., Rodakis G.C. (2004) Evi­ dence that the large noncoding sequence is the main control region of maternally and paternally transmitted mitochon­ drial genomes of the marine mussel (Mytilus spp.). Genetics, 167, 835-850. DeSalle R., Williams A.K., George M. (1993) Isolation and characterization o f animal mitochondrial DNA. Methods in Enzymology, 224, 176-234. Diz A.P., Presa P. (2008) Regional patterns of microsatellite variation in Mytilus galloprovincialis from the Iberian Peninsula. Marine Biology, 154, 277-286. Excoffier L., Laval G., Schneider S. (2005) Arlequin ver. 3.0: an integrated software package for population genet­ ics data analysis. Evolutionary Bioinformatics Online, 1, 47-50. Felsenstein J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783-791. Gosling E.M. ( 1992) Systematics and geographic distribution of Mytilus. In: Gosling E. (Eds), The Mussel Mytilus: Ecology, Physiology, Generics and Culture. Elsevier, Amsterdam: 1- 20 .

Ladoukakis E., Saavedra C., Magoulas A., Zouros E. (2002) Mitochondrial DNA variation in a species with two m ito­ chondrial genomes: the case of Mytilus galloprovincialis from the Atlantic, the Mediterranean and the Black Sea. Molecular Ecology, 11, 755-769. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. (2007) Clustal W and Clustal X version 2.0. Bioinfor­ matics, 23, 2947-2948. Nei M. (1987) Molecular Evolutionary Genetics. Columbia University Press, New York: 512 pp. Perkins H., Kinder T.H., La Violette P.E. (1990) The Atlantic inflow in the western Alboran Sea. Journal o f Physical Oceanography, 20, 242-263. Pielou E.C. (1979) Biogeography. John Wiley 8 c Sons, Inc., London: 351 pp. Quesada H., Zapata C., Alvarez G. ( 1995a) A multilocus allozyme discontinuity in the mussel Mytilus galloprovincialis:

106

Luis, C o m esañ a & Sanjuan

the interaction of ecological and life-history factors. Marine Ecology Progress Series, 116, 99-115. Quesada H., Beynon C.M., Skibinski D.O.F. (1995b) A m ito­ chondrial DNA discontinuity in the mussel Mytilus gallopro­ vincialis Lmk: pleistocene vicariance biogeography and secondary intergradation. Molecular Biology and Evolution, 12, 521-524. Quesada H., Gallagher C., Skibinski D.A.G., Skibinski D.O.F. ( 1998) Patterns o f polymorphism and gene flow of genderassociated mitochondrial DNA lineages in European mussel populations. Molecular Ecology, 1, 1041-1051. Reynolds J., W eir B.S., Cockerham C.C. (1983) Estimation for the coancestry coefficient: basis for a short-term genetic distance. Genetics, 105, 767-779. Saitou N., Nei M. (1987) The neighbor-joining method: a new m ethod for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406-425. Sanjuan A., Zapata C., Alvarez G. (1994) Mytilus galloprovin­ cialis and M. edidis on the coasts of the Iberian Peninsula. Marine Ecology Progress Series, 113, 131-146. Sanjuan A., Comesaña A.S., De Carlos A. (1996) Macrogeo­ graphic differentiation by mtDNA restriction site analysis in the S.W. European Mytilus galloprovincialis Lmk. Journal of Experimental Marine Biology and Ecology, 198, 89-100. Sanjuan A., Zapata C., Alvarez G. (1997) Genetic differentia­ tion in Mytilus galloprovincialis Lmk. throughout the world. Ophelia, 47, 13-31. Skibinski D.O., Gallagher C., Beynon C.M. (1994) Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics, 138, 801-809. Slatkin M. ( 1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139, 457-462. Smietanka B., Zbawicka M., Wolowicz M., Wenne R. (2004) M itochondrial DNA lineages in the European populations of mussels Mytilus. Marine Biology, 146, 79-92. Tajima F. (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics, 105, 437-460. Tamura K., Nei M. (1993) Estimation of the num ber of nucle­ otide substitutions in the control region o f mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512-526. Tamura K., Dudley J., Nei M., Kumar S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599. Tintore J., La Violette P.E., Blade I., Cruzado A. (1988) A study o f an intense density front in the eastern Alboran Sea: the Almeria-Oran front. Journal o f Physical Oceanography, 18, 1384-1397. Zouros E., Ball A.O., Saavedra C., Freeman K.R. (1994) An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proceedings o f the National Academy of Sciences o f the United States o f America, 91, 7463-7467.

M arine Ecology 32 (Suppl. 1) (2011 ) 1 02 -10 6 © 2011 Blackwell Verlag GmbH

marine ecology

an evolutionary perspective

O /

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

(Anthozoa, Octocorallia) loss in the Marine Protected Area of Tavolara (Sardinia, Italy) due to a mass m ortality event

Param uricea clavata

Carla H u e t e - S t a u f f e r 1, Maria V ie lm in i2, M arco P a lm a 1, A u g u s t o N a v o n e 3, Pier P a n z a lis3, Luigi V e z z u lli4, Cristina Misic1 & Carlo C er ra n o 1 1 D epartm ent for the Study of the Territory and its Resources (Dip.Te.Ris), University of Genoa, Genoa, Italy 2 D epartm ent of Biology, University of Pisa, Pisa, Italy 3 MPA and SPAMI Tavolara Punta Coda Cavallo, Olbla, Italy 4 D epartm ent of Biology (Di.Bio), University of Genoa, Genoa, Italy

K eywords

Abstract

Conservation; global warming; Octocorals;

Vibrio. C orrespondence Carla Huete-Stauffer, D epartm ent for the study of the Territory and its Resources, Corso Europa 26, 16132, Genoa, Italy. E-mail: [email protected] Accepted: 15 February 2011 doi: 10.1111/j. 1439-0485.2011,00429.x

R ecent studies highlight an increase in th e frequency an d in ten sity o f m arine m ass m ortalities o f several species over th e past 30 -4 0 years, m ainly in tropical an d tem p erate areas. In th e M ed iterran ean Sea these episodes p articu larly affect benthic suspension feeders, such as sponges an d cnidarians. The m a in objective o f this w o rk was to d o c u m e n t th e loss o f one o f th e m ain M ed iterran ean sea­ scapes, Paramuricea clavata forests at th e M arine P ro tected A rea o f Tavolara P u n ta C oda Cavallo, Sardinia (Italy), d u rin g th e su m m e r o f 2008. D ata reg ard­ ing colony height, density, level o f dam age, a n d m icrobiological c o m m u n ity w ere collected at tw o sites. Such param eters help us u n d e rsta n d how m ass m o rtality m echanism s act o n this ecosystem engineer. W e identified a change in size class d istrib u tio n follow ing a m ass m o rtality th a t leaves m ain ly sm all colonies w ith a decrease in h ab itat com plexity. Several tests o n w ater chem istry d em o n strate th a t th e m o rtality event was n o t caused b y local co n tam in ation. M oreover, m icrobiological tests o n p o ten tial pathogenic agents suggest th at b acteria belonging to th e genus Vibrio are p resen t as an o p p o rtu n istic a n d n o t an etiological cause o f P. clavata m o rtality events. Possible resto ratio n ap proaches are discussed.

Introduction M arine co m m unities ap p ear to be facing one o f th e w orst periods in th eir recent history. T he d irect negative effects o f several h u m a n activities (e.g. oil spills, coastal h ab itat m odification, overfishing) are n o w am plified b y clim ate change, w hich is co m p ro m isin g b o th th e resistance an d the resilience o f m an y m arin e organism s. D u rin g th e last decades, the N orth w estern M ed iterran ean Sea has been h it by a series o f m ass m o rtality events, w hich im p act b enthic suspensivore organism s, such as sponges, cn id ari­ ans, bivalves, bryozoans an d tunicates, an d associated assem blages (C erran o & Bavestrello 2009). These m o rta l­

Marine Ecology 32 (Suppl. 1) (2011 ) 1 07 -11 6 © 2011 Blackwell Verlag GmbH

ity events coincide w ith th erm al anom alies generally caused b y u n u su al w ater w arm in g d u rin g pro lo n g ed p eri­ ods o f w ater co lu m n stability (CIESM , 2008). Affected species often show m odifications in their physiology (Previati et a í 2010), d istrib u tio n s, a n d som e­ tim es pheno lo g y (Bavestrello et a í 2006), w hich can have u n p red ictab le consequences o n species’ in teractions (H ughes 2000). O ften th e affected species are ecosystem engineers a n d th eir rarefaction a n d /o r disappearance has p ro fo u n d consequences o n th e h ab itat architecture, such as reducing spatial com plexity a n d decreasing biodiversity richness (M afias et al. 2010). In th e M ed iterran ean Sea, several causes o f these m o rtality events have been

107

P. clavata loss in t h e MPA o f T avolara

identified, typically associated w ith en v iro n m en tal factors (C errano et a í 2000, 2005; Pérez et al. 2000; Calvisi et al. 2003; Linares e t al. 2005, 2008b; Cigliano & G am bi 2007; Previati et al. 2010) b u t a n u m b er o f p athogens have also been im plicated (M artin et al. 2002; G ay et al. 2004; Bally & G arrabou 2007; Vezzulli e t a í, 2010). A m ong th e affected areas in th e M editerranean, p erh ap s th e Ligurian Sea can be considered th e m o st severely affected (G arra­ b o u et al. 2009). H ow ever, in th e late su m m er o f 2008, one o f these p articu lar therm al anom alies was registered in th e M arine P ro tected A rea o f Tavolara P u n ta C oda Cavallo (C entral W estern T y rrh en ian Sea) a n d h ad a d ra ­ m atic effect o n sea-fan (O ctocorallia: G orgonacea) p o p u ­ lations, particu larly o n tw o rocky shoals adjacent to Tavolara Island, w here presence o f large n u m b ers o f th e gorgonian Paramuricea clavata characterizes one o f th e m o st fam ous dive spots in th e area. Paramuricea clavata is k n o w n to be sensitive to high tem peratures (C igliano & G am bi 2007; C om a et al. 2009; Fava et al. 2010; Previati et a l 2010) a n d can show an im m ediate response to these events. Crucially, this spe­ cies is considered an ecosystem engineer a n d facilitator species (B runo & Bertness 2001; Scinto et al. 2009) w ith in coralligenous assemblages. T he aim s o f this w ork were: (i) to describe th e m ass m o rtality event th a t affected p o p u latio n s o f P. clavata an d (ii) to determ ine w hether a range o f enviro n m en tal p aram eters are co rre­ lated w ith P. clavata m ass m ortality. Possible pathw ays for resto ratio n a n d m an ag em en t o f this species are also discussed.

Material and M e th o d s Study area Tavolara Island (40°54, 19' N; 9°42, 28' E) is form ed from lim estone-d o lo m ite rock. T ogether w ith th e granitic M olara, M o laro tto an d o th er m in o r islets, Tavolara form s a sm all archipelago w ith an epibenthic co m m u n ity th a t has been well described b y N avone & T rain ito (2008) an d N avone et a í (1992). In th e stu d y area, th e effects o f th e m ass m o rtality event o n th e pre-coralligenous a n d coral­ ligenous assem blages o f tw o n earb y sites (term e d P apa 1 and P apa 2) w ere quantified. P apa 1 ranges in d ep th from 15 to 39 m , an d P apa 2 fro m 24 to 43 m . T he cu rren t direction flows in a N E -S W direction, fro m P apa 2 tow ards P apa 1. A t b o th sites th ere is a dense forest of Paramuricea clavata a n d also Eunicella cavolinii (Calvisi et al. 2003; Bianchi et al. 2007). SCUBA diving surveys w ere u n d ertak en d u rin g O cto b er 2008, D ecem ber 2008 and June 2009, w hich co rresp o n d ed to th e p erio d w hen m o rtality was first n o te d for P. clavata an d 3 an d 9 m o n th s subsequently.

108

H uete-Stauffer, Vielmini, Palma, N avone, Panzalis, Vezzulli, Misic & C errano

Population structure and mortality dynamics: field surveys To stu d y p o p u la tio n dynam ics, a m in im u m o f six q u a d ­ rats (50 X 50 cm ) w ere ran d o m ly sam pled fro m 40 to 20 m d ep th every 5 m fro m th e b o tto m to th e to p o f each shoal, follow ing stan d ard m eth o d o lo g y set o u t by sim ilar studies (C erran o et al. 2005; C om a et al. 2006; Linares et al. 2008a) a n d in relatio n to th e g eo m o rp h o l­ ogy o f th e sites (P apa 1 fro m - 3 5 to - 2 0 m ; P apa 2 from - 4 0 to - 2 5 m ). W ith in each q u a d ra t th e n u m b e r o f colo­ nies (converted to colony density), colony heights, colony health (defined as th e percentage o f colony w ith dam aged coenenchym e: 0% was considered healthy, <25, <50, <75, <99 a n d 100% ), an d th e n u m b er o f fishing lines a n d /o r nets w rapped aro u n d th e colonies w ere recorded. F u rth er­ m ore, for each colony th e epibiosis level was recorded (according to m eth o d s pro v id ed b y Bavestrello et al. 1997) an d th e epibiontic organism s w ere identified. O n th e basis o f organism s th a t h ad settled o n th e scleraxis we defined different tem p o ral phases: (i) d en u d ed (w hen the scleraxis is visible, w ith tissue o n scleraxis), (ii) new (covered w ith filam entous green a n d /o r red algae, a n d /o r h y drozoans), (iii) m e d iu m (possessing a th ick coat o f algae, a n d /o r sponges) an d (iv) old (m ain ly colonized by calcareous organism s such as bryozoans). T o test the dif­ ferences in p o p u la tio n com p o sitio n , w ith in sites and a m o n g tim es, ANOVA tests w ere p erfo rm ed after verify­ ing th a t data w ere no rm ally d istrib u ted a n d th ere was equality o f variances. W e assum ed th a t th e p re -m o rtality p o p u la tio n stru c ­ tu re was very close to th a t observed in O cto b er (i.e. d u r­ in g /ju s t after m ortality) for th ree reasons: (i) m ost colonies h ad only ju st died, w ith naked scleraxis a n d w ith necrotic coenenchym e p o rtio n s still p resen t o n th e colo­ nies, (ii) n o fragm ents or w hole colonies w ere fo u n d (im plying th a t colonies h ad n o t detached fro m the base) a n d (iii) colonies w ere always m easured - in clu ding the d en u d ed a n d ep ib io n ted parts o f th e colonies. T he p o st­ m o rtality stru ctu re o f colonies was considered to be ty p i­ cal o f th a t observed fro m D ecem ber 2008.

Environmental features - laboratory analyses To evaluate w h eth er chem ical features o f seaw ater a n d /o r bacterial infections could be involved in th e m ortality, b o th seaw ater sam ples a n d p o rtio n s o f colonies w ere col­ lected.

Seawater temperature and water chemistry T em p eratu re was m easured d u rin g survey dives using tw o types o f u n d erw ater com puters: (i) U W ATEC (± 0.5 °C), w ith a system th a t records an d m em orizes autom atically

M arine Ecology 32 (Suppl. 1) (2011 ) 1 07 -11 6 © 2011 Blackwell Verlag GmbH

P. clavata loss in th e MPA o f T avolara

H uete-Stauffer, Vielmini, Palma, N avone, Panzalis, Vezzulli, Mlslc & C errano

w ater tem p eratu re d u rin g th e dives every 4 s, creating a profile, an d (ii) un d erw ater co m p u ters w ith a p u n ctu al tem p eratu re m easu rem en t (variatio n o f + 1 °C) th a t divers recorded m anually every 5 m d u rin g th e dive ascent. W ate r tem p eratu re d ata w ere tak en in b o th sites. Average values o f w ater tem p eratu re w ere accom plished w ith b o th m anually recoded an d au to m atic UW ATEC data, separated b y d ep th ranges: SST (sea surface te m p e r­ ature) or 0, 5, 10, 15, 20, 25, 30, 35 an d 40 m depth. To determ ine dissolved oxygen co n cen tratio n s (D O C ) d u rin g the m o rtality event, separate seaw ater sam ples w ere carefully collected, avoiding air bubbles, an d im m e­ diately fixed follow ing C arp en te r’s (1965) p rotocol. In o r­ ganic n u trie n t concen tratio n s w ere d eterm in ed according to H ansen & G rasshoff (1983). M arin e w ater was p re-fil­ tered w ith cellulose acetate filters (0.45 jLim p o re d iam e­ ter) and m ain tain ed at - 2 0 °C u n til lab o rato ry analysis. N itrates, nitrites, am m o n ia an d pho sp h ates w ere analyzed w ith SYSTEA (n u trie n t analyzer) an d silica concentrations w ere quantified using a Jasco V-500 sp ectro p h o to m eter.

bile salt sucrose (TCBS) agar to isolate th e m ain m o rp h o types o f bacteria belonging to th e genus Vibrio. O ther pieces o f tissue w ere frozen (at - 2 0 °C) u n til to tal geno­ m ic D N A could be extracted. A fter D N A extraction, bac­ terial sam ples w ere identified o n th e basis o f th eir 16S rR N A gene sequences (see Vezzulli et a í , 2010 for full details o f m eth o d s). To identify isolates, PC R am plifica­ tio n o f a 798-bp region was p erfo rm ed using th e u n iv er­ sal p rim ers BRI (5'-A G A G TTTG A TC C TG G C T-3') an d BR 2 (5'-G G A C TA C CA G G G TA TCTA A T-3'), am plifying p ositio n s 8-8 0 6 o f th e Escherichia coli n u m b e rin g o f the 16S rRN A gene th a t include hyper-variable regions. 16S rRN A gene sequence sim ilarity was d eterm in ed w ith SEQM A T C H (version 2) analysis o f R ibosom al D atabase P ro ­ ject (R D P-II, Release 9) o f th e C enter for M icrobial Ecology, M ichigan State U niversity (h ttp ://rd p .c m e . m su .ed u /seq m atch ). T o assess th e pathogenic p o ten tial of isolated strains tow ards P. clavata colonies, infection experim ents w ere p erfo rm ed in aquaria at different te m ­ p eratu res a n d enviro n m en tal co n d itio n s sim u latin g those observed in th e e n v iro n m en t d u rin g th e occurrence of m o rtality events (see Vezzulli et a í, 2010 for full details o f experim ents).

