Physiological Entomology (2004) 29, 169–175
Reproductive responses to photoperiod and temperature by diapausing and nondiapausing populations of Sesamia nonagrioides Lef. (Lepidoptera – Noctuidae) A R G Y R O A . F A N T I N O U 1 , D I O N Y S S I O S C H . P E R D I K I S 2 and KONSTANTINA F. ZOTA1 1
Laboratory of Ecology and Environmental Sciences and 2Laboratory of Agricultural Zoology and Entomology, Agricultural University of Athens, Athens, Greece Abstract. The influence of long- and short-day cycles on ovipostion and egg hatch of the corn stalk borer, Sesamia nonagrioides were investigated at a range of temperatures. Oviposition was suppressed when insects are exposed to long days through their immature stages and then transferred to short days after mating. Moreover, mean oviposition and egg hatch increased from 15 to 27.5 C, whereas oviposition declined significantly at 30 C at both photoperiodic regimes. Females derived from a diapausing population exposed to long days after mating showed a significantly higher egg production compared to females derived from a nondiapausing population. However, when females from a diapausing population were left to oviposit under short days, fewer eggs were produced compared to those exposed to long days after mating. Thus, photoperiod appears to affect reproductive traits of this species in a quantitative manner. Larval diapause duration is positively correlated with fecundity of the adults. There is also a positive correlation between pupal weight of individuals derived from a diapausing population and the postdiapause fecundity of adults. Key words. Diapause duration, egg hatch, oviposition rate, photoperiod, reproduction, Sesamia nonagrioides, temperature.
Introduction The corn stalk borer Sesamia nonagrioides (Lepidoptera: Noctuidae) is distributed across southern Europe, has multiple generations (three to four) and overwinters in the larval stage (Eizaguirre et al., 1994; Fantinou et al., 1995). According to Gillyboeuf et al. (1994) and Fantinou et al. (1996), overwintering larvae suffer high mortality, but those that survive pupate in spring. Adults emerge from late March to May and mated females oviposit in the leaf
Correspondence: Dr A. A. Fantinou, Agricultural University of Athens, Laboratory of Ecology and Environmental Sciences, Iera Odos 75, 188 55 Athens, Greece. Tel.: þ32 10 5294404; fax: þ32 10 5294462; e-mail:
[email protected]
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2004 The Royal Entomological Society
sheath of young corn plants. First-stadium larvae burrow into the stems and cause significant damage, especially to the late corn crop (Tsitsipis, 1990). Photoperiod is a major factor in determining the developmental pathway (continued development vs. diapause) of S. nonagrioides (Eizaguirre et al., 1994; Fantinou et al., 1995). Moreover, the effect of photoperiod on other developmental characteristics has also been determined (Lopez et al., 1995; Fantinou et al., 1996). However, data in the literature on the oviposition behaviour of this insect are scarce. Salti (1983), found that more than 200 eggs could be deposited per female at the range of 15–28 C at LD 12 : 12 h, whereas Salti & Galichet (1986) reported that the spring generation shows reduced egg laying compared to the following two generations under natural conditions in southern France. However, Thanopoulos et al. (1994) 169
170 A. A. Fantinou et al. observed that egg production is significantly higher in females derived from diapause larvae from laboratory or field populations in Greece. Reproductive success is one of the most important measures of the fitness of an insect and its study is a prerequisite for the understanding of insect evolutionary biology. The influence of the external factors on the life history traits involved in reproduction is essential for the evaluation and understanding the complex life cycles of insects and some factors (i.e. temperature, population size and resource quality and availability) have been well documented (Leather, 1995; Moehrlin & Juliano, 1998; Wermelinger & Seifert, 1999; Awmack & Leather, 2002). However, apart from diapause, there has been limited research on the investigation of photoperiod as a factor influencing the reproduction and oviposition traits of insects. Photoperiod is an ideal seasonal cue for organisms and often life history events change because of photoperiodic responses (Leather et al., 1993; Danks, 2002). Apart from the significant role of photoperiod on the diapause syndrome, the length of photoperiod has been shown to influence several other characteristics of the life cycle of insects (Beck, 1980). Based on examples from literature, Philogene & McNeal (1984) also refer to the demonstration of photoperiodic affects on various aspects of development and reproduction. According to those researchers, light intensity and quality can directly affect development and reproduction and, along with the length of the photophase, can have indirect affects on insect development (e.g. via food plants). One aspect of the photoperiodic influence on insect fitness that has received considerable attention is the relationship of diapause to oviposition (Leather et al., 1993). Despite the considerable contributions made by several studies on the necessity of diapause as a major physiological adaptation of insects for sustaining survival during adverse seasons, there are also negative correlations of diapause with different traits of insect reproduction. Fujie (1980) found that Bucculatrix pyrivorella (Lepidoptera: Lyonetiidae) was less fecund in the spring diapause generations than in the nondiapause summer ones. A negative phenotypic correlation between diapause duration and postdiapause reproduction or adult fitness has been also reported in Tetranychus urticae (Acarina: Tetranychidae) (Kroon & Veenendaal, 1996) and Calliphora vicina (Diptera: Calliphoridae) (Saunders, 2000). Nevertheless, short photoperiods have been found to favour reproduction in several studies. For example, Hodek & Iperti (1983) revealed that females of Semiadalia undecimnotata (Coleoptera: Coccinellidae) when exposed to a short photoperiod that would normally induce diapause, are twice as fecund even though the fecundity of individuals that enter diapause is usually reduced. The biotic factors that determine the quality (fitness) of offspring and population growth rate, as well as the influence of the abiotic factors on the reproduction of S. nonagrioides, must be quantified to develop a more accurate account of its seasonality. However, there has been limited research on the influence of these factors and especially that of photoperiod. To our knowledge, no study #
has evaluated specifically the differential effect of photoperiod on the reproductive response of this species outside of diapause. Therefore, the first aim of this work was to quantify the photoperiodic effects on insects derived from different developmental pathways. More precisely, the study was designed to investigate: (i) the affects of the length of photophase on the oviposition and egg hatch at a broad range of temperatures; (ii) the alteration in the reproductive responses of insects that are derived from diapausing or nondiapausing populations; (iii) and the relationship between the length of the larval diapause and the oviposition of the postdiapausing adults. Materials and methods Experimental animals A laboratory culture of S. nonagrioides, derived from larvae collected in Kopais (latitude 38 140 , Central Greece) in 1999, was maintained at 25 1 C and 55 5% RH at LD 16 : 8 h, and reared on artificial diet that was changed twice a week (Fantinou et al., 1995). For all experiments, newly emerged and mated females were placed individually in wooden boxes (10 10 10 cm) with wire screening on the sides and top, a glass front, plywood back and formica on the bottom, and immediately transferred to controlled chambers. In each cage, stalks of small corn plants (5–8 cm long) were offered daily for oviposition. An aqueous sucrose solution (10%) was supplied to adults in small plastic containers with a dental wick passing through a hole in the cover. Realized fecundity was determined by counting the number of eggs produced per female per day until death. Egg masses were collected from the plants every day, surface-sterilized in 1% chlorine bleach solution for 5 min, then rinsed with distilled water for 5 min and placed in small Petri dishes on filter paper impregnated with 1% propionic acid. Egg hatch was recorded daily and 10 females were used in each experiment. The females that did not oviposit were excluded from the study and were replaced in order to attain 10 replicates in each experimental regime. Observations were always taken after the first 2 h of the photophase of the photoperiodic cycle selected. All experiments were conducted in incubators provided with controlled illumination, temperature and humidity. Light intensity in the incubators was measured using a quantum sensor Li 188 B (Li-Cor Inc., Lincoln, NE) at 22.5 mEin m1s1 (400–700 nm) at 60–65% RH. Effects of temperature and photoperiod Newly-mated females were subjected to photoperiods of LD 16 : 8 and 10 : 14 h, at seven temperature regimes, 15, 17.5, 20, 22.5, 25, 27.5 and 30 C. Immature stages had been exposed to LD 16 : 8 h and 25 C. Preoviposition period, longevity and number of eggs deposited each day were recorded.
