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Keywords:

  • bet-hedging;
  • metabolic cost;
  • protandry;
  • seed masting;
  • sexual dimorphism

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • 1
    Although metabolic resource losses are maintained at low rates during diapause, the accumulation of losses over a long period negatively affects organisms with prolonged diapause usually extending beyond 1 year. The seed-predatory weevil Exechesops leucopis (Jordan) (Coleoptera: Anthribidae) enters winter diapause at the final-instar larval stage within seeds of Styrax japonica Sieb. et Zucc. (Styracaceae) at a density of one larva per seed. After diapause, larvae pupate within the seeds and then emerge as adults.
  • 2
    The adult emergence pattern of a single cohort of E. leucopis was monitored for 5 years under seminatural conditions in the laboratory. The duration of diapause varied from 1 year (single winter) to 4 years (four winters). Adults that emerged after 1 year were smaller than those that emerged after 2 years or more. When temperature was not decreased experimentally in winter, no adults emerged in the following season.
  • 3
    Metabolic resource losses during diapause were examined by comparing adult body sizes between controls and groups in which emergence was delayed by 1 year under manipulated winter temperature regimes. Adults that emerged after an additional year in the larval stage were smaller than those in the control group. Moreover, the rates of reduction in body size as a consequence of diapause being extended experimentally were greater in smaller individuals. Thus smaller individuals have disadvantages in longer diapause, suggesting that weevils may vary the duration of diapause depending on individual body size.
  • 4
    Exechesops leucopis shows sexual dimorphism in the degree of eye protrusion. Eyestalk length affects male fitness through intrasexual selection. The duration of diapause affected the length of the eyestalks: when an additional year was spent in diapause, eyestalk length was nearly maintained in larger males but was greatly decreased in smaller males. In all females eyestalk length decreased according to the duration of diapause.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Diapause is an important means by which organisms avoid unfavourable environmental conditions. Prolonged diapause extending for more than 1 year is often observed in organisms that inhabit unpredictable and fluctuating environments, such as desert plants (Phillipi 1993); bees (Danforth 1999); pond-dwelling copepods (Hairstone 1998); and seed-predatory insects (Menu & Desouhant 2002). In these organisms, termination of diapause usually occurs polymodally within a cohort (Phillipi 1993; Hairstone 1998; Danforth 1999; Menu & Desouhant 2002). Such variation occurring within offspring is considered a bet-hedging strategy, spreading the risk of unpredictable fluctuations in food availability, predation pressure or habitat suitability.

However, prolonged diapause is associated with costs, including the loss of metabolic resources, additional mortality, and loss of reproductive opportunities (Danks 1987; Leather, Walters & Bale 1993; Hairstone 1998). Although metabolism is maintained at low rates during diapause (Lees 1955), accumulated metabolic resource losses increase, which may significantly affect fitness when diapause lasts for a long time (Danks 1987). Because small individuals generally reserve fewer metabolic resources and have relatively higher metabolic rates than large individuals (Peters 1983), small individuals suffer a greater disadvantage if diapause is extended. In this case, body size-dependent variation in the duration of diapause would be expected.

In several insect species, diapause is longer in larger individuals (Bakke 1971; Nesin 1985; Powell 1989; Danforth 1999; Menu & Desouhant 2002). Carne (1969) reported an inverse relationship between the duration of diapause and body size. In this case, however, the duration of diapause was strongly density-dependent, and consequently size-dependent because body size decreased at high density (Carne 1969). Menu & Desouhant (2002) pointed out the importance of energy resources for individuals to extend diapause. No study to date has reported costs of prolonged diapause, because it is generally difficult to estimate the costs of diapause. Powell (1989) failed to determine the costs of diapause, probably because he was unable to compare changes in weight (or size) of the same individual before and after diapause.

The seed-predatory weevil Exechesops leucopis (Jordan) (Coleoptera: Anthribidae) enters diapause at the end of the final-instar larval stage within seeds of Styrax japonica and Styrax obassia (Styracaceae; Tokunaga 1937). Seeds of these trees contain the toxin ‘Jegosaponin’ (Aizawa 1989), so are rarely used as food. According to Tokunaga (1937), Curculio styracis (Coleoptera: Curculionidae) and a lepidopteran species are the only species of insects other than E. leucopis that feed on seeds of these trees.