Microbiological analysis T op colony pieces (n = 45 in total) o f a b o u t 5 cm of healthy an d dam aged P. clavata colonies w ere taken (20 healthy an d 25 dam aged, all sam ples fro m different colo­ nies). Samples w ere m ain tain ed in cold seaw ater (4 °C) u n til laboratory m an ip u latio n , th e n w ashed in sterile sea­ w ater to rem ove o th er b acteria o r fauna th a t w ere n o t strictly related to P. clavata dam age a n d in cu b ated in an enriched A PW (alkaline p e p to n e w ater) cu ltu re b ro th . A fter 10 h, sam ples w ere plated o n to thiosulfate citrate

October 2008

II. n

h

n

Results Population structure and mortality dynamics: field surveys In total, 476 colonies w ere observed in 158 quadrats. R ecords o f colony densities, h eight a n d size class d istrib u ­ tio n show ho w th e tw o sites (shoals) have a different p o p u la tio n stru ctu re, a n d this appears to have elicited a different response to th e m o rtality event.

June 2009

December 2008

I »9

is

»

j*

n

ill n

m

n

Papa 1

ao

Papa 2

» M

H

¡

»

»

I »

Depth (m) Fig. 1. Density averages for Papa 1 and Papa 2 at different depths In time with ± SE.

Marine Ecology 32 (Suppl. 1) (2011 ) 1 07 -11 6 © 2011 Blackwell Verlag GmbH

109

P. clavata loss in t h e MPA o f T avolara

H uete-Stauffer, Vielmini, Palma, N avone, Panzalis, Vezzulli, Misic & C errano

Papa 1. In this site th e m ean density (+ SE) was 9.12 + 2.18 colonies p er m 2. Significant differences in densities w ere detected a m o n g dep th s (P < 0.05, Fig. 1), p red o m in an tly d u e to th e low n u m b e r o f colonies in the u p p er lim its o f this species’ d istrib u tio n . T he m ean height o f Paramuricea clavata (+ SE) was 21.03 + 4.24 cm d u r­ ing the m o rtality event an d 27.72 + 3.12 cm d u rin g th e last survey, w ith n o significant differences detected b o th in m ean height o f th e colonies o n th e investigated te m p o ­ ral scale (P > 0.05, see also Fig. 2) a n d betw een th e differ­ ent depths (P > 0.05). D am aged colonies o f P. clavata w ere fo u n d at all depths, b u t a t 35 m d ep th th e p ercen t­ age o f dam age was m ainly co n stan t a n d generally low er th a n a t the o th er (m ostly shallow er) depths (Fig. 3). Between 30 a n d 20 m d epth, m o rtality occurred a t a high percentage o f colonies, an d was especially prevalent in th e larger sized classes. A t 25 m d epth, all size classes o f colo­ nies w ere 100% dam aged, b o th in O cto b er 2008 a n d in D ecem ber 2008. In th e last survey, in June 2009, m o re

October 2008

healthy colonies (co m p ared w ith previous surveys) w ere fo u n d an d th e average size o f th e p o p u la tio n h ad shifted tow ards sm aller sized classes (i.e. 0 -3 0 cm ) (see Figs 1, 2 a n d 4). Papa 2. In this site m ean density (+ SE) o f P. clavata was 17.33 + 2.13 colonies per m 2. N o differences in d en ­ sity w ere detected b o th am o n g dep th s an d th e investi­ gated periods (P > 0.05) (Fig. 1). M ean colony height (+ SE) d u rin g th e m o rtality event was 29.72 + 6 . 8 6 cm an d 28.54 + 2.01 cm d u rin g th e last survey. T he sm allest colonies w ere fo u n d at 25 m d ep th (Fig. 2), w hile colony h eight elsewhere was significantly greater (P < 0.001), alth o u g h th ere was n o obvious correlation betw een col­ ony h eight an d th e d ep th o f th e substrate they occupied. D am aged colonies w ere fo u n d at all dep th s d u ring the entire p erio d o f study. A t 40 m d ep th th e percentage o f dam aged colonies was generally low an d varied betw een a b o u t 20 an d 40% . By con trast, a t 35 a n d 25 m depths th e frequency o f m o rtality was h igher betw een O ctober

December 2008

June 2009

40 - j ui 14 -

M ii 35

30

25

40■

I i i

20

P apa 1

lii

CJ,

'53 43

Papa 2 20

IO -

U

L

h

l

l

i

D epth (m) Fig. 2. Height averages for Papa 1 and Papa 2 a t different depths In time with ± SE.

'120

r 120

c 100

: loo

'Sm I

60

ô

40

S.

0

October 2008

December 2008

June 2009

October 2008

December 2008

Date 1 85 m depth

■ 3 0 m depth

■ 25 m depth

June 2009

Date ■ 20 m depth

140 m depth ■ 3 5 m d e p t h

■ 30 m depth ■ 2 5 m depth

Fig. 3. Percentage of dam aged colonies In time a t all depths for the tw o study areas: Papa 1 (left) and Papa 2 (right). At deeper depths there are fewer dam aged colonies, w hereas a t the superficial parts of the shoals, dam age Is greater and has affected more colonies. There Is a general reduction In the last studied period, probably due to natural recovery and the loss of the larger and more dam aged colonies.

110

M arine Ecology 32 (Suppl. 1) (2011 ) 1 07 -11 6 © 2011 Blackwell Verlag GmbH

Huete-Stauffer, Vielmini, Palma, Navone, Panzalis, Vezzulli, Misic & Cerrano

October 2008

P. clavata loss in t h e MPA o f T avolara

December 2008

June 2009

35 m

U iU •P 'P Q

■ ^

1 j l . i.P -i> &

S i iP

/ / W

p p p P

❖

iÿ

*

1 : 1 11 1 1

’

.

■ I l i i

^

N = 17

N t = 21

«

I

jS> $

.

j » <&

&$ * ? ^ ^ ^ ^ ^

40

I Iill

A V^ A í A ® - ❖* ^

30 m

« i»

V S* i-'

N = 13

o c

25 m

I «■V V V 3¡r< r1

ilu ,

«■y

^ V V V «> V

fi

,& jS>


N o P. clavata found in this depth range

20 m

...I, A A V A A Size class (cm) Fig. 4 . Size class percentage frequency. Frequencies in damaged percentage per size class (black) and healthy percentage per size class (light grey). Papa 1. Frequencies are the percentage o f dam aged/healthy colonies found in a determinate size class.

an d D ecem ber, especially for th e 21 -3 0 cm size class in d i­ viduals. In June, th e size class d istrib u tio n shifted tow ards the sm aller size classes {i.e. th ere w ere m o re colonies in the range 0 -3 0 cm ) (Figs 1, 2 a n d 5). Overall, th e m ean percentage o f dam age o f colonies indicates th a t dam age is generally greater in th e shallow er p arts o f th e shoals, in som e cases up to 1 0 0 % th ro u g h o u t th e w hole size class of individuals (Fig. 3). A t b o th sites, epibiosis o n th e d en u d ed p arts o f th e col­ onies follow ed a p a tte rn o f fo u r tem porally successive steps: (i) d en u d ed branches, here recorded in O ctober, (ii) new ly settled organism s such as filam entous algae an d hydroids, (iii) a m e d iu m stage o f epizootic colonization w ith algae and sm all sponges, w hich was n o ted in D ecem ­ ber, an d finally (iv) a n old stage w ith co lonization by algae, sponges, bryozoans an d o th er calcareous organism s,

O ctober) along th e w ater co lu m n a n d th e absence (in the investigated d ep th range o f betw een 20 an d 43 m ) of th erm o clin e in O ctober, co nfirm ing a pro lo n g ed w ater stability over it (Fig. 6 ). T em p eratu re is d ep th -d ep en d en t; a t all dep th s considered, w ater tem p e ra tu re was at least a degree h igher d u rin g th e m o n th s o f Septem ber an d O cto­ b e r 2008 th a n in th e previous year. D ata for D ecem ber 2007 w ere n o t available. A lthough th e dissolved oxygen co n cen tratio n s were always high in b o th th e sam pling sites (close to healthy a n d dam aged colonies), w ater results have highlighted h igher levels o f n itrite, n itrate an d am m o n ia d u rin g the m o rtality event, especially aro u n d th e dam aged colonies w here tissue d eg rad atio n was taking p a rt (Table 2). In con trast, p h o sp h ate co n cen tratio n s w ere h igher n ex t to th e healthy colonies. These co n cen tratio n s led to P-lim ita-

w hich was (Table 1).

tio n con d itio n s (higher N /P ratio w here N is th e su m of n itrite, n itrate a n d a m m o n ia concentrations) next to the

fo u n d

d u rin g

th e

last

surveys

in

June

Environm ental features: laboratory analyses Seawater tem p eratu re m easurem ents confirm ed th e high tem p eratu re (22 + 1 °C in Septem ber an d 21 + 0 .5 °C in

Marine Ecology 32 (Suppl. 1) (2011 ) 1 07 -11 6 © 2011 Blackwell Verlag GmbH

co m p ro m ised colonies, especially d u rin g O ctober. M icrobiological tests revealed th a t Vibrio b acteria were consistently m o re a b u n d a n t in diseased organism s w ith u p to a tw ofold h igher co n cen tratio n com p ared w ith those fo u n d o n th e healthy corals (Fig. 7). T he 16S rRNA

111

P. clavata loss in th e MPA of Tavolara

Huete-Stauffer, Vielmini, Palma, Navone, Panzalis, Vezzulli, Misic & Cerrano

October 2008

December 2008

June 2009

40 m

A A A A A A * •> A A A

V // 1 30

iJ jL il Cu

: ,l*$> 1,■$1> . 1 1 35 m

304

.iilli

: 1 1 1. . I

4> « A a A * «f y -?■ •i- í> ’

»

30 m

$

fi

J j

,A

A

A

* ■> A V A

' .lili A ,A A

» 4> ,❖

* O’ -i» A A

h illii .. ,A ,A p

A ■fi’

A A A A

25 m

1 1 1 A ,A

* A A y

A & &

$ "P ^ ^

< V ,/*

./

^

1

Size class (cm) Fig. 5. Size class percentage frequency. Frequencies of dam aged percentage per size class (black) and healthy percentage per size class (light grey). Papa 2. Frequencies are percentage of dam aged/healthy colonies found in a determ inate size class.

T able 1. Number of colonies affected and the type of epibiosis recorded on the colonies of the studied sites during and after the mass mortality event. epibiosis type

October 2008

December 2008

June 2009

Papa 1 denuded new

60 25

26 52

0 40

medium

10

15

55

old Papa 2 denuded new

5

6

5

70 11

43 27

36

medium

11

22

53

8

9

10

old

1

gene sequencing o f 61 Vibrio isolates associated to dis­ eased and healthy Paramuricea clavata colonies show ed a close hom ology o f th e m ajo rity o f th e strains w ith Vib­ rio harveyi (n = 24), Vibrio splendidus (n = 22) an d Vib­ rio coralliilyticus (n = 15), th e latter only being identified in diseased organism s.

112

Discussion T he m ain aim s o f M PAs, as identified in th e IU C N G uidelines for Establishing M arin e P ro tected Areas (Kelleh er & K enchington 1992), are (i) to m a in tain essential ecological an d life-su p p o rt systems, (ii) to ensure the sus­ tainable u tilizatio n o f species an d ecosystem s an d (iii) to preserve b iotic diversity. M o n ito rin g , defined as c o n tin u ­ ous o bservation o f con d itio n s over tim e, is a crucial tool for th e conservation o f m arin e biological diversity and provides m anagers w ith im p o rta n t d ata fro m w hich they can m ake in fo rm ed decisions a b o u t p attern s a n d p ro ­ cesses th a t affect biodiversity, an d th u s th e fu n ctioning (o r n o t) o f an M PA. H ere, we presen t o u r m o n ito rin g d ata to describe som e o f th e factors associated w ith a m ass m o rta lity o f th e go rg o n ian Paramuricea clavata at th e M PA at Tavolara Island, Italy. T he m o rtality event described h ere affected a p o p u la ­ tio n o f octocoral th a t is well k n o w n a n d utilized by the diving to u rism in d u stry in a ‘Specially P ro tected A rea o f M ed iterran ean Im p o rta n c e ’ (SPAM I). O u r results rep re­ sent an im p o rta n t baseline for fu tu re m o n ito rin g

M arine Ecology 32 (Suppl. 1) (2011 ) 1 07 -11 6 © 2011 Blackwell Verlag GmbH

P. clavata loss in th e MPA of Tavolara

Huete-Stauffer, Vielmini, Palma, Navone, Panzalis, Vezzulli, Misic & Cerrano

T em pt 15 20 5 10

Temp*C

25

30

15

— 5*2008 — Oct20Q8

lo­

— Dtc2008

15

is

£ 30

g 20

I» 30

30-

M 40

«

45 J

Fig. 6. Tem perature profile from 2008 of the m onths of Interest In the Investigated area, recorded by SCUBA operators and SST (sea surface tem perature) from http://w w w .poseldon.ogs.lt. Data from December 2007 w ere not available. T able 2. Environmental features recorded for the sea-w ater collected next the decaying (damaged) and the control (healthy) colonies. Dissolved oxygen

Silicate

ml r 1

SD

/(M

Nltrite+nltrate

Ammonia

Phosphate

SD

/(M

SD

/(M

SD

/(M

SD

N/P ratio

October

Healthy Damaged

7.49 7.23

0.13 0.14

1.15 1.54

0.05 0.21

2.40 3.11

0.18 0.41

1.63 2.10

0.08 0.42

0.18 0.15

0.01 0.01

22.9 35.4

December

Healthy Damaged

nd 7.77

nd nd

2.42 2.12

0.28 0.36

0.92 0.96

0.10 0.06

0.96 1.23

0.19 0.37

0.12 0.10

0.01 0.02

15.2 22.0

N, nitrogen; nd, not detected; P, phosphate; SD, standard deviation.

Vibrio spp.

1ô*3 T ë <3 m ie + 2 ID u. Ü 1e*1

H ealthy

D ise a se d

Fig. 7. Concentration of Vibrio found In the colonies (healthy and dam aged) of Papa 1 and Papa 2. CFU = unity of bacteria colony for­ mation with ± SE. This graph considers all the Vibrio species found on the Paramuricea colonies: of these V. harveyi and V. splendidus were the main com ponents on the healthy colonies and V. coralHlyticus was also present on the dam aged or diseased colonies.

program s o n this long-lived, sessile species w ith slow p o p ­ u latio n dynam ics (M istri & Ceccherelli 1994). Even th o u g h the m ean colony density o f th e stu d ied areas was low er th a n in o th er M ed iterran ean areas (C errano & Bavestrello 2008; C u pido et al. 2009; G arrab o u et al. 2009), the seascape before th e m o rtality episode was d o m in ated by large colonies.

Marine Ecology 32 (Suppl. 1) (2011 ) 1 07 -11 6 © 2011 Blackwell Verlag GmbH

B roadly speaking, P apa 1 is less dense an d has sm aller colonies th a n P ap a 2. M ean colony h eight d id n o t differ over a relatively sh o rt perio d o f 1-3 m o n th s after the m o rtality episode, b u t th ere was a clear shift tow ards sm all size classes b y 9 m o n th s after th e m o rtality event. T his tre n d was rep o rted also in o th er m o n ito rin g studies o n go rg o n ian m o rtality (C errano et a í 2005; C upido et a í 2008, 2009; Linares et al. 2008a,b,c). This p h e n o m e­ n o n is m ainly due to th e loss o f th e colonies fro m th e lar­ ger size classes a n d also th e frag m en tatio n a n d /o r dam age to branches. M oreover, th e presence o f recruits caused a shift tow ards sm aller colonies, leading to a general loss of h a b ita t com plexity. F u rth erm o re, th ere was evidence th at m o st o f th e colony branches w ith epibionts th a t were c o u n ted in D ecem ber 2008 h a d either fallen off o r were b ro k e n in June 2009. F rom 35 m (for P ap a 2) an d 30 m d ep th (for P apa 1), up to th e surface o f th e shoals, th e larger colonies w ere m ore affected (i.e. h ad a h igher percentage o f dam age) b y the m o rtality event: deeper colonies w ere less affected in b o th sites. C olonies living at greater depths could hence consti­ tu te a reservoir for th e p ro d u c tio n o f p lanulae for fu tu re p o p u la tio n recoveries (b o tto m -u p a n d lateral supply). In coralligenous assemblages, p erh ap s th e m o st im p o r­ ta n t hab itats in th e M ed iterran ean Sea (Ballesteros 2006),

113

P. clavata loss in t h e MPA o f T avolara

gorgonians an d particularly P. clavata, are considered key species, being im p o rta n t engineering a n d /o r fo u n d atio n species (sensu D ayton, 1972; M istri & Ceccherelli 1994; C upido et a í 2009). M ass m o rta lity events have w ide consequences for g orgonian p o p u latio n s (Linares & D oak 2 0 1 0 ) an d for th e c o m m u n ity th a t depends o n th em , as the loss o f these species alters sed im en tatio n , tu rb id ity and w ater m ovem en t, w hich negatively affect th e com plex stru ctu re o f th e h a rd -b o tto m benthic co m m u n ities an d the local biodiversity richness (Scinto et a í 2009). In b o th Septem ber and O ctober 2008, th e p o sitio n o f th e th erm o cline could n o t b e detected dow n to 40 m d ep th d u rin g the m o rtality event an d tem p e ra tu re was ~ 2 °C higher th a n d u rin g Septem ber 2007. T he verified th erm al a n o m ­ alies an d the co n stan t w arm in g o f th e M ed iterran ean m ay have im p o rta n t consequences for th e n atu ral biocenosis (B ianchi 2007; C om a et a í 2009) an d m ay be th e cause o f the m ass m o rtality events o ccurring in th e last few years (Pérez et al. 2000; Pérez 2008; C om a et al. 2009). In O ctober, seaw ater analyses in dicated altered values o f am m o n ia, n itrite an d n itra te close to dam aged colo­ nies, w hich w ere higher th a n usual a n d likely due to tis­ sue degradation. These anom alies w ere n o t recorded in D ecem ber, after th e m o rta lity episode h ad finished. C hanges in p h o sp h ate values could have been related to the su m m er increase o f u rb a n sewage outflow d u e to high to u rist density. A n alteratio n o f th e n u trie n t co n cen tra­ tions was highlighted b y th e change o f th e N /P ratio val­ ues (Table 2), w hich m ay p o ten tially favor u n u su al phytoplanktonic a n d /o r bacterial species. The P -lim ited situ atio n could have added an energetic co n strain t o n th e w eak P. clavata p o p u latio n . These general con d itio n s (high seaw ater tem p eratu re, altered N /P ratio) could have facilitated the increase o f b acteria o n dam aged colonies. W e uncovered th ree m ain g roups o f Vibrio, o f w hich Vib­ rio coralliilyticus has been im plicated as an im p o rta n t cause o f m o rtality for M ed iterran ean P. clavata (M artin et al. 2002; Bally & G arrab o u 2007) an d C aribbean corals (C ervino et al. 2004). Vibrio b acteria are n o rm ally fo u n d in seaw ater an d are th erm o d ep en d en t: at high tem p era­ tures (22-24 °C) Vibrio grows rapidly. Vibrio coralliilyti­ cus show ed th e highest virulence to w ard P. clavata colonies a n d satisfied K och p ostulates for pathogenicity. This b acteriu m appears to act as a n o p p o rtu n istic agent, infecting weak, th erm ally stressed colonies a n d c o m p ro ­ m ising colony recovery (Vezzulli et a í, 2010). U ntil now th ere have been n o standardized actions to m itigate the im p act o f m ass m ortalities o f P. clavata. In terv en tio n strategies rem ain to be validated a n d it is im p o rta n t, especially w here diving activity is frequent, to avoid p o p u latio n frag m en tatio n th a t w ould lead to a p ro ­ gressive red u ctio n in p o p u la tio n density (Linares & D oak 2010) and a general loss o f b iodiversity (C erran o &

114

H uete-Stauffer, Vielmini, Palma, N avone, Panzalis, Vezzulli, Misic & C errano

Bavestrello 2009). For this reason, m o n ito rin g is th e only effective a p p ro ach to p lan ad eq u ate p ro g ram s o f interven­ tion. H ypotheses to lim it dam ages a n d /o r im p ro v e recov­ ery dam aged colonies include: (i) developm ent o f an ‘early w arning system ’ to m easure w ater stratification and p red ict m ass m ortalities an d (ii) utilizatio n o f p ru n in g a n d tra n sp la n t tech n iq u e p rotocols. For exam ple, co n ­ trolled m in ia tu riz a tio n o f larger colonies could lead to m o re resistant an d resilient specim ens th a t will also fu r­ n ish a n u m b e r o f fragm ents for tran sp lan ts to highly dam aged areas to be used for resto ratio n . Certainly, m an ip u la tio n a n d tra n sp la n t experim ents need to be designed a n d tested before this strategy can be used ro u ­ tinely (see for exam ple th e p ilo t stu d y o f Linares et al. 2008c). Sites w ith in M PAs have greater possibilities for recovery an d ad eq u ate m anagem ent, as th e anthro pogenic im pacts are red u ced a n d controlled; b u t as show n in this a n d o th er studies, M PA p ro te c tio n certainly does n o t p re ­ vent m ass m o rtalities related to enviro n m en tal causes.