2004 The Royal Entomological Society, Physiological Entomology, 29, 169–175
Photoperiodic effects on reproduction of S. nonagrioides
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period and temperature. Data regarding ovipostion rate were compared by repeated measures ANOVA with factors the photoperiod, temperature and day of oviposition. Means were separated with the Tukey-Kramer HSD test (a ¼ 0.05). Before analysis, the percentages of ovipositing females and of egg hatch were arcsine pffi(x)-transformed. A linear regression was used to correlate mean ovipostion with pupal weight. All statistical analyses were performed using Statistica software (StatSoft. Inc., 1995).
Oviposited eggs were collected daily from each female and placed in a Petri dish under the same temperature and photoperiodic regime as the adults experienced. Egg hatch was recorded daily 2 h after lights on.
Differential role of photoperiod on diapausing and nondiapausing insects Insects induced to diapause under LD 10 : 14 h, were held at the same photoperiod after the termination of diapause until the emergence of the adults. Newly emerged, mated females were kept at LD 10 : 14 h or transferred after mating to LD 16 : 8 h and daily oviposition was recorded. In addition, mean oviposition was recorded in mated females held from their immature stages in LD 16 : 8 h or transferred after mating to LD 10 : 14 h. All treatments were kept at 25 1 C, and 55 5% RH.
Results Longevity, preoviposition period and the percentage of nonovipositing females exposed to either long or short photoperiod are presented in Table 1. Females exposed to the long days appeared to live longer at the range of 15–25 C; however, no significant differences were found between the two photoperiodic treatments (F ¼ 1.18; d.f. ¼ 1126; P > 0.28). Moreover, in both treatments, longevity was reduced with an increase in temperature. Although no differences between the preoviposition periods at different day lengths at the same temperature were revealed by the Tukey–Kramer HSD test (Table 1), ANOVA indicated that there was an overall photoperiodic effect (F ¼ 5.01; d.f. ¼ 1126; P < 0.028) and the length of the photoperiod affected the percentage of ovipositing females (F ¼ 41.25; d.f. ¼ 1,12; P < 0.001) (Table 1). Females of S. nonagrioides oviposited at all temperatures in both the photoperiodic regimes (Fig. 1). Temperature had a significant affect on cumulative egg production for either the long or short photoperiod (F ¼ 37.89; d.f. ¼ 6,63; P < 0.001 and F ¼ 13.64; d.f. ¼ 6,63; P ¼ 0.001, respectively). Moreover, oviposition was significantly greater at the range of 20–27.5 C than at 15, 17.5 or 30 C. As temperature increased from 17.5 to 20 C, a significant increase in fecundity appeared at LD 16 : 8 h whereas a gradual increase of oviposition was observed under LD
Duration of diapause and oviposition Larvae induced to diapause at LD 10 : 14 h and 25 C were held under diapausing conditions until the age of 60, 80, 100, 120 and 150 days and then transferred to LD 16 : 8 h at 25 C. Ten to 14 days after transfer, larvae terminated diapause (Fantinou et al., 1998). Pupae derived from diapausing larvae of different ages were weighed at the day of formation, emerged females mated and left to oviposit under the long photophase. Eggs-laid by females from each experimental treatment were counted.
Statistical analysis Longevity, preoviposition period, oviposition, number of females that oviposited and egg hatch were analysed using a two-way factorial analysis of variance (ANOVA) for photo-
Table 1. Longevity, preoviposition (mean SE) in days and oviposited females of Sesamia nonagrioides exposed under two photoperiodic regimes (LD 16 : 8 h and 10 : 14 h) and different temperatures. Photoperiod LD 16 : 8 h
LD 10 : 14 h
Temperature ( C)
Longevity (days)
Preoviposition (days)
Ovipositing females (%)
Longevity (days)
Preoviposition (days)
Ovipositing females (%)
15 17.5 20 22.5 25 27.5 30
7.6 0.27Aa 6.2 0.36Aab 5.8 0.25Ab 6.0 0.33Ab 5.0 0.21Abc 4.2 0.25Ac 3.9 0.23Ac
1.5 0.17Aa 1.6 0.16Aa 1.3 0.15Aa 1.3 0.15Aa 1.2 0.13Aa 1.2 0.13Aa 1.4 0.16Aa
90 100 100 100 100 100 90
6.8 0.36Aa 6.2 0.33Aab 5.2 0.29Abc 5.4 0.34Aabc 4.8 0.33Abc 5.1 0.28Abc 4.0 0.26Ac
1.7 0.15Aa 1.7 0.15Aa 1.6 0.16Aa 1.5 0.17Aa 1.2 0.13Aa 1.5 0.17Aa 1.6 0.16Aa
80 80 80 70 60 60 50
Means followed by the same capital superscript letter in each row are not significantly different between the two photoperiodic regimes are not significantly different. Means followed by the same lower case superscript letter in each column are not significantly different (Tukey–Kramer HSD test, a ¼ 0.05).
