Vol. 19 No. 1 (2024)
Articles

The tale of the black viper: distribution and bioclimatic niche modelling of melanistic Vipera aspis in Italy

PDF
  • Matteo R. Di Nicola,
  • Francesco P. Faraone,
  • Andrea V. Pozzi,
  • Nicolò Borgianni,
  • Lorenzo Laddaga,
  • Jean-Lou M. C. Dorne,
  • Gianmarco Minuti
Matteo R. Di Nicola
Unit of Dermatology and Cosmetology, IRCCS San Raffaele Hospital, Via Olgettina 60, 20132 Milan
Francesco P. Faraone
Dipartimento Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, University of Palermo, Via Archirafi 18, 90123 Palermo
Andrea V. Pozzi
Molecular Ecology and Evolution Group, School of Environmental and Natural Sciences, Bangor University, Bangor, Wales
Nicolò Borgianni
Rewilding Apennines ETS, Gioia dei Marsi (AQ)
Lorenzo Laddaga
Società di Scienze Naturali del Verbano Cusio Ossola, Museo di Scienze Naturali, Collegio Mellerio Rosmini, Domodossola
Jean-Lou M. C. Dorne
Methodology and Scientific Support Unit, European Food Safety Authority (EFSA), Via Carlo Magno 1A, Parma 43126
Gianmarco Minuti
Department of Biology, Ecology & Biodiversity Research Unit, Vrije Universiteit Brussels, Brussels
DOI: https://doi.org/10.36253/a_h-15271

Published 2024-06-21

Keywords

  • Bioclimatic model,
  • Habitat suitability,
  • MaxEnt,
  • Mediterranean,
  • Melanism,
  • Snake,
  • Vipera aspis
    • ...More
    Less

How to Cite

Di Nicola, M. R., Faraone, F. P., Pozzi, A. V., Borgianni, N., Laddaga, L., Dorne, J.-L. M. C., & Minuti, G. (2024). The tale of the black viper: distribution and bioclimatic niche modelling of melanistic Vipera aspis in Italy. Acta Herpetologica, 19(1), 13–27. https://doi.org/10.36253/a_h-15271

Copyright (c) 2024 Matteo Riccardo Di Nicola, Francesco Paolo Faraone, Andrea Vittorio Pozzi, Nicolò Borgianni, Lorenzo Laddaga, JEAN-LOU M. C. DORNE, Gianmarco Minuti

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Crossref
Scopus
Google Scholar
Europe PMC

Abstract

For decades, the evolutionary role of melanism in reptiles has been highly debated. According to the thermal melanism hypothesis, melanistic phenotypes should provide thermal advantages, thus positively impacting various biological aspects of these individuals. Nevertheless, these benefits seem to be countered by environmental constraints and predatory pressure. Here, we mapped for the first time the distribution of the melanistic phenotypes in the highly polymorphic asp viper (Vipera aspis). We focused our research effort on the Italian peninsula, where this species reaches its highest level of taxonomic diversity with three currently described subspecies. Furthermore, we investigated via bioclimatic niche modelling, the influence of a wide array of bioclimatic variables on the distribution of melanism in Italian asp vipers. In general, our results seem to support the implications of the thermal melanism hypothesis, highlighting the central influence of mean annual temperature and elevation on the geographic distribution of melanistic V. aspis. At the finest scale, our analyses have highlighted a distinction in bioclimatic niches among the three assessed subspecies. However, further fine-scale investigations are needed in order to exclude the potential influence of latitude and elevation on the observed the intersubspecific bioclimatic niche segregation pattern.

PDF

Metrics

Metrics Loading ...