Conclusions S h o rt-term effects o f m o rta lity events include h a b itat sim ­ plification a n d red u cin g th e econom ic value due to a decrease o f to u ristic ap p reciatio n (T rain ito 2007; N avone & T rain ito 2008). E valuation o f lo n g -term consequences needs ad eq u ate m o n ito rin g program s. O n th e basis o f p re ­ vious m o rtality episodes described in different areas (Liguro -P ro v en çal Basin an d T y rrh en ian Sea), long-term effects m ay vary in relatio n to th e presence o f healthy ‘pock et reservoir’ p o p u latio n s living below th e w ater sta­ bility area delim iting th e th erm al anom alies. T heir pres­ ence m ay rep resen t an im p o rta n t larval supply to facilitate th e recovery o f shallow p o p u latio n s. H igh w ater tem p era­ tu re an d pro lo n g ed su m m e r cond itio n s are am ong the m ost relevant causes o f these m ass m o rtality events (including th e one rep o rted here), reducing n atu ral defences o f colonies. In these co m p ro m ised conditions, colonies are m o re vulnerable to infections an d energetic constraints.

A c k n o w le d g e m e n t s A u thors are in d eb ted to th e T avolara M PA staff for logis­ tic su p p o rt. This w o rk was p artially financed by 2008 G enoa U niversity fu n d s to C.C.

References Ballesteros E. (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanography and Marine Biology: An Annual Review, 44, 123-195. Bally M., Garrabou J. (2007) Thermodependent bacterial pathogens and mass mortalities in temperate benthic

M arine Ecology 32 (Suppl. 1) (2011 ) 1 07 -11 6 © 2011 Blackwell Verlag GmbH

P. clavata loss in th e MPA o f T avolara

H uete-Stauffer, Vielmini, Palma, N avone, Panzalis, Vezzulli, Mlslc & C errano

communities: a new case of emerging disease linked to cli­ mate change. Global Change Biology, 13, 2078-2088. Bavestrello G., Cerrano C., Zanzi D., Cattaneo-Vietti R. (1997) Damage by fishing activities to the gorgonian coral Paramu­ ricea clavata in the Ligurian Sea. Aquatic Conservation: Marine and Freshwater Ecosystems, 7, 253-262. Bavestrello C., Puce S., Cerrano C., Zocchi E., Boero N. (2006) The problem of seasonality o f benthic hydroids in temperate waters. Chemistry and Ecology, 22, 197-205. Bianchi C.N. (2007) Biodiversity issues for the forthcoming tropical Mediterranean Sea. Eiydrobiologia, 580, 7-21. Bianchi C.N., Cattaneo-Vietti R., M orri C., Navone A., Panzal­ is P., O rrù P. (2007) II coralligeno dell’Area Marina Protetta di Tavolara Punta Coda Cavallo (Sardegna Nord.Orientale). Biología Marina del Mediterráneo, 14, 148-149. Bruno J.F., Bertness M.D. (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness M.D., Gaines S.D., Hay M.E. (Eds), Marine Community Ecology. Sinauer, Sunderland: 8 , 201-218. Calvisi G., Trainito E., Pais M., Franci S., Schiaparelli S. (2003) Prima segnalazione di un episodio di mortalità di gorgonacei lungo la costa dell’Isola di Tavolara (Sardegna Settentrionale). Biología Marina Mediterranea, 10, 506-508. Carpenter J.H. (1965) The Chesapeake Bay Institute technique for the Winkler dissolved oxygen method. Limnology and Oceanography, 10, 141-143. Cerrano C., Bavestrello G. (2008) M edium-term effects of die-off of rocky benthos in the Ligurian Sea. W hat can we learn from gorgonians? Chemistry and Ecology, 24, 73-82. Cerrano C., Bavestrello G. (2009) Massive mortalities and extinctions. In: Wahl M. (Ed.), Marine Hard Bottom Commu­ nities. Patterns, Dynamics, Diversity, and Change. SpringerVerlag, Berlin: Ch. 21. Ecological Studies. 206, 295-307. Cerrano C., Bavestrello G., Bianchi C.N., Cattaneo-Vietti R., Bava S., Morganii C., M orri C., Picco P., Sara G., Schiapar­ elli S., Siccardi A., Sponga F. (2000) A catastrophic massmortality episode of gorgonians and other organisms in the Ligurian Sea (NW Mediterranean), summer 1999. Ecology Letters, 3, 284-293. Cerrano C., Arillo A., Azzini F., Calcinai B., Castellano L., Muti C., Valisano L., Zega G., Bavestrello G. (2005) Gorgo­ nian population recovery after a mass mortality event. Aquatic Conservation: Marine and Freshwater Ecosystems, 15, 147-157. Cervino J.M., Hayes R.L., Poison S.W., Poison S.C., Goreau T.J., Martinez R.J., Smith G.W. (2004) Relationship of Vibrio species infection and elevated temperatures to yellow Blotch/band disease in Caribbean corals. Applied and Environmental Microbiology, 70, 6855-6864. CIESM. (2008) Climate warming and related changes in Medi­ terranean marine biota. In: Briand F. (Ed.), Marine Science Commission (CIESM) Workshop Monographs, N o.35 Monaco: 152. Cigliano M., Gambi M.C. (2007) The long hot summer: a fur­ ther mortality event of gorgonians along the Phlaegrean

Marine Ecology 32 (Suppl. 1) (2011 ) 1 07 -11 6 © 2011 Blackwell Verlag GmbH

Islands (Tyrrhenian Sea). Biología Marina del Mediterráneo, 14, 292-293. Coma R., Linares C., Ribes M., Diaz D., Garrabou J., Ballester­ os E. (2006) Consequences of a mass mortality in popula­ tions of Eunicella singularis (Cnidaria: Octocorallia) in Menorca (NW Mediterranean). Marine Ecology Progress Series, 327, 51-60. Coma R., Ribes M., Serrano E., Jiménez E., Salat J., Pascuals J. (2009) Global warming - enhanced stratification and mass mortality events in the Mediterranean. Proceedings of the National Academy o f Sciences o f the United States o f America, 106, 6176-6181. Cupido R., Cocito S., Sgorbini S., Bordone A., Santangelo G. (2008) Response of a gorgonian (Paramuricea clavata) pop­ ulation to mortality events: recovery or loss? Aquatic Conser­ vation: Marine and Freshwater Ecosystems, 18, 984-992. Cupido R., Cocito S., Barsanti M., Sgorbini S., Peirano A., Santangelo G. (2009) Unexpected long-term population dynamics in a canopy-forming gorgonian coral following mass mortality. Marine Ecology Progress Series, 394, 195— 200 .

Dayton P.K. (1972) Toward an understanding o f community resilience and potential effects of enrichments to the benthos at McMurdo Sound, Antartica. In: Parker B.C. (ed), Pro­ ceedings of the colloquium on conservation problems in Antar­ tica. Allen press, Lawrence, Kansas: 81-95. Fava F., Bavestrello G., Valisano L., Cerrano C. (2010) Sur­ vival, growth and regeneration in explants of four temperate gorgonian species. Italian Journal o f Zoology, 77, 44-52. Garrabou J., Coma R., Bensoussan N., Bally M., Chelvaldonné P., Cigliano M., Diaz D., Harmelin J.G., Gambi M.C., Ker­ sting D.K., Ledoux J.B., Lejeusne C., Linares C., Marschal C., Perez T., Ribes M., Romano J.C., Serrano E., Torrents O., Zabala M., Zuberer F., Cerrano C. (2009) A new large scale mass mortality event in the NW Mediterranean rocky benthic communities: effects of the 2003 heat wave. Global Change Biology, 15, 1090-1103. Gay M., Renault T., Pons A.M., Le Roux F. (2004) Two Vibrio splendidus related strains collaborate to kill Crassostrea gigas: taxonomy and host alterations. Diseases o f Aquatic Organ­ isms, 62, 65-74. Hansen P., Grasshoff K. (1983) Automated chemical analysis, methods of seawater analysis (2nd edn). Verlag Chemie, Weinheim: 347-379. Hughes L. (2000) Biological consequences of global warming: is the signal already apparent? Trends in Ecology and Evolu­ tion, 15, 56-63. Kelleher G., Kenchington R. (1992) Guidelines for establishing marine protected areas. A Marine Conservation and Develop­ ment Report. IUCN - The W orld Conservation Union, Gland, Switzerland: vii + 79 pp. Linares C., Doak D.F. (2010) Forecasting the combined effects o f disparate disturbances on the persistence of long-lived gorgonians: a case study of Paramuricea clavata. Marine Ecology Progress Series, 402, 59-68.

115

P. clavata loss in t h e MPA o f T avolara

H uete-Stauffer, Vielmini, Palma, N avone, Panzalis, Vezzulli, Misic & C errano

Linares C., Coma R., Diaz D., Zabala M., Hereu B., D antart L. (2005) Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic com ­ munity structure in the NW Mediterranean Sea. Marine Ecology Progress Series, 305, 127-137. Linares C., Coma R., Garrabou J., Diaz D., Zabala M. (2008a) Size distribution, density and disturbance in two M editerra­ nean gorgonians: Paramuricea clavata and Eunicella singular­ is. Journal o f Applied Ecology, 45, 688-699. Linares C., Coma R., Zabala M. (2008b) Effects of a mass mortality event on gorgonian reproduction. Coral Reefs, 27, 27-34. Linares C., Coma R., Zabala M. (2008c) Restoration of threatened red gorgonian populations: an experimental and modelling approach. Biological Conservation, 141, 427-437. M artin Y., Bonnefont J.L., Chancerelle L. (2002) Gorgonians mass mortality during the 1999 late summer in French Med­ iterranean coastal waters: the bacterial hypothesis. Water Research, 36, 779-782. Matías M.G., Underwood A.J., Hochuli D.F., Coleman R.A. (2010) Independent effects of patch size and structural com ­ plexity on diversity o f benthic macroinvertebrates. Ecology, 91, 1908-1915. Mistri M., Ceccherelli V.U. (1994) Growth and secondary p ro­ duction of the Mediterranean gorgonian Paramuricea clavata. Marine Ecology Progress Series, 103, 291-296. Navone A., Trainito E. (2008) Tavolara: Nature at W ork.. .Work­ ing in Nature. Delfino Carlo Editore 8 c Co., Olbia, Rome: 285 pp.

116

Navone A., Bianchi C.N., O rrù P., Ulzega A. (1992) Saggio di cartografía geomorfologica nei parco marino di TavolaraCapo Coda cavallo. Oehalia, 17(Suppl), 469-478. Pérez T. (2008) UNEP-MAP-RAC/SPA. Impact of climate change on biodiversity in the Mediterranean Sea. The Regio­ nal Activity Centre for Specially Protected Areas. RAC/SPA, Tunisi-Cedex, Tunisia: 1-90. Pérez T., Garrabou J., Sartoretto S., Harmelin J.G., Francour P., Vacelet J. (2000) Mass mortality of marine invertebrates: an unprecedent event in the Northwestern Mediterranean. Compte Rendus de l’Académie des Sciences III, 323, 853-865. Previati M., Scinto A., Cerrano C., Osinga R. (2010) Oxygen consum ption in four Mediterranean octocorals during tem ­ perature increase. Journal o f Experimental Marine Biology and Ecology, 390, 39-48. Scinto A., Bertolino M., Calcinai B., Huete-Stauffer C., Previati M., Romagnoli T., Cerrano C. (2009) Role o f a Paramuricea clavata forest in modifying the coralligenous assemblages. Proceedings o f the 1st Mediterranean Symposium on the conservation o f the coralligenous and other calcareous bioconstructors. The Regional Activity Centre for Specially Protected Areas (RAC/SPA). Tabarka, 136-140 pp. Trainito E. (2007) Progetto mappaggio, valutazione di risorse sottomarine per lo sviluppo sostenibile del turismo subacqueo nell’AMP Tavolara Punta Coda Cavallo. MPA Tavolara. 140 pp. Vezzulli L., Previati M., Pruzzo C., Marchese A., Bourne D.G., Cerrano C.; Vibrio Consortium. (2010) Vibrio infections triggering mass mortality events in a warming M editerra­ nean Sea. Environmental Microbiology, 12, 2007-2019.

M arine Ecology 32 (Suppl. 1) (2011 ) 1 07 -11 6 © 2011 Blackwell Verlag GmbH

marine ecology

an evolutionary perspective

' »

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

Short and mid-long term effects of cockle-dredging on non-target m acrobenthic species: a before-after-controlim pact experim ent on a tidal m udflat in th e Oosterschelde (The Netherlands) S a n d e r W i j n h o v e n 1, V in c e n t E sca ra v a g e1, P eter M. J. H e r m a n 2, A a d C. S m a a l3 & H erm an H u m m e l1 1 Monitor Taskforce, Netherlands Institute of Ecology, Centre for Estuarine and Marine Ecology (NIOO-CEME), Yerseke, The Netherlands 2 D epartm ent of Spatial Ecology, Netherlands Institute of Ecology, Centre for Estuarine and Marine Ecology (NIOO-CEME), Yerseke, The Netherlands 3 Aquaculture Department, W ageningen IMARES (Institute for Marine Resources & Ecosystem Studies) (WUR), Yerseke, The Netherlands

K eywords Before-and-after-impact design; benthic

Abstract

macrofauna; Cerastoderma edule; cockle fishery effects; short and mid-long term; species composition.

T o stu d y th e possible en v iro n m en tal im p act o f hydraulic cockle-dredging on m acro b en th ic co m m u n ities an d th e env iro n m en t, a fishing ex p erim en t was executed o n a tidal m u d flat in th e O osterschelde (SW N etherlands) according to a BACI (befo re-after-co n tro l-im p act) design. Following th e ch aracterization of th e initial situ atio n , a p a rt o f th e m u d flat was com m ercially fished, after w hich dredged an d un d red g ed areas w ere com p ared o n th e basis o f m acro fauna descriptors an d sed im en t co n stitu tio n appro x im ately 2 m o n th s (sh o rt term ) an d 1 year (m id -lo n g term ) after fishing. W hereas a clear re d u c tio n o f th e larger Cerastoderma edule cockles (>23 m m ) in th e fished areas was fo u n d , n o effect of dredging o n to tal m acro fau n a densities o r m ed ian grain size was observed. N o negative effect o f fishing o n to tal m acro fau n a biom ass was fo u n d ; in contrast, an increase o f th e biom ass o f th e n o n -ta rg e t species alm o st com pensated for th e loss in w eight d u e to th e extraction o f th e larger cockles. N o significant effect of dredging o n species diversity, richness o r evenness was fo u n d in th e sh o rt or m id -lo n g term , these descriptors ten d in g to have increased ra th e r th a n decreased in th e dredged plots after 1 year. T he selective fishing for larger cockles reduced th e average cockle size, b u t 1 year after fishing th e average size h ad re tu rn e d to th e initial values in th e dredged area. H ow ever, co m p ared to th e co n tro l area, the average size m ig h t still be reduced, as th e size o f th e cockles in th e con tro l area also increased d u rin g th e year. Local enviro n m en tal cond itio n s, w ith th e ir spe­ cific m acro b en th ic com m unities, seem to be crucial for th e type o f effects a n d the im p act o f dredging. It is therefore o f em in en t im p o rtan ce to follow a research design w ith p re-defined enviro n m en tal conditio n s, ra th e r th a n a co m p ariso n of different areas th a t are o p en o r closed to fisheries. T he presen t stu d y based o n a BACI ap p ro ach indicates th a t m echanical cockle fisheries h ad n o overall negative im p act in o u r stu d y area.

