Phenotypic variability of Aphantopus hyperantus and Coenonympha arcania (Lepidoptera: nymphalidae) in the vicinity of the Sredneuralsk copper smelter. 1. Metal content and wing length

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

We tested the hypotheses that near a copper smelter, marigolds Aphantopus hyperantus and Coenonympha arcania accumulate metals in higher concentrations compared to the background territory and that the accumulation of metals in the body of adults negatively correlates with wing length, but positively with fluctuating asymmetry of wing length. We measured the length of the forewing and individual concentrations of Zn, Cu, Pb and Cd in the body of adults captured at different distances from the Sredneuralsk copper smelter (Revda, Russia). The metal content reaches very high levels, with Zn concentrations higher than Cu and Pb concentrations by an order of magnitude, and Cd concentrations by two orders of magnitude. In both species, males accumulate metals significantly more than females. The maximum concentrations of Zn, Cu and Cd were found near the plant. Wing length either did not differ between sites or was higher near the plant. Only for females of one of the species (A. hyperantus) a statistically significant negative relationship was found between Cu concentrations and wing size. In both species, fluctuating wing size asymmetry did not differ between sites and was not affected by metal concentrations at the individual level.

About the authors

A. O. Shkurikhin

Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences

Email: ashkurikhin@yandex.ru
Yekaterinburg, Russia

E. Yu. Zakharova

Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences

Email: ashkurikhin@yandex.ru
Yekaterinburg, Russia

E. L. Vorobeichik

Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences

Author for correspondence.
Email: ashkurikhin@yandex.ru
Yekaterinburg, Russia

References

  1. Воробейчик Е.Л., Козлов М.В. Воздействие точечных источников эмиссии поллютантов на наземные экосистемы: методология исследований, экспериментальные схемы, распространенные ошибки // Экология. 2012. № 2. С. 83–91. [Vorobeichik E.L., Kozlov M.V. Impact of point polluters on terrestrial ecosystems: Methodology of research, experimental design, and typical errors // Russ. J. Ecol. 2012. V. 43. № 2. P. 89–96. https://doi.org/10.1134/S1067413612020166]
  2. Воробейчик Е.Л. Естественное восстановление наземных экосистем после прекращения промышленного загрязнения. 1. Обзор современного состояния исследований // Экология. 2022. № 1. С. 3–41. [Vorobeichik E.L. Natural recovery of terrestrial ecosystems after the cessation of industrial pollution: 1. A state-of-the-art review // Russ. J. Ecol. 2022. V. 53. № 1. P. 1–39. https://doi.org/10.1134/S1067413622010118]
  3. Moroń D., Grześ I.M., Skórka P. et al. Abundance and diversity of wild bees along gradients of heavy metal pollution // J. Appl. Ecol. 2012. V. 49. P. 118–125.
  4. Belskaya E., Gilev A., Trubina M., Belskii E. Diversity of ants (Hymenoptera, Formicidae) along a heavy metal pollution gradient: Evidence of a hump-shaped effect // Ecol. Indic. 2019. V. 106. Art. 105447.
  5. Monchanin C., Devaud J.-M., Barron A.B., Lihoreau M. Current permissible levels of metal pollutants harm terrestrial invertebrates // Sci. Total Environ. 2021. V. 779. Art. 146398.