Each seed hosts a single larva. Aizawa (1989) suggested that this weevil may undergo prolonged and variable diapause because 40·4% of larvae emerged as adults in the year following collection, whereas the remainder survived as larvae in the seeds after this period. However, his observations were terminated without examining the fate of the remaining larvae.

The findings of Aizawa (1989) were re-examined by monitoring the adult emergence patterns of a single weevil cohort for 5 years under seminatural conditions in the laboratory. As a result, prolonged diapause was confirmed, and its duration varied from 1 to 4 years. I was able to control the duration of diapause by rearing weevils without winter chilling. This enabled the costs of diapause to be examined by comparing adult body size and timing of emergence between a normally reared group, and a group in which emergence was artificially delayed by 1 year. If body size is decreased by delayed emergence, considerable metabolic resource losses would be expected to occur. If survival rate is reduced by delayed emergence, additional mortality should occur, even though predation is avoided. Increasing diapause length can also affect later events such as reproductive success. In the flesh fly Sarcophaga crassipalpis, a long pupal diapause results in a reduction of survival and egg number produced by the female after diapause is over (Denlinger 1981). Based on examinations of these hypotheses, the possible patterns of size-dependent variation in diapause duration are discussed.

In this weevil, the eyes of males protrude very far (Yoshitake & Kawashima 2004; Matsuo 2004, 2005). This is a sexually selected trait: males with longer eyestalks defeat those with shorter eyestalks in male–male combat, whereas in female–female contests prior residency is a more important determinant of victory than any morphological trait (Matsuo 2005). The effects of the costs of diapause on this sexually selected trait were also examined.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

insects

Female E. leucopis oviposit in midsummer when host seeds have matured, and the eggs are deposited into fresh seeds of the host trees (the single fruit includes only one seed and one egg is laid per seed; Tokunaga 1937). Eggs hatch ≈3 days after oviposition, and the larvae feed on the entire inner part of the seed. The larvae develop completely over 3 weeks (Aizawa 1989) and then overwinter within the seeds as final (third)-instar larvae. Pupation occurs within the seed in June and adults emerge in July (Aizawa 1989).

rearing and measurements

On 9 April 2000, about 2000 seeds of S. japonica produced in 1999 were collected using a single seed trap set under a tree at Tennodai, Tsukuba, Ibaraki, Japan. I selected 1486 seeds that showed small oviposition scars (≈0·5 mm long) and maintained them at 23 ± 1 °C in a 14 h light : 10 h dark cycle (LD 14 : 10, summer conditions), increasing the temperature by 3 °C per week (Fig. 1). These seeds were placed individually in 48-well microplates (10 mm diameter). Spaces between wells were filled with water to avoid seed desiccation. During adult emergence periods the seeds were checked every day. Emerged adults were frozen at −20 °C until morphological measurements could be made. Each November the ambient temperature was reduced by 3 °C per week until seeds were exposed to winter conditions of 7 ± 1 °C and LD 10 : 14 for 3 months. The larvae were then maintained again under summer conditions by increasing the temperature by 3 °C per week. The seeds were maintained until June 2004; after this time, all remaining seeds were opened to determine whether live larvae were present.

image

Figure 1. Yearly emergence patterns of adult Exechesops leucopis from 1486 seeds under two experimental designs. In experiment 1, 54 larvae were removed from seeds and maintained individually in plastic microplate wells for observation. In experiment 2, 372 larvae did not emerge as adults in the second year because they were not exposed to low temperatures in the winter of 2000. Numerals indicate the number of adults (in squares) or the number of seeds (in circles); c, exposure to low temperatures.

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The pronotum width (maximum width) and eye span (maximum distance between the outer edges of the left and right eyes) of weevils were measured to the nearest 0·056 mm using a binocular microscope. To estimate seed volume, the height, width and thickness (h, w and t, respectively) of seeds were measured using a slide calliper. Assuming an ellipsoid shape, seed volume (V) was then calculated as V = πhwt/6. Mean values are given with standard deviations (± SD).

experiments

In experiment 1, larvae were removed from seeds to examine the relationship between larval size and seed volume, and to record larval growth patterns. On the day following seed collection (10 April 2000), 54 of 1486 seeds were carefully opened after measuring the seed size; of these seeds, 48 contained live larvae (88·9%). Live larvae were transferred individually into wells of plastic microplates for direct observation after their fresh body weights were measured to the nearest 0·01 mg. The larvae were maintained at 23 ± 1 °C (LD 14 : 10) and monitored to record the date of pupation and adult eclosion nearly every day for 7 months (until November 2000). No larvae died during this observation period.