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2004 The Royal Entomological Society, Physiological Entomology, 29, 169–175
Mean oviposition ( eggs / female )
172 A. A. Fantinou et al. 500 Photoperiod LD 16 : 8 h LD 10 : 14 h b
400
b
b
b
300 a
f
df
a
f
df
200 cd
cd
c
100
cd
0 15
17.5
20
22.5
25
27.5
30
Temperature (°C)
Fig. 1. Mean (SE) oviposition (eggs/female) of Sesamia nonagrioides exposed to two photoperiodic regimes (LD 16 : 8 and 10 : 14 h) at different temperatures. Immature stages were exposed to LD 16 : 8 h. Values followed by the same letter are not significantly different (Tukey-Kramer HSD test, a ¼ 0.05).
10 : 14 h. However, a sharp decline in mean oviposition was recorded from 27.5 to 30 C in both photoperiodic treatments. In all treatments, most eggs were laid during first and second day after mating. This observation confirms that fecundity is higher just after emergence and mating (Fig. 2). Moreover, no eggs were laid after day 5 or 6.
LD 16 : 8 h
Number of eggs
300
Temperature (°C)
250
15 17.5 20 22.5 25 27.5 30
200 150 100 50 0
0
1
2
3
4
Significant interactions were recorded between the factors temperature and day of oviposition (F ¼ 34.61; d.f. ¼ 30 270; P < 0.001), between photoperiod and day of oviposition (F ¼ 101.63; d.f. ¼ 5,45; P < 0.001) as well as between photoperiod and temperature (F ¼ 7.01; d.f. ¼ 6,54; P < 0.001). There were no differences between the two photoperiodic treatments for egg hatch (F ¼ 1.91; d.f. ¼ 1,26; P > 0.17) (Fig. 3). By contrast, temperature did affect the number of eggs hatching and significant differences were observed, especially at the extreme temperatures in either long or short days (F ¼ 6.98; d.f. ¼ 6,63; P < 0.001 and F ¼ 12.03; d.f. ¼ 6,63; P < 0.001, respectively). The exposure of the immature stages to either long or short days affected the observed fecundity of adults (Table 2). Adults derived from insects that were exposed to either long or short days and left to oviposit in the same condition did not differ in the number of eggs laid. A daylength switch after mating significantly influenced oviposition (F ¼ 33.65; d.f. ¼ 1,36; P < 0.001). Oviposition was suppressed, when insects were exposed to LD 16 : 8 h through their immature period, and then transferred to LD 10 : 14 h after mating. By contrast, egg numbers from insects derived from a diapausing population were significantly higher than all of the other treatments (Table 2). Thus, it appears that larval diapause had a significant affect on the number of eggs produced by adults. There was a correlation between the duration of the larval diapause and the mean egg production (r2 ¼ 0.09; P ¼ 0.032) (Fig. 4). In general, when the larval diapause period increased from 60 to 100 days, there was an increase in eggs laid, with longer diapause periods egg production declined. Differences in egg production were significant (F ¼ 4.09; d.f. ¼ 4,45; P < 0.006). Moreover, a significant correlation was indicated between the duration of diapause and the mean pupal weight (r2 ¼ 0.095; P ¼ 0.030). Pupal weight was affected by larval diapause duration (F ¼ 2.89; d.f. ¼ 4,45; P < 0.033) and there was a significant
5
Day 200
Photoperiod 80 Egg hatch (%)
Number of eggs
100
LD 10 : 14 h
150 100
c 60
a ab
LD 16 : 8 h c
LD 10 : 14 h
a a
40
c c
ab a
ab
ab
b
b
27.5
30
20
50
0 15
0 0
1
2
3
4
5
Day Fig. 2. Number of eggs produced per female Sesamia nonagrioides (mean SE) exposed to two photoperiodic regimes (LD 16 : 8 and 10 : 14 h) and different temperatures. Immature stages were exposed to LD 16 : 8 h.