  6. Kozlov M.V., Zverev V., Zvereva E.L. Diversity but not overall abundance of moths and butterflies (Insecta: Lepidoptera) decreases around two arctic polluters // Insects. 2022. № 13. Art. 1124.
  7. Kozlov M.V., Castagneyrol B., Zverev V., Zvereva E.L. Recovery of moth and butterfly (Lepidoptera) communities in a polluted region following emission decline // Sci. Total Environ. 2022. V. 838. Art. 155800.
  8. Zvereva E.L., Kozlov M.V. Responses of terrestrial arthropods to air pollution: a meta-analysis // Environ. Sci. Pollut. Res. 2010. V. 17. P. 297–311.
  9. Lindquist L. Accumulation of cadmium, copper, and zinc in five species of phytophagous insects // Environ. Entomol. 1992. V. 21. № 1. P. 160–163.
  10. Gintenreiter S., Ortel J., Nopp H.J. Bioaccumulation of cadmium, lead, copper and zinc in successive developmental stages of Lymantria dispar L. (Lymantriidae, Lepid.) – a life cycle study // Arch. Environ. Contam. Toxicol. 1993. V. 25. P. 55–61.
  11. Jensen P., Trumble J.T. Ecological consequences of bioavailability of metals and metalloids in insects // Recent Res. Dev. Entomol. 2003. V. 42. P. 1–17.
  12. Sharma R.K., Agrawal M. Biological effects of heavy metals: an overview // J. Environ. Biol. 2005. V. 26 (Suppl. 2). P. 301–313.
  13. Janssens T.K.S., Roelofs D., Van Straalen N.M. Molecular mechanisms of heavy metal tolerance and evolution in invertebrates // Insect Sci. 2009. V. 16. P. 3–18.
  14. Jin P., Chen J., Zhan H. et al. Accumulation and excretion of zinc and their effects on growth and food utilization of Spodoptera litura (Lepidoptera: Noctuidae) // Ecotoxicol. Environ. Saf. 2020. V. 202. Art. 110883.
  15. Shu Y., Gao Y., Sun H. et al. Effects of zinc exposure on the reproduction of Spodoptera litura Fabricius (Lepidoptera: Noctuidae) // Ecotoxicol. Environ. Saf. 2009. V. 72. P. 2130–2136.
  16. Huang D., Kong J., Seng Y. Effects of the heavy metal Cu2+ on growth, development, and population dynamics of Spodoptera litura (Lepidoptera: Noctuidae) // J. Econ. Entomol. 2012. V. 105 (1). P. 288–294.
  17. Shephard A.M., Mitchell T.S., Henry S.B. et al. Assessing zinc tolerance in two butterfly species: consequences for conservation in polluted environments // Insect Conserv. Diver. 2020. P. 201–210.
  18. Zverev V., Kozlov M.V. Decline of Eulia ministrana (Lepidoptera: Tortricidae) in polluted habitats is not accompanied by phenotypic stress responses // Insect Sci. 2021. V. 28. P. 1482–1490.
  19. Бельская Е.А., Золотарев М.П. Изменение размерной структуры сообществ жужелиц при техногенной трансформации лесных экосистем // Экология. 2017. № 2. С. 107–115. [Belskaya E.A., Zolotarev M.P. Changes in the size structure of carabid communities in forest ecosystems under technogenic transformation // Russ. J. Ecol. 2017. V. 48. № 2. P. 152–160. https://doi.org/10.1134/S1067413617010040]
  20. Wickman P.-O. Territorial defence and mating success in males of the small heath butterfly, Coenonympha pamphilus L. (Lepidoptera: Satyridae) // Anim. Behav. 1985. V. 33. I. 4. P. 1162–1168.
  21. Karlsson B., Wickman P.-O. Increase in reproductive effort as explained by body size and resource allocation in the speckled wood butterfly, Pararge aegeria (L.) // Function. Ecol. 1990. V. 4. P. 609–617.
  22. Blanckenhorn W.U. The evolution of body size: what keeps organisms small? // Quarter. Rev. Biol. 2000. V. 75. P. 385–407.
