Eur. J. Entomol. 118: 214-224, 2021 | DOI: 10.14411/eje.2021.023

Changes in the body size of black-veined white, Aporia crataegi (Lepidoptera: Pieridae), recorded in a natural population in response to different spring weather conditions and at different phases of an outbreakOriginal article

Igor A. SOLONKIN ORCID..., Aleksei O. SHKURIKHIN ORCID..., Tatyana S. OSLINA ORCID..., Elena Yu. ZAKHAROVA ORCID...
Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences, Ekaterinburg, 620144, Russia; e-mails: igorsolonkin@yandex.ru, ashkurikhin@yandex.ru, oslina_ts@ipae.uran.ru, zakharova@ipae.uran.ru

Changes in body size in response to environmental factors (especially temperature) is one of the crucial traits studied in connection with insect adaptation to climate change. However, current data on the strength and direction of temperature-size responses in Lepidoptera are inconsistent and the reasons for this are unclear. This study investigates the relationship between the adult size of Aporia crataegi L. (Lepidoptera: Pieridae) and spring weather conditions (temperature and rainfall) at different phases in its outbreak cycle (low population density or high abundance). The forewing area of A. crataegi, a univoltine and irruptive Lepidopteran species, was used as a proxy for overall body size. It was found that temperature in the last month before imago emergence (May) and temperature in the larval growth period following overwintering (April) had differing effects on imago size. The fact that the wing size of both male and female A. crataegi increased following higher temperatures in May corresponds with the converse temperature-size rule and is consistent with the predictions of life history theory for univoltine species. Conversely, while imago size decreased following higher temperatures in April, increased rainfall had a slightly positive effect on imago size. The wings of A. crataegi at the peak of abundance were larger than when sampled during periods of low population density, contradicting available data on changes in the body weight of A. crataegi recorded during outbreaks.

Keywords: Lepidoptera, Pieridae, Aporia crataegi, body size, phenotypic plasticity, temperature-size response, outbreak

Received: January 13, 2021; Revised: June 17, 2021; Accepted: June 17, 2021; Published online: July 12, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
SOLONKIN, I.A., SHKURIKHIN, A.O., OSLINA, T.S., & ZAKHAROVA, E.Y. (2021). Changes in the body size of black-veined white, Aporia crataegi (Lepidoptera: Pieridae), recorded in a natural population in response to different spring weather conditions and at different phases of an outbreak. EJE118, Article 214-224. https://doi.org/10.14411/eje.2021.023
Download citation