C orrespondence Sander Wijnhoven, Monitor Taskforce, Netherlands Institute of Ecology, Centre for Estuarine and Marine Ecology (NIOO-CEME), Korringaweg 7, PO Box 140, NL-4401 NT, Yerseke, The Netherlands. E-mail: [email protected] Accepted: 16 November 2010 doi: 10.1111/j. 1439-0485.2010.00423.x

Introduction Several studies have investigated th e p o ten tial im p act of dredging or sed im en t-d istu rb in g activities o n m a cro b en ­ thic co m m unities an d o n th e n o n -targ e t species in p a rtic­

Marine Ecology 32 (Suppl. 1) (2011) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

ular. Som e o f these show stro n g effects (e.g. B eukem a 1995; P iersm a et a í 2001; L eopold et a í 2004), b u t o ther studies show m in o r effects o r n o n e at all (e.g. Craeym eersch & H u m m el 2004; Ens et al. 2004; B eukem a & D ekker 2005). These studies differ in th e severity o f the

117

S h o rt a n d m id -long te rm effe cts o f co ck le-d red g in g o n n o n - ta rg e t m a c ro b e n th ic species

W i j n h o v e n , E sc a ra v a g e , H e r m a n , Smaal & Hummel

disturbances, especially th e d istu rb an ce d ep th (H aii & H ard in g 1997; K aiser e t al. 2001), th e season o f th e dis­ tu rb an ce (H aii & H ard in g 1997), th e frequency o f d istu r­ bance (e.g. Kaiser et al. 2001), th e possible selectivity of the different fishing techniques used (Ferns et al. 2000) and the m ethodological a p p ro ach involving co m p ariso n o f different areas th a t w ere fished or unfished for an extended perio d (P iersm a et al. 2001) versus an experi­ m ental ap p ro ach w ith exclusion o f fishery in cockle beds (C raeym eersch & H u m m el 2004). T he m an y studies o n this topic differ also w ith respect to th eir research questions. T hey ascertain nega­ tive effects o f fishing disturbances o n (i) th e en v iro n ­ m e n t as a w hole (e.g. L eopold et a í 2004; Zw arts 2004), (ii) th e stru ctu re o f co m m u n ities (Leitäo & G aspar 2007), (iii) the ab u n d an ce o f targ et species (Piersm a et a í 2 0 0 1 ), or (iv) processes as settlem ent, p o p u la tio n dynam ics and reco lo n ization o f selected species (C o tter et al. 1997; H id d in k 2003; B eukem a & D ekker 2005). These studies m ostly consist o f inventories after large im pacts, an d th e next step consists o f th eir in teg ratio n in policies aim ing a t a m itig atio n o f th e risk th a t takes in to acco u n t th e o p p o rtu n ities for sustainable fisheries (B eukem a & C adée 1999). T h u s an im p act is expected beforehand, w here th e stu d y investigates th e rehabilita­ tio n p otential o r d u ra tio n o f reh ab ilitatio n o f th e target or n o n -targ et p o p u latio n s or th e enviro n m ental c o n d i­ tions (H aii & H ard in g 1997). G iven th a t different env iro n m en ts have th eir specific com m unities an d species assemblages, various im pacts of fisheries m ig h t be expected dep en d in g o n th e substrate specifications (Ferns et a í 2000), tidal range a n d elevation or d epth (Leitäo & G aspar 2007). F u rth erm o re, different evaluations o f effects can be expected according to th e sam pling design, ranging fro m ad hoc inventories in extensive areas th a t are either fished o r p ro tected over various tim e spans (e.g. P iersm a et a í 2001; B eukem a & D ekker 2005) to a priori elaborated experim ental designs o n local sites w ith an exact know ledge o f th e fishing intensity an d tim in g (Ferns et a í 2000). W e are interested in w hether dredging has a destru c­ tive effect on n o n -targ e t species, w hich m ig h t be d a m ­ aged by being lifted u p fro m th e sed im en t or processed th ro u g h the fishing device. These effects m ig h t be visible in th e sh o rt te rm th ro u g h increased m o rtality resulting from injuries o r fro m exacerbated p re d atio n b y o th er m acrobenthic species o r vertebrates (Ferns et a í 2000; H id d in k 2003). T his im plies th a t th e p red ato rs o f th e highly dredging -im p acted species m ig h t p ro fit fro m this disturbance. D redging can also ind u ce shifts in th e spe­ cies com p o sitio n as a result o f th e alteratio n o f th e environm ental co n d itio n s such as th e sed im en t co m p o ­ sition in the sh o rt a n d especially th e m id -lo n g term

118

(H id d in k 2003). C om p ariso n s betw een observations at sh o rt an d m id -lo n g term can show w h eth er th e effects o n th e species assem blages are transito ry , w hereas m idlong te rm observations are req u ired to detect effects on species re c ru itm e n t an d larval settlem en t (P iersm a et a í 2001). In this stu d y we specifically investigated w h ether the sed im en t characteristics (grain size) an d th e m acrobenthic com m u n ities (including n o n -ta rg et species) are negatively affected b y hydraulic dredging for cockles o n a soft-sedim e n t tidal flat. To acco u n t for th e various sources o f v ar­ iatio n besides th e d irect effect o f dredging, a BACI (b efo re-after-co n tro l-im p act) design was used (Sm ith 2002). A substantial p a rt o f a m u d flat was com m ercially fished, a n d o th er parts w ere left u n d istu rb ed . In the dredged a n d u n d red g ed areas, 100 X 100 m plots w ere delim ited an d ran d o m ly sam pled before an d shortly (sh o rt term ) a n d 1 year (m id -lo n g term ) after fishing. This stu d y is th e first to investigate th e im p act o f co m ­ m ercial cockle fisheries w ith su ctio n dredgers o n n o n -ta r­ get b en th ic m acro fau n a species a n d co m m u n ities using a BACI ap p ro ach in w hich th e sensitivity o f th e exp erim en­ tal design to detect quantitativ e changes is also taken into account.

Material and M e th o d s Study area an d experim ental design T he experim ental research o n th e effects o f cockle dredg­ ing was carried o u t o n th e Slikken van de D o rtsm an tidal flats in th e O osterschelde, a sem i-o p en tidal b ay in the S outhw est N etherlands (Fig. 1) w ith a salinity o f above 30%o (C oosen et al. 1994). N ext to th e blue m ussel M y ti­ lus edulis, th e cockle Cerastoderma edule is th e d o m in an t suspension feeder in th e O osterschelde. H ow ever, n ow a­ days, to ta l cockle biom ass is low er th a n it used to be d u r­ ing th e 1980s an d before. Besides th e intensive fishing on th e cockle p o p u latio n s over several years, th e co n stru ctio n o f a sto rm surge b arrier in th e m o u th o f th e O ostersc­ helde (fro m 1976 to 1986) h ad a great im p act o n the suitability o f th e area for cockles. T he c o n stru ctio n o f the sto rm surge b arrier led to a 3 0 -7 0 % re d u ctio n in cu rren t velocities, a n d a 1 2 % red u ctio n in th e tidal range, p ro ­ ducing clearer w aters, cru m b lin g aw ay o f th e elevated areas, an d sed im en tatio n a t th e b rim s o f th e tidal flats (G eurts van Kessel et al. 2003). T he tidal range in the research area varies betw een 1.7 an d 3.8 m. Since th e early 1990s, cockle fishery in th e O o ster­ schelde has been subject to au th o rizatio n , w hich is only granted in years w ith a b u n d a n t cockle biom ass. N o au th o riz a tio n h ad been given since 2 0 0 1 in o u r research area (G eurts v an Kessel et al. 2003). As a consequence,

M arine Ecology 32 (Suppl. 1) (2011 ) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

Wijnhoven, Escaravage, Herman, Smaal & Hummel

Short and m id-long term effects of cockle-dredging on n o n -targ e t m acrobenthic species

Oosterschelde The Netherlands

‘Slikken van de Dortsman'

i j D red g ed plot

C ontrol plot

'» S am p le s ite s

—

R oute of cockle b o a ts a s re c o rd e d by saté lite tracking s y ste m s (STS)

Fig. 1. Positioning of the experimental plots (plot num bers Indicated) on the Slikken van de Dortsman tidal flats in the Oosterschelde area (SW Netherlands).

the cockle banks in th e p resen t stu d y h ad been free of any dredging activity for a 5-year p erio d before th e t0 sam pling (Septem ber 2006). N ine plots o f 100 X 100 m w ere ran d o m ly selected w ith in th e research area. Because o f the expected spatial heterogeneity o f h ab itat a n d living com m unities on th e tid al flat, w hich is largely o n a N o rth -S o u th gradient, it was decided to separate th e nine plots in to three g roups th a t w ere spatially clustered (n o rth , m iddle an d so u th p a rt o f th e stu d y area). The positio n in g and d ep th o f th e plots are ind icated in Fig. 1. W ith in each gro up , tw o plots w ere dredged an d th e last p lo t was used as an u n d re d g e d /c o n tro l reference. W ith in each o f the n ine plots, five sam ple sites w ere ran d o m ly selected. O n 6 Septem ber 2006 (io), 45 m acro fau n a an d sedim ent sam ples w ere taken, after w hich th e w hole area was dredged, w ith th e exception o f th e th ree con tro l plots. T he fishing o p eratio n was perfo rm ed for co m m er­ cial purposes by three cockle b o ats equ ip p ed w ith h y d rau ­ lic dredges. T he dredging activity o f th e ships was recorded w ith a satellite tracking system (STS) th at revealed, after in terp o la tio n o f th e 1 -m in interval signals, dredging tracks all over th e experim ental plots b u t n o t in the control plots (Fig. 1). A fter dredging, th e tracks in the field clearly visible in th e sed im en t w ere also checked, an d w ere indeed fo u n d all over th e dredged plots an d n o t in the control plots. Fishing activity to o k place fro m 5 Septem ber u n til 9 N ovem ber an d was restricted to u n ­ sam pled areas d u rin g th e first day o f fishing. O n 9 N ovem ber 2006 (iy), all sam ple sites w ere sam pled for

Marine Ecology 32 (Suppl. 1) (2011) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

m acro fau n a an d sed im en t to detect possible sh o rt-term effects, a n d o n 1 a n d 2 O cto b er 2007 (/?)> th e sam ple sites w ere sam pled again to detect possible m id -lo n g term effects. T he cu rre n t experim ent is a stan d ard BACI design (S m ith 2002), w hich enables th e changes observed in experim ental plots to be com p ared w ith those occurring in co n tro l plots, taking in to ac co u n t a u to n o m ic develop­ m en ts d u rin g th e stu d y period.

Sampling and m easurem ents A t each sam ple site, five m acro fau n a an d five sedim ent sam ples w ere tak en at each sam ple tim e. M acrofauna sam ples consisted o f th ree cores (3 X 0.005 m 2) p u shed 30 cm in to th e sed im en t w ith in a 1-m rad iu s o f th e sam ­ ple site, located w ith a GPS. The m acro fau n a sam ples w ere sieved over a 1-m m m esh, fixed w ith 4% buffered fo rm alin a n d stained w ith Rose Bengal, after w hich speci­ m en s w ere d eterm in ed to th e species level, w ith the exception o f th e O ligochaeta, A ctinaria a n d N em ertea. T he n u m b ers p er species w ere c o u n ted an d densities determ ined. T o establish th e density o f species th a t are frequently fragm ented, such as polychaetes, th e n u m b er o f heads was counted. W h en only b o d y p arts w ere fo u n d a n d n o head, th e n u m b e r o f specim ens was co u n ted as one. Small or fragm ented specim ens th a t could n o t be classified to species level w ere classified to genus level (e.g. Cerastoderma sp., Spio sp. an d Arenicola sp.). The

119

S h o rt a n d m id -long te rm effe cts o f co ck le-d red g in g o n n o n - ta rg e t m a c ro b e n th ic species

W i j n h o v e n , E sc a ra v a g e , H e r m a n , Smaal & Hummel

length o f th e cockles was also m easured as th e m ax im u m m easurable shell length to th e nearest m illim eter. T he total biom ass (g A D W , ash-free dry-w eight) of each species was d eterm in ed either directly fro m th e dried specim ens (2 days at 80 °C) as th e decrease in w eight after 2 h scorching at 560-580 °C, or indirectly by length-w eight regressions (W = aLb, w here W is w eight in g A D W and L is length in m m ). T he len g th -w eig h t regressions used w ere based o n (i) specim ens scorched d u ring this study, (ii) existing data in o u r BIS (benthos in fo rm atio n system) database fro m th e sam e area/seaso n , and (iii) the fresh-w eight o f th e specim ens a n d taxon-specific conversion factors fro m o th er m o n ito rin g cam paigns in BIS. Sedim ent sam ples w ere taken w ith a 1-cm diam eter tu be p u sh ed 3 cm in to th e sedim ent. T he m ed ian grain size (/im ) o f th e sam ples was d eterm in ed b y laser-diffrac­ tio n m ethodolo g y using a M astersizer 2000 (M alvern Instrum ents).

D escriptors Plots, treatm en ts an d sam ple tim es w ere com p ared for total m acrofau n a a n d species densities a n d biom asses, species com positio n , an d frequencies an d diversity. The length d istrib u tio n o f th e cockles (Cerastoderma sp. an d Cerastoderma edule com bined) was also com pared betw een treatm en ts. D iversity was m easured as species diversity according to th e S h an n o n index, species ric h ­ ness as the n u m b e r o f in d ividual species an d according to M argalef, a n d evenness according to Pielou, calculated w ith the softw are PRIM ER 5.2.8 for W indow s (C larke & W arw ick 2001). All to tal m acro fau n a an d diversity in d i­ cators w ere calculated w ith a n d w ith o u t taking Cerasto­ derma sp. an d C. edule in to acco u n t, because it is expected th a t these cockles are affected b y dredging as the (larger) cockle is th e target species. Further, top-10 lists o f th e m o st ab u n d a n t in d ividual species in chance o f occurrence in sam ples, in densities an d in biom asses w ere p u t togeth er for each o f th e sam ple dates an d treatm ents; 18 lists in total. Species m en tio n ed in at least one o f th e lists for one o f th e descriptors were selected to be related in a m ultivariate w ay to tim e an d treatm ent. D ifferences in th e sed im en t grain size betw een th e treatm en ts w ere also analyzed. To c o n fo rm to th e re q u ire­ m ents o f th e p aram etric statistical testing regarding n o r­ m ality in the d istrib u tio n o f th e data, th e density an d biom ass d ata w ere lo g -tran sfo rm ed before analyses. The diversity indicato rs (S hannon, M argalef a n d P ielou), th e m edian grain size a n d cockle length data appeared to be norm ally d istrib u ted in all cases (K o lm o g o ro v -S m irn o v test at P < 0.05).

120

D ata analysis T he com p ariso n s betw een treatm en ts w ere p erform ed according to a stan d a rd BACI-ANOVA design w here the effects o f treatm en t, tim e an d tim e -tre a tm e n t in teractio n w ere tested a t P < 0.05. As a result o f a ra th e r strong ‘p lo t’ effect, th e in d ividual sam ples can n o t be considered to be taken ran d o m ly (w ith o u t co n sid eratio n o f p lo t o ri­ gin) w ith in th e treatm en ts. T herefore a nested design according to: ‘C hange in P aram eter’ = ‘P aram eter aver­ age’ + ‘T re atm e n t effect’ + ‘P lo t effect w ith in each tre a t­ m e n t’ + ‘U nexplained v ariatio n ’ w here ‘U nexplained v ariatio n ’, w hich is th e E rro r term , equals th e variation am o n g sam ples w ith in plots (Sokal & R o h lf 1995). Because o f th e decrease in th e degree o f freed o m due to th e nesting o f plots w ith in each treatm en t, th e present A N O VA design is a relatively conservative test, w hich could fail to detect slight responses to th e dredging. W e are aw are th a t d ata p er tre atm e n t should n o t be gathered for testing w hen th ere are differences betw een plots w ith in treatm en ts. H ow ever, we w an ted to m ake sure th a t possible negative effects o f cockle-dredging, w h en present, do n o t pass u n n o ticed . W e therefore used th e m o re sensi­ tive [i.e. w ith o u t d istin ctio n o f p lo t origin) Student-/- test (P < 0.05) for p lain com parisons betw een th e treatm ents or sam pling tim es. Even th e rob u stn ess o f these m o re sensitive tests m ay b e relatively low, due to th e large v ari­ ance am o n g sam ple sites already at th e sta rt o f th e experi­ m ents (f0), or due to th e n o n -n o rm a l distrib u tio n s. As we are especially in terested in th e developm ents over tim e for different treatm en ts, in d e p en d e n t o f a u to n o m o u s developm ents, we calculated th e differences betw een t x a n d f0 o r f2 a n d f0, a n d com p ared those p er treatm en t using th e S tu d e n t-f test (P < 0.05). Effects o n in d ividual species w ere investigated w ith re d u n d an cy analysis (RDA), w hich is a linear m eth o d o f canonical o rd in a tio n w here enviro n m en tal variables are com bined to b u ild th e o rd in a tio n axes, locating the sam ­ ples w ith in th e m ultivariate space defined b y th e species data, i.e. th e lo g -tran sfo rm ed density, biom ass o r presence frequency data (T er B raak & Sm ilauer 1998). T he analyses w ere restricted to th e m o st a b u n d a n t a n d d o m in an t spe­ cies d eterm in ed as belonging to th e to p - 1 0 species w ith respect to th e descrip to r to b e analyzed (density, biom ass or presence frequency) in a t least one o f th e plots at one o f th e sam ple dates. T he suitability o f th e linear response m odel was tested based o n th e value o f th e gradient length estim ated w ith a d etren d ed correspondence analy­ sis (DCA); for a g rad ien t length betw een 1.5 a n d 3 SD, b o th linear a n d u n im o d al m odels could be applied. H igh species score (density, biom ass o r presence frequency) at a given location m ig h t be driven by outof-scope factors coincidental w ith th e treatm en t, w hich

M arine Ecology 32 (Suppl. 1) (2011 ) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

W i j n h o v e n , E s c a ra v a g e , H e r m a n , S m aa l & H u m m e l

S h o rt a n d m id-long te rm effe cts o f co ck le-d red g in g o n n o n - ta rg e t m a c ro b e n th ic species

could lead to m isin te rp re ta tio n based o n th e RDA plots. Therefore, the effect o f th e treatm en ts o n densities an d biom asses o f individual species w ere tested using S tudent /■-tests at P < 0.1. A gain, this is a ra th e r sensitive test to avoid m issing possible negative im pacts. To cope w ith the bias in tro d u ced w ith th e m u ltip le /--testing, a B onferroni correctio n according to P < a /n (Sokal & R o h lf 1995) was also applied to identify th e ‘real’ significant effects on species. All statistics w ere executed in SYSTAT for W in ­ dow s 1 1 . Pow er analyses w ere p erfo rm ed in cases o f absence of significant differences to determ ine th e robustness o f the tests. T he m in im u m difference th a t could possibly be detected w ith P < 0.05 was d eterm in ed taking th e varia­ tio n betw een sam ples a n d th e n u m b e r o f sam ples into acco u n t (Sokal & R o h lf 1995). T he n u m b e r o f available observations an d th e ir stan d ard deviations w ere tested at the level o f 80% probability, assum ing th a t th e data belong to one n o rm al d istrib u ted p o p u la tio n o f observa­ tions. T he K o lm og o ro v -S m irn o v test ind icated th a t the values for each o f th e p aram eter X tre atm e n t X tim e intervals can indeed be considered to b e no rm ally d istrib ­ u ted, except for th e difference in biom ass betw een f0 an d t2 a t the dredged sites.

