Eur. J. Entomol. 119: 250-259, 2022 | DOI: 10.14411/eje.2022.027

Temporal and climatic variation in the colour forms of Adalia bipunctata and Harmonia axyridis (Coleoptera: Coccinellidae) populations in the United KingdomIvo Hodek special issueOriginal article

Ayman ASIRI ORCID...1, Chris FOSTER ORCID...2
1 Cardiff University, Cardiff, Wales, CF10 3AT, UK; e-mail: AsiriA2@cardiff.ac.uk
2 University of Reading, Whiteknights, Reading, Berkshire, RG6 6AH, UK; e-mail: c.w.foster@reading.ac.uk

Colour form polymorphism in Adalia bipunctata (Linnaeus, 1785) and Harmonia axyridis (Pallas, 1773) has been extensively studied in the past. Climate, season, and region are known to influence the colour form frequencies of these species, however, this effect is region specific, and the response of populations has changed over time. Here, 5862 photographic records from the UK Ladybird Survey from 2013-2017 were used to assess the geographic variation in colour form frequency (melanic versus non-melanic) of A. bipunctata and H. axyridis across the United Kingdom (UK) in relation to climate and season. Climate data from the UK Met Office were used to determine the effect of climate on melanic form. Seasonal variation in melanic form was observed in H. axyridis but not A. bipunctata. For H. axyridis, the probability of being melanic decreased in areas with higher annual sunlight hours. In A. bipunctata, there was an interaction between sunlight hours and rainfall. In areas with low rainfall, the probability of being melanic was negatively correlated with sunlight hours. Where rainfall was high, the probability of being melanic was positively correlated with sunlight hours. These findings highlight the role of climate in determining the proportion of colour forms in UK populations of A. bipunctata and H. axyridis. Furthermore, the results support the hypothesis that seasonal variation in melanism does not occur in A. bipunctata populations with a low overall proportion of melanics.

Keywords: Melanism, ladybirds, overwintering, climate

Received: January 17, 2022; Revised: June 22, 2022; Accepted: June 22, 2022; Published online: July 29, 2022  Show citation

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ASIRI, A., & FOSTER, C. (2022). Temporal and climatic variation in the colour forms of Adalia bipunctata and Harmonia axyridis (Coleoptera: Coccinellidae) populations in the United Kingdom. EJE119, Article 250-259. https://doi.org/10.14411/eje.2022.027


This paper was contributed to a virtual special issue in memory of Ivo Hodek, a long-time editor of the European Journal of Entomo­logy, who died on June 11, 2021, shortly after his ninetieth birthday.