References

  1. Allen, W.L., Baddeley, R., Scott-Samuel, N.E., Cuthill, I.C. (2013): The evolution and function of pattern diversity in snakes. Behav. Ecol. 24: 1237-1250.
  2. Andersen, D., Litvinchuk, S.N., Jang, H.J., Jiang, J., Koo, K.S., Maslova, I., Kim, D., Jang, Y., Borzée, A. (2022): Incorporation of latitude-adjusted bioclimatic variables increases accuracy in species distribution models. Ecol. Model. 469: 109986.
  3. André, G., Lavergne, S., Carcaillet, C. (2023): Unsuspected prevalence of Pinus cembra in the high-elevation sky islands of the western Alps. Plant Ecol. 224: 865-873.
  4. Andrén, 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.
  5. Attorre, F., Alfo’, M., De Sanctis, M., Francesconi, F., Bruno, F. (2007): Comparison of interpolation methods for mapping climatic and bioclimatic variables at regional scale. Int. J. Climatol. 27: 1825-1843.
  6. Baena, O., Oliveras, I. (2015): Nou cas de melanisme en Vipera aspis (Linnaeus, 1758) al massís del Montseny (Vallès Oriental; Catalunya). Butll. Soc. Catalana d’Herpetologia 22: 29-30.
  7. Barbanera, F., Zuffi, M.A.L., Guerrini, M., Gentilli, A., Tofanelli, S., Fasola, M., Dini, F. (2009): Molecular phylogeography of the asp viper Vipera aspis (Linnaeus, 1758) in Italy: Evidence for introgressive hybridization and mitochondrial DNA capture. Mol. Phylogenet. Evol. 52: 103-114.
  8. Bassini, E., Bruno, S., Mazzei, P., Stagni, G. (1991): I serpenti dell’Emilia-Romagna e in particolare della provincia di Bologna (Italia settentrionale). Mediterránea. Serie de Estudios Biológicos, N. 13 (1991); Pp. 27-66.
  9. Benito, M., Pérez-Salerno, A., Gómez, S., Albero, L. (2022): New cases of melanism in Chalcides striatus, Coronella austriaca, and Vipera seoanei from Burgos, northern Spain. Herpetol. Notes 15: 687-689.
  10. Bittner, T.D., King, R.B., Kerfin, J.M. (2002): Effects of body size and melanism on the thermal biology of garter snakes (Thamnophis sirtalis). Copeia 2002: 477-482.
  11. Bonanomi, G., Zotti, M., Mogavero, V., Cesarano, G., Saulino, L., Rita, A., Tesei, G., Allegrezza, M., Saracino, A., Allevato, E. (2020): Climatic and anthropogenic factors explain the variability of Fagus sylvatica treeline elevation in fifteen mountain groups across the Apennines. For. Ecosyst. 7: 5.
  12. Borgianni, N., Paolino, G. (2020): Melanism in Vipera aspis francisciredi (Laurenti, 1768) (Reptilia Serpentes) in the Lazio Region (Parco Naturale Regionale dei Monti Simbruini), Italy. Biodivers. J. 11: 615-618.
  13. Boria, R.A., Olson, L.E., Goodman, S.M., Anderson, R.P. (2014): Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol. Model. 275: 73-77.
  14. Brodmann, P. (1987): Die Giftschlangen Europas und die Gattung Vipera in Afrika und Asien. Bern, Kümmerly u. Frey.
  15. Broennimann, O., Ursenbacher, S., Meyer, A., Golay, P., Monney, J.-C., Schmocker, H., Guisan, A., Dubey, S. (2014): Influence of climate on the presence of colour polymorphism in two montane reptile species. Biol. Lett. 10: 20140638.
  16. Brooks, J., Rohrer, J., Beck, D.D. (2022): Color Variation, Tail Banding, and Sexual Dichromatism in Washington Populations of Northern Pacific Rattlesnakes, Crotalus oreganus. Herpetologica 78: 192-200.
  17. Bruni, G., Di Nicola, M.R., Banfi, F., Faraone, F.P. (2022): Distribution and characterization of melanism in Grass Snakes from Italy. Nat. Sicil. 46: 41-48.
  18. Bruno, S. (1976): L’ornamentazione della Vipera aspis (L., 1758) in Italia (Serpentes Viperidae) (Studi sulla fauna erpetologica italiana. XXI). Atti Soc. ital. Sci. Nat. Mus. Civ. Stor. Nat. Milano 117: 165-194.
  19. Bruno, S. (1985): Le vipere d’Italia e d’Europa. Edagricole, Bologna.
  20. Bury, S., Kolanek, A., Chylarecki, P., Najbar, B., Kurek, K., Mazgajski, T.D. (2022): Climatic conditions and prevalence of melanistic snakes-contrasting effects of warm springs and mild winters. Int. J. Biometeorol. 66: 1329-1338.