#
17.5
20
22.5
25
Temperature (°C)
Fig. 3. Egg hatch of Sesamia nonagrioides exposed to two photoperiodic regimes (LD 16 : 8 and 10 : 14 h) and different temperatures. Immature stages were exposed to LD 16 : 8 h. Values (mean SE) followed by the same letter are not significantly different (Tukey-Kramer HSD test, a ¼ 0.05).
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Table 2. Mean oviposition (number of eggs/female), longevity and preoviposition in days (mean SE) of Sesamia nonagrioides after the exposure of immature stages to long (LD 16 : 8 h) or short (LD 10 : 14 h) photoperiod and the transfer of adults to either long or short photoperiod. Immatures at LD
Adults at LD
16 : 8 16 : 8 10 : 14 10 : 14
Mean oviposition (eggs/female) (days)
Longevity (days)
a
372.42 0.57 218.12 2.80b 513.63 0.18c 394.11 8.95a
16 : 8 10 : 14 16 : 8 10 : 14
Preoviposition
a
1.2 0.13a 1.2 0.13a 1.4 0.16a 1.8 0.14b
5.0 0.21 4.8 0.32a 6.8 0.20b 7.4 0.16b
Means in each column followed by the same letter are not significantly different (Tukey–Kramer HSD test, a ¼ 0.05).
positive correlation between pupal weight and observed fecundity (Fig. 5).
Discussion The current study confirms that S. nonagrioides fecundity and hatching success are affected by daylength and temperature. Neither photoperiod nor temperature influence the longevity of adults but there is some indication that daylength affects the preoviposition (ANOVA) whereas temperature does not. This may be due the limited time for mating and oviposition since this species has a shortlived adult stage. However, photoperiod and temperature are deciding factors in regulating oviposition. Oviposition can occur at the range of 15–30 C and the response curve for egg laying activity exhibits a bell-shaped, fecundity– temperature response under both daylengths tested (Leather, 1994). The optimum temperature range is between 25 and 27.5 C (Figs 2 and 3). Because oviposition is observed at 30 C, the upper threshold may be higher. This is not surprising given that daily temperatures of 35–40 C are common in fields in Greece during the period when adults are present. Moreover, photoperiod appears to influence ovipositional activity and ovipositional rate. Therefore, it appears that the reproductive output would be reduced by late season photoperiods. This may also have implications for the geographical distribution of this species. It is known that the insect has not been found further 500 ab
ab
ab
500 a
b 400 a
ab
60
80
400 ab
ab
300
300 100
120
150
Duration of larval diapause (days)
Fig. 4. Oviposition and pupal weight (mean SE) of Sesamia nonagrioides when larvae were exposed under diapause conditions (LD 10 : 14 h) for different time periods. Adults were exposed to LD 16 : 8 h.Values in each line followed by the same letter are not significantly different (Tukey-Kramer HSD test, a ¼ 0.05).
