Counterintuitive size patterns in bivoltine moths: late-season larvae grow larger despite lower food quality

Abstract

Within a season, successive generations of short-lived organisms experience different combinations of environmental parameters, such as temperature, food quality and mortality risk. Adult body size of e.g. insects is therefore expected to vary both as a consequence of proximate environmental effects as well as adaptive responses to seasonal cues. In this study, we examined intraspecific differences in body size between successive generations in 12 temperate bivoltine moths (Lepidoptera), with the ultimate goal to critically compare the role of proximate and adaptive mechanisms in determining seasonal size differences. In nearly all species, individuals developing late in the season (diapausing generation) attained a larger adult size than their conspecifics with the larval period early in the season (directly developing generation) despite the typically lower food quality in late summer. Rearing experiments conducted on one of the studied species, Selenia tetralunaria also largely exclude the possibility that the proximate effects of food quality and temperature are decisive in determining size differences between successive generations. Adaptive explanations appear likely instead: the larger body size in the diapausing generation may be adaptively associated with the lower bird predation pressure late in the season, and/or the likely advantage of large pupal size during overwintering.

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References

  1. Abrams PA, Rowe L (1996) The effects of predation on the age and size of maturity of prey. Evolution 50:1052–1061

    Article  Google Scholar 

  2. Angilletta MJ, Dunham AE (2003) The temperature–size rule in ectotherms: simple evolutionary explanations may not be general. Am Nat 162:332–342

    Article  PubMed  Google Scholar 

  3. Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509

    Article  Google Scholar 

  4. Atkinson D, Sibly RM (1997) Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol Evol 12:235–239

    Article  Google Scholar 

  5. Ayres MP, MacLean SF Jr (1987) Development of birch leaves and the growth energetics of Epirrita autumnata (Geometridae). Ecology 68:558–568

    Article  Google Scholar 

  6. Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–674

    Article  Google Scholar 

  7. Berger D, Walters R, Gotthard K (2006) What keeps insects small? Size dependent predation on two species of butterfly larvae. Evol Ecol 20:575–589

    Article  Google Scholar 

  8. Blanckenhorn WU, Demont M (2004) Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integr Comp Biol 44:413–424

    Article  Google Scholar 

  9. Brower LP (1989) Chemical defence in butterflies. In: Vane-Wright RI, Ackery PR (eds) The biology of butterflies. Princeton University Press, Princeton, NJ, pp 109–134

    Google Scholar 

  10. Cornell HV, Hawkins BA (1995) Survival patterns and mortality sources of herbivorous insects: some demographic trends. Am Nat 145:563–593

    Article  Google Scholar 

  11. Danks HV (2007) The elements of seasonal adaptations in insects. Can Entomol 139:1–44

    Article  Google Scholar 

  12. EMHI (Estonian Meteorological and Hydrological Institute) (2008) Mean temperature 1961–1990. http://www.emhi.ee/?ide=6,299,302

  13. Esperk T, Tammaru T, Nylin S (2007a) Intraspecific variability in number of larval instars in insects. J Econ Entomol 100:627–645

    Article  PubMed  Google Scholar 

  14. Esperk T, Tammaru T, Nylin S, Teder T (2007b) Achieving high sexual size dimorphism in insects: females add instars. Ecol Entomol 32:243–256

    Article  Google Scholar 

  15. Fischer K, Fiedler K (2001) Sexual differences in life-history traits in the butterfly Lycaena tityrus: a comparison between direct and diapause development. Entomol Exp Appl 100:325–330

    Article  Google Scholar 

  16. Fischer K, Fiedler K (2002) Reaction norms for age and size at maturity in response to temperature: a test of the compound interest hypothesis. Evol Ecol 16:333–349

    Article  Google Scholar 

  17. Gotthard K (2000) Increased risk of predation as a cost of high growth rate: an experimental test in a butterfly. J Anim Ecol 69:896–902

    Article  Google Scholar 

  18. Gotthard K (2001) Growth strategies of ectothermic animals in temperate environments. In: Atkinson D, Thorndyke M (eds) Environment and animal development: genes, life histories and plasticity. BIOS Scientific Publishers, Oxford, pp 287–304