In experiment 2, I examined the effects of artificially delayed diapause on the body size and shape of eclosed adults. After the adult emergence period in the first year, seeds were divided into control and experimental groups. The control group (557 seeds) was subjected to the chilling treatment each winter, whereas the experimental group (372 seeds) was not chilled during the second winter (Fig. 1). The experimental larvae spent an additional year in diapause; therefore a comparison of body size between the control and experimental groups allowed an examination of the cost of diapause.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

life history of the control group

Diapause ranged from 1 to 4 years in this single cohort of weevils (Fig. 1). In the first year, 168 males and 143 females emerged (proportion of males = 0·54; binomial test, P = 0·17). In the second year, 126 males and 134 females emerged (0·48, P = 0·66). In the third year, 10 males and eight females emerged (0·36, P = 0·81). In the fourth year, no males and two females emerged (Fig. 2). No adults emerged in the fifth year. After the fifth emergence season, no live larvae were found among the remaining 277 seeds.

image

Figure 2. Daily emergence patterns in four successive adult emergence seasons from a 1999 cohort of Exechesops leucopis. Closed and open bars represent males and females, respectively.

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Males emerged significantly earlier than females in every year (difference in median emergence date between the sexes = 3 days in the first year, Mann–Whitney U-test, N1 = 168, N2 = 143, Z = 5·58, P < 0·0001; 5 days in the second year, N1 = 126, N2 = 134, Z = 7·64, P < 0·0001; 6 days in the third year, N1 = 10, N2 = 8, U = 6·5, P = 0·003; Fig. 2).

Mean pronotum width in males was 3·11 ± 0·31 mm in the first year; 3·37 ± 0·17 mm in the second year; and 3·34 ± 0·19 mm in the third year. In females, corresponding values were 3·07 ± 0·28, 3·30 ± 0·17 and 3·22 ± 0·14 mm. Pronotum width differed significantly among the three emergence-year groups in both males (Kruskal–Wallis test, df = 2, H = 58·33, P < 0·0001) and females (df = 2, H = 58·09, P < 0·0001). Thus adults that emerged in the first year were smaller than those that emerged in the second and third years in both sexes.

Pronotum width was correlated with seed volume in every year and in both sexes (all Pearson's coefficients, P < 0·001). Pronotum width relative to the seed volume of the first-year group was smallest among the three groups both in males (ancova, F2,223 = 0·113, P = 0·89 for slopes; F2,225 = 25·19, P = 0·0001 for intercept; adjusted means 3·15, 3·36 and 3·30 mm in the first, second and third years, respectively) and in females (F2,250 = 0·053, P = 0·95 for slopes; F2,252 = 15·73, P = 0·0001 for intercept; adjusted means 3·31, 3·48 and 3·44 mm, respectively).

experiment 1 (observation of larvae)

Of 54 field-collected seeds with oviposition scars, 48 contained live larvae and six did not. The survival rate from eggs to overwintering larvae was therefore estimated to be 88·9%. Of these 48 larvae, 12 males and 18 females emerged in June, whereas the remaining larvae remained in diapause and did not emerge until November. Males pupated significantly earlier than females (median emergence date 23 May in males, 25 May in females; Mann–Whitney U-test, N1 = 12, N2 = 18, Z = 3·38, P < 0·001). Pupal periods did not differ between sexes (male, N = 12, 13·2 ± 0·7 days; female, N = 16, 13·1 ± 0·8 days; Student's t-test, t26 = 0·142, P = 0·89). Eclosed adults were whitish in colour and gradually sclerotized 3–5 days after eclosion. Larvae with significantly higher fresh weight entered into prolonged diapause (35·7 ± 4·5 mg in diapausing larvae; 27·9 ± 8·5 mg in emerged larvae; Mann–Whitney U-test, N1 = 18, N2 = 30, Z = 3·38, P = 0·0007). Larval fresh weight was correlated with seed volume both for diapausing larvae (Pearson's correlation coefficient, N = 18, r = 0·498, P = 0·034) and emerged larvae (N = 30, r = 0·657, P < 0·0001; Fig. 3). Thus seed volume was considered an indicator of the size of the final-instar larvae. Lighter larvae relative to seed volume terminated diapause earlier (ancova, F1,44 = 2·20, P = 0·15 for slopes; F1,45 = 13·76, P = 0·0006 for intercepts; Fig. 3).

image

Figure 3. Relationships between seed size (seed volume) and larval body weight when larvae were removed from seeds. Closed symbols (broken line), larvae from which male (triangles) and female (circles) adults emerged after a 1-year diapause; open symbols (solid line), larvae that did not emerge after 1 year (larvae would emerge after 2 or more years and the sexes could not be determined).