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References

  1. Adriaens T., San Martin y Gomez G. & Maes D. 2008: Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. - BioControl 53: 69-88. Go to original source...
  2. Ball-Damerow J.E., M'Gonigle L.K. & Resh V.H. 2014: Changes in occurrence, richness, and biological traits of dragonflies and damselflies (Odonata) in California and Nevada over the past century. - Biodiv. Conserv. 23: 2107-2126. Go to original source...
  3. Bengtson S.-A. & Hagen R. 1975: Polymorphism in the two-spot ladybird Adalia bipunctata in western Norway. - Oikos 26: 328-331. Go to original source...
  4. Bengtson S.-A. & Hagen R. 1977: Melanism in the two-spot ladybird Adalia bipunctata in relation to climate in western Norway. - Oikos 28: 16-19. Go to original source...
  5. Brakefield P.M. 1984a: Selection along clines in the ladybird Adalia bipunctata in The Netherlands: A general mating advantage to melanics and its consequences. - Heredity 53: 37-49. Go to original source...
  6. Brakefield P.M. 1984b: Ecological studies on the polymorphic ladybird Adalia bipunctata in The Netherlands. I. Population biology and geographical variation of melanism. - J. Anim. Ecol. 53: 761-774. Go to original source...
  7. Brakefield P.M. 1984c: Ecological studies on the polymorphic ladybird Adalia bipunctata in The Netherlands. II. Population dynamics, differential timing of reproduction and thermal mela­nism. - J. Anim. Ecol. 53: 775-790. Go to original source...
  8. Brakefield P.M. 1985: Differential winter mortality and seasonal selection in the polymorphic ladybird Adalia bipunctata (L.) in The Netherlands. - Biol. J. Linn. Soc. 24: 189-206. Go to original source...
  9. Brakefield P.M. & De Jong P.W. 2011: A steep cline in ladybird melanism has decayed over 25 years: A genetic response to climate change? - Heredity 107: 574-578. Go to original source...
  10. Brakefield P.M. & Lees D.R. 1987: Melanism in Adalia ladybirds and declining air pollution in Birmingham. - Heredity 59: 273-277. Go to original source...
  11. Brakefield P.M. & Willmer P.G. 1985: The basis of thermal mela­nism in the ladybird Adalia bipunctata: Differences in reflectance and thermal properties between the morphs. - Heredity 54: 9-14. Go to original source...
  12. Brown M.W. & Miller S.S. 1998: Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. - Entomol. News 109: 143-151.
  13. Brown P.M.J., Adriaens T., Bathon H., Cuppen J., Goldarazena A., Hägg T., Kenis M., Klausnitzer B.E.M., Kováĝ I. et al. 2008: Harmonia axyridis in Europe: Spread and distribution of a non-native coccinellid. - BioControl 53: 5-21. Go to original source...
  14. Brown P.M.J., Thomas C.E., Lombaert E., Jeffries D.L., Estoup A. & Lawson Handley L.-J. 2011a: The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): Distribution, dispersal and routes of invasion. - BioControl 56: 623-641. Go to original source...
  15. Brown P.M.J., Frost R., Doberski J., Sparks T.I.M., Harrington R. & Roy H.E. 2011b: Decline in native ladybirds in response to the arrival of Harmonia axyridis: Early evidence from England. - Ecol. Entomol. 36: 231-240. Go to original source...
  16. Chapin J.B. & Brou V.A. 1991: Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera: Coccinellidae). - Proc. Entomol. Soc. Wash. 93: 630-635.
  17. Creed E.R. 1966: Geographic variation in the two-spot ladybird in England and Wales. - Heredity 21: 57-72. Go to original source...
  18. Creed E.R. 1971a: Melanism in the two-spot ladybird, Adalia bipunctata, in Great Britain. In Creed E.R. (ed.): Ecological Genetics and Evolution. Blackwell, Oxford, pp. 134-151. Go to original source...
  19. Creed E.R. 1971b: Industrial melanism in the two-spot ladybird and smoke abatement. - Evolution 25: 290-293. Go to original source...
  20. Creed E.R. 1974: Two spot ladybirds as indicators of intense local air pollution. - Nature 249: 390-392. Go to original source...
  21. Creed E.R. 1975: Melanism in the two spot ladybird: The nature and intensity of selection. - Proc. R. Soc. Lond. (B) 190: 135-148. Go to original source...
  22. Cribari-Neto F. & Zeileis A. 2010: Beta Regression in R. - J. Stat. Softw. 34(2): 1-24. Go to original source...
  23. De Jong P.W. & Brakefield P.M. 1998: Climate and change in clines for melanism in the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). - Proc. R. Soc. Lond. 265: 39-43. Go to original source...
  24. Dobzhansky T. 1933: Geographical variation in lady-beetles. - Am. Nat. 67: 97-126. Go to original source...
  25. Gautier M., Yamaguchi J., Foucaud J., Loiseau A., Ausset A., Facon B., Gschloessl B., Lagnel J., Loire E., Parrinello H. et al. 2018: The genomic basis of color pattern polymorphism in the harlequin ladybird. - Curr. Biol. 28: 3296-3302. Go to original source...
  26. Grez A.A., Zaviezo T., Roy H.E., Brown P.M.J. & Bizama G. 2016: Rapid spread of Harmonia axyridis in Chile and its effects on local coccinellid biodiversity. - Divers. Distrib. 22: 982-994. Go to original source...