    Google Scholar 

  19. Gotthard K, Nylin S, Wiklund C (1999) Seasonal plasticity in two satyrine butterflies: state-dependent decision making in relation to daylength. Oikos 84:453–462

    Article  Google Scholar 

  20. Higgins L (2000) The interaction of season length and development time alters size at maturity. Oecologia 122:51–59

    Article  Google Scholar 

  21. Iwasa Y, Ezoe H, Yamauchi A (1994) Evolutionarily stable seasonal timing of univoltine and bivoltine insects. In: Danks HV (ed) Insect life-cycle polymorphism: theory, evolution and ecological consequences for seasonality and diapause control. Kluwer, Dordrecht, pp 69–89

    Google Scholar 

  22. Karl I, Fischer K (2008) Why get big in the cold? Towards a solution to a life-history puzzle. Oecologia 155:215–225

    Article  PubMed  Google Scholar 

  23. Karlsson B, Wickman P-O (1989) The cost of prolonged life: an experiment on a nymphalid butterfly. Funct Ecol 3:399–405

    Article  Google Scholar 

  24. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute, Cary

    Google Scholar 

  25. Liu Z, Gong P, Wu K, Wei W, Sun J, Li D (2007) Effects of larval host plants on over-wintering preparedness and survival of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). J Insect Physiol 53:1016–1026

    Article  CAS  PubMed  Google Scholar 

  26. Mänd T, Tammaru T, Mappes J (2007) Size dependent predation risk in cryptic and conspicuous insects. Evol Ecol 21:485–498

    Article  Google Scholar 

  27. Marttila O, Saarinen K, Haahtela T, Pajari M (1996) Suomen kiitäjät ja kehrääjät. Kirjayhtymä, Helsinki

    Google Scholar 

  28. Mikkola K, Jalas I (1977) Suomen perhoset. Yökköset 1. Otava, Helsinki

    Google Scholar 

  29. Mikkola K, Jalas I, Peltonen O (1985) Suomen perhoset. Mittarit 1. Tampereen kirjapaino Oy, Tampere

    Google Scholar 

  30. Mikkola K, Jalas I, Peltonen O (1989) Suomen perhoset. Mittarit 2. Hangon kirjapaino, Hanko

    Google Scholar 

  31. Nijhout HF (2003) Development and evolution of adaptive polyphenisms. Evol Dev 5:9–18

    Article  PubMed  Google Scholar 

  32. Nylin S (1992) Seasonal plasticity in life-history traits—growth and development in Polygonia c-album (Lepidoptera, Nymphalidae). Biol J Linn Soc 47:301–323

    Article  Google Scholar 

  33. Nylin S, Svärd L (1991) Latitudinal patterns in the size of European butterflies. Holarctic Ecol 14:192–202

    Google Scholar 

  34. Nylin S, Wickman P-O, Wiklund C (1989) Seasonal plasticity in growth and development of the speckled wood butterfly, Pararge aegeria (Satyrinae). Biol J Linn Soc 38:155–171

    Article  Google Scholar 

  35. Peckarsky BL, Taylor BW, Lytle DA, McIntosh AR, McPeek MA (2001) Variation in mayfly size at metamorphosis as a developmental response to risk of predation. Ecology 82:740–757

    Article  Google Scholar 

  36. Relyea RA (2007) Getting out alive: how predators affect the decision to metamorphose. Oecologia 152:389–400

    Article  PubMed  Google Scholar 

  37. Remmel T, Tammaru T (2009) Size-dependent predation risk in tree-feeding insects with different colouration strategies: a field experiment. J Anim Ecol 78:973–980

    Article  PubMed  Google Scholar 

  38. Remmel T, Tammaru T, Mägi M (2009) Seasonal mortality trends in tree-feeding insects: a field experiment. Ecol Entomol 34:98–106

    Article  Google Scholar 

  39. Roff DA (1980) Optimizing development time in a seasonal environment: the “ups and downs” of clinal variation. Oecologia 45:202–208