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experiment 2 (effects of artificially delayed diapause)

No adults emerged during the second year without artificial chilling (Fig. 1). However, after being chilled in the third year, 71 males and 79 females emerged (proportion of males = 0·47; binomial test, P = 0·57). In the fourth year, 18 males and 15 females emerged (0·55, P = 0·73). After the fifth emergence season, the remaining 189 seeds contained no live larvae. Thus experiencing low temperatures was essential for larvae to terminate diapause and pupate. The pronotum width relative to seed size was smaller in the third-year emergence group in the experiment than the second-year emergence group in the control, both in males (ancova, F1,174 = 0·138, P = 0·71 for slopes; F1,175 = 32·52, P = 0·0001 for intercepts) and in females (F1,201 = 0·0004, P = 0·98 for slopes; F1,202 = 25·62, P = 0·0001 for intercepts; Fig. 4, left). A similar tendency was observed in adults emerging in the subsequent year: the third-year emergence group in the control vs the fourth-year emergence group in the treatment, both in males (ancova, F1,24 = 0·03, P = 0·86 for slopes; F1,25 = 7·35, P = 0·012 for intercepts) and in females (F1,19 = 0·254, P = 0·62 for slopes; F1,20 = 8·56, P = 0·008 for intercepts; Fig. 4, right). Thus experimentally prolonged diapause of one additional year decreased adult body size. The rate of reduction in adult body size increased as seed size decreased, with one exception of males compared between the control third-year emergence group and the experimental fourth-year emergence group. Because prediapause body size is usually correlated with seed size, smaller individuals may lose a greater proportion of their mass (Fig. 4).

image

Figure 4. Seed size–adult body size relationships between control (open circles, solid lines) and experimental (closed circles, broken lines) groups of Exechesops leucopis with different emergence schedules. (a) Control group in 2nd year vs experimental group in 3rd year. (b) Control group in 3rd year vs experimental group in 4th year. The experimental group was not exposed to low temperatures in the second winter, which delayed adult emergence by 1 year. Comparisons were made between adults of the control and experimental groups (Fig. 1). Reduction rates in adult body size by spending one additional year in diapause were calculated as the difference in expected pronotum width between the two groups/expected pronotum width in the control (percentage).

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Male eye span exhibited body size-dependent changes: it was nearly maintained in larger individuals but greatly decreased in smaller individuals when diapause was extended for an additional year (ancova, F1,174 = 11·38, P = 0·0009 for slopes). In females, eye span decreased according to the duration of diapause in any body size (F1,136 = 1·04, P = 0·30 for slopes; F1,137 = 8·19, P = 0·005 for intercepts; Fig. 5, left). In the subsequent year (control third-year emergence group vs experimental fourth-year emergence group), the pronotum width–eye span relationships did not differ in males (ancova, F1,24 = 1·153, P = 0·29 for slopes; F1,25 = 0·52, P = 0·47 for intercepts). In females, although based on a small sample size, the pronotum width–eye span relationships showed a weak tendency for decreased eye span in smaller individuals (F1,19 = 4·62, P = 0·045 for slopes; Fig. 5, right).

image

Figure 5. Pronotum width–eye span relationships between control (open symbols, solid lines) and experimental (closed symbols, broken lines) groups of Exechesops leucopis with different emergence schedules (Fig. 1) in males (triangles) and females (circles). (a) Control group in 2nd year vs experimental group in 3rd year. (b) Control group in 3rd year vs experimental group in 4th year. Insets, male and female heads with eye-span measurements.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

factors affecting variation in the duration of diapause

Observations of adult emergence from the single cohort revealed that E. leucopis had variable diapause, ranging from 1 to 4 years. The yearly emergence patterns did not differ between the sexes. Variation in diapause has been confirmed within offspring produced by a single female (unpublished data). Prolonged and variable diapause has been reported in several insect species, in particular, seed predators (reviewed by Danks 1987). In seed-bearing trees the number of seeds produced fluctuates unpredictably among years, particularly in species that undergo mast seeding (masting), which is the intermittent production of large seed crops by a population of trees (Kelly 1994). Extended diapause observed in seed-predatory insects may be an adaptive bet-hedging strategy for unpredictable fluctuations in seed production (Maeto & Ozaki 2003; Soula & Menu 2003). In the host plants of E. leucopis, seed production fluctuates considerably among years (Mizui 1993; H. Nagase, personal communication for S. japonica; Mizui 1993; Kato & Hiura 1999 for S. obassia). Therefore variation in diapause may be an adaptive response by E. leucopis to spread a possible risk, such as low oviposition rate, as the result of a poor seed crop among host trees.