#
Mean oviposition (eggs/female)
b
Eggs Weight
Pupal weight (mg)
Mean oviposition (eggs/female)
600
north than 37 (Anon, 1979) indicating that it probably does not withstand very low temperatures. The results concerning the effect of photoperiod on insect oviposition are very contradictory. Thus, the wasp Ooencyrtus nezarae (Hymenoptera: Encyrtidae), the phytophagous bug Euschistus heros (Hemiptera: Pentatomidae) and the weevil Otiorhynchus ovatus (Coleoptera: Curculionidae) produce fewer eggs under short-day than under long-day regimes (Numata, 1993; Mourao & Panizzi, 2002; Umble & Fisher, 2002). In the coccinellid Semiadalia undecimnota, females exposed to short days have twice the fecundity of long-day females (Hodek & Iperti, 1983). There are significantly more eggs laid by adults derived from diapausing than from nondiapausing populations (Table 2). Thus, the photoperiod experienced by the immature stages of the insect appears to provide information about the progression of the season and influence observed fecundity. According to Gillyboeuf et al. (1994), mortality in diapausing populations of S. nonagrioides in southern France reaches 90% due to the absence of physiological cold hardiness. The developmental delay in laboratorydiapausing larvae has been reported to be associated with additional moults (Fantinou et al., 1996). According to Danks (2002), stationary moults do not provide insects with any adaptive value (Danks, 2002). However, stationary moults in this species involve an increase in size and, therefore, it is adaptive because the final pupa is heavier, and the adult is larger and consequently more fecund. In view of the fact that the process of prolonged diapause requires energy
700 600 500 y = 1.84x – 148.24 R2 = 0.78,P < 0.001
400 300 250
300
350
400
450
Pupal weight (mg)
Fig. 5. Relationship between oviposition and pupal weight of Sesamia nonagrioides. Immature stages were exposed to LD 10 : 14 h, and adults to LD 16 : 8 h.
2004 The Royal Entomological Society, Physiological Entomology, 29, 169–175
174 A. A. Fantinou et al. to be stored, larvae that do not succeed in gaining adequate nutrition die when energy reserves are depleted. Thus, a sufficient amount of energy needs to be acquired to provide energy for the next stage (pupa) and for the initiation and maintenance of oviposition in adult females. Because significantly lower fecundity is observed between adults derived from diapausing or nondiapausing populations when exposed to short days, compared with those derived from a diapausing population exposed to long days, it is assumed that photoperiod might allow the efficient recovery of population numbers after winter mortality. Moreover, these responses appear to be related to the prolonged dormant period of larvae, which produces heavier pupae. Consequently, these larger adults are more fecund than adults appearing later in the year (Fantinou et al., 1996; Gadenne et al., 1996). The fact that diapausing larvae continued periodic feeding on weeds (e.g. Avena sterilis, Phalaris brachystachys) and winter cereals (e.g. Triticum aestivum) means that these insects can accumulate nutrients during the prolonged larval stage, which is an important factor in determining the reproductive potential of postdiapause adults (Deseo & Sarringer, 1975). Salti & Galichet (1986) reported that spring generation of S. nonagrioides are less fecund than the two later generations. The differences that appear in the reported research may be due to the collection of senescent corn plants in autumn with diapausing individuals that were left outdoors for pupation (Salti & Galichet, 1986). Thus, there is a possibility that the low quality of the plants influences the weight gain of the diapausing larvae and, as a result, the number of oviposited eggs. Moreover, results similar to those reported in the present study are found with fecundity of overwintered postdiapause females of Tetrix undulata (Orthoptera: Tetrigidae), whose fecundity was greater compared to females that oviposited without overwintering (Poras, 1976). On the other hand, in Busseolae fuska (Lepidoptera: Noctuidae) and Chilo partellus Lepidoptera: Pyralidae), diapause is linked to a decrease in weight and reproductive ability (Kfir, 1991). The positive relationship between the larval diapause duration and fecundity suggests that larvae surviving through winter do not run out of reserves (Fig. 4). Therefore, cold winters in nature may be a means of conserving metabolic reserves and preventing postdiapause morphogenesis, which in turn synchronizes spring emergence (Hodek & Hodkova, 1988) and increases fecundity (Irvin & Lee, 2000). According to Fantinou et al. (1998), almost all of S. nonagrioides enter diapause by mid-August. Diapause development is complete by mid-January and borers exhibit a quiescence that prevents postdiapause development until the necessary summation of thermal units. Moreover, variation in intensity of diapause of this species has not been found, regardless of photoperiod or temperature of larval exposure (Fantinou et al., 2003). A strong relationship was found between pupal weight and adult oviposition. Considering that pupae derived from the diapausing population are heavier than those from the nondiapausing population (Fantinou et al., 1996; Gadenne #
et al., 1996), there is a possibility that the differences in initial pupal weight resulted in differences in the egg numbers deposited by the females from different generations. Throughout the duration of the dormant period, and also through the interval required for postdiapause morphogenesis, larvae could continue feeding and gain more weight. Furthermore, wild plants and native hosts of S. nonagrioides generally bloom 3–4 weeks in advance of commercially grown corn; thus, host availability may influence the reproductive success of the adults. The findings presented here suggest that this species responds to environmental variation in different ways throughout its life. The prolonged larval development in diapause, which is related to the occurrence of the supernumerary molts, the absence of physiological cold hardiness and continued food consumption in diapausing individuals, is an adaptation to harsh conditions that allows the species to survive. The behavioural strategy, where high reproductive potential is traded against high winter mortality, is of great interest and needs further evaluation in the field.