  21. Bury, S., Mazgajski, T.D., 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: 22.
  22. Capula, M., Luiselli, L. (1994): Reproductive strategies in alpine adders, Vipera berus. The black females bear more often. Acta Oecol. 15: 207-214.
  23. Castella, B., Golay, J., Monney, J. ‐C., Golay, P., Mebert, K., Dubey, S. (2013): Melanism, body condition and elevational distribution in the asp viper. J. Zool. 290: 273-280.
  24. Chang, C., Zheng, R. (2003): Effects of ultraviolet B on epidermal morphology, shedding, lipid peroxide, and antioxidant enzymes in Cope’s rat snake (Elaphe taeniura). J. Photoch. Photobio. B 72: 79-85.
  25. Clusella Trullas, S., Terblanche, J.S., Van Wyk, J.H., Spotila, J.R. (2007a): Low repeatability of preferred body temperature in four species of Cordylid lizards: Temporal variation and implications for adaptive significance. Evol. Ecol. 21: 63-79.
  26. Clusella Trullas, S., Van Wyk, J.H., Spotila, J.R. (2007b): Thermal melanism in ectotherms. J. Therm. Biol. 32: 235-245.
  27. Clusella‐Trullas, S., Terblanche, J.S., Blackburn, T.M., Chown, S.L. (2008): Testing the thermal melanism hypothesis: a macrophysiological approach. Funct. Ecol. 22: 232-238.
  28. Cox, C.L., Davis Rabosky, A.R. (2013): Spatial and Temporal Drivers of Phenotypic Diversity in Polymorphic Snakes. Am. Nat. 182: E40-E57.
  29. Cox, C.L., Rabosky, A.R.D., Chippindale, P.T. (2013): Sequence variation in the Mc1r gene for a group of polymorphic snakes. Gene 513: 282-286.
  30. Cyriac, V.P., Kodandaramaiah, U. (2019): Conspicuous colours reduce predation rates in fossorial uropeltid snakes. PeerJ 7: e7508.
  31. De Avila, F., Oliveira, J., De Oliveira, M., Borges-Martins, M., Valiati, V.H., Tozetti, A. (2019): Does color polymorphism affect the predation risk on Phalotris lemniscatus (Duméril, Bibron and Duméril, 1854) (Serpentes, Dipsadidae)? Acta Herpetol. 14: 57-63.
  32. De Smedt, J. (2006): The Vipers of Europe. Halblech, JDS Verlag.
  33. Delhey, K. (2017): Gloger’s rule. Curr. Biol. 27: R689-R691.
  34. Di Nicola, M.R. (2019): A revised dichotomous key to the snakes of Italy (Reptilia, Squamata, Serpentes), according to recent systematic updates. Zootaxa 4686: 294-296.
  35. Di Nicola, M.R., Cavigioli, L., Luiselli, L., Andreone, F. (2019): Anfibi & Rettili d’Italia. Edizioni Belvedere, Latina.
  36. Di Nicola, M.R., Cavigioli, L., Luiselli, L., Andreone, F. (2021): Anfibi & Rettili d’Italia. Edizione aggiornata. Edizioni Belvedere, Latina.
  37. Di Nicola, M.R., Faraone, F.P. (2020): Vipera aspis hugyi (Southern Italian Asp). Coloration. Herpetol. Rev. 51: 631.
  38. Di Nicola, M.R., Faraone, F.P., Zabbia, T. (2022): An updated dichotomous key to the snakes of Europe. Basic Appl. Herpetol. 36: 47-64.
  39. Di Nicola, M.R., Meier, G.J. (2013): Vipera aspis hugyi (Southern Italian asp) melanism. Herpetol. Rev. 44: 698.
  40. Dubey, S., Zwahlen, V., Mebert, K., Monney, J.-C., Golay, P., Ott, T., Durand, T., Thiery, G., Kaiser, L., Geser, S.N., Ursenbacher, S. (2015): Diversifying selection and color-biased dispersal in the asp viper. BMC Evol. Biol. 15: 99.
  41. Ducrest, A.-L., Ursenbacher, S., Golay, P., Monney, J.-C., Mebert, K., Roulin, A., Dubey, S. (2014): Pro-opiomelanocortin gene and melanin-based colour polymorphism in a reptile: Colour Polymorphism. Biol. J. Linn. Soc. Lond. 111: 160-168.
  42. Elith, J., Phillips, S.J., Hastie, T., Dudík, M., Chee, Y.E., Yates, C.J. (2011): A statistical explanation of MaxEnt for ecologists: Statistical explanation of MaxEnt. Divers. Distrib. 17: 43-57.
  43. Fănaru, G., Telea, A.E., Gherghel, I., Melenciuc, R. (2022): Melanism in the grass snake Natrix natrix (Linnaeus, 1758) from the Danube Delta Biosphere Reserve, Romania. Herpetozoa 35: 257-263.