Factors terminating diapause include temperature, photoperiod, moisture, food and host-derived cues (reviewed by Danks 1987). The physiological mechanisms producing variation in diapause length remain unexamined in E. leucopis. However, my results suggest that exposure to low temperatures is absolutely necessary to terminate diapause because no adults emerged without artificial chilling during rearing. If chilling is required to break diapause and cause emergence, this could be used to determine the emergence based on the severity of the winter.

costs of diapause

The length of diapause differed with body size among final-instar larvae. Smaller individuals tended to terminate diapause earlier. Similar results have been reported for the moths Laspeyresia strobilella (Bakke 1971; Nesin 1985), Prodoxus y-inversus (Powell 1989) and Barbara colfaxiana (Sahota & Ibaraki 1991); the desert bee Perduta portalis (Danforth 1999); and the chestnut weevil Curculio elephas (Menu & Desouhant 2002). In these insects, size dependency in the length of diapause has been explained primarily by the amount of energy resources that individuals can metabolize during diapause, because extending diapause is more costly in terms of relative weight loss for smaller individuals. In E. leucopis, I have demonstrated that smaller individuals suffer a higher metabolic cost because their body size significantly decreased as a result of the extra year in diapause. Therefore smaller individuals should emerge earlier than heavier individuals because of resource limitations. On the other hand, individuals with a longer diapause may become smaller because of greater resource consumption. This may explain the fact that the third-year emergence group tended to be smaller than the second-year emergence group.

The effects of the costs of diapause on sexually selected traits were also analysed. Despite a long and variable duration of diapause, adults emerged relatively synchronously every year. The sex ratio was nearly 0·5, and the protandrous emergence patterns (early emergence of males) were also repeated. In several insect species with non-overlapping generations, protandry occurs in both diapausing and non-diapausing generations, a context in which selection could act directly on a sexual difference (Rutowsky 1997). Selection may favour males that emerge before females to compete among males for mates, and may favour females that minimize the cumulative probability of mortality between emergence and mating. Male E. leucopis fight on fruit of the host plants, making contact with their flat faces and pushing each other (Yoshitake & Kawashima 2004; Matsuo 2005). Such strong male–male competition at female oviposition sites may be one of the causes of protandry.

Experimental elongation of diapause for one additional year decreased the body size of E. leucopis. However, body size changed disproportionately in males. Eyestalks tended to be longer in larger than in smaller individuals, according to the duration of diapause. The male eyestalk is a sexually selected trait because its size affects the outcome of male–male combat (Matsuo 2005). Therefore males appear to allocate more resources to sexually selected traits than to other body parts when pupating after a long and costly larval diapause. Smaller males, however, suffered a relatively higher cost of diapause than larger males, which may have exceeded the cost of maintaining the expected eyestalk size after the long diapause.

A disproportional allocation of resources to adult body parts was not detected in females, as expected by general sexual selection theory. Females also combat each other on the surface of fruit in which they oviposit, but infrequently and not as strongly as males. In female–female interactions prior residency is an important determinant of victory, irrespective of morphological traits (Matsuo 2005). During conditions causing diapause costs, females seem to maintain a constant body size rather than eye span. This may be related to female fitness, because the number of eggs produced during a lifetime is positively correlated with the pronotum width of the female (unpublished data). Thus the costs of diapause affect the body shape of males and females through different selection forces.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