Results

□ C ontrol

200

: I I I I I : a a a a a a

E zi­ E

ft 180 05

C

co

O)

?

10,000 :

-S'

2

1 id L b L ’: c * 0 . :

1000

1

wi l l *

CD

J 160 CD S

I

.................................

140

1

i

i

i

1 2 3 4 5

Plot

Plot 2.5 : ab ab a a

a

*

a ab b at? : •

11 T

| |

i

:

*5

.

■

"i :

2.0 05 CD

"O SZ

o sz

cro 0.5 j

!

0 3 4

5 6

Plot

!

0.0 Plot

Fig. 2. Between plots variation before fishing (to). Variation In (A) median grain size (um), (B) total density (n-rrT2), (C) total biomass (g ADW-rrT2), and (D) species diversity according to Shannon. Significant differences (P < 0.0S) are Indicated with different letters, w hereas the sam e letter In com mon m eans no significant differences.

Initial situation (f0) D ata collected a t th e sta rt o f th e experim ents (f0) show distrib u tio n pattern s over th e research area w ith a clear differentiation o f th e th ree n o rth e rn plots fro m th e so u th ­ ern plots (Fig. 2). T he th ree n o rth e rn plots are ch aracter­ ized by sm aller m ed ian grain sizes a n d low er to tal m acrofauna densities a n d biom asses (an d th ereb y higher S hannon, M argalef an d P ielou diversity indices) th a n the so u th ern plots (ANOVA, P < 0.05). T he in term ed iate plots show ed interm ed iate values o r resem bled the so u th ern or n o rth e rn plots. In all cases, as show n also in Fig. 2, th e experim ental plots clearly resem bled the reference plots (an d th u s show ed th e sam e geographic N -S gradient). T herefore, at f0 th e averages o f the reference plots for m ed ian grain size (Fig. 3A), to tal density (Fig 6 A ), to tal biom ass (Fig. 6 C ), species diver­ sity (Fig. 7E), species richness (Fig. 7A) a n d evenness (Fig. 7C) are the sam e as for th e experim ental plots. The initial large variance betw een plots was dealt w ith b y n est­ ing the variance w ith in th e treatm en ts, w hich th e n serves as the error term for th e tre a tm e n t-tim e in teractio n to be tested. The sm allest detectable differences w ith th e used design, taking initial variability in to acco u n t, equals 1 % in m edian grain size, 1 0 % in evenness, 2 2 % in species

Marine Ecology 32 (Suppl. 1) (2011) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

richness, 24% in species diversity, 48% in to tal densities a n d 55% in to tal biom ass, w ith a p ro b ab ility o f 80% at P < 0.05, as calculated using pow er analyses.

Median grain size It was expected th a t th e m ed ian grain size w o u ld be directly influenced b y dredging because o f th e sedim ent resuspension th a t occurs d u rin g fishing activity. H ow ever, n o difference in m ed ian grain size could be detected betw een th e co n tro l a n d th e dredged areas at an y tim e (f0, or t2; t-test, P < 0.05) or betw een sam pling occa­ sions (fo-fi, t0- t 2) (Fig. 3; Table 1). T he average m edian g rain size over all sam ples equals 175 /zm, varying locally a n d in d ep en d e n tly o f trea tm e n t or tim e betw een 150 an d 190 /zm.

Cockles T he presen t dataset allows an estim atio n to be m ad e of th e im p act o f th e fisheries o n th e cockle popu latio n s. Sig­ nificantly low er cockle n u m b ers w ere fo u n d in the dredged area co m p ared to th e con tro l area at A (f-test, P < 0.05), an d low er cockle biom ass was fo u n d in the

121

S h o rt an d m id-long te rm effe cts o f co ck le-d red g in g on n o n -ta rg e t m a c ro b e n th ic species

W i j n h o v e n , E s c a ra v a g e , H e r m a n , S m aa l & H u m m e l

A

B

□ t0 ED ^ H t2

used by th e cockle ships (H id d in k 2003). H ow ever, due to the low n u m b ers o f observations a n d th e ir high v ari­ ance, only differences o f 82% (larger size classes) to 85% (sm aller size classes) can be detected (pow er analysis; P = 80%, P < 0.05). A t A, o n average, 38.3% o f the cock­ les in th e dredged area are large, w hereas in th e control area, this figure is 72.2% (significant at P < 0.1). W e also fo u n d a significant (P < 0.1) decrease in larger cockles betw een t0 an d A in th e dredged area co m p ared to the co n tro l area.

D Control b Dredged

200

190 180

'I 170

0

co 160 150 140

Control

--2 0

Dredged

Fig. 3. Median grain size of the top layer of the experimental plots. (A) Median grain size fitm) in control and dredged plots before fi0), shortly after fid and 1 year after fi2) fishing. (B) Increase or decrease of median grain size betw een t0 and U and betw een t0 and f2.

Total m acrofauna indicators The to tal density o f m acro fau n a excluding th e cockles was relatively stable over tim e an d n o significant differ­ ences were fo u n d betw een the dredged an d co n tro l areas (Fig. 6 A; Table 1). A lthough differences in developm ent o f the densities m ig h t have been presen t betw een the tw o treatm en ts, densities do n o t ap p ear to have been decreased over tim e in th e dredged plots, w hereas the au to n o m o u s tre n d (visible in th e co ntrol) shows a slight decrease (Fig. 6 B). As n o significant differences were observed, any differences m u st have been sm aller th an 48% at A a n d 54% at t2, as calculated by a pow er analy­ sis.

dredged area th a n in th e co n tro l area at b o th A an d t2 (P < 0.05) (Fig. 5). The effect o f fishing was m o re evident in the biom ass changes, as it was prim arily th e larger cockles th a t were fished (Fig. 4). The size d istrib u tio n o f th e cockles m easured in this study can be used to estim ate the size selectivity o f the dredging w ith respect to th e cockles. As in dicated by th e average cockle length an d length d istrib u tio n (Fig. 5A), clear shifts are fo u n d tow ards sm all-sized individuals betw een t0 and A an d back to th e original size d istrib u ­ tio n at t2 in the dredged areas. In the reference area, size d istrib u tio n s at t0 a n d A are quite sim ilar, w hereas there is a slight increase in size d istrib u tio n m o d e betw een t0 and t2 (Figs 4 an d 5). D istinguishing different size classes (sm all <23 m m an d large >23 m m ) o f cockles could p ro ­ vide in fo rm atio n ab o u t th e differential effect o f dredging as a fun ctio n o f shell size. Indeed, a 23-m m shell length is approxim ately th e size o f separation o f a 15-m m grid as

cant (P = 0.444 fro m t0 to A an d P = 0.099 fro m t0 to t2; Table 1 ). W h en th e to tal biom ass is calculated including the cockles, th e possible difference in tren d s is alm ost

mu

I—I A

20

In th e to tal biom ass, th e a u to n o m o u s effect o f decrease over tim e seems to be even stronger th a n indicated by the num b ers, an d here also such a tre n d is absent in the d redged area (Fig. 6 C,D ). H ow ever, co n d u ctin g BACIANOVA, differences in tren d s do n o t appear to be signifi­

in

X) 10

E

Ii ! 20

E 10

0

J in ] 10

20

30

tL 40

Cockle length (mm)

1 22

50 0

10

20

□

30

rjfrn 40

Cockle length (mm)

50 0

10

20

30

40

Cockle length (mm)

50

Fig. 4. Numbers of cockles distributed over size classes within the control and dredged plots (rows) before fi0), shortly after fid and 1 year after fi2) fishing (columns).

Marine Ecology 32 (Suppl. 1) (2011) 117 -12 9 © 2011 Blackwell Verlag GmbH

S hort an d m id-long te rm effe cts of co ck le-d red g in g on n o n -ta rg e t m a c ro b en th ic

W i j n h o v e n , E s c a ra v a g e , H e r m a n , S m a a l & H u m m e l

species □ Control ® Dredged

□ Control ra Dredged

B

2

CO CO CD

c

40

-C

^

o

1000

co 1 CD

'o 0

w

100

CD

1.0

Cl CO 0 CO CD

0

o0 "O c

0

■1

Fig. 5. Cockle length in mm (A) and biomass in g ADW-m 2 (B) in control and dredged plots before (f0), shortly after (ffi and 1 year after (f2) fishing. Significant differences in lengths betw een treatm ents are indicated with *P < 0.05. 0.0 n

Control D redged

100,000

£ -0 .5

10,000

to-ti W

to-t2

1000

t0 h 100.00

t0 t2

CL o CO u

D io °CD - 1i

10.00

-2

&

Fig. 7. Macrobenthic assem blage biodiversity descriptors. (A) Species richness according to Margalef in control and dredged plots before

0.10

-1 0

to h

t0 t2

Fig. 6. Total macrobenthic density and biomass of the experimental plots. (A) Total density (n-m-2) in control and dredged plots before (i0), shortly after (ffi and 1 year after (f2) fishing. (B) Relative increase or decrease of total density betw een t0 and t-\ and betw een t0 and f2 calculated as the difference betw een the natural logarithms. (C) Total biomass (g ADW-m-2) in control and dredged plots before (f0), shortly after (ffi and 1 year after (f2) fishing. (D) Relative increase or decrease of total biomass betw een t0 and U and betw een t0 and t2 calculated as th e difference betw een the natural logarithms.

com pensated by th e cockle biom ass. H ow ever, it is clear th a t on b o th the sh o rt an d th e m id -lo n g term , w ith o r w ith o u t the cockles included, no decrease in densities or biom ass is seen as a result o f dredging.

M arine Ecology 32 (Suppl. 1) (2011) 117-129 © 2011 Blackwell Verlag GmbH

(t0), shortly after (ffi and 1 year after (f2) fishing. (B) Increase or decrease of species richness betw een t0 and U and betw een t0 and t2. (C) Pielou's evenness in control and dredged plots before (f0), shortly after (id and 1 year after (f2) fishing. (D) Increase or decrease of evenness betw een t0 and t-\ and betw een t0 and f2. (E) Shannon's species diversity in control and dredged plots before (t0), shortly after (fd and 1 year after (f2) fishing. (F) Increase or decrease of species diversity betw een t0 and U and betw een t0 and f2.

Species richness an d species diversity show sim ilar p a t­ tern s w hen co m p arin g th e tw o treatm en ts over tim e (Fig. 7A,E). Initially th e tw o treatm en ts d id n o t differ and this was still the case ju st after dredging. H owever, 1 year after dredging the indicators ten d ed to be increased for th e dredged area, w hereas th e co n tro l area rem ained unchanged. The observed tren d s can n o t be considered significantly different as show n by BACI-ANOVA

123

S h o rt a n d m id -long te rm effe cts o f co ck le-d red g in g o n n o n - ta rg e t m a c ro b e n th ic species

W i j n h o v e n , E sc a ra v a g e , H e r m a n , Smaal & Hummel

Table 1. Test results of BACI-ANOVA for tlm e-treatm ent Interactions taking 'plot nested within treatm ent x tim e' [tlme*plot (treatment)] as error; df(( tim e * tre a tm e n t) = 1; dfprrnr = 7; cockle data excluded.

Arenicola me

t Crangon crangon

Short-term effects

mid-long term

(fo-fi)

effects (f0- f 2)

4^ Lanice conchilega

j¡ a Dredged OLIGOCHA 'TA Streble spio shrubsolii

Spio martinensis Mya arenaria

F-ratlo

P

F-ratlo

P

median grain size

1.007

0.444

0.000

1.000

log (density) log (biomass) Margalef richness

1.285 0.061 0.642

0.3S2 0.979 0.612

0.157 3.627 3.S60

0.922 0.099 0.101

Plelou's evenness Shannon diversity

0.2S1 0.494

0.8S8 0.698

0.866 3.271

0.S02 0.113

(P = 0.101 for th e tren d s in richness an d P = 0.113 for the trends in diversity betw een t0 an d t2) (Table 1). H o w ­ ever, there was definitely n o negative effect o f dredging o n species richness an d diversity. E ither n o effect was fo u n d o n the evenness, or it m u st have been sm aller th a n 1 0 % according to a pow er analysis, b u t th en , th e im p act o f dredging seem s to be positive instead o f negative (Fig. 7C). W

Effects o n singular non-target species

■ammarus locusta

mûmçiasp

Spio sp

Gammarus sp üTumun Capitel 'a capitata

Hydrobia ulvae

ispip'^legtfí^^^:-;::j^ Platynereis dumerilli P'OÎÿdçra ligTri*^^, coloplos armiger

t

^ tl 2 urothoe poseidonis . Nephtys horni ergii

Cerastoderma edule f Cb n t r o l Tharyx marioi

F 7

-1.5

1.0

Nephtys sp

t

armiger 5 :oloplos A . Gammarus locusta

2 kA Gammarus sp

i f 4Platynereis dumerilli I ƒƒ 4 Nereis longissima Urothoe poseidonis I ¡krenicola marina Capitella capitata r ! il k Scrobicularia pia e lunulata Carcinus m aen\ mchilega Cerastoderma edule althica ---------------- - Arenicola sp •W iSfftm . ""“**■ Nephtys a rrosa £í¿:~*f£¡ephtys hombe rgii Control b„pw.-martaken M V siAA Cerastoderma sp m \ Crangon crangon BRACHYURA ^ Mya arenaria

Hydrobia ^ulvae

D redging could be species-selective in its im p act o n th e m acrofauna, either th ro u g h d irect effects o n recru itm en t and m o rtality rates or, indirectly, th ro u g h changes in h a b ­ itat-in d u ced shifts in species com position. Figure 8 shows the results o f RDAs based o n densities (Fig. 8 A) a n d b io ­ m ass (Fig. 8 B) for th e m o st a b u n d a n t species. Results of the presence frequency analyses are n o t show n, as they are very sim ilar to th e density analyses. T he graphs show the pro jectio n o f th e g rad ien t axes o f th e species descrip­ to r (from low to high values) to g eth er w ith th a t o f th e tw o environm en tal treatm en ts (co n tro l a n d dredged) an d sam pling tim es (t0, h an d t2). T he closeness o f b o th p ro ­ jections o f species an d factor gradients p o in ts to a direct or in d irect relationship betw een th e species descriptors and either th e dredging a n d /o r tim e (a u to n o m o u s tren d ). Species like Cerastoderma edule, Tharyx m arioni an d H ydrobia ulvae seem to be p articu larly n u m ero u s at t0, indicating an a u to n o m o u s tren d , alth o u g h th e first tw o are also related to th e control, w hich indicates a negative im pact o f dredging. Species fo u n d in h igher n u m b ers in the co n tro l plots at t2, such as N ephtys hombergii an d Urothoe poseidonis, m ig h t also be im p acted b y dredging. O n the o th er h an d , for m an y m o re species, th e highest n u m b ers w ere fo u n d in th e dredged area at /y (Arenicola m arina, Lanice conchilega) an d , especially, at t2. A sim ilar tren d can be fo u n d for th e analyzed biom ass data (Fig. 8 B), altho u g h o th er species ap p ear in certain co r­ ners o f th e graph. It sh o u ld be n o te d th a t coincidental

124

-1.5 Fig. 8. Results of

1.5 redundancy

analyses

(RDA)

showing

relations

betw een species, treatm ents and sample dates. (A) RDA plot based on log-transformed species densities. (B) RDA plot based on log-trans­ formed species biomass.

ap pearance o f larger n u m b ers or larger specim ens (higher biom ass) in certain plots at certain dates, especially for low density species, can n o t be discrim inated from real trea tm en t effects in RDAs. Therefore, for fu rth e r detailed statistical analyses, p e r species /--testing w ould be needed. T he series o f t-tests o n individual species (Table 2) show ed m an y species po ten tially affected b y dredging, especially show ing increases in densities o r biom ass. H o w ­ ever, in m u ltip le tests as p erfo rm ed w ith these /--tests, a (conservative) B onferroni correction should be p e r­ form ed, after w hich n o n e o f th e observed differences are really significant. Besides th e negative effects on th e cockle p o p u latio n s, as show n earlier (Figs 4 a n d 5), th e /--tests o n in d ividual species (Table 2) indicated possible negative im pacts o f dredging co m p ared to th e a u to n o m o u s tren d for th ree o th er taxo n o m ic groups. These negative trends are only detected in th e sh o rt term . W hereas an a u to n o ­ m o u s increasing tre n d in densities is observed 6 weeks after th e onset o f fishing for H . ulvae an d th e sub-class o f th e O ligochaeta, b o th w ere decreased in th e dredged area. Arenicola sp., w hich is a special gro u p as it very likely

M arine Ecology 32 (Suppl. 1) (2011 ) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

W i j n h o v e n , E s c a ra v a g e , H e r m a n , S m aa l & H u m m e l

S h o rt a n d m id-long te rm effe cts o f co ck le-d red g in g o n n o n - ta rg e t m a c ro b e n th ic species

T able 2. Possible differences in density a n d /o r biomass developments betw een control (C) and dredged (D) plots for the non-target m acroben­ thic species, from f0 to f, and from f0 to f2, as indicated from paired f-tests w ithout Bonferronl correction. negative effects of dredging species

positive effects of dredging

class

developm ent

P-level

species

class

developm ent

P-level

Gastropoda Clitellata

?D, Tc ?D, ÎC

0.042 0.006

Carcinus maenasa

Malacostraca

=D, Tc

0.054

Polychaeta

ÎD , Î Î C

0.069

Arenicola marina Capitella capitata Pygospio elegansa Streblospio shrubsoliia Urothoe sp.a

Polychaeta Polychaeta

ÎD , Tc ÎD , Tc

0.059 0.016

Polychaeta Polychaeta Malacostraca

ÎD , Tc ÎD , =C ÎD , Tc

0.016 0.030 0.098

Anaitides mucosaa Carcinus maenasa Harmothoe lunulataa Spio sp.