  44. Fick, S.E., Hijmans, R.J. (2017): WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37: 4302-4315.
  45. Fielding, A.H., Bell, J.F. (1997): A review of methods for the assessment of prediction errors in conservation presence/absence models. Envir. Conserv. 24: 38-49.
  46. Forsman, A. (2016): Is colour polymorphism advantageous to populations and species? Mol. Ecol. 25: 2693-2698.
  47. Forsman, A., Ahnesjö, J., Caesar, S., Karlsson, M. (2008): A model of ecological and evolutionary consequences of color polymorphism. Ecology 89: 34-40.
  48. Fu, T.-T., Sun, Y.-B., Gao, W., Long, C.-B., Yang, C.-H., Yang, X.-W., Zhang, Y., Lan, X.-Q., Huang, S., Jin, J.-Q., Murphy, R.W., Zhang, Y., Lai, R., Hillis, D.M., Zhang, Y.-P., Che, J. (2022): The highest-elevation frog provides insights into mechanisms and evolution of defenses against high UV radiation. Proc. Natl. Acad. Sci. U.S.A. 119: e2212406119.
  49. García-Roa, R.G., Carbonell, G. (2020): The dark side of Vipera aspis: a case of melanismin the Iberian Peninsula. Bol. Asoc. Herpetol. Esp. 31: 34-36.
  50. GBIF.org (2023): GBIF Occurrence Download https://doi.org/10.15468/dl.3nht55.
  51. Geniez, P. (2015): Serpents d’Europe, d’Afrique du Nord et du Moyen-Orient. Paris, Delachaux et Niestlé.
  52. Gibson, A.R., Falls, B. (1979): Thermal biology of the common garter snake Thamnophis sirtalis (L.): II. The effects of melanism. Oecologia 43: 99-109.
  53. Golay, P., Monney, J.-C., Conelli, A., Durand, T., Thiery, G., Zuffi, M.A.L., Ursenbacher, S. (2008): Systematics of the Swiss asp vipers: some implications for the European Vipera aspis (Linnaeus, 1758) complex (Serpentes: Viperidae) - A tribute to Eugen Kramer. Amphibia-Reptilia 29: 71-83.
  54. Goldenberg, J., D’Alba, L., Bisschop, K., Vanthournout, B., Shawkey, M.D. (2021): Substrate thermal properties influence ventral brightness evolution in ectotherms. Commun. Biol. 4: 26.
  55. Grano, M., Meier, G., Cattaneo, C. (2017): Vipere Italiane. Gli ultimi studi sulla sistematica, l’ecologia e la storia naturale. Aicurzio, Castel Negrino.
  56. Hantak, M.M., Guralnick, R.P., Cameron, A.C., Griffing, A.H., Harrington, S.M., Weinell, J.L., Paluh, D.J. (2022): Colour scales with climate in North American ratsnakes: a test of the thermal melanism hypothesis using community science images. Biol. Lett. 18: 20220403.
  57. Huey, R.B., Kingsolver, J.G. (1989): Evolution of thermal sensitivity of ectotherm performance. Trends Ecol. Evol. 4: 131-135.
  58. Jin, Y., Tong, H., Shao, G., Li, J., Lv, Y., Wo, Y., Brown, R.P., Fu, C. (2020): Dorsal Pigmentation and Its Association with Functional Variation in MC1R in a Lizard from Different Elevations on the Qinghai–Tibetan Plateau. Genome Biol. Evol. 12: 2303-2313.
  59. Jong, P.W.D., Gussekloo, S.W.S., Brakefield, P.M. (1996): Differences in Thermal Balance, Body Temperature and Activity Between Non-Melanic and Melanic Two-Spot Ladybird Beetles (Adalia bipunctata ) Under Controlled Conditions. J. Exp. Biol. 199: 2655-2666.
  60. Kalogiannis, S. (2021): Cases of melanism in Dolichophis caspius (Gmelin, 1789) (Squamata: Colubridae) from Greece and a new distribution record. Parnassiana Archives 9: 19-22.
  61. Kassambara, A., Mundt, F. (2020): Factoextra: Extract and Visualize the Results of Multivariate Data Analyses. R Package Version 1.0.7.
  62. Körner, C. (2007): The use of ‘altitude’ in ecological research. Trends Ecol. Evol. 22: 569-574.
  63. Kumar, B. (2009): Nove najdbe laškega gada (Vipera aspis) v Sloveniji. Natura Sloveniae 11: 59-63.
  64. Lê, S., Josse, J., Husson, F. (2008): FactoMineR : An R Package for Multivariate Analysis. J. Stat. Soft. 25.
  65. Lorioux, S., Bonnet, X., Brischoux, F., De Crignis, M. (2008): Is melanism adaptive in sea kraits? Amphibia-Reptilia 29: 1-5.