  27. Harmon J.P., Stephens E. & Losey J. 2007: The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. - J. Insect Conserv. 21: 85-94. Go to original source...
  28. Honek A. 1975: Colour polymorphism in Adalia bipunctata in Bohemia (Coleoptera: Coccinellidae). - Entomol. German. 1: 293-299. Go to original source...
  29. Honek A., Martinková Z. & Pekár S. 2005: Temporal stability of morph frequency in central European populations of Adalia bipunctata and Adalia decempunctata (Coleoptera: Coccinellidae). - Eur. J. Entomol. 102: 437-442. Go to original source...
  30. Honek A., Brown P.M., Martinkova Z., Skuhrovec J., Brabec M., Burgio G., Evans E.W., Fournier M., Grez A.A., Kulfan J. et al. 2020: Factors determining variation in colour morph frequencies in invasive Harmonia axyridis populations. - Biol. Invas. 22: 2049-2062. Go to original source...
  31. Hosino Y. 1940: Genetical studies on the pattern types of the lady-bird beetle, Harmonia axyridis Pallas. - J. Genet. 40: 215-228. Go to original source...
  32. Kahle D. & Wickham H. 2013: ggmap: Spatial visualization with ggplot2. - The R Journal 5: 144-161. Go to original source...
  33. Kholin S. 1990: Stability of the genetical polymorphism in elytra colour of Harmonia axyridis Pall. (Coccinellidae, Coleoptera) in Maritime province, USSR. - Genetika 26: 2207-2214 [in Russian].
  34. Klausnitzer B. & Schummer R. 1983: Zum vorkommen der formen von Adalia bipunctata L. in der DDR (Insecta, Coleo­ptera). - Entomol. Nachr. 27: 159-162.
  35. Knop E. 2016: Biotic homogenization of three insect groups due to urbanization. - Global Change Biol. 22: 228-236. Go to original source...
  36. Komai T. & Chino M. 1969: Observations on geographic and temporal variations in the ladybeetle Harmonia. I. Elytral patterns. - Proc. Jap. Acad. 45: 284-288. Go to original source...
  37. Komai T., Chino M. & Hosino Y. 1950: Contributions to the evolutionary genetics of the lady-beetle, Harmonia. I. Geographic and temporal variations in the relative frequencies of the elytral pattern types and in the frequency of elytral ridge. - Genetics 35: 589-601. Go to original source...
  38. Komai T., Chino M. & Hosino Y. 1956: Population genetics on the lady-beetle Harmonia axyridis. In Komai T. & Sakai K. (eds): Population Genetics. Baifukan, Tokyo, pp. 45-60 [in Japanese with English abstract].
  39. Lenssen N., Schmidt G., Hansen J., Menne M., Persin A., Ruedy R. & Zyss D. 2019: Improvements in the GISTEMP uncertainty model. - J. Geophys. Res. Atmos. 124: 6307-6326. Go to original source...
  40. Lombaert E., Malausa T., Devred R. & Estoup A. 2007: Phenotypic variation in invasive and biocontrol populations of the harlequin ladybird, Harmonia axyridis. In Roy H.E. & Wajnberg E. (eds): From Biological Control to Invasion: The Ladybird Harmonia axyridis as a Model Species. Springer, Basel, pp. 89-102. Go to original source...
  41. Lusis Y.Y. 1932: An analysis of the dominance phenomenon in the inheritance of the elytra and pronotum colour in Adalia bipunctata. - Trudy Lab. Genet. 9: 135-162.
  42. Majerus M. & Zakharov I. 2000: Does thermal melanism maintain melanic polymorphism in the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae)? - Zh. Obsh. Biol. 61: 381-392.
  43. Majerus M., Strawson V. & Roy H. 2006: The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. - Ecol. Entomol. 31: 207-215. Go to original source...
  44. McClure M.S. 1987: Potential of the asian predator, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), to control Matsucoccus resinosae Bean and Godwin (Homoptera: Margarodidae) in the United States. - Environ. Entomol. 16: 224-230. Go to original source...
  45. Met Office, Hollis D., McCarthy M., Kendon M., Legg T. & Simpson I. 2018: HadUK-Grid Gridded and Regional Average Climate Observations for the UK. Centre for Environmental Data Analysis, URL: http://catalogue.ceda.ac.uk/uuid/4dc8450d889a491ebb20e724debe2dfb (last accessed 22 Feb. 2021).
  46. Michie L.J., Mallard F., Majerus M.E.N. & Jiggins F.M. 2010: Melanic through nature or nurture: Genetic polymorphism and phenotypic plasticity in Harmonia axyridis. - J. Evol. Biol. 23: 1699-1707. Go to original source...
  47. Michie L.J., Masson A., Ware R.L. & Jiggins F.M. 2011: Seasonal phenotypic plasticity: Wild ladybirds are darker at cold temperatures. - Evol. Ecol. 25: 1259-1268. Go to original source...
  48. Muggleton J., Lonsdale D. & Benham B.R. 1975: Melanism in Adalia bipunctata L. (Col., Coccinellidae) and its relationship to atmospheric pollution. - J. Appl. Ecol. 12: 451-464. Go to original source...
  49. Murrells T.P., Passant N.R., Thistlethwaite G., Wagner A., Li Y., Bush T., Norris J., Walker C., Stewart R.A., Tsagatakis I. et al. 2010: UK Emissions of Air Pollutants 1970 to 2008. Issue 1. Department for Environment, Food and Rural Affairs, Didcot, OX, 200 pp.
  50. Olden J.D., Poff N.L. & Mckinney M.L. 2006: Forecasting faunal and floral homogenization associated with human population geography in North America. - Biol. Conserv. 127: 261-271. Go to original source...
  51. Osawa N. & Nishida T. 1992: Seasonal variation in elytral colour polymorphism in Harmonia axyridis (the ladybird beetle): The role of non-random mating. - Heredity 69: 297-307. Go to original source...
  52. Pebesma E.J. & Bivand R.S. 2005: Classes and methods for spatial data in R. - R News 5(2): 9-13. Go to original source...
  53. Purse B.V., Comont R., Butler A., Brown P.M.J., Kessel C. & Roy H.E. 2015: Landscape and climate determine patterns of spread for all colour morphs of the alien ladybird Harmonia axyridis. - J. Biogeogr. 42: 575-588. Go to original source...
  54. R Core Team 2021: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, URL: https://www.R-project.org/.
  55. Roy H., Brown P. & Majerus M. 2006: Harmonia axyridis: A successful biocontrol agent or an invasive threat? In Eilenberg J. & Hokkanen H.M.T. (eds): An Ecological and Societal Approach to Biological Control. Springer, Basel, pp. 295-309. Go to original source...
  56. Roy H.E., Adriaens T., Isaac N.J.B., Kenis M., Onkelinx T., San Martin G., Brown P.M.J., Hautier L., Poland R., Roy D.B. et al. 2012: Invasive alien predator causes rapid declines of native European ladybirds. - Divers. Distrib. 18: 717-725. Go to original source...
  57. Roy H.E., Brown P.M., Adriaens T., Berkvens N., Borges I., Clusella-Trullas S., Comont R.F., De Clercq P., Eschen R., Estoup A. et al. 2016: The harlequin ladybird, Harmonia axyridis: Global perspectives on invasion history and ecology. - Biol. Invas. 18: 997-1044. Go to original source...
  58. Scali V. & Creed E. 1975: Influence of climate on melanism in the two-spot ladybird, Adalia bipunctata, in central Italy. - Trans. R. Entomol. Soc. Lond. 127: 163-169. Go to original source...
  59. Seo M., Kim G. & Youn Y. 2008: Differences in biological and behavioural characteristics of Harmonia axyridis (Coleoptera: Coccinellidae) according to colour patterns of elytra. - J. Appl. Entomol. 132: 239-247. Go to original source...
  60. Shaw J.D., Spear D., Greve M., Chown S.L. & Fernández-Palacios J.M. 2010: Taxonomic homogenization and differentiation across southern ocean islands differ among insects and vascular plants. - J. Biogeogr. 37: 217-228. Go to original source...
  61. Soares A.O., Coderre D. & Schanderl H. 2003: Effect of temperature and intraspecific allometry on predation by two phenotypes of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). - Environ. Entomol. 32: 939-944. Go to original source...
  62. Su W., Michaud J.P., Runzhi Z., Fan Z. & Shuang L. 2009: Seasonal cycles of assortative mating and reproductive behaviour in polymorphic populations of Harmonia axyridis in China. - Ecol. Entomol. 34: 483-494. Go to original source...
  63. Talloen W., Dyck H.V. & Lens L. 2004: The cost of melanization: Butterfly wing coloration under environmental stress. - Evolution 58: 360-366. Go to original source...
  64. Tan C.-C. & Li J.-C. 1934: Inheritance of the elytral color patterns of the ladybird beetle, Harmonia axyridis Pallas. - Am. Nat. 68: 252-265. Go to original source...
  65. Tedders W.L. & Schaefer P.W. 1994: Release and establishment of Harmonia axyridis (Coleoptera: Coccinellidae) in the southeastern United States. - Entomol. News 105: 228-243.
  66. Timofeeff-Ressovsky N. 1940: Zur analyse des polymorphismus bei Adalia bipunctata L. - Biol. Zentralbl. 60: 130-137.
  67. Tscharntke T., Steffan-Dewenter I., Kruess A. & Thies C. 2002: Characteristics of insect populations on habitat fragments: A mini review. - Ecol. Res. 17: 229-239. Go to original source...
  68. Warren M., Hill J., Thomas J., Asher J., Fox R., Huntley B., Roy D.B., Telfer M.G., Jeffcoate S., Harding P. et al. 2001: Rapid responses of British butterflies to opposing forces of climate and habitat change. - Nature 414: 65-69. Go to original source...
  69. Wickham H. 2016: ggplot2: Elegant Graphics for Data Analysis. Springer, New York, 268 pp. Go to original source...
  70. Wickham H., Averick M., Bryan J., Chang W., McGowan L.D., François R., Grolemund G., Hayes A., Henry L., Hester J., et al. 2019: Welcome to the tidyverse. - J. Open Source Softw. 4(43): 1686, 6 pp. Go to original source...
  71. Ya L.Y. 1961: On the biological meaning of colour polymorphism of lady-beetle Adalia bipunctata L. - Latv. Entomol. 4: 2-29 [in Russian, English abstract].
  72. Zakharov I.A. & Sergievsky S.O. 1978: Studies on the variation of Adalia bipunctata populations in Leningrad city and suburbs. - Genetika 14: 281-284 [in Russian].
  73. Zakharov I.A. & Sergievsky S.O. 1980: Study of the genetic-polymorphism of 2-spot ladybird Adalia bipunctata (L.) populations in Leningrad district. 1. Seasonal dynamics of polymorphism. - Genetika 16: 270-275 [in Russian].

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