References Anon (1979) Distribution Maps of Pests. Series A. Agricultural, Map 339. Pest: Sesamia nonagrioides (Lef.). Commonwealth Agricultural Bureau, U.K. Awmack, C.S. & Leather, S.R. (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47, 817–844. Beck, S.D. (1980) Insect Photoperiodism, 2nd edn. Academic Press, New York. Danks, H.V. (2002) The range of insect dormancy responses. European Journal of Entomology, 99, 127–142. Deseo, K.V. & Sarringer, Gy. (1975) Photoperiodic effect on fecundity of Laspeyresia pomonella, Grapholitha funebrana and G. molesta: the sensitive period. Entomologia Experimentalis et Applicata, 18, 187–93. Eizaguirre, M., Lopez, C., Asin, L. & Albajes, R. (1994) Thermoperiodism, photoperiodism and sensitive stage in the diapause induction of Sesamia nonagrioides (Lepidoptera: Noctuidae). Journal of Insect Physiology, 40, 113–119. Fantinou, A.A., Karandinos, M.G. & Tsitsipis, J.A. (1995) Diapause induction in the Sesamia nonagrioides (Lepidoptera: Noctuidae) effect of photoperiod and temperature. Environmental Entomology, 24, 1458–1466. Fantinou, A.A., Tsitsipis, J.A. & Karandinos, M.G. (1996) Effects of short- and long-photoperiods on growth and development of Sesamia nonagrioides (Lepidoptera: Noctuidae). Environmental Entomology, 25, 1337–1343. Fantinou, A.A., Tsitsipis, J.A. & Karandinos, M.G. (1998) Diapause termination in Sesamia nonagrioides (Lepidoptera: Noctuidae) under laboratory and field conditions. Environmental Entomology, 27, 53–58. Fantinou, A.A., Kourti, A.T. & Saitanis, C. (2003) Photoperiodic and temperature effects on the intensity of larval diapause in Sesamia nonagrioides. Physiological Entomology, 88, 82–87. Fujie, A. (1980) Ecological studies on the population of the pear leaf miner, Bucculatrix pyrivorella Kuroko (Lepidoptera: Lyonetiidae). III. Fecundity fluctuation from generation to generation within a year. Applied Entomology and Zoology, 15, 1–9.
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Photoperiodic effects on reproduction of S. nonagrioides Gadenne, C., Dufour, M.C., Rossignol, F., Becard, J. & Couillaud, F. (1996) Occurance of non-stationary moults during diapause in the corn-stalk borer, Sesamia nonagrioides (Lepidoptera: Noctuidae). Journal of Insect Physiology, 43, 425–431. Gillyboeuf, N., Angade, P., Lavenseau, L. & Peypelut, L. (1994) Cold hardiness and overwintering strategy of the pink maize stalk borer Sesamia nonagrioides (Lepidoptera, Noctuidae). Oecologia, 99, 366–373. Hodek, I. & Hodkova, M. (1988) Multiple role of temperature during insect diapause: a review. Entomologia Experimentalis et Applicata, 49, 153–165. Hodek, I. & Iperti, G. (1983) Sensitivity to photoperiod in relation to diapause in Semiadalia undecimnotata females. Entomologia Experimentalis et Applicata, 34, 9–12. Irvin, J.T. & Lee, R.E. (2000) Mild winter temperatures reduced survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae). Journal of Insect Physiology, 46, 655–661. Kfir, R. (1991) Effect of diapause on development and reproduction of the stem borers Busseola fusca (Lepidoptera: Noctuidae) and Chilo partellus (Lepidoptera: Pyralidae). Journal of Economic Entomology, 84, 1677–1680. Kroon, A. & Veenendaal, R.L. (1996) Trade-off between diapause and other life-history traits in the spider mite Tetranychus urticae. Ecological Entomology, 23, 298–304. Leather, S.R. (1994) The effect of temperature on oviposition, fecundity and egg hatch in the pine