  23. Van Valen L. A study of fluctuating asymmetry // Evolution. 1962. V. 16. P. 125–142.
  24. Møller A.P., Swaddle J.P. Asymmetry, developmental stability, and evolution. Oxford: Oxford University Press, 1997. 291p.
  25. Palmer A.R., Strobeck C. Fluctuating asymmetry analyses revisited // Developmental instability: causes and consequences / Ed. Polak M. New York: Oxford University Press, 2003. P. 279–319.
  26. Beasley D.A.E., Bonisoli-Alquati A., Mousseau T.A. The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: A meta-analysis // Ecol. Indic. 2013. V. 30. P. 218–226.
  27. Szentgyörgyi H., Moroń D., Nawrocka A. et al. Forewing structure of the solitary bee Osmia bicornis developing on heavy metal pollution gradient // Ecotoxicology. 2017. V. 26. P. 1031–1040.
  28. Zverev V., Kozlov M.V. The fluctuating asymmetry of the butterfly wing pattern does not change along an industrial pollution gradient // Symmetry. 2021. V. 13. Art. 626.
  29. Dahmani-Muller H., Van Oort F., Gélie B., Balabane M. Strategies of heavy metal uptake by three plant species growing near a metal smelter // Environ. Pollut. 2000. V. 109. № 2. P. 231–238.
  30. Kozlov M.V., Zvereva E.L., Zverev V. Impacts of point polluters on terrestrial biota: Comparative analysis of 18 contaminated areas. Dordrecht: Springer, 2009. 466 p.
  31. Воробейчик Е.Л., Кайгородова С.Ю. Многолетняя динамика содержания тяжелых металлов в верхних горизонтах почв в районе воздействия медеплавильного завода в период снижения его выбросов // Почвоведение. 2017. № 8. С. 1009–1024.
  32. Шималина Н.С., Позолотина В.Н., Орехова Н.А., Антонова Е.В. Оценка биологических эффектов у семенного потомства Plantago major L. в зоне воздействия медеплавильного производства // Экология. 2017. № 6. С. 420–430. [Shimalina N.S., Pozolotina V.N., Orekhova N.A., Antonova E.V. Assessment of biological effects in Plantago major L. seed progeny in the zone of impact from a Copper Smelter // Russ. J. Ecol. 2017. V. 48. P. 513–523. https://doi.org/10.1134/S1067413617060108]
  33. Хантемирова Е.В. К характеристике смен растительности импактной зоны СУМЗа // Экология промышленного региона и экологическое образование: Мат-лы Всерос. науч.-практ. конф. Нижний Тагил, 2004. С. 106–108.
  34. Хантемирова Е.В. Техногенное загрязнение и послелесные луга // Особь и популяция – стратегии жизни: Мат-лы IX Всерос. популяционного семинара. Ч. 1. Уфа, 2006. С. 442–447.
  35. Van Swaay C.A.M., Warren M.S., Lois G. Biotope use and trends of European butterflies // J. Insect Conserv. 2006. V. 10. P. 189–209.
  36. Settele J., Kudrna O., Harpke A. et al. Climatic risk atlas of European butterflies. Pensoft, 2008. 712 p.
  37. Gorbunov P., Kosterin O. The butterflies (Hesperioidea and Papilionoidea) of North Asia (Asian part of Russia) in nature. M.: Rodina & Fodio, 2007. V. 2. 408 p.
  38. Seppänen R. Differences in spotting pattern between populations of Aphantopus hyperantus (Lepidoptera, Satyridae) in southern Finland // Ann. Zool. Fennici. 1981. V. 18. № 1. P. 1–36.
  39. Valtonen A., Saarinen K. A highway intersection as an alternative habitat for a meadow butterfly: effect of mowing, habitat geometry and roads on the ringlet (Aphantopus hyperantus) // Ann. Zool. Fennici. 2005. V. 42. P. 545–556.
  40. Saarinen K., Jantunen J. Grassland butterfly fauna under traditional animal husbandry: contrasts in diversity in mown meadows and grazed pastures // Biodiv. Conserv. 2005. V. 14. P. 3201–3213.
