Abstract
Climate change is one of the greatest challenges that wildlife is facing. Rapid shifts in climatic conditions may accelerate evolutionary changes in populations as a result of strong selective pressure. Most studies focus on the impact of climatic conditions on phenologies and annual cycles, whereas there are fewer reports of empirical support for climate-driven changes in the phenotypic variability of free-living populations. We investigated whether climatic variables explain the prevalence of colour polymorphism in a population of the grass snake (Natrix natrix) with two morphotypes, the melanistic and non-melanistic ones, in the period 1981–2013. We found that the prevalence of the black phenotype was negatively related to spring temperature and winter harshness, expressed as the number of snow days. According to the thermal melanism hypothesis, a high predation rate during warmer springs may override relaxed thermal benefits and vice versa, i.e. black individuals may perform better than typical ones when thermal conditions in spring are unfavourable. In turn, because they are smaller, melanistic individuals may be exposed to a higher risk of winter mortality, particularly during longer winters. We highlight the need for more studies on the effects of climatic conditions on temporal variation in melanism prevalence in other populations and species as well as in various geographic regions.
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Dataset on the frequency of melanistic snakes and climatic variables is available in supplementary file.
References
Adolph SC, Porter WP (1993) Temperature, activity, and lizard life histories. Am Nat 142(2): 273–295. https://https://doi.org/10.1086/285538
Adolph SC, Porter WP (1996) Growth, seasonality, and lizard life histories: age and size at maturity. Oikos 77:267–278. https://doi.org/10.2307/3546065
Altwegg R, Dummermuth S, Anholt BR, Flatt T (2005) Winter weather affects asp viper Vipera aspis population dynamics through susceptible juveniles. Oikos 110(1):55–66. https://doi.org/10.1111/j.0030-1299.2005.13723.x
Andren C, Nilson G (1981) Reproductive success and risk of predation in normal and melanistic colour morphs of the adder, Vipera berus. Biol J Linn Soc 15:235–246. https://doi.org/10.1111/j.1095-8312.1981.tb00761.x
Araújo MB, Thuiller W, Pearson RG (2006) Climate warming and the decline of amphibians and reptiles in Europe. J Biogeogr 33(10):1712–1728. https://doi.org/10.1111/j.1365-2699.2006.01482.x
Baeckens S, Van Damme R (2018) Immunocompetence and parasite infestation in a melanistic and normally-coloured population of the lacertid lizard, Podarcis siculus. Amphibia-Reptilia 39:471–478. https://doi.org/10.1163/15685381-20181008
Bartoń K. (2019) MuMIn: multi-model inference. R package version 1.43.6. https://CRAN.R-project.org/package=MuMIn
Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Let 15:365–377. https://doi.org/10.1111/j.1461-0248.2011.01736.x
Blazejczyk K (2006) Climate and bioclimate of Poland. In: Degórski M (ed) Natural and human environment of Poland. Institute of Geography and Spatial Organization Polish Geographical Society, PAS, Warsaw, A geographical overview, pp 31–48
Błażuk J (2007) Herpetofauna doliny Sanu pod Otrytem i terenów przyległych (Bieszczady Zachodnie). Gady. Roczniki Bieszczadzkie 15:181–229
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. https://doi.org/10.1016/j.tree.2008.10.008
Brenner M, Hearing VJ (2007) The protective role of melanin against uv damage in human skin. Photochem Photobiol 84:539–549. https://doi.org/10.1111/j.1751-1097.2007.00226.x
Brischoux F, Dupoué A, Lourdais O, Angelier F (2016) Effects of mild wintering conditions on body mass and corticosterone levels in a temperate reptile, the aspic viper (Vipera aspis). Comp Biochem Physiol A 192:52–56. https://doi.org/10.1016/j.cbpa.2015.11.015
Broennimann O, Ursenbacher S, Meyer A, Golay P, Monney JC, Schmocker H, Guisan A, Dubey S (2014) Influence of climate on the presence of colour polymorphism in two montane reptile species. Biol Let 10(11):20140638. https://doi.org/10.1098/rsbl.2014.0638
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Bury S (2011) Frekwencja melanistycznej formy zaskrońca zwyczajnego Natrix natrix w Bieszczadach. BSC thesis. Jagiellonian University
Bury S, Mazgajski TD, Najbar B, Zając B, Kurek K (2020) Melanism, body size, and sex ratio in snakes—new data on the grass snake (Natrix natrix) and synthesis. Sci Nat 107(3). https://doi.org/10.1007/s00114-020-01678-x