Polychaeta Malacostraca Polychaeta

Tc Tc

0.064 0.054 0.066

Polychaeta

ÎD , =D, Td , Td ,

Crangon crangon Gammarus sp. Gammarus locusta Mya arenaria Nephtys hombergii Platynereis dumerili? Polydora HgnP Scoloplos armiger

Malacostraca Malacostraca Malacostraca Bivalvia Polychaeta

Td , T c TT d , T c TT d , T c T d , TT c Td , T c

0.014 0.054 0.009 0.086 0.097

Polychaeta Polychaeta

TT d , T c TT d , T c

0.049 0.027

Polychaeta

TT d , T c

0.051

density t0-t,

Hydrobia ulvae Oligochaeta biomass f0-fr Arenicola sp

density t0- t2

TT c Tc

0.036

biomass t0- t2

T Decrease; TT stronger decrease than for the other treatm ent of the sam e species;? Increase; TT stronger Increase than for the other treatm ent of the same species; (=) unchanged. P-levels for significant differences after Bonferroni correction are P < 0.0001 for the dom inant species only and P < 0.00002 for all observed species, which w ere achieved by none of the species. aSpecles not belonging to the 10 m ost dom inant species In densities or biomass in one of the treatm ent x time combinations.

represents sm all individuals an d b o d y parts o f A. m arina, ten d ed to increase less in th e dredged area th a n in the co n tro l area (P < 0.1). In co n trast to th e th ree g roups th a t m ig h t be affected negatively b y dredging in th e sh o rt term , there are six species show ing a n increase after dredging in th e sh o rt term . T he biom asses o f A . m arina, Capitella capitata, Pygospio elegans, Streblospio shrubsolii an d Urothoe sp. ap p ear to increase d u rin g th e first 6 weeks after the onset o f dredging, w hereas th e opposite o r at least no increase was fo u n d in th e co n tro l area. For Carcinus maenas, th e a u to n o m o u s decreasing tre n d in density was n o t observed in th e dredged area. The differ­ ence (P < 0.1 in th e t-test) betw een th e treatm en ts for C. maenas was still observable after 1 year. M any m o re species show an increase after dredging in the m id -lo n g term . A naitides mucosa, H arm othoe lunulata an d Spio sp. did n o t show a decreasing tre n d o r such a stro n g decreasing tre n d in density in th e dredged area as in the co n tro l area after a year. F urther, seven species app ear to show a stro n g er increase in biom ass in the dredged area th a n in th e co n tro l area in th e m id -lo n g

Marine Ecology 32 (Suppl. 1) (2011) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

term , an d th e decreasing tre n d in M ya arenaria biom ass seem s to be less stro n g in th e dredged area th a n in the co n tro l area. W hereas m o st species th a t ten d ed to increase after dredging belong to th e polychaetes, there are also several m alacostracans as well as M . arenaria, w hich is a bivalve.

D iscussion Selective fisheries o n large cockles O u r stu d y dem o n strates th e efficiency o f th e fishing p ro ­ cess w ith a clear red u ctio n o f th e larger sized (>23 m m ) cockles in th e dredged areas. T his observation confirm s, a p a rt fro m th e visual observation o f dredging tracks on th e experim ental areas, th a t fishing effectively to o k place o n th e dredged experim ental plots. P artial recovery of th e cockle p o p u latio n was observed after th e fishing. R ecru itm en t an d grow th o f th e cockles occurred in the dredged areas, b u t th e average size o f th e cockles was still sm aller after 1 year w hen com p ared to th e co n trol

125

S h o rt a n d m id -long te rm effe cts o f co ck le-d red g in g o n n o n - ta rg e t m a c ro b e n th ic species

W i j n h o v e n , E sc a ra v a g e , H e r m a n , Smaal & Hummel

areas. N o effect o f dredging was detected o n sm aller sized cockles. The failure to detect an y effect o n th e sm all-sized cockles sh o u ld be considered, taking into acco u n t th e low pow er o f th e test, w hich is insensitive to differences o f less th a n 85%. A th o ro u g h analysis addressing the effects o n sm aller sized cockles w ould require larger sam pling surfaces to reduce th e variance in th e d ata a n d thereby increase th e discrim in ato ry pow er o f the test. W h eth er dredging influences cockle re cru itm en t, as suggested b y P iersm a et al. (2001), could n o t be d eter­ m ined, as n o large settlem ent occurred d u rin g th e exper­ im ent. B eukem a & D ekker (2005) suggest th a t negative effects o f dredging o n cockle rec ru itm e n t m ostly occur in sedim ents w ith very low m u d content, w here d red g ­ ing m ig h t ind u ce a fu rth er re d u c tio n o f th e fine m aterial in the sedim en t below values req u ired for th e cockles. In the case o f th e p resen t stu d y area, w here sed im en t is rath er m uddy, this effect is therefore n o t expected to be o f great im portance. M oreover, th e presen t stu d y did n o t find an y effect o f dredging o n m ed ian grain size, despite the pow er o f th e tests used to detect differences being large. N atu ral tem p o ral v ariatio n in m ed ian grain size m ig h t have a bigger im p act th a n dredging in th e investigated area.

Effects on the environment As indicated above, dredging m ig h t affect th e co m p o si­ tio n o f the env iro n m en t, a n d th e to p layer o f th e sedi­ m e n t in particular. O n th e o th er h an d , sedim ent d isturbance can also lead to an increased availability of n u trien ts in the to p sed im en t layer or w ater layer (Kaiser et al. 2002; W arn k en et al. 2003; N ayar et a í 2007), espe­ cially in areas w ith relatively low w ater tu rb u len ce an d cu rren t velocities. Sedim ent d isturbance can u n d o sedi­ m e n t co m p actio n a n d increase sed im en t aeratio n o r porew ater renew al (Falcâo et al. 2006). Increased n u trie n t availability can also lead to a n oxygen decrease due to increased m icrobial activities (R iem an n & H o ffm an n 1991). T he fo rm a n d d ep th o f d istu rb an ce a n d th e type o f en v iro n m en t are crucial for w h eth er dredging will have a negative effect o n certain m acro b en th ic species an d w hether certain m acro b en th ic species m ig h t profit. Irrespective o f these p o ten tial im pacts, o u r study failed to detect a n effect o f dredging o n m ed ian grain size, although th e pow er to detect differences was large. This is in contrast to findings in th e W ad d en Sea, w here changes in m ed ian grain size a n d silt c o n te n t were rep o rted in areas th a t w ere fished for cockles, although the role o f w in ter storm s an d th e vicinity o f m ussel beds w ere also considered relevant factors (Piersm a et a í 2001).

126

Effects on communities and non-target species In th e presen t case, n o severe enviro n m en tal im p act (o n either density o r biom ass) o f dredging was detected in the sh o rt-te rm observations. M oreover, m id -lo n g te rm sam ­ pling show ed a slight increase for b o th densities a n d b io ­ m ass in th e dredged area, leading to larger biom ass com pared to th e co n tro l area after 1 year. This difference in biom ass m ostly resulted fro m a decrease in th e control area (a u to n o m o u s developm ent), w hich seem ingly was co m pensated b y an increase in th e dredged area. The h igher biom ass in th e dredged areas was n o t d u e to a few d o m in a n t species th a t m ig h t benefit fro m th e d isturbed conditions, b u t to m an y species, as show n b y th e parallel increase in species richness an d species diversity u n d er steady levels o f evenness. Even in such a situ atio n , w ith increasing biom ass, spe­ cies richness a n d species diversity, one can argue a b o u t w hether this is a positive or negative developm ent, as cer­ ta in species m ig h t be favored above others, an d som e spe­ cies m ig h t be reduced. T herefore we also focused on im pacts o n th e in d ividual species. W ith respect to th e in d i­ vidual species, only th ree sp ecies/g ro u p s show ed a re d u c­ tio n o n th e sh o rt term , i.e. w ith recovery w ith in a year. O ne o f th e negatively im p acted species was th e gastropod Hydrobia ulvae, in accordance w ith Ferns et al. (2000), w ho show ed a depletion o f th e H . ulvae p o p u latio n s u n d er th e influence o f m echanical cockle harvesting. In th e pres­ ent study. H. ulvae was th e m o st n u m ero u s species, w hich could positively affect th e diversity indices in th e dredged areas. This species is also an im p o rta n t fo o d source for sev­ eral o th er species (M end on ça et a l 2007). P revious studies have show n possible negative effects o f dredging o n sm aller w orm s (C raeym eersch & H u m m el 2004; Ens et al. 2004), in concordance w ith th e re d u ctio n o f oligochaetes observed in th e presen t stu d y u n d e r the influence o f dredging. O th er studies suggested th e o p p o ­ site response, i.e. an increase o f d o m in an ce b y w orm s as a result o f sed im en t disturbances o r increased n u trie n t availability in th e e n v iro n m en t (Reise 1982; Kaiser et al. 2002). T he positive response o f several w o rm species [i.e. Arenicola m arina, Capitella capitata, Pygospio elegans, Streblospio shrubsolii, N ephtys hombergii, Platynereis dum erilii, Polydora ligni, Scoloplos armiger) as observed in th e presen t ex perim ent m ig h t ind eed p o in t to a shift tow ards w o rm d o m in an ce in th e d istu rb ed conditions after th e dredging. In this respect, it is su rprising th a t oli­ gochaetes, w hich are k n o w n to b e th e first to colonize a n d d o m in a te in deterio rated co n d ition s (Ysebaert et al. 2003; W ijn h o v en et al. 2008), show ed decreased abundances in o u r study. Several M alacostraca species [i.e. Carcinus maenas, Urothoe sp., Crangon crangon, G am m arus sp., G amm arus

M arine Ecology 32 (Suppl. 1) (2011 ) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

W i j n h o v e n , E s c a ra v a g e , H e r m a n , S m aa l & H u m m e l

S h o rt a n d m id-long te rm effe cts o f co ck le-d red g in g o n n o n - ta rg e t m a c ro b e n th ic species

locusta) also seem to p ro fit in term s o f n u m b ers o r b io ­ m ass from th e new co n d itio n s in th e dredged area. These are m obile species a n d therefore fast colonizers of disturbed areas. T heir increase m ig h t result fro m th e fol­ low ing tw o non-exclusive processes. First, th ey m ig h t p ro fit fro m a n increased fo o d availability, i.e. th e p res­ ence o f dam aged a n d dead organism s (large m acro fa­ una) in the dredged en v iro n m en t o n w hich they can scavenge. Secondly, th e increase in space availability due to the dredging (w ith rem oval o f cockles) m ig h t sustain the observed increase o f th e m alacostracans. T he h y p o th ­ esis o f increased space availability as a result o f the dredging m ig h t also explain th e a tte n u atio n in the decrease (a u to n o m o u s tren d ) o f th e bivalve M ya arena­ ria th a t is observed in th e dredged area w h en com p ared w ith th e control area. O u r hypothesis o f decreased co m ­ p etitio n a n d /o r increased space availability for n o n -ta r­ get species seem s to be su p p o rte d b y th e p artial co m pensation o f th e fished-aw ay cockle biom ass b y b io ­ m ass o f n o n -targ et species a n d th e ap p a re n t slight accel­ eratio n in grow th o f th e cockles rem ain in g in the dredged area. The present stu d y did n o t detect an y negative effect on bivalve species o th er th a n cockles, w hich are, how ever, poten tially influenced b y dredging, as sh o w n b y o th er studies. This result indicates th a t either dredging has no im p act on those bivalves, as they m ain ly in h a b it deeper parts o f the sedim en t (e.g. M . arenaria), o r th a t th e bival­ ves are n o t significantly dam aged after th e processing th ro u g h the dredge w hen they are re tu rn e d to th e sedi­ m e n t (e.g. M acom a balthica). T he equivocal effects o f the dredging on Arenicola sp. an d A. marina sh o u ld be in te r­ p reted as a m ethodological artifact, because Arenicola sp. m ostly consists o f juveniles an d in com plete p arts of A. m arina, no o th er Arenicola species being observed in the research area. The use o f th e t-test w ith im p ro v ed sensitivity, co m ­ p ared w ith the nested A N O VA, b y a n increase o f the degrees o f freedom (n o d istin ctio n betw een th e plots) m ad e it possible to reject th e hypothesis th a t large-scale negative effects o n m acro fau n a density, biom ass an d diversity w ould result fro m th e dredging in th e investi­ gated area. Actually, only tw o g roups (H. ulvae a n d the oligochaetes) show ed a negative effect o f dredging in the sh o rt term in this experim ent, an d th e differences were n o t significant (ANOVA, P > 0.05). T his also accounts for th e range o f species th a t show ed positive effects of dredging on the sh o rt a n d m id -lo n g term . F rom this, it can be concluded th a t th ere was n o negative im p act on the w hole range o f species, w ith th e exception o f the tw o groups ju st m en tio n ed . W h eth e r som e species m ig h t have benefitted fro m th e dredging rem ains u n su b sta n ti­ ated.

Marine Ecology 32 (Suppl. 1) (2011) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

Consequences o f the cu rren t design A lthough th e cu rre n t stu d y was able to show , or ru le out, significant differences in th e developm ent o f certain param eters w ith a reasonable statistical pow er, th e u n b al­ anced design is n o t ideal. A pairw ise experim ental design w ith as m an y u n d red g ed as dredged plots w o u ld increase th e pow er o f th e tests a n d w o u ld m ake detectio n o f sm al­ ler differences in developm ent betw een th e treatm ents possible w ith o u t increasing th e to tal n u m b e r of p lo ts/sam p les. As th ere is a large v ariatio n betw een plots an d less v ariatio n w ith in plots, th e pow er can be increased th e m o st b y increasing th e n u m b e r o f plots, ra th e r th a n increasing th e n u m b e r o f sam ples w ithin plots.

Cockle fisheries in a broader context U n d e r th e cond itio n s in th e presen t experim ent, it can be concluded th a t th e im p act o f dredging o n n o n -ta rg et spe­ cies a n d th e sed im en t did n o t ap p ear to be overly d estruc­ tive in th e m id -lo n g te rm an d therefore likely also n o t in th e longer term . T he negative effects observed for a few species in th e sh o rt te rm w ere n o t detected in th e m idlong term , even w ith th e m o st sensitive tests. T he results th u s indicate th a t in th e longer term , effects o n n o n -ta rg et species o f cockle fisheries such as carried o u t in this study are n o t to be expected. O n th e o th er h an d , a longer term effect o n th e cockle p o p u latio n s can n o t be excluded. A lthough th e cockle stock itself recovered after th e dredg­ ing a n d individual grow th was observed, a lag in th e aver­ age size was still detected 1 year later in th e dredged area co m p ared w ith th e con tro l area. A n overview o f som e relevant elem ents th a t can help place th e presen t obser­ vations in a larger context is presented below. T he distance betw een dredged sam ple sites an d u n d red g ed areas varied in this stu d y betw een 1 0 an d 300 m . In previous studies, show ing negative effects of cockle-dredging o n n o n -targ e t species, this distance was larger (H id d in k 2003), an d th u s it m ig h t be argued th at reco lo n izatio n fro m neig h b o rin g areas in o u r stu d y was easier. T he extent o f reco lo n izatio n fro m u n d red ged n eig h b o rin g areas for b o th th e recovery o f th e cockles a n d th e increase in n o n -ta rg e t species was n o t addressed directly in this stu d y because th e u n d red g ed experim ental areas w ere very sm all com pared to th e to tal area dredged. W e believe therefore th a t th e u n d red g ed areas can only have co n trib u ted in a m in o r w ay to th e recolo n ization in th e m u ch larger dredged area. R ecolonization fro m w ithin th e dredged area m ig h t also have been possible, as the dredging in ten sity was n o t u n ifo rm ly d istrib u ted over th e dredged area. H ow ever, satellite tracking system registrations did ind icate th a t u n d istu rb ed p arts were

127

S h o rt a n d m id -long te rm effe cts o f co ck le-d red g in g o n n o n - ta rg e t m a c ro b e n th ic species

W i j n h o v e n , E sc a ra v a g e , H e r m a n , Smaal & Hummel

scarce. T herefore, we conclude th a t reco lo n izatio n only co n trib u ted in a m in o r w ay to th e absence o f significant results o f cockle fisheries o n th e zo o m acro b en th ic co m ­ m unity. T he present stu d y deals w ith th e im p act o f a single dredging event, w hereas m o re disruptive effects o n co m ­ m unities can be reasonably postu lated b y re cu rren t (yearly or even m o re frequent) dredging activities. A t th e m o re disruptiv e in ten sity level, it can be reasonably expected th a t dredging activities m ay p revent th e estab­ lishm ent o f long-living ecostructures such as m ussel/oyster banks a n d seagrass fields, to g eth er w ith th eir associated flora an d fau n a (D ittm a n n 1990; B oström & B onsdorff 2000; Jaram illo et al. 2007). The negative im pact fo u n d b y m an y o th er studies o n a range o f n o n ­ target species could be th e result o f o th er dredging tech ­ niques th a t are m o re destructive (H aii & H ard in g 1997; Ferns et a í 2000) th a n th e hydraulic dredging used in th e present case. Local co nditio n s o f th e fishing area should also be taken in to acco u n t w hen considering th e effects o f fisher­ ies on ben thos. Q ueirós et al. (2006) a n d H id d in k et a l (2007) clearly p o in t a t th e stro n g effect o f h ab itat charac­ teristics such as sed im en t an d p ro d u ctiv ity in relatio n to the sensitivity to dredging disturbances. A co m m o n co n ­ clusion b y b o th papers was th a t th e degree o f n atu ra l dis­ tu rb an ce determ ines th e degree o f sensitivity to fishing activities. It is th u s possible th a t co m m u n ities o f sandy substrates as in th e W ad d en Sea are differentially sensitive to disturbances com p ared w ith co m m u n ities fo u n d o n m u d d y sedim ents, as in o u r study. This could explain th e differences betw een th e negative im pacts o f cockle fisher­ ies fo u n d in th e W ad d en Sea (Piersm a et a í 2001) an d the absence o f significant results in o u r area. H owever, the relationship w ith th e m u d c o n ten t is n o t consistent, as effects o f fisheries, as ind icated b y Q ueirós et a l (2006), w ere m o re negative o n th e m u d d ie r areas, w hereas in o u r m u d d y area n o significant effects could be found. F u rth er studies sh o u ld focus m o re o n these aspects. Several studies also show negative effects of dredging o n th e bivalve re cru itm en t (P iersm a et al. 2001; H id d in k 2003). In th e absence o f massive bivalve re c ru it­ m e n t in th e area d u rin g th e research perio d , n o con clu ­ sion can be draw n relative to th e effect o f dredging o n the recru itm en t fro m th e presen t study. F rom the results o f o u r stu d y we conclude th a t su stain ­ able cockle fisheries m ay be possible, taking in to consider­ atio n th e abov e-m en tio n ed aspects. T he sensitivity an d the recovery p o ten tial o f a dredged area, am o n g st o th er factors related to th e type o f h ab ita t an d pro b ab ly also to the p erio d o f n o n -d istu rb an ce, sh o u ld be specified o n the basis o f adequate field-experim ents, preferably using a BACI approach.