References

  1. Angilletta M.J., Steury T.D. & Sears M.W. 2004: Temperature, growth rate, and body size in ectotherms: fitting pieces of a life history puzzle. - Integr. Comp. Biol. 44: 498-509. Go to original source...
  2. Atkinson D. 1994: Temperature and organism size: a biological law for ectotherms. - Adv. Ecol. Res. 25: 1-58. Go to original source...
  3. Atkinson D. & Sibly R.M. 1997: Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. - Trends Ecol. Evol. 12: 235-239. Go to original source...
  4. Atterholt A.L. & Solensky M.J. 2010: Effects of larval rearing density and food availability on adult size and coloration in monarch butterflies (Lepidoptera: Nymphalidae). - J. Entomol. Sci. 45: 366-377. Go to original source...
  5. Audzijonyte A., Barneche D.R., Baudron A.R., Belmaker J., Clark T. D., Marshall C.T., Morrongiello J.R. & van Rijn I. 2019: Is oxygen limitation in warming waters a valid mechanism to explain decreased body sizes in aquatic ectotherms? - Global Ecol. Biogeogr. 28: 64-77. Go to original source...
  6. Baranchikov Yu.N. 1987: Trophic Specialization of Lepidoptera. ILiD SB AS USSR, Krasnoyarsk, 171 pp. [in Russian].
  7. Barton M., Sunnucks P., Norgate M., Murray N. & Kearney M. 2014: Co-gradient variation in growth rate and development time of a broadly distributed butterfly. - PLoS ONE 9(4): e95258, 8 pp. Go to original source...
  8. Bauerfeind S.S. & Fischer K. 2013: Testing the plant stress hypothesis: stressed plants offer better food to an insect herbivore. - Entomol. Exp. Appl. 149: 148-158. Go to original source...
  9. Beckwith R.C. 1982: Effects of constant laboratory temperatures on the Douglas-fir tussock moth (Lepidoptera: Lymantriidae). - Environ. Entomol. 11: 1159-1163. Go to original source...
  10. Boggs C.L. 2009: Understanding insect life histories and senescence through a resource allocation lens. - Funct. Ecol. 23: 27-37. Go to original source...
  11. Boggs C.L. & Niitepõld K. 2016: Effects of larval dietary restriction on adult morphology, with implications for flight and life history. - Entomol. Exp. Appl. 159: 189-196. Go to original source...
  12. Bowden J.J., Eskildsen A., Hansen R.R., Olsen K., Kurle C.M. & Høye T.T. 2015: High-Arctic butterflies become smaller with rising temperatures. - Biol. Lett. 11: 20150574, 4 pp. Go to original source...
  13. Carter M.R., Ravlin F.W. & McManus M.L. 1991: Changes in gypsy moth (Lepidoptera: Lymantriidae) fecundity and male wing length resulting from defoliation. - Environ. Entomol. 20: 1042-1047. Go to original source...
  14. Chown S.L. & Nicolson S. 2004: Insect Physiological Ecology: Mechanisms and Patterns. Oxford University Press, New York, 253 pp. Go to original source...
  15. Couture J.J., Serbin S.P. & Townsend P.A. 2015: Elevated temperature and periodic water stress alter growth and quality of common milkweed (Asclepias syriaca) and monarch (Danaus plexippus) larval performance. - Arthropod Plant Interact. 9: 149-161. Go to original source...
  16. Davidowitz G. & Nijhout H.F. 2004: The physiological basis of reaction norms: the interaction among growth rate, the duration of growth and body size. - Integr. Comp. Biol. 44: 443-449. Go to original source...
  17. Davies W.J. 2019: Multiple temperature effects on phenology and body size in wild butterflies predict a complex response to climate change. - Ecology 100(4): e02612, 11 pp. Go to original source...
  18. Dmitriew C.M. 2011: The evolution of growth trajectories: what limits growth rate? - Biol. Rev. 86: 97-116. Go to original source...
  19. Fang J., Piao S., Zhou L., He J., Wei F., Myneni R.B., Tucker C.J. & Tan K. 2005: Precipitation patterns alter growth of temperate vegetation. - Geophys. Res. Lett. 32(21): L21411, 5 pp. Go to original source...
  20. Fenberg P.B., Self A., Stewart J.R., Wilson R.J. & Brooks S.J. 2016: Exploring the universal ecological responses to climate change in a univoltine butterfly. - J. Anim. Ecol. 85: 739-748. Go to original source...
  21. Fischer K. & Karl I. 2010: Exploring plastic and genetic responses to temperature variation using copper butterflies. - Clim. Res. 43: 17-30. Go to original source...
  22. Gely C., Laurance S.G. & Stork N.E. 2020: How do herbivorous insects respond to drought stress in trees? - Biol. Rev. 95: 434-448. Go to original source...
  23. Ghosh S.M., Testa N.D. & Shingleton A.W. 2013: Temperature-size rule is mediated by thermal plasticity of critical size in Drosophila melanogaster. - Proc. R. Soc. (B) 280(1760): 20130174, 8 pp. Go to original source...
  24. Gibbs M., Wiklund C. & Van Dyck H. 2011a: Phenotypic plasticity in butterfly morphology in response to weather conditions during development. - J. Zool. 283: 162-168. Go to original source...
  25. Gibbs M., Wiklund C. & Van Dyck H. 2011b: Temperature, rainfall and butterfly morphology: does life history theory match the observed pattern? - Ecography 34: 336-344. Go to original source...
  26. Gorbunov P.Yu. & Kosterin O.E. 2003: The Butterflies (Hesperioidea and Papilionoidea) of North Asia (Asian Part of Russia) in Nature. Vol. 1. Rodina & Fodio, Gallery Fund, Moscow, Chelyabinsk, 392 pp.
  27. Gotthard K. 2008: Adaptive growth decisions in butterflies. - Bioscience 58: 222-230. Go to original source...
  28. Gutbrodt B., Mody K. & Dorn S. 2011: Drought changes plant chemistry and causes contrasting responses in lepidopteran herbivores. - Oikos 120: 1732-1740. Go to original source...
  29. Honek A. 1993: Intraspecific variation in body size and fecundity in insects: a general relationship. - Oikos 66: 483-492. Go to original source...
  30. Horne C.R., Hirst A.G. & Atkinson D. 2015: Temperature size responses match latitudinal size clines in arthropods, revealing critical differences between aquatic and terrestrial species. - Ecol. Lett. 18: 327-335. Go to original source...
  31. Horne C.R., Hirst A.G., Atkinson D., Almeda R. & Kiørboe T. 2019: Rapid shifts in the thermal sensitivity of growth but not development rate causes temperature-size response variability during ontogeny in arthropods. - Oikos 128: 823-835. Go to original source...
  32. Hothorn T., Bretz F. & Westfall P. 2008: Simultaneous inference in general parametric models. - Biom. J. 50: 346-363. Go to original source...
  33. Huberty A.F. & Denno R.F. 2004: Plant water stress and its consequences for herbivorous insects: a new synthesis. - Ecology 85: 1383-1398. Go to original source...
  34. Inbar M., Doostdar H. & Mayer R.T. 2001: Suitability of stressed and vigorous plants to various insect herbivores. - Oikos 94: 228-235. Go to original source...
  35. Isaev A.S., Hlebopros R.G., Nedorezov L.V., Kondakov Yu.P., Kiselev V.V. & Sukhovol'skiĭ V.G. 2001: Population Dynamics of Forest Insects. Nauka, Moscow, 374 pp. [in Russian].
  36. Isaev A.S., Sukhovol'skiĭ V.G., Tarasova O.V., Palnikova E.N. & Kovalev A.V. 2017: Forest Insect Population Dynamics, Outbreaks, and Global Warming Effects. Scrivener, Beverly, 286 pp. Go to original source...
  37. Juhasz E., Vegvari Z., Toth J.P., Pecsenye K. & Varga Z. 2016: Climate-induced changes in the phenotypic plasticity of the Heath Fritillary, Melitaea athalia (Lepidoptera: Nymphalidae). - Eur. J. Entomol. 113: 104-112. Go to original source...
  38. Kamata N. & Igarashi M. 1995: Relationship between temperature, number of instars, larval growth, body size, and adult fecundity of Quadricalcarifera punctatella (Lepidoptera: Notodontidae): cost-benefit relationship. - Environ. Entomol. 24: 648-656. Go to original source...
  39. Karl I. & Fischer K. 2008: Why get big in the cold? Towards a solution to a life-history puzzle. - Oecologia 155: 215-225. Go to original source...
  40. Kingsolver J.G. & Huey R.B. 2008: Size, temperature, and fitness: three rules. - Evol. Ecol. Res. 10: 251-268.
  41. Kingsolver J.G., Massie K.R., Ragland G.J. & Smith M.H. 2007: Rapid population divergence in thermal reaction norms for an invading species: breaking the temperature-size rule. - J. Evol. Biol. 20: 892-900. Go to original source...
  42. Klemola T., Ruohomäki K., Andersson T. & Neuvonen S. 2004: Reduction in size and fecundity of the autumnal moth, Epirrita autumnata, in the increase phase of a population cycle. - Oecologia 141: 47-56. Go to original source...
  43. Klockmann M., Karajoli F., Kuczyk J., Reimer S. & Fischer K. 2017: Fitness implications of simulated climate change in three species of copper butterflies (Lepidoptera: Lycaenidae). - Biol. J. Linn. Soc. 120: 125-143. Go to original source...
  44. Kulikov P.V., Zolotareva N.V. & Podgaevskaya E.N. 2013: Endemic Plants of the Ural in the Flora of the Sverdlovsk Region. Goshchickij, Ekaterinburg, 612 pp. [in Russian].
  45. Kuznetsova V.V. & Palnikova E.N. 2014: Factors affecting abundance dynamics of the thorn butterfly (Aporia crataegi L.) in suburban standing woods of Krasnoyarsk city. - Izv. S-Peterb. Lesotehn. Akad. 207: 49-59 [in Russian, English abstract].