beauty moth, Panolis flammea (Lepidoptera: Noctuidae). Bulletin of Entomological Research, 84, 515–520. Leather, S.R. (1995) Factors affecting fecundity, fertility, oviposition, and larviposition in insects. Insect Reproduction (ed. by S. R. Leather and R. J. Hardie), pp. 143–174. CRC, Boca Raton, Florida. Leather, S.R., Walters, K.F.A. & Bale, J.S. (1993) The Ecology of Overwintering. Cambridge University Press, U.K. Lopez, C., Eizaguirre, M. & Albajes, R. (1995) Diapause detection and monitoring in the Mediterranean corn stalk borer. Physiological Entomology, 20, 330–336. Moehrlin, G.S. & Juliano, S.A. (1998) Plasticity of insect reproduction: testing models of flexible and fixed development in response to different growth rates. Oecologia, 115, 492–500. Mourao, A.P.M. & Panizzi, A.R. (2002) Photophase influence on the reproductive diapause, seasonal morphs, and feeding activity of Eushchistus heros (Fab., 1798) (Hemiptera: Pentatomidae). Brazilian Journal of Biology, 62, 231–238.
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Numata, H. (1993) Induction of adult diapause and of low and high reproductive states in a parasitoid wasp, Ooencyrtus nezarae, by photoperiod and temperature. Entomologia Experimentalis et Applicata, 66, 127–134. Philogene, B.J.R. & McNeal, J.N. (1984) The influence on the nondiapause related aspects of development and reproduction in insects. Photochemistry and Photobiology, 40, 753–761. Poras, M. (1976) Inluence de la photoperiode et de la temperature sur queques aspects de la diapause imaginable chez les femelles de Tetrix undulata (Sow.) (Orthoptera, Tetrigidae). Annals of Zoology and Ecology of Animals, 8, 373–380. Salti, M.N. (1983) Influence de la temperature pendant la vie imaginable sur les potentialities reproductrices de l’espece Sesamia nonagrioides Levebvre (Lep., Noctuidae). Acta Oecologia, 5, 103–112. Salti, M.N. & Galichet, P.F. (1986) Etude pluriannuelle des fluctuations saisonnieres de la potentialite reproductrice chez Sesamia nonagrioides Levebvre (Lepidoptera, Noctuidae). Acta Oecologia, 7, 115–122. Saunders, D.S. (2000) Larval diapause duration and fat metabolism in three geographical strains of the blow fly, Calliphora vicina. Journal of Insect Physiology, 46, 509–517. StatSoft Inc. (1995) STATISTICA for Windows, Release 5. http:// www.statsoft.com. Thanopoulos, R., Tsitsipis, J.A., Alexandri, M. & Fantinou, A. (1994) Egg production and survival of corn stalk borer females, Sesamia nonagrioides, in relation to temperature and pupal weight. Proceedings of the Fourth Panhellenic Entomology Meeting, Hellenic Entomological Society (ed. by J. Tsitsipis, E. T. Kapatos and A. G. Koutroubas), pp. 27–29. Tsitsipis, J.A. (1990) Contribution toward the development of an integrated control method for the corn stalk borer Sesamia nonagrioides (Lef.). Pesticides and Alternatives (ed. by J. E. Casida), pp. 217–228. Elsevier, The Netherlands. Umble, J.R. & Fisher, J.R. (2002) Influence of temperature and photoperiod on preoviposition duration and oviposition of Otiorhynchus ovatus (Coleoptera: Curculionidae). Annals of the Entomological Society of America, 95, 231–235. Wermelinger, B. & Seifert, M. (1999) Temperature-dependent reproduction of the spruce bark beetle Ips typographus, and analysis of the potential population growth. Ecological Entomology, 24, 103–110.
Accepted 26 January 2004
2004 The Royal Entomological Society, Physiological Entomology, 29, 169–175