128

A c k n o w le d g e m e n t s W e w o u ld like to th a n k th e research assistants o f the M o n ito r Taskforce (N IO O -C E M E ) for sam pling and m acro fau n a d eterm in atio n . T hanks to th e crew o f the ships YE172, YE98 a n d YE42, a n d to Joke K estelooH endrikse an d D ouw e v an de E nde (IMARES) for th eir assistance d u rin g th e fieldw ork. T he research has been executed in th e fram e o f th e ‘P roject Research Sustain­ able Shellfish Fisheries’ (PR O D U S), an d we w ould like to th a n k th e ‘C ooperative P roducers O rg an izatio n o f the D u tch Cockle Fisheries’ a n d Jaap H olstein in p articular for th eir co operation. T hanks to th e organizing co m m it­ tee o f th e 44th EMBS 2009, w ho gave us th e o p p o rtu ­ n ity to presen t a n d discuss this study. T his is p u b licatio n 4892 o f th e N etherlands In stitu te o f Ecology (N IO O -K N A W ), a n d M o n ito r Taskforce P u b lication Ser­ ies 2 0 1 0 - 1 0 .

References Beukem a J.J. ( 1995) L ong-term effects o f m echanical harvest­ ing o f lugw orm s Arenicola marina on the zoobenthic co m m unity o f a tidal flat in the W adden Sea. Netherlands

Journal o f Sea Research, 33, 219-227. Beukem a J.J., Cadée G.C. (1999) An estim ate o f the sustainable rate o f shell extraction from the D utch W adden Sea. Journal

o f Applied Ecology, 36, 49-58. Beukem a J.J., Dekker R. (2005) Decline o f recruitm ent success in cockles and other bivalves in the W adden Sea: possible role o f clim ate change, p redation o n postlarvae a n d fisheries.

Marine Ecology Progress Series, 287, 149-167. B oström C., B onsdorff E. (2000) Z oobenthic com m unity establishm ent a n d habitat com plexity - the im portance o f seagrass shoot-density, m orphology a n d physical disturbance for faunal recruitm ent. Marine Ecology Progress Series, 205, 123-138. Clarke K.R., W arw ick R.M. (2001) Change in Marine Commu­

nities: an Approach to Statistical Analysis and Interpretation, 2nd edn. PRIM ER-E, Plym outh: 178 pp. Coosen J., Twisk F., V an der Tol M .W .M ., Lam beck R.H.D., V an Stralen M.R., M eire P.M . (1994) Variability in stock assessm ent o f cockles ( Cerastoderma edide L.) in the O osterschelde (in 1980-1990), in relation to environm ental factors. Hydrobiologia, 282/283, 381-395. C otter A.J.R., W alker P., Coates P., C ook W ., D are P.J. (1997) Trial o f a tractor dredger for cockles in Burry Inlet, South W ales. ICES Journal o f Marine Science, 54, 72-83. Craeym eersch J.A., H um m el H . (2004) Effectonderzoek kokkel-

visserij Voordelta. R IV O -rapport C 012/04, RIVO, Yerseke, The N etherlands: 41 pp (in D utch). D ittm an n S. (1990) M ussel beds - am ensalism or am eliora­ tio n for intertidal fauna? Helgoländer Meeresunters, 44, 335-352.

M arine Ecology 32 (Suppl. 1) (2011 ) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

W i j n h o v e n , E s c a ra v a g e , H e r m a n , S m aa l & H u m m e l

S h o rt a n d m id-long te rm effe cts o f co ck le-d red g in g o n n o n - ta rg e t m a c ro b e n th ic species

Ens B.J., Smaal A.C., De Vlas J. (2004) The Effects o f Shellfish Fishery on the Ecosystems o f the Dutch Wadden Sea and Oosterschelde; Final report on the Second Phase o f the Scientific Evaluation of the Dutch Shellfish Fishery Policy (EVA II). Alterra-rapport 1011, RIVO-rapport C056/04, RIKZ-rapport RKZ/2004.031, Wageningen, The Nether­ lands: 2 1 2 pp. Falcâo M., Caetano M., Serpa D., Gaspar M., Vale C. (2006) Effects of infauna harvesting on tidal flats of a coastal lagoon (Ria Formosa, Portugal): implications on phosphorus dynamics. Marine Environmental Research, 61, 136-148. Ferns P.N., Rostron D.M., Siman H.Y. (2000) Effects of mechanical cockle harvesting on intertidal communities. Journal of Applied Ecology, 37, 464-474. Geurts van Kessel A.J.M., Kater B.J., Prins T.C. (2003) Verand­ erende draagkracht van de Oosterschelde voor kokkels. Rap­ portage van Thema’s 2 en 3 uit het ‘Lange Termijn Onderzoeksprogramma Voedselreservering Oosterschelde’, in het kader van de Tweede Evaluatie van het Nederlands Schelpdiervisserijbeleid, EVA II. Rapport RIKZ/2003.043, RIVO rapport C062/03, Middelburg, The Netherlands: 128 pp. (in Dutch). Hall S.J., Harding M.J.C. (1997) Physical disturbance and m ar­ ine benthic communities: the effects o f mechanical harvest­ ing of cockles on non-target benthic infauna. Journal of Applied Ecology, 34, 497-517. Hiddink J.G. (2003) Effects of suction-dredging for cockles on non-target fauna in the W adden Sea. Journal o f Sea Research, 50, 315-323. Hiddink J.G., Jennings S., Kaiser M.J. (2007) Assessing and predicting the relative ecological impacts of disturbance on habitats with different sensitivities. Journal o f Applied Ecol­ ogy, 44, 405-413. Jaramillo E., Contreras H., Duarte C. (2007) Community structure of the macroinfauna inhabiting tidal flats charac­ terized by the presence of different species of burrowing bivalves in Southern Chile. Hydrobiologia, 580, 85-96. Kaiser M.J., Broad G., Hall S.J. (2001) Disturbance of intertidal soft-sediment benthic communities by cockle hand raking. Journal of Sea Research, 45, 119-130. Kaiser M.J., Collie J.S., Hall S.J., Jennings S., Poiner I.R. (2002) Modification of marine habitats by trawling activi­ ties: prognosis and solutions. Fish and Fisheries, 3, 114— 136. Leitâo F.M.S., Gaspar M.B. (2007) Immediate effect of inter­ tidal non-mechanised cockle harvesting on macrobenthic communities: a comparative study. Scientia Marina, 71, 723-733. Leopold M.F., Dijkman E.M., Cremer J.S.M., Meijboom A., Goedhart P.W. (2004) De effecten van mechanische kokkelvisserij op de benthische macrofauna en hun habitat. Eindverslag EVA II (Evaluatie Schelpdiervisserij tweede fase), Deelproject

Marine Ecology 32 (Suppl. 1) (2011) 1 17 -12 9 © 2011 Blackwell Verlag GmbH

C l/3 . Alterra-rapport 955, Wageningen, The Netherlands: 146 pp. (in Dutch). M endonça V.M., Raffaelli D.G., Boyle P.R. (2007) Interactions between shorebirds and benthic invertebrates at Culbin Sands lagoon, NE Scotland: effects o f avian predation on their prey comm unity density and structure. Scientia Marina, 71, 579-591. Nayar S., Miller D.J., H unt A., Goh B.P.L., Chou L.M. (2007) Environmental effects of dredging on sediment nutrients, carbon and granulometry in a tropical estuary. Environmen­ tal Monitoring and Assessment, 127, 1-13. Piersma T., Koolhaas A., Dekinga A., Beukema J.J., Dekker R., Essink K. (2001) Long-term indirect effects o f mechanical cockle-dredging on intertidal bivalve stocks in the Wadden Sea. Journal o f Applied Ecology, 38, 976-990. Queirós A.M., H iddink J.G., Kaiser M.J., Hinz H. (2006) Effects o f chronic bottom trawling disturbance on benthic biomass, production and size spectra in different habitats. Journal of Experimental Marine Biology and Ecology, 335, 91-103. Reise K. (1982) Long-term changes in the macrobentric inver­ tebrate fauna o f the W adden Sea: Are polychaetes about to takeover?. Netherlands Journal of Sea Research, 61, 29-36. Riemann B., Hoffmann E. (1991) Ecological consequences of dredging and bottom trawling in the Limfjord, Denmark. Marine Ecology Progress Series, 69, 171-178. Smith E.P. (2002) BACI design. In: El-Shaarawi A.H., Piegorsch W.W. (Eds), Encyclopedia o f Environmetrics, Vol. 1. John Wiley 8 c Sons, Ltd, Chichester: pp. 141-148. Sokal R.S., Rohlf F.J. (1995) Biometry: the Principles and Practice of Statistics in Biological Research. 3rd edn. W.H. Freeman and Company, New York: 887pp. Ter Braak C.J.F., Smilauer P. (1998) CANOCO Reference M an­ ual and User’s Guide to Canoco for Windows. Software for Canonical Community Ordination (Version 4). Centre for Biometry Wageningen, The Netherlands: 351pp. W arnken K.W., Gili G.A., Dellapenna T.M., Lehman R.D., Harper D.E., Allison M.A. (2003) The effect of shrimp trawling on sediment oxygen consum ption and the fluxes of trace metals and nutrients from estuarine sediments. Estuariae, Coastal and Shelf Science, 57, 25-42. W ijnhoven S., Sistermans W., H ummel H. (2008) Historic developments in macrozoobenthos of the Rhine-Meuse estuary: from a tidal inlet to a freshwater lake. Estuarine, Coastal and Shelf Science, 76, 95-110. Ysebaert T., Herman P.M.J., Meire P., Craeymeersch J., Verbeek H., Heip C.H.R. (2003) Large-scale spatial patterns in estuaries: estuarine macrobenthic communities in the Schelde estuary, NW Europe. Estuarine, Coastal and Shelf Science, 57, 335-355. Zwarts L. (2004) Bodemgesteldheid en mechanische kokkelvisserij in de Waddenzee. Rapport RIZA/2004.028, Lelystad, The Netherlands: 129 pp. (in Dutch).

129

marine ecology

an evolutionary perspective

»

Marine Ecology. ISSN 0173-9565

O R I G I N A L ARTI CLE

Charles Darwin and m arine biology Philip S. R a in b o w Departm ent of Zoology, Natural History Museum, London, UK

K eywords Barnacle; Beagle; coral reefs; Darwin; Grant; Lyell; transm utation; unlformltarlanlsm. C orrespondence Philip S. Rainbow, Departm ent of Zoology, Natural History Museum, London SW7 5BD, UK. E-mail: p.ralnbow@ nhm.ac.uk Accepted: 17 November 2010 doi : 10.1111/j. 1439-0485.2010.00421 .x

Abstract In a celebration o f th e 200th anniversary o f his b irth in 1809, this sh o rt essay explores th e influence o f m arin e biology o n C harles D arw in, an d vice versa. D arw in m ad e his first forays in to th e w orld o f m arin e biology as a m edical stu ­ d e n t in E din b u rg h fro m 1825 to 1827. H e cam e u n d e r th e influence there o f th e L am arckian R obert G rant, an d developed an u n d e rsta n d in g o f th e sim ple org an isatio n o f th e early developm ental stages o f m arin e invertebrates. Yet D a r­ w in balked at L am arckian tran sm u ta tio n . T he voyage o f th e Beagle led to D a r­ w in ’s perceptive th eo ry o f th e origin o f coral reefs, an o rigin still m ainly accepted today. This th eo ry was steeped in th e u n ifo rm itarian ism o f th e geolo­ gist Lyell, dep en d in g o n th e slow, gradual grow th o f billions o f coral polyps keeping pace w ith slow sinking o f land to p ro d u ce a n atoll. P rom 1846 to 1854 D arw in revolutionised th e u n d e rstan d in g o f barnacles, p ro d u cin g m on ographs still relevant today. H is barnacle studies gave h im th e credibility to p ro n o u n ce o n th e origin o f species; he fo u n d great v ariatio n in m o rphology, a n d a series o f related species w ith rem arkable rep ro d u ctiv e a d a p ta tio n cu lm in atin g in the presence o f dw arf males. Barnacles show ed h im an ev o lutionary narrative laid o u t before him , an d c o n trib u ted greatly to his qualification an d confidence to w rite w ith a u th o rity o n th e origin o f species.

B orn in Shrew sbury o n 12 P ebruary 1809, C harles R obert D arw in could hard ly have been said to have h ad th e sea in his blood, b u t as a child he was an inveterate collector o f objects such as shells an d b ird s eggs a n d developed an early in terest in n atu ra l history. By his teens, h u n tin g had b ecom e C harles’ passion, an d in 1825 his exasperated father, the well respected local d o c to r R obert D arw in, cam e to u tte r th e o ft-q u o ted p red ic tio n ‘Y ou care for n o th in g b u t shoo tin g , dogs, a n d rat-catching, an d y o u will be a disgrace to y ourself an d all y o u r fam ily’ (D es­ m o n d & M oore 1991). S trong a ctio n was needed to h alt C harles’ aim less w ay o f life an d so, follow ing his father and elder b ro th e r E rasm us, m edicine was chosen as th e required rem edy. In O ctober 1825, C harles D arw in, aged 16, fo u n d him self enrolled in th e U niversity o f E din b u rg h to study m edicine, accom panied for th e first year b y Erasm us w ho, alth o u g h a m edical stu d e n t at C am bridge, was able

130

to carry o u t his external hospital stu d y in E dinburgh (D esm o n d & M o o re 1991). Charles, how ever, becam e disillusioned w ith his m edical studies as he experienced th e dru d g ery o f his lectures a n d p o o r quality o f his lec­ turers, an d th e n th e distress o f clinical studies w ith associated b lo o d , gore a n d suffering. Initial diligence gave w ay to th e sam pling o f stu d en t life. O n his ow n in his second year, D arw in fo u n d a diversion in m arine biology. In N ovem ber 1826, C harles D arw in jo in ed th e P linian Society, an u n d erg rad u ate gro u p discussing n a tu ral h is­ to ry an d an tiq u a ria n researches, an d occasionally going o n collecting expeditions together. T his p roved a safety valve fro m m edicine, and, over th e academ ic year, D arw in accom panied his P lin ian friends o n zoological walks on th e shores o f th e F irth o f F orth, a n d v en tu red o u t on traw lers fishing at sea. H e becam e fam iliar w ith a h o st o f m arin e invertebrates previously strange to him , including

M arine Ecology 32 (Suppl. 1) (2011 ) 1 30 -13 4 © 2011 Blackwell Verlag GmbH

Rainbow

sponges, soft corals (A lcyonium d igitatum ), sea slugs ( Tritonia hombergi), polychaetes (the sea m o u se Aphrodite aculeata) and bryozoans (Flustra foliacea). A t this tim e D arw in cam e u n d e r th e influence an d m en to rsh ip o f a m a n w ho w ould be key to th e later developm ent o f D arw in ’s ideas o n evolution. R obert E dw ard G rant was a m arin e in vertebrate zoologist an d a fellow Plinian, living in E d in b u rg h o n a decreasing legacy fro m his late father (D esm o n d & M oore 1991). G rant becam e D arw in’s unofficial tu to r o n m arin e invertebrates, teaching h im to m ake observations an d to dissect speci­ m ens. T h ro u g h G rant, D arw in developed an u n d e rsta n d ­ ing o f anim al developm ent an d th e sim ple org an isatio n of the early life-history stages o f p articu lar invertebrates. G ran t was a n expert o n sponges recognised b y his peers, as exem plified by th e n am in g o f th e new ly erected sponge genus Grantia in his h o n o u r b y Jo h n Flem ing in 1828; the co m m o n local sponge Spongia compressa, th e purse sponge, becam e Grantia compressa. It was G rant w ho coined the nam e ‘P o rifera’ for th e sponges. A fter w orking w ith G rant, D arw in (aged 18) gave a talk to th e P linian Society o n 17 M arch 1827, show ing th a t the larvae o f the b ry ozo an Flustra foliacea use cilia for lo co m o tio n an d th a t th e black m arkings (sea p ep p e r­ corns) on the shells o f oysters are th e eggs o f th e m arin e leech Pontobdella muricata. A triu m p h for a b u d d in g m arin e biologist b u t, according to D arw in ’s d aughter E lenrietta, D arw in h ad been scooped 3 days earlier by G ran t in a talk to th e m o re form al (graduate) stu d en t society, the W ern erian N atu ral H isto ry Society - a n in tro ­ du ctio n for D arw in to ‘th e jealousy o f scientific m e n ’ (B row ne 1995). G rant, how ever, represented som eth in g m o re - sedition personified (D esm o n d & M oore 1991). G ran t was a fran ­ cophile w ho h ad stu d ied an a to m y a n d em bryology in France w ith G eoffroy Saint-H ilaire. C orrespondingly, G ran t was a Lam arckian, m o re openly so later, for his views w ere still form in g at this tim e. Lam arck (1809) used the term ‘tra n sm u ta tio n ’ for his th eo ry th a t described the altering o f one species in to an o th er. Lam arck did n o t p ropose co m m o n ancestry b u t considered th a t com plex form s tra n sm u tated fro m sim ple form s o f life created contin u o u sly b y sp o n tan eo u s generation. As a L am arck­ ian, G rant arranged life in to chains, considering th a t the origins o f anim als a n d plants lay in th e sim plest form s; an d th a t th e n atu ral o rdering, sim ple to com plex, of sponges represented th e historical o rd er o f ap pearance of sponges. T hus G ran t directly exposed D arw in to evolu­ tio n ary theory, w ith th e associated concepts o f stru ctu ral hom olo gy a n d u n ity o f p lan w ith sim ilar organs present in different anim als. G ran t w en t o n in 1827 to becom e P rofessor o f C om parative A n ato m y for life (1874) a t U n i­ versity College, L ondon. U niversity College h a d been