    Article  Google Scholar 

  40. SAS Institute (2008) SAS/STAT 9.2 user’s guide. SAS Institute, Cary

    Google Scholar 

  41. Schroeder LA (1986) Changes in tree leaf quality and growth-performance of lepidopteran larvae. Ecology 67:1628–1636

    Article  Google Scholar 

  42. Scriber JM (1994) Climatic legacies and sex chromosomes: latitudinal patterns of voltinism, diapause, size, and host-plant selection in two species of swallowtail butterflies at their hybrid zone. In: Danks HV (ed) Insect life-cycle polymorphism: theory, evolution and ecological consequences for seasonality and diapause control. Kluwer, Dordrecht, pp 133–171

    Google Scholar 

  43. Sillén-Tullberg B (1988) Evolution of gregariousness in aposematic butterfly larvae: a phylogenetic analysis. Evolution 42:293–305

    Article  Google Scholar 

  44. Stoks R (2001) Food stress and predator-induced stress shape developmental performance in a damselfly. Oecologia 127:222–229

    Article  Google Scholar 

  45. Svensson I (1993) Fjärilkalender. Kristianstad

  46. Tanaka K, Tsubaki Y (1984) Seasonal dimorphism, growth and food consumption in the swallowtail butterfly, Papilio xuthus L. Kontyû 52:390–398

    Google Scholar 

  47. Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, Oxford

    Google Scholar 

  48. Van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52:37–55

    Article  PubMed  CAS  Google Scholar 

  49. Viidalepp J, Remm H (1996) Eesti liblikate määraja. Valgus, Tallinn

    Google Scholar 

  50. Werner EE, Anholt BR (1993) Ecological consequences of the trade of between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272

    Article  CAS  PubMed  Google Scholar 

  51. Wiklund C, Fagerström T (1977) Why do males emerge before females? A hypothesis to explain the incidence of protandry in butterflies. Oecologia 31:153–158

    Article  Google Scholar 

  52. Wiklund C, Järvi T (1982) Survival of distasteful insects after being attacked by naive birds: a reappraisal of the theory of aposematic coloration evolving through individual selection. Evolution 36:998–1002

    Article  Google Scholar 

  53. Wiklund C, Nylin S, Forsberg J (1991) Sex-related variation in growth rate as a result of selection for large size and protandry in a bivoltine butterfly, Pieris napi. Oikos 60:241–250

    Article  Google Scholar 

  54. Windig JJ (1999) Trade-offs between melanization, development time and adult size in Inachis io and Araschnia levana (Lepidoptera: Nymphalidae)? Heredity 82:57–68

    Article  Google Scholar 

  55. Windig JJ, Lammar P (1999) Evolutionary genetics of seasonal polyphenism in the map butterfly Araschnia levana (Nymphalidae: Lepidoptera). Evol Ecol Res 1:875–894

    Google Scholar 

  56. Zvereva EL (2002) Effects of host plant quality on overwintering success of the leaf beetle Chrysomela lapponica (Coleoptera: Chrysomelidae). Eur J Entomol 99:189–195

    Google Scholar 

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Acknowledgements

We are thankful for the possibility to use the material accumulated through the Estonian Environmental Monitoring Programme, coordinated by Erki Õunap. We thank Rein Karulaas and Taavet Kukk for technical help. The study was supported by the Estonian Science Foundation (grants 6619, 7406 and 7522), the Estonian Ministry of Education and Science (targeted financing project SF0180122s08) as well as by the European Union through the European Regional Development Fund (Center of Excellence FIBIR). All the experiments complied with the laws of Estonia.

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Correspondence to Tiit Teder.

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Communicated by Thomas Hoffmeister.

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Teder, T., Esperk, T., Remmel, T. et al. Counterintuitive size patterns in bivoltine moths: late-season larvae grow larger despite lower food quality. Oecologia 162, 117–125 (2010). https://doi.org/10.1007/s00442-009-1439-1

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Keywords

  • Phenology
  • Phenotypic plasticity
  • Predation risk
  • Time stress
  • Voltinism