  41. Pollard E., Yates T.J. Monitoring butterflies for ecology and conservation. London: Chapman and Hall, 1993. 274 p.
  42. Sutcliffe O.L., Thomas C.D., Peggie D. Area-dependant migration by ringlet butterflies generates a mixture of patchy population and metapopulation attributes // Oecologia. 1997. V. 109. P. 229–234.
  43. Захарова Е.Ю., Шкурихин А.О. Морфологическая изменчивость бархатниц Aphantopus hyperantus L. и Erebia ligea L. (Lepidoptera, Satyridae) в аллопатрических и аллохронных микропопуляциях // Зоол. журн. 2021. Т. 100. Вып. 10. С. 1110–1123.
  44. Рыжкова М.В., Лопатина Е.Б. Сезонный цикл развития бабочки Aphantopus hyperantus (L.) (Lepidoptera, Nymphalidae: Satyrinae) в Ленинградской области // Энтомол. обозр. 2016. Т. 95. № 3. С. 449–472.
  45. Коршунов Ю.П. Булавоусые чешуекрылые Северной Азии. М.: КМК, 2002. 424 с.
  46. Binzenhöfer B., Schröder B., Strauss B. et al. Habitat models and habitat connectivity analysis for butterflies and burnet moths – The example of Zygaena carniolica and Coenonympha arcania // Biol. Conserv. 2005. V. 126. P. 247–259.
  47. Hein S., Binzenhöfer B., Poethke H.-J. et al.The generality of habitat suitability models: A practical test with two insect groups // Basic Appl. Ecol. 2007. № 8. P. 310–320.
  48. Захарова Е.Ю. Фенотипическая изменчивость сенницы Coenonympha arcania L. (Lepidoptera, Satyridae) в естественных и антропогенно трансформированных местообитаниях Среднего и Южного Урала // Энтомол. обозр. 2012. Т. 91. № 2. С. 250–268.
  49. Захарова Е.Ю., Юсупова О.В. Морфологическая изменчивость и ландшафтно-биотопическая приуроченность микропопуляций сенницы Coenonympha arcania (L.) (Lepidoptera: Satyridae) в условиях гор Южного Урала // Бюл. МОИП. Отд. биол. 2017. Т. 122. Вып. 2. С. 18–26.
  50. Козлов М.В. Функциональная морфология крыльев и изменчивость их жилкования у низших чешуекрылых (Lepidoptera: Micropterigidae – Tischeriidae) // Журн. общ. биол. 1987. Т. 48. № 2. С. 238–247.
  51. Rasband W.S. ImageJ. 2014. URL: http://imagej.nih.gov/ij/.
  52. Kozlov M.V., Zvereva E.L. Confirmation bias in studies of fluctuating asymmetry // Ecol. Indic. 2015. V. 57. P. 293–297.
  53. Hammer Ø., Harper D.A.T., Ryan P.D. PAST: Paleontological Statistics Software Pack-age for Education and Data Analysis // Palaeont. Electr. 2001. V. 4. № 1. P. 1–9.
  54. Xia Q., Sun H., Hu X., Shu Y. Apoptosis of Spodoptera litura larval hemocytes induced by heavy metal zinc // Chin. Sci. Bull. 2005. V. 50. №. 24. P. 2856–2860.
  55. Shu Y., Zhang G., Wang J. Response of the common cutworm Spodoptera litura to zinc stress: Zn accumulation, metallothionein and cell ultrastructure of the midgut // Sci. Total Environ. 2012. V. 438. P. 210–217.
  56. Hocking B. Insect flight // Scientific American. 1958. V. 199. P. 92–98.
  57. Karadjova I., Markova E. Metal accumulation in insects (Orthoptera, Acrididae) near a copper smelter and copper-flotation factory (Pirdop, Bulgaria) // Biotechnol. Biotechnol. Equip. 2014. V. 23. P. 204–207.
  58. Tőzsér D., Magura T., Simon E. et al. Pollution intensity-dependent metal accumulation in ground beetles: a meta-analysis // Environ. Sci. Pollut. Res. 2019. V. 26. P. 32092–32102.
  59. Aydoğan Z., Gürol A., Ínsecara Ü. The investigation of heavy element accumulation in some Hydrophilidae (Coleoptera) species // Environ. Monitor. Asses. 2016. V. 188. Art. 204.