  46. Lie Z., Xue L. & Jacobs D.F. 2018: Allocation of forest biomass across broad precipitation gradients in China's forests. - Sci. Rep. 8: 10536, 8 pp. Go to original source...
  47. Mega N.O. 2014: The adult body size variation of Dryas iulia (Lepidoptera, Nymphalidae, Heliconiinae) in different populations is more influenced by temperature variation than by host plant availability during the seasons. - Entomol. Sci. 17: 376-387. Go to original source...
  48. Merrill R.M., Gutiérrez D., Lewis O.T., Gutiérrez J., Díez S.B. & Wilson R.J. 2008: Combined effects of climate and biotic interactions on the elevational range of a phytophagous insect. - J. Anim. Ecol. 77: 145-155. Go to original source...
  49. Miller W.E. 1977: Weights of Polia grandis pupae reared at two constant temperatures (Lepidoptera: Noctuidae). - Great Lakes Entomol. 10: 47-49. Go to original source...
  50. Myers J.H. & Cory J.S. 2013: Population cycles in forest Lepidoptera revisited. - Annu. Rev. Ecol. Syst. 44: 565-592. Go to original source...
  51. Nijhout H.F & Grunert L.W. 2010: The cellular and physiological mechanism of wing-body scaling in Manduca sexta. - Science 330: 1693-1695. Go to original source...
  52. Nijhout H.F., Davidowitz G. & Roff D.A. 2006: A quantitative analysis of the mechanism that controls body size in Manduca sexta. - J. Biol. 5(5): 16, 15 pp. Go to original source...
  53. Nylin S. & Gotthard K. 1998: Plasticity in life-history traits. - Annu. Rev. Entomol. 43: 63-83. Go to original source...
  54. Olszewska M.A. & Kwapisz A. 2011: Metabolite profiling and antioxidant activity of Prunus padus L. flowers and leaves. - Nat. Prod. Res. 25: 1115-1131. Go to original source...
  55. Palanichamy S., Ponnuchamy R. & Thangaraj T. 1982: Effect of temperature on food intake, growth and conversion efficiency of Eupterote mollifera (Insecta: Lepidoptera). - Proc. Indian Acad. Sci. (Anim. Sci.) 91: 417-422. Go to original source...
  56. Renaud O. & Victoria-Feser M.P. 2010: A robust coefficient of determination for regression. - J. Stat. Plann. Infer. 140: 1852-1862. Go to original source...
  57. R Core Team 2020: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, URL: https://www.R-project.org
  58. Rhainds M. 2020: Variation in wing load of female spruce budworms (Lepidoptera: Tortricidae) during the course of an outbreak: evidence for phenotypic response to habitat deterioration in collapsing populations. - Environ. Entomol. 49: 238-245. Go to original source...
  59. Rohlf F.J. 2006: TpsDig Version 2.10. URL: https://life.bio.sunysb.edu/morph
  60. Rohlf F.J. 2008: TpsUtil Version 1.40. URL: https://life.bio.sunysb.edu/morph
  61. Russell L. 2020: Emmeans: Estimated Marginal Means, Aka Least-squares Means. R Package Version 1.4.6. URL: https://CRAN.R-project.org/package=emmeans
  62. Schielzeth H. 2010: Simple means to improve the interpretability of regression coefficients. - Methods Ecol. Evol. 1: 103-113. Go to original source...
  63. Tammaru T., Esperk T. & Castellanos I. 2002: No evidence for costs of being large in females of Orgyia spp. (Lepidoptera, Lymantriidae): larger is always better. - Oecologia 133: 430-438. Go to original source...
  64. Tarasova O.V., Kalashnikova I.I. & Kuznecsova V.V. 2015: Energy balance of fodder consumption by phyllophagous insects: optimization model. - Sib. Lesn. Zh. 2015(3): 83-92 [in Russian, English abstract].
  65. Tatarinov A.G. & Dolgin M.M. 1999: Fauna of the European North-East of Russia. Rhopalocera Lepidoptera. Nauka, Saint Petersburg, 183 pp. [in Russian].
  66. Tigreros N. & Davidowitz G. 2019: Flight-fecundity tradeoffs in wing-monomorphic insects. - Adv. Insect Physiol. 56: 1-41. Go to original source...
  67. Vshivkova T.A. 2009: Evaluation of food suitability for the gypsy moth (Lymantria dispar L.) neonate larvae. - Forestry Bull. 2009(5): 107-110 [in Russian, English abstract].
  68. Wilson R.J., Brooks S.J. & Fenberg P.B. 2019: The influence of ecological and life history factors on ectothermic temperature-size responses: Analysis of three Lycaenidae butterflies (Lepidoptera). - Ecol. Evol. 9: 10305-10316. Go to original source...
  69. Yohai V.J. 1987: High breakdown-point and high efficiency estimates for regression. - Ann. Statist. 15: 642-665. Go to original source...
  70. Zakharova E.Yu., Shkurikhin A.O., Solonkin I.A. & Oslina T.S. 2020: Effect of host plants on the viability of black-veined white Aporia crataegi L. at low natural population density. - Russ. J. Ecol. 51: 549-555. Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.