Chmielewski FM, Müller A, Bruns E (2004) Climate changes and trends in phenology of fruit trees and field crops in Germany, 1961–2000. Agr Forest Meteorol 121(1–2): 69–78. https://https://doi.org/10.1016/S0168-1923(03)00161-8
Churchill TA, Storey KB (1992) Freezing survival of the garter snake Thamnophis sirtalis parietalis. Can J Zool 70(1):99–105. https://doi.org/10.1139/z92-015
Clusella Trullas S, van Wyk JH, Spotila JR (2007) Thermal melanism in ectotherms. J Therm Biol 32:235–245. https://doi.org/10.1016/j.jtherbio.2007.01.013
Costanzo JP (1989) Effects of humidity, temperature, and submergence behavior on survivorship and energy use in hibernating garter snakes, Thamnophis Sirtalis. Can J Zool 67(10):2486–2492. https://doi.org/10.1139/z89-351
Czernecki B, Głogowski A, Nowosad J (2020) Climate: an R package to access free in-situ meteorological and hydrological datasets for environmental assessment. Sustainability 12:394. https://doi.org/10.3390/su12010394
Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, Mcclean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Dubey S, Roulin A (2014) Evolutionary and biomedical consequences of internal melanins. Pigm Cell Melanoma R 27:327–338. https://doi.org/10.1111/pcmr.12231
Dubey S, Shine R (2011) Predicting the effects of climate change on reproductive fitness of an endangered montane lizard, Eulamprus leuraensis (Scincidae). Clim Change 107(3–4):531–547. https://doi.org/10.1007/s10584-010-9963-x
Ducrest A, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evols 23:502–510. https://doi.org/10.1016/j.tree.2008.06.001
Forsman A (1995a) Heating rates and body temperature variation in melanistic and zigzag Vipera berus: does colour make a difference? Ann Zool Fenn 32:365–374
Forsman A (1995b) Opposing fitness consequences of colour pattern in male and female snakes. J Evol Biol 8:53–70. https://doi.org/10.1046/j.1420-9101.1995.8010053.x
Fox J, Weisberg S. (2018) Visualizing fit and lack of fit in complex regression models with predictor effect plots and partial residuals. J Stat Softw 87(9): 1–27. https://doi.org/10.18637/jss.v087.i09
Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage Publications, Thousand Oaks, CA
Gardner JL, Peters A, Kearney MR, Joseph L, Heinsohn R (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26(6):285–291. https://doi.org/10.1016/j.tree.2011.03.005
Gibbons JW (1987) Activity patterns. In: Seigel RA, Collins JT, Novak SS (eds) Snakes, ecology and evolutionary biology. The Blackburn Press. pp 396–421
Gislen T, Kauri H (1959) Zoogeography of the Swedish amphibians and reptiles with notes on their growth and ecology. Acta Vertebratica 1:197–397
Goldenberg J, D’Alba L, Bisschop K, Vanthournout B, Shawkey MD (2021) Substrate thermal properties influence ventral brightness evolution in ectotherms. Comm Biol 4(1):1–10. https://doi.org/10.1038/s42003-020-01524-w
Gordo O (2007) Why are bird migration dates shifting? A review of weather and climate effects on avian migratory phenology. Clim Res 35(1–2):37–58. https://doi.org/10.1098/rspb.2013.2161
Greenwald OE, Kanter ME (1979) The effects of temperature and behavioral thermoregulation on digestive efficiency and rate in corn snakes (Elaphe guttata guttata). Physiol Zool 52(3):398–408. https://doi.org/10.1086/physzool.52.3.30155760
Gregory PT (1982) Reptilian hibernation. In: Gans C, Pough HF (eds) Biology of the Reptilia, 13. Academic Press, London, pp 53–154
Gregory PT, Isaac LA (2004) Food habits of the grass snake in southeastern England: is Natrix natrix a generalist predator? J Herpetol 38(1):88–95. https://doi.org/10.1017/10.1670/87-03A
Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 74(1):1–40. https://doi.org/10.1017/s0006323198005258
Harrell FE Jr (2015) Regression modeling strategies – with applications to linear models, logistic regression, and survival analysis, 2nd edn. Springer, New York
Hussein MF, Badir N, El Ridi R, El Deeb S (1979) Effect of seasonal variation on immune system of the lizard, Scincus Scincus. J Exp Zool 209(1):91–96. https://doi.org/10.1002/jez.1402090111
Jacquin L, Lenouvel P, Haussy C, Ducatez S, Gasparini J (2011) Melanin-based coloration is related to parasite intensity and cellular immune response in an urban free living bird: the feral pigeon Columba livia. J Avian Biol 42(1):11–15. https://doi.org/10.1111/j.1600-048X.2010.05120.x
Juszczyk W (1987) Płazy i gady krajowe. Państwowe Wydawnictwo Naukowe