Marine Ecology 32 (Suppl. 1) (2011) 1 30 -13 4 © 2011 Blackwell Verlag GmbH

C harles D arw in a n d m a rin e biolo g y

fo u n d ed as L o n d o n U niversity in 1826, ad m ittin g stu ­ dents regardless o f religion a n d gender, a secular alterna­ tive to O xford a n d C am bridge. L o n d o n U niversity was clearly a m o re suitable v enue for G ra n t’s seditious views th a n G od-fearing E dinburgh. T he 2 years at E din b u rg h convinced C harles D arw in th a t m edicine was n o t for him , a n d in 1827 he left E din­ b u rg h a disap p o in ted m an: he d id n o t like m edicine, n o r th e m en w ho p u rsu ed it; he h ad fo u n d n o qualities in professors to generate long-lasting respect (even G rant h a d d isap p o in ted h im ); an d he was n o t ready to be a tra n sm u ta tio n ist o r be labelled a radical like his g randfa­ th er, E rasm us D arw in (B row ne 1995). M edicine was n o t for him , b u t he n o w h ad little choice - th e fam ily fell back o n th e typical safety n et for second sons, th e C hurch o f England. So fro m 1827 to 1831, Charles D arw in fo u n d h im self at C h rist’s College at th e U niversity o f C am bridge o n th e first stage o f his jo u rn ey to H oly O rders. T here was still ro o m for n atu ral history, n o w u n d e r th e in flu ­ ence o f Jo h n H enslow , th e P rofessor o f B otany, an d for geology u n d e r th e influence o f A dam Sedgwick, Professor o f Geology. H ow ever, th ere was n o m o re im m ed iate access to m a r­ ine biology for D arw in u n til th e p o rte n to u s year o f 1831. T h en H enslow in tro d u c e d D arw in to R obert FitzRoy, cap tain o f H M S Beagle, w ho subsequently invited to D ar­ w in to jo in a voyage a ro u n d th e w o rld as a self-financing gentlem an naturalist. T he voyage lasted fro m D ecem ber 1831 to O cto b er 1836. D arw in regularly sen t back n atu ral h isto ry an d geology collections w hich gained h im a scien­ tific re p u ta tio n in his absence, an d th e voyage changed his life for ever. In January 1835, D arw in collected m an y specim ens o f a large in tertid al g astro p o d m ollusc o n a shore in th e C ho­ n os archipelago, Chile, a collection n o t considered even w o rth y o f reference in several editions o f D arw in ’s jo u rn al o f th e voyage (D arw in 1839). The m ollusc concerned was a m u ricid g astropod, Concholepas concholepas (as Conc­ holepas peruviana), th e shells o f w hich w ere rid d led w ith cavities co n tainin g m in u te anim als, n o bigger th a n p in ­ heads. These w ere to be later identified as b o rin g b a rn a ­ cles, an d these w ere also destined to affect D arw in’s fu tu re life enorm ously. Before leaving o n th e Beagle, D arw in h ad been greatly influenced b y Sir C harles Lyell, a leading geologist o f the tim e, w ho h ad p ublished th e first ed itio n o f his Principles o f Geology in th ree volum es (1830, 1832, 1833). Lyell was a believer in u n ifo rm itarian ism , a p h ilo so p h y claim ing th a t geological a n d biological forces have always been w orking in th e sam e w ay an d a t th e sam e in ten sity over ages. This view o f u n ifo rm itarian ism was in conflict w ith th e th en-prevailing th e o ry o f catastrophism , w hich con­ sidered th a t th e earth experienced m ajo r changes only as

131

C harles D arw in a n d m arin e biology

a result o f large catastrophic events. A key consideration was w hether th e earth was old enough to experience large-scale changes in any o th er way, b u t Lyell th o u g h t it necessary to create a vast tim e scale for E arth ’s h isto ry to v ouch for fossil rem ain s o f extinct species, excluding su d ­ den geological catastrophes. C harles D arw in shared a su p ­ p o rt for unifo rm itarian ism . T he fo rm atio n o f coral reefs was a lively topic for debate at th e tim e, an d in th e second v olum e (1832) of Principles o f Geology, Lyell h ad explained th e origin of coral atolls as coral reefs grow ing u p fro m th e crater rim s o f und erw ater volcanoes. V olum e 2 was sent o u t to D a r­ w in by his m e n to r an d faithful co rresp o n d en t Professor H enslow , to reach h im in M ontevideo in N ovem ber 1832. D arw in’s observations o n th e Beagle, how ever, h a d co n ­ vinced h im otherw ise. D arw in d rafted an alternative th e ­ ory for the origin o f coral reefs th a t essentially stands today. Lyell accepted it im m ediately. A n essential p o in t in coral reef fo rm atio n is th a t reefbuild in g corals only grow in w ell-lit shallow w aters, su p ­ plying light to th eir sym biotic zooxanthellae, an d could n o t grow up fro m deeper, d ark depths. In D arw in ’s explanation, corals fo rm fringing reefs ju st below low tide along tropical coastlines, an d eventually th e coral reef will grow o u t to becom e a b arrie r reef. D arw in h ad seen th e effects o f earthquakes in Chile an d knew th a t lan d could rise or fall. If th e coast is sinking slowly, th e n th e grow th o f coral could keep pace. If th e land sinks b en eath the waves - an atoll is form ed. H is first h a n d observations in Keeling A toll helped convince h im o f his views. D arw in could see th at, alth o u g h coral reefs w ere huge geological structures on a w orld scale, th ey w ere created b y th e slow, gradual grow th o f billions o f tin y creatures over vast reaches o f tim e. T his was an exam ple o f Lyell’s ‘unifo rm ita ria n ’ principle in action, th e cu m u latio n o f sm all changes over a long perio d , to be repeated in D arw in ’s studies o n earthw orm s years later. Later observations of cores o f coral lim estone to great depths (cu lm in atin g in studies in B ikini A toll in th e 1950s) pro v id ed su p p o rtin g evidence for land sinking at an ap p ro p riate rate - coral could sim ply n o t have grow n u p fro m these depths in th e absence o f light. D arw in publish ed Coral Reefs in 1842 (D arw in 1842). It show ed the tig h t logical stru ctu re to b ecom e evident again in th e Origin o f Species to be p ublished in 1859. O n his re tu rn fro m th e Beagle in 1836, D arw in sou g h t to place his collections w ith experts to identify an d describe th em - n o t altogether an easy task. T he m a m ­ m als w ere placed w ith R ichard O w en - later to fo u n d th e N atural H isto ry M u seu m in S outh K ensington an d vehe­ m ently oppose D arw in ’s views o n evolution. H e avoided R obert B row n (K eeper o f Botany) at th e B ritish M useum w ho h ad been sitting o n a collection o f G alapagos plants,

132

Rainbow

u n stu d ied for 6 years. R obert G rant, n o w in L ondon, volu n teered to help, p articularly w ith ‘low er anim als’, b u t was tu rn e d dow n b y D arw in w ho h ad becom e a com pe­ te n t (an d com peting) coral expert, given his in terest in coral reef form atio n . In fact, ironically, th e corals w ere n o t m o n o g rap h ed . N o r d id D arw in an d G ran t have any­ th in g m o re to do w ith each o th er (D esm o n d & M oore 1991). By O ctober 1846, D arw in th o u g h t th a t he had described all his Beagle specim ens, an d tu rn e d his a tte n ­ tio n to a single rem ain in g barnacle species, th e b o ring barnacles in th e g astro p o d shells collected in S outhern Chile in Jan u ary 1835. T he barnacle was clearly ‘quite new an d cu rio u s’ - he called it th a t ‘ill-form ed little m o n ster’ - certainly ab erra n t a n d th e w o rld ’s sm allest barnacle. D arw in did n o t know how to classify it, refer­ ring to it as ‘M r A rth ro b alan u s’. A new m icroscope was necessary, b u t so was a co m p ariso n w ith ‘m o re n o rm a l’ barnacles. So D arw in started b o rro w in g th e necessary specim ens, an d th e p ro ject grew an d grew as he soon appreciated th e state o f chaos o f th e know ledge o f b a r­ nacles. W h y d id D arw in em bark o n a p roject th a t was to occupy th e next 8 years? D arw in h ad been fo rm ulating his ideas o n v ariatio n an d n atu ral selection, resulting eventually in The Origin o f Species (D arw in 1859), and he agreed w ith th e view o f his b o ta n ist friend Joseph H o o k er th a t n o -o n e h ad a rig h t to exam ine th e questio n o f spe­ cies w ho h ad n o t described m any. So D arw in w ould earn th a t right. Barnacles w ould establish his credentials, an d a th o ro u g h ex am in atio n o f all barnacle varieties could p u t h im in a co m m an d in g p o sitio n w hen discussing n atu ral selection. In fact, as he proceeded, he began to uncover th e m o st ex trao rd in ary proofs o f his n o teb o o k specula­ tions (D esm o n d & M oore 1991). So D arw in stu d ied barnacles (‘m y beloved barnacles’) in his stu d y at D ow n H o u se in K ent fro m 1846 to 1854. H e w ould go o n to deliver a th o ro u g h reappraisal o f b o th living an d fossil barnacles, m o n o g rap h s th a t still co m ­ m a n d th e field to d ay (D arw in 1851a,b, 1854a,b). So w h at are barnacles? Z oological folklore has it th a t Louis Agassiz described a barnacle as ‘n o th in g m o re th a n a little shrim p-like anim al, stan d in g o n its head in a lim e­ stone h o u se a n d kicking food in to its m o u th ’. Barnacles are ind eed crustaceans, crustaceans th a t lack a n ab d o m en a n d w ith a head eno rm o u sly developed as a stalk or, as in th e sessile barnacles, th a t lim estone house o f overcalcified cuticle. D arw in (1851a) drew a diagram (Fig. 1) o f th e relationship betw een th e an ato m y o f a stalked b arnacle (Lepas) an d a d ecapod crustacean (Luci­ fe r ) discussing sim ilarities o r differences in term s o f th e hom ologies o f th e b o d y parts, a conceptual way o f th in k in g w ith w hich he was clearly happy. Typically we

M arine Ecology 32 (Suppl. 1) (2011 ) 1 30 -13 4 © 2011 Blackwell Verlag GmbH

C harles D arw in a n d m a rin e biolo g y

Rainbow

Fig. 1. The diagram drawn by Darwin (1851a) of the relationship betw een the anatom y of a stalked barnacle (Lepas) and a planktonic decapod crustacean (Lucifer) to show the homologies of the external parts (m, mouth).

T able 1. Barnacles and their relatives are members of the class Max­ illopoda, together with the likes of tantulocarids, branchiurans, pentastomids, mystacocarids and copepods (Martin & Davis 2001). Subclass Thecostraca Infraclass Facetotecta Infraclass Ascothoracida Infraclass Cirripedia Superorder Acrothoracica Superorder Rhicocephala Superorder Thoracica Order Pedunculata Order Sessilia

recognize three groups o f cirripede barnacles to d ay (A cro­ thoracica, R hizocephala, T horacica), closely related to tw o o th er taxa, th e A scothoracida an d Facetotecta (Table 1, after M artin & Davis 2001). So w hat was th a t ‘ill-form ed little m o n ste r’ ‘M r A rth ro balan u s’ fo u n d b o rin g in to th e shells o f Concholepas conc­ holepas, collected in so u th ern Chile in Jan u ary 1835? In 1849, H ancock described a b o rin g barnacle fro m th e colu­ m ella o f w helk shells, Buccinum u n d a tu m , occupied by the h erm it crab Pagurus bernhardus - Alcippe (now Try­ petesa) lampas (H an co ck 1849). ‘M r A rth ro b alan u s’ tu rn e d o u t to be a close relative. D arw in (1854a) described it as Cryptophialus m inutus, an d placed b o th species in a new ord er, th e A bdom inalia. T he o rd er was renam ed th e A crothoracica b y G ruvel (1905) because these bu rro w in g barnacles lack an a b d o m en , th e taxon featuring as a su p ero rd er in Table 1. A crothoracicans live in b u rro w s in calcareous rocks an d shells, a n d have a b o d y a n d cirri n o t dissim ilar to th a t o f th e m o re co m ­ m o n thoracicans. D arw in discovered rep ro d u ctiv e m o d es in som e b a rn a ­ cles th a t asto u n d ed him . M o st barnacles are h e rm a p h ro ­ dite, b u t n o t all. D arw in (1851a) discovered th a t different

Marine Ecology 32 (Suppl. 1) (2011) 1 30 -13 4 © 2011 Blackwell Verlag GmbH

species o f th e stalked barnacle genus Scalpellum show ed a g rad ien t fro m com plete h erm ap h ro d itism to h e rm a p h ro ­ dites w ith sm all co m plem ental ‘d w a rf m ales w ith th e lar­ ger ‘h e rm a p h ro d ite’ acting as a fem ale (e.g. Scalpellum scalpellum). W as this an exam ple o f w h at tra n sm u ta tio n m ig h t lo o k like? D arw in (1851a) also discovered th a t the stalked barnacle Ibla cum ingii also has large fem ales w ith sm all co m plem ental males. T he d w arf m ale show s great red u ctio n in fo rm as it becom es specialised for re p ro d u c­ tio n only. T ran sm u tatio n ? T he stu d y o f barnacles indeed pro v id ed C harles D ar­ w in w ith m an y o f th e facts th a t he needed to su p p o rt his ideas o n ev olution - b o th th ro u g h com parative a n a to m y an d th ro u g h th e stu d y o f fossils. W h a t D arw in fo u n d in his barnacles (S to tt 2003) was variation b eyond his w ildest im aginings, a n d rep ro d u ctiv e m odes th a t to o k his b reath away, w ith th e developm ent of com plem ental m ales living parasitically o n th e female, n o m o re th a n rep ro d u ctiv e sacs o f sperm , w ith no heads, stom achs or digestive systems. Barnacles had a d ap ted to th eir enviro n m ents a n d an evolutionary n a r­ rative b ran ch ed o u t before his eyes (S to tt 2003). D ar­ w in ’s barnacles show ed h im w h at tra n sm u ta tio n could lo o k like. Bit b y bit, each ap p aren tly trivial a d ap ta tio n in living stru ctu re accum ulated, one after an o th er, u n til anim als becam e so d istin ct fro m th eir p aren ts an d cous­ ins th a t they could be called a different species (B row ne 1995). W hile D arw in m ad e fu n d am en tal c o n trib u tio n s to the stu d y o f coral reefs an d barnacles, clearly in re tu rn , m a r­ ine biology co n trib u ted m u ch to D arw in ’s developm ent o f evolutionary thinking. T he in teractio n o f m arin e b io l­ ogy an d th e intellect o f D arw in was key to th e develop­ m e n t o f his su p rem e c o n trib u tio n to biology - the m ech an ism o f n a tu ra l selection acting o n n atu ral varia­ tio n to explain th e origin o f species an d th e ev olution of organism s.

A c k n o w le d g e m e n t s T his essay results fro m an invited lecture given at the 44th E u ro p ean M arin e Biology Sym posium in Liverpool in 2009 in acknow ledgem ent o f th e 200th anniversary of th e b irth o f C harles D arw in. T he lecture a ttem p ted to b rin g D arw in’s specific c o n trib u tio n s in m arin e biology to a w ide au dience o f m arin e biologists, p erh ap s u n d e r­ standably only aw are o f D arw in ’s hugely significant con­ trib u tio n o f n a tu ral selection as a m echanism u n d erp in n in g evolution. I am in d eb ted to Professor C hris Frid for th e invitation. It will com e as n o surprise to readers th a t this is n o t a p a p er o f original scholarship, b u t sim ply a secondary co m p ilatio n fro m excellent w orks o f real biographical scholarship p ublished o n C harles

133

C harles D arw in a n d m arin e biology

D arw in. I have leant heavily o n th e o u tstan d in g b io g ra­ phies by Janet B row ne (1995, 2002) an d b y A d rian D es­ m o n d and Jam es M o o re (1991), to w h o m interested readers are referred. Rebecca S tott (2003) has p ro d u ced a fascinating acco u n t o f th e barnacle years w hich d o m i­ nated the life o f D arw in an d his fam ily a t D ow n H ouse from 1846 to 1854.

R eferences Browne J. ( 1995) Charles Darwin: Voyaging. Jonathan Cape, London: 605 pp. Browne J. (2002) Charles Darwin: The Power o f Place. Jonathan Cape, London: 591 pp. Darwin C.R.. (1839) Journal o f Researches into the Geology and Natural Histoiy o f the Various Countries Visited by H.M.S. Beagle etc.. Henry Colburn: London: 629 pp. Darwin C.R. (1842) The Structure and Distribution o f Coral Reefs. Part 1 o f The Geology o f the Voyage o f the Beagle etc. Smith Elder and Co., London: 214 pp. Darwin C.R. (1851a) A Monograph on the Subclass Cirripedia. Vol.l The Lepadidae. Ray Society, London: 400 pp. Darwin C.R. (1851b) A Monograph on the Fossil Lepadidae, or, Pedunculated Cirripedes o f Great Britain. Palaeontographical Society, London: 88 pp.

134

Rainbow

Darwin C.R. (1854a) A Monograph on the Subclass Cirripedia. Vol.2 The Balanidae, The Verrucidae, etc.. Ray Society, Lon­ don: 684 pp. Darwin C.R. (1854b) A Monograph on the Fossil Balanidae and Verrucidae o f Great Britain. Palaeontographical Society, Lon­ don: 44 pp. Darwin C.R. (1859) On the Origin o f Species by Means of N atu­ ral Selection, or the Preservation o f Favoured Races in the Struggle for Life. John Murray, London: 502 pp. Desmond A.J., Moore J.R. (1991) Darwin. Michael Joseph, London: 808 pp. Gruvel A. ( 1905) Monographie des Cirrhipèdes ou Thécosracés. Masson et Cie, Paris: 472 pp. Hancock A. (1849) Notice of the occurrence on the British coast o f a burrowing barnacle belonging to a new order of the class Cirripedia. Annals and Magazine of Natural History, 4, 305-314. Lamarck J.-B. (1809) Philosophie Zoologique, ou Exposition des Considérations Relatives à l’Histoire Naturelle des Animaux. Dentu et l’Auteur, Paris: 422 pp. M artin J.W., Davis G.E. (2001) An updated classification of the recent Crustacea. Natural History Museum o f Los Angeles County Contributions in Science. 39, 1-124. Stott R. (2003) Darwin and the Barnacle. Faber and Faber, London: 309 pp.

M arine Ecology 32 (Suppl. 1) (2011 ) 1 30 -13 4 © 2011 Blackwell Verlag GmbH