This study was conducted under the supervision of Tadashi Suzuki (Tokyo Metropolitan University). I thank Tamotsu Kusano, Fumio Hayashi and Yoshitaka Kamimura for valuable advice during the study. I also thank T. Suzuki and F. Hayashi for improving earlier versions of the manuscript.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • Aizawa, M. (1989) Life history of the fungus weevil, Exechesops leucopis. MSc thesis, Tsukuba University, Ibaraki, Japan (in Japanese).
  • Bakke, A. (1971) Distribution of prolonged diapausing larvae in populations of Laspeyresia strobilella (L.) (Lep., Tortricidae) from spruce cones. Norsk Entomologisk Tidsskrift 18, 8993.
  • Carne, P.B. (1969) On the population dynamics of the eucalypt-defoliating sawfly Perga affinis Kirby (Hymenoptera). Australian Journal of Zoology 17, 113141.
  • Danforth, B.N. (1999) Emergence dynamics and bet hedging in a desert bee Perdita portalis. Proceedings of the Royal Society of London B 266, 19851994.
  • Danks, H.V. (1987) Insect dormancy: an ecological perspective. Biological Survey of Canada. National Museum of Natural Science, Ottawa, Ontario, Canada.
  • Denlinger, D.L. (1981) Basis for a skewed sex ratio in diapause-destined flesh flies. Evolution 35, 12471248.
  • Hairstone, N.G. Jr (1998) Time travelers: what's timely in diapause research? Archives of Hydrobiology Special Issue. Advances in Limnology 52, 115.
  • Kato, E. & Hiura, T. (1999) Fruit set in Styrax obassia (Styracaceae): the effect of light availability, display size, and local floral density. American Journal of Botany 86, 495501.
  • Kelly, D. (1994) The evolutionary ecology of mast seeding. Trends in Ecology and Evolution 9, 465470.
  • Leather, S.R., Walters, K.F.A. & Bale, J.S. (1993) The Ecology of Insect Overwintering. Cambridge University Press, Cambridge, UK.
  • Lees, A.D. (1955) The Physiology of Diapause in Arthropods. Cambridge University Press, Cambridge, UK.
  • Maeto, K. & Ozaki, K. (2003) Prolonged diapause of specialist seed-feeders makes predator satiation unstable in masting of Quercus crispula. Oecologia 137, 392398.
  • Matsuo, Y. (2004) Diel activity periodicity of Exechesops leucopis (Coleoptera: Anthribidae) monitored by actography using infrared beams. Natural Environmental Science Research 17, 5961.
  • Matsuo, Y. (2005) Extreme eye projection in the male weevil Exechesops leucopis (Coleoptera: Anthribidae): its effect on intrasexual behavioral inteferences. Journal of Insect Behavior 18, 465477.
  • Menu, F. & Desouhant, E. (2002) Bet-hedging for variability in life cycle duration: bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause. Oecologia 132, 167174.
  • Mizui, T. (1993) Ecological studies on seed reproduction in deciduous trees. Bulletin of the Hokkaido Forest Experiment Station 30, 167 (in Japanese).
  • Nesin, A.P. (1985) Contribution to the knowledge of the diapause of some pests of cones and seeds of conifers. Entomological Review 68, 3843.
  • Peters, R.H. (1983) The Ecological Implications of Body Size. Cambridge University Press, Cambridge, UK.
  • Phillipi, T. (1993) Bet-hedging germination of desert annuals: beyond the first year. American Naturalist 142, 474487.
  • Powell, F.A. (1989) Synchronized, mass-emergences of a yucca moth, Prodoxus y-inversus (Lepidoptera: Prodoxidae) after 16 and 17 years in diapause. Oecologia 81, 490493.
  • Rutowsky, R.L. (1997) Sexual dimorphism, mating systems and ecology in butterflies. The Evolution of Mating Systems in Insects and Arachnids (eds J.C.Choe & B.J.Crespi), pp. 257272. Cambridge University Press, Cambridge, UK.
  • Sahota, T.S. & Ibaraki, A. (1991) 1- and 2-year dormancy of the Douglas-fir cone moth, Barbara colfaxiana KFT (Lepidoptera: Olethreutidae): possible relation to individual weights. Canadian Entomologist 123, 11531155.
  • Soula, B. & Menu, F. (2003) Variability in diapause duration in the chestnut weevil: mixed ESS, genetic polymorphism or bet-hedging. Oikos 100, 574580.
  • Tokunaga, M. (1937) Insects as fishing bait 1: Exechesops leucopis. Kansai Kontyu Zasshi 4, 122 (in Japanese).
  • Yoshitake, H. & Kawashima, I. (2004) Sexual dimorphism and agonistic behavior of Exechesops leucopis (Jordan) (Coleoptera: Anthribidae: Anthribinae). Coleopterists Bulletin 58, 7783.