Kjaergaard J (1981) The distribution af Black Viper in Denmark. Flora Og Fauna 87:27–29
Kondracki J (2000) Geografia regionalna polski. Wydawictwo. Naukowe PWN
Kurek K, Król W, Najberek K, Ćmiel AM, Solarz W, Bury S, Baś G, Najbar B, Okarma H (2018) Habitat use of the Aesculapian snake at different spatial scales. J Wildlife Manage 82(8):1746–1755. https://doi.org/10.1002/jwmg.21534
Lane JE, Kruuk LE, Charmantier A, Murie JO, Dobson FS (2012) Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489(7417):554–557. https://doi.org/10.1038/nature11335
Lepetz V, Massot M, Chaine AS, Clobert J (2009) Climate warming and the evolution of morphotypes in a reptile. Glob Change Biol 15:454–466. https://doi.org/10.1111/j.1365-2486.2008.01761.x
Luiselli L (1992) Reproductive success in melanistic adders: a new hypothesis and some considerations on Andrén and Nilson’s (1981) suggestions. Oikos, 601-604https://doi.org/10.2307/3545182
Mader S, Goldenberg J, Massetti F, Bisschop K, D’Alba L, Etienne RS, Clusella-Trulas S, Shawkey M (2022) How melanism affects the sensitivity of lizards to climate change. Funct Ecol. In press https://doi.org/10.1111/1365-2435.13993
Madsen T (1984) Movements, home range size and habitat use of radio-tracked grass snakes (Natrix natrix) in southern Sweden. Copeia 3:707–713. https://doi.org/10.2307/1445153
Madsen T (1987) Are juvenile grass snakes, Natrix natrix, aposematically coloured? Oikos 48:265. https://doi.org/10.2307/3565512
Madsen T, Stille B (1988) The effect of size dependent mortality on colour morphs in male adders, Vipera Berus. Oikos 52:73. https://doi.org/10.2307/3565984
Makarieva AM, Gorshkov VG, Li BL, Chown SL, Reich PB, Gavrilov VM (2008) Mean mass-specific metabolic rates are strikingly similar across life’s major domains: evidence for life’s metabolic optimum. PNAS 105(44):16994–16999. https://doi.org/10.1073/pnas.0802148105
Martínez-Freiría F, Toyama KS, Freitas I, Kaliontzopoulou A (2020) Thermal melanism explains macroevolutionary variation of dorsal pigmentation in Eurasian vipers. Sci Rep 10(1):1–10. https://doi.org/10.1038/s41598-020-72871-1
Mertens D (1994) Some aspects of thermoregulation and activity in free-ranging grass snakes (Natrix natrix L.). Amphibia-Reptilia, 15(3):322–326. https://doi.org/10.1163/156853894X00100
Michna E, Paczos S (1972) Zarys klimatu Bieszczadów Zachodnich. Zakład Narodowy im. Ossolińskich, Wydawnictwo Polskiej Akademii Nauk
Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. PNAS 105(42):16195–16200. https://doi.org/10.1073/pnas.0803825105
Monney JC, Luiselli L, Capula M (1996) Body size and melanism in Vipera aspis in the Swiss Prealps and central Italy and comparison with different Alpine populations of Vipera berus. Rev Suisse Zool 103(1):81–100. https://doi.org/10.1111/jzo.12037
Muri D, Schuerch J, Trim N, Golay J, Baillifard A, El Taher A, Dubey S (2015) Thermoregulation and microhabitat choice in the polymorphic asp viper (Vipera aspis). J Therm Biol 53:107–112. https://doi.org/10.1016/j.jtherbio.2015.06.009
Murray DL, Bastille-Rousseau G, Beaty LE, Hornseth ML, Row JR, Thornton DH (2020) From research hypothesis to model selection. In: Murray DL, Sandercock BK (eds) Population ecology in practice. John Wiley & Sons, pp 17–45
Najbar B (2004) Wąż Eskulapa Elaphe (Zamenis) longissima (Laurenti, 1768) Bieszczadach Zachodnich. Oficyna Wydawnicza Uniwersytetu Zielonogórskiego
Najbar B, Borczyk B (2012) Zaskroniec zwyczajny: biologia i Ochrona. Zielona Góra, Poland: Oficyna Wydawnicza Uniwersytetu Zielonogórskiego
Nash DJ, Robinson S, Lewis TR (2016) Observations on the distribution of melanistic snakes in Britain. Herp Bull 136:19
Nilson G, Andren C (1981) Morphology and taxonomic status of the grass snake, Natrix natrix (L.) (Reptilia, Squamata, Colubridae) on the island of Gotland. Sweden Zool J Linn Soc 72:355–368. https://doi.org/10.1111/j.1096-3642.1981.tb01576.x
Patterson JW (1984) The influence of temperature, sexual condition, and season on the metabolic rate of the lizard Psammodromus hispanicus. J Comp Physiol B 154(3):311–316. https://doi.org/10.1007/BF02464412
Quintero I, Wiens JJ (2013) Rates of projected climate change dramatically exceed past rates of climatic niche evolution among vertebrate species. Ecol Let 16:1095–1103. https://doi.org/10.1111/ele.12144
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. <https://www.R-project.org/>