  60. Heliövaara K., Väisänen R. Heavy-metal contents in pupae of Bupalus piniarius (Lepidoptera: Geometridae) and Panolis flammea (Lepidoptera: Noctuidae) near an industrial source // Environ. Entomol. 1990. V. 19(3). P. 481–485.
  61. Heikens A., Peijnenburg W.J.G.M., Hendriks A.J. Bioaccumulation of heavy metals in terrestrial invertebrates // Environ. Pollut. 2001. V. 113. P. 385–393.
  62. Boyd R.S. High-nickel insects and nickel hyperaccumulator plants: A review // Insect Sci. 2009. V. 16. № 1. P. 19–31.
  63. Захарова Е.Ю., Шкурихин А.О. Морфологическая изменчивость крыла Erebia ligea (Linnaeus, 1758) (Lepidoptera: Satyridae) в бициклических и моновольтинных популяциях на Урале // Евраз. энтомол. журн. 2017. Т. 16. Вып. 4. С. 344–352.
  64. Нестерков А.В., Воробейчик Е.Л. Изменение структуры населения беспозвоночных-хортобионтов под действием выбросов медеплавильного завода // Экология. 2009. № 4. P. 303–313. [Nesterkov A.V., Vorobeichik E.L. Changes in the structure of chortobiont invertebrate community exposed to emissions from a Copper Smelter // Russ. J. Ecol. 2009. V. 40. № 4. P. 286–296. https://doi.org/10.1134/S1067413609040109]
  65. Zvereva E.L., Kozlov M.V. Effects of air pollution on natural enemies of the leaf beetle Melasoma lapponica // J. Appl. Ecol. 2000. V. 37. P. 298–308.
  66. White T.C.R. The abundance of invertebrate herbivory in relation to the availability of nitrogen in stressed food plants // Oecologia. 1984. V. 63. P. 90–105.
  67. Awmack C.S., Leather S.R. Host plant quality and fecundity in herbivorous insects // Ann. Rev. Entomol. 2002. V. 47. P. 817–844.
  68. Bauerfeind S.S., Fischer K. Testing the plant stress hypothesis: stressed plants offer better food to an insect herbivore // Entomol. Experim. Appl. 2013. V. 149. P. 148–158.
  69. Nijhout H.F. A threshold size for metamorphosis in the tobacco hornworm, Manduca sexta (L.) // Biol. Bull. 1975. V. 149. № 1. P. 214–225.
  70. Berger D., Walters R., Gotthard K. What keeps insects small? – Size dependent predation on two species of butterfly larvae // Evol. Ecol. 2006. V. 20. P. 575–589.
  71. Belskii E., Belskaya E. Thermal effect of the Middle Ural copper smelter (Russia) and growth of birch leaves // Environ. Sci. Pollut. Res. 2021. V. 28. P. 26064–26072.
  72. Atkinson D. Temperature and organism size: a biological law for ectotherms // Adv. Ecol. Res. 1994. V. 25. P. 1–58.
  73. Horne C.R., Hirst A.G., Atkinson D. Temperature size responses match latitudinal size clines in arthropods, revealing critical differences between aquatic and terrestrial specie // Ecol. Lett. 2015. V. 18. P. 327–335.
  74. 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 // Europ. J. Entomol. 2021. V. 118. P. 214–224.
  75. Symanski C., Redak R.A. Does fluctuating asymmetry of wing traits capture relative environmental stress in a lepidopteran? // Ecol. Evol. 2021. V. 11. P. 1199–1213.
  76. Rabitsch W.B. Levels of asymmetry in Formica pratensis Retz. (Hymenoptera, Insecta) from a chronic metal-contaminated site // Environ. Toxicol. Chem. 1997. V. 16. № 7. P. 1433–1440.

Supplementary files

Supplementary Files
Action
1. JATS XML
2.

Download (616KB)
3.

Download (314KB)
4.

Download (238KB)
5.

Download (73KB)
6.

Download (178KB)

Copyright (c) 2023 А.О. Шкурихин, Е.Ю. Захарова, Е.Л. Воробейчик

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies