The Fluctuating Asymmetry of the Butterfly Wing Pattern Does Not Change along an Industrial Pollution Gradient

The rapid and selective responses to changes in habitat structure and climate have made butterflies valuable environmental indicators. In this study, we asked whether the decline in butterfly populations near the copper-nickel smelter in Monchegorsk in northwestern Russia is accompanied by phenotypic stress responses to toxic pollutants, expressed as a decrease in body size and an increase in fluctuating asymmetry. We measured the concentrations of nickel and copper, forewing length, and fluctuating asymmetry in two elements of wing patterns in Boloria euphrosyne, Plebejus idas, and Agriades optilete collected 1–65 km from Monchegorsk. Body metal concentrations increased toward the smelter, confirming the local origin of the collected butterflies. The wings of butterflies from the most polluted sites were 5–8% shorter than those in unpolluted localities, suggesting adverse effects of pollution on butterfly fitness due to larval feeding on contaminated plants. However, fluctuating asymmetry averaged across two hindwing spots did not change systematically with pollution, thereby questioning the use of fluctuating asymmetry as an indicator of habitat quality in butterfly conservation projects.

[1]  R. Dennis,et al.  Gaps in butterfly inventory data: A global analysis , 2019, Biological Conservation.

[2]  R. Laskowski Are the top carnivores endangered by heavy metal biomagnification , 1991 .

[3]  E. Zvereva,et al.  Responses of terrestrial arthropods to air pollution: a meta-analysis , 2010, Environmental science and pollution research international.

[4]  M. Kozlov,et al.  Abundance of day-flying Lepidoptera along an air pollution gradient in the northern boreal forest zone¹ , 1996 .

[5]  Michael G. Kenward,et al.  An improved approximation to the precision of fixed effects from restricted maximum likelihood , 2009, Comput. Stat. Data Anal..

[6]  C. Strobeck,et al.  Fluctuating Asymmetry: Measurement, Analysis, Patterns , 1986 .

[7]  W. Rabitsch Levels of asymmetry in Formica pratensis Retz. (Hymenoptera, insecta) from a chronic metal‐contaminated site , 1997 .

[8]  F. Ollevier,et al.  Metamorphosis offsets the link between larval stress, adult asymmetry and individual quality , 2008 .

[9]  N. Prat,et al.  Relationship between pollution and fluctuating asymmetry in the pollution-tolerant caddisfly Hydropsyche exocellata (Trichoptera, Insecta) , 2005 .

[10]  Shmuel Raz,et al.  Fluctuating Asymmetry: Methods, Theory, and Applications , 2010, Symmetry.

[11]  E. Zvereva,et al.  Growth and reproduction of dwarf shrubs, Vaccinium myrtillus and V. vitis-idaea, in a severely polluted area , 2005 .

[12]  V. Zverev,et al.  Decline of Eulia ministrana (Lepidoptera: Tortricidae) in polluted habitats is not accompanied by phenotypic stress responses , 2020, Insect science.

[13]  E. Snell-Rood,et al.  Nickel Exposure Has Complex Transgenerational Effects in a Butterfly. , 2018, Integrative and comparative biology.

[14]  G. Nave,et al.  Is there a Publication Bias in Behavioural Intranasal Oxytocin Research on Humans? Opening the File Drawer of One Laboratory , 2016, Journal of neuroendocrinology.

[15]  Timothy A Mousseau,et al.  The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: A meta-analysis , 2013 .

[16]  Eugene P. Odum,et al.  Trends Expected in Stressed Ecosystems , 1985 .

[17]  P. Parsons,et al.  Fluctuating asymmetry: a biological monitor of environmental and genomic stress , 1992, Heredity.

[18]  C. Strobeck,et al.  Fluctuating Asymmetry Analyses Revisited , 2001 .

[19]  V. Zverev,et al.  Consequences of long-term severe industrial pollution for aboveground carbon and nitrogen pools in northern taiga forests at local and regional scales. , 2015, Science of the Total Environment.

[20]  T. Tammaru,et al.  Density and performance of Epirrita autumnata (Lepidoptera : Geometridae) along three air pollution gradients in northern Europe , 1996 .

[21]  N. Pierce,et al.  Effects of mating history on ejaculate size, fecundity, longevity, and copulation duration in the ant-tended lycaenid butterfly, Jalmenus evagoras , 2000, Behavioral Ecology and Sociobiology.

[22]  E. Wagenmakers,et al.  Detecting and avoiding likely false‐positive findings – a practical guide , 2017, Biological reviews of the Cambridge Philosophical Society.

[23]  Thornhill,et al.  Individual differences in developmental precision and fluctuating asymmetry: a model and its implications , 1999 .

[24]  James Mallet,et al.  Genetic Analysis of Founder Bottlenecks in the Rare British Butterfly Plebejus argus , 1997 .

[25]  S. Kark,et al.  Asymmetry patterns across the distribution range: does the species matter? , 2004 .

[26]  R. Albajes,et al.  The Catalan butterfly monitoring scheme has the capacity to detect effects of modifying agricultural practices , 2020 .

[27]  L. H. Weinstein,et al.  Effects of Air Pollutants on Insect Populations , 1982 .

[28]  T. Aldenberg,et al.  Evaluating the impact of pollution on plant–Lepidoptera relationships , 2005 .

[29]  M. WallisDeVries,et al.  Global warming and excess nitrogen may induce butterfly decline by microclimatic cooling , 2006 .

[30]  C. Waddington Canalization of Development and the Inheritance of Acquired Characters , 1942, Nature.

[31]  Scott N. Martens,et al.  Nickel hyperaccumulated by Thlaspi montanum var. montanum is acutely toxic to an insect herbivore , 1994 .

[32]  B. Freedman,et al.  Long-term effects of smelter pollution at Sudbury, Ontario, on forest community composition , 1980 .

[33]  Mikhail V. Kozlov,et al.  Variation in Leaf Size and Fluctuating Asymmetry of Mountain Birch (Betula pubescens var. pumila) in Space and Time: Implications for Global Change Research , 2020, Symmetry.

[34]  M. Eubanks,et al.  Nickel hyperaccumulation by Streptanthus polygaloides protects against the folivore Plutella xylostella (Lepidoptera: Plutellidae) , 2006, Plant Ecology.

[35]  E. Zvereva,et al.  Confirmation bias in studies of fluctuating asymmetry , 2015 .

[36]  K. Fischer,et al.  Maternal body size as a morphological constraint on egg size and fecundity in butterflies , 2008 .

[37]  Christian Peter Klingenberg,et al.  The genetics and evolution of fluctuating asymmetry , 2005 .