Ryan MP, Neuman-Lee LA, Durham SL, Smith GD, French SS (2018) A sex-dependent change in behavioral temperature regulation in African house snakes (Lamprophis fuliginosus) challenged with different pathogens. J Therm Biol 73:8–13. https://doi.org/10.1016/j.jtherbio.2018.02.001
Sanz JJ, Potti J, Moreno J, Merino S, Frias O (2003) Climate change and fitness components of a migratory bird breeding in the Mediterranean region. Glob Change Biol 9(3):461–472. https://doi.org/10.1046/j.1365-2486.2003.00575.x
Shine R, Madsen T (1994) Sexual dichromatism in snakes of the genus Vipera: a review and a new evolutionary hypothesis. J Herpetol 28(1):114–117. https://doi.org/10.2307/1564692
Shine R, Mason RT (2004) Patterns of mortality in a cold-climate population of garter snakes (Thamnophis sirtalis parietalis). Biol Conserv 120(2):201–210. https://doi.org/10.1016/j.biocon.2004.02.014
Sinervo B et al. (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328: 894–899. 0.1126/science.1184695
Skoczylas R (1970) Influence of temperature on gastric digestion in the grass snake, Natrix natrix L. Comp Biochem Physiol 33:793–804. https://doi.org/10.1016/0010-406X(70)90028-9
Stenseth NC, Mysterud A (2002) Climate, changing phenology, and other life history traits: nonlinearity and match–mismatch to the environment. PNAS 99(21):13379–13381. https://doi.org/10.1073/pnas.212519399
Strugariu A, Zamfirescu ŞR (2011) Population characteristics of the adder (Vipera berus berus) in the Northern Romanian Carpathians with emphasis on colour polymorphism: is melanism always adaptive in vipers? Anim Biol 61(4):457–468. https://doi.org/10.1163/157075511X597601
Thomas CD et al (2010) A framework for assessing threats and benefits to species responding to climate change. Methods Ecol Evol 2:125–142. https://doi.org/10.1111/j.2041-210X.2010.00065.x
Thuiller W, Lavorel S, Araujo MB, Sykes MT, Prentice IC (2005) Climate change threats to plant diversity in Europe. PNAS 102:8245–8250
Ultsch GR (1989) Ecology and physiology of hibernation and overwintering among freshwater fishes, turtles, and snakes. Biol Rev 64(4):435–515. https://doi.org/10.1111/j.1469-185X.1989.tb00683.x
Wiedl H, Böhme W (1992) Wiederentdeckung der Ringelnatter (Natrix natrix) auf Zypernvorlaufiger Bericht. Herpetofauna 14(20):6–10
Williams CM, Henry HA, Sinclair BJ (2015) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol Rev 90(1):214–235. https://doi.org/10.1111/brv.12105
Wilson BS, Cooke DE (2004) Latitudinal variation in rates of overwinter mortality in the lizard Uta stansburiana. Ecology 85(12):3406–3417. https://doi.org/10.1890/03-4075
Wright RK, Cooper EL (1981) Temperature effects on ectotherm immune responses. Dev Comp Immunol 5:117–122. https://doi.org/10.1016/0145-305X(81)90016-1
Zani PA, Irwin JT, Rollyson ME, Counihan JL, Healas SD, Lloyd EK, Kojanis LC, Fried B, Sherma J (2012) Glycogen, not dehydration or lipids, limits winter survival of side-blotched lizards (Uta stansburiana). J Exp Biol 215(17):3126–3134. https://doi.org/10.1242/jeb.069617
Zuffi M (2008) Colour pattern variation in populations of the European Whip snake, Hierophis viridiflavus: does geography explain everything? Amphibia-Reptilia 29:229–233. https://doi.org/10.1163/156853808784124929
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We thank Peter Senn for proof-reading the text and providing linguistic corrections. We also thank Todd Lewis and two anonymous reviewers for valuable comments on an earlier version of the manuscript.
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The study was financially supported by the Jagiellonian University of Kraków (N18/DBW/000008) and START Programme from the Foundation for Polish Science.
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SB led the writing of the manuscript; TDM helped with writing the manuscript; BN led the collection of the majority field data on snakes; KK helped with writing the manuscript; AK and PCh collected climatic data from the Institute of Meteorology and Water Management. PCh performed the statistical analyses. All the authors gave their final approval to the manuscript.
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Bury, S., Kolanek, A., Chylarecki, P. et al. Climatic conditions and prevalence of melanistic snakes—contrasting effects of warm springs and mild winters. Int J Biometeorol 66, 1329–1338 (2022). https://doi.org/10.1007/s00484-022-02279-1
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DOI: https://doi.org/10.1007/s00484-022-02279-1