  66. Lucchini, N., Kaliontzopoulou, A., Val, G.A., Martínez-Freiría, F. (2020): Sources of intraspecific morphological variation in Vipera seoanei: allometry, sex, and colour phenotype. Amphibia-Reptilia 42: 1-16.
  67. Luiselli, L. (1992): Reproductive Success in Melanistic Adders: A New Hypothesis and Some Considerations on Andrén and Nilson’s (1981) Suggestions. Oikos 64: 601.
  68. Luiselli, L. (1993): The ecological role of color polymorphism in male adders Vipera berus: testing the hypotheses. Rev. Ecol. 48: 49-56.
  69. Madsen, T. (1987): Are Juvenile Grass Snakes, Natrix natrix, Aposematically Coloured? Oikos 48: 265.
  70. Madsen, T., Stille, B. (1988): The Effect of Size Dependent Mortality on Colour Morphs in Male Adders, Vipera berus. Oikos 52: 73.
  71. Majerus, M. (1998): Melanism: evolution in action. Oxford university press, Oxford, New York, Tokyo.
  72. Martínez-Freiría, F., Toyama, K.S., Freitas, I., Kaliontzopoulou, A. (2020): Thermal melanism explains macroevolutionary variation of dorsal pigmentation in Eurasian vipers. Sci. Rep. 10: 16122.
  73. Masseti, M., Zuffi, M.A.L. (2011): On the origin of the asp viper Vipera aspis hugyi Schinz, 1833, on the island of Montecristo, Northern Tyrrhenian Sea (Tuscan archipelago, Italy). Herpetol. Bull. 117: 1-9.
  74. Matthews, G., Goulet, C.T., Delhey, K., Chapple, D.G. (2016): The effect of skin reflectance on thermal traits in a small heliothermic ectotherm. J. Therm. Biol. 60: 109-124.
  75. McRobie, H.R., Moncrief, N.D., Mundy, N.I. (2019): Multiple origins of melanism in two species of North American tree squirrel (Sciurus). BMC Evol. Biol. 19: 140.
  76. Mebert, K., Zwahlen, V., Golay, P., Thierry, D., Ursenbacher, S. (2011): Ungewöhnlich hoher Farb-Polymorphismus in alpinen Aspisvipern in Frankreich - Zufall oder natürliche Selektion? Elaphe 1: 13-19.
  77. Monney, J.-C., Luiselli, L., Capula, M. (1995): Correlates of melanism in a population of adders (Vipera berus) from the Swiss Alps and comparisons with other alpine populations. Amphibia-Reptilia 16: 323-330.
  78. Monney, J.-C., Luiselli, L., Capula, M. (1996): Taille et mélanisme chez Vipera aspis dans les Préalpes suisses et en Italie centrale et comparaison avec différentes populations alpines de Vipera berus. Rev. Suisse Zool. 103: 81-100.
  79. Moreno Azócar, D.L., Nayan, A.A., Perotti, M.G., Cruz, F.B. (2020): How and when melanic coloration is an advantage for lizards: the case of three closely-related species of Liolaemus. Zoology 141: 125774.
  80. 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.
  81. Pérez-Tris, J., Bensch, S., Carbonell, R., Helbig, A.J., Tellería, J.L. (2004): Historical diversification of migration patterns in a passerine bird. Evolution 58: 1819.
  82. Pernetta, A.P., Reading, C.J. (2009): Observations of two melanistic smooth snakes (Coronella austriaca) from Dorset, United Kingdom. Acta Herpetol. 4: 109-112.
  83. Phillips, S.J., Anderson, R.P., Dudík, M., Schapire, R.E., Blair, M.E. (2017): Opening the black box: an open‐source release of Maxent. Ecography 40: 887-893.
  84. Pizzatto, L., Dubey, S. (2012): Colour-polymorphic snake species are older. Biol. J. Linn. Soc. 107: 210-218.
  85. Pizzigalli, C., Banfi, F., Ficetola, G.F., Falaschi, M., Mangiacotti, M., Sacchi, R., Zuffi, M.A.L., Scali, S. (2020): Eco-geographical determinants of the evolution of ornamentation in vipers. Biol. J. Linn. Soc. 130: 345-358.
  86. Pottier, G. (2001): Notes sur trois cas de mélanisme chez Vipera aspis zinnikeri Kramer, 1958 (Ophidia, Viperidae) dans les Hautes-Pyrénées (France). Bull. Soc. Herpétol. Fr. 49-53.
  87. QGIS Development Team (2020): QGIS Geographic Information System. Open Source Geospatial Foundation Project, http://qgis.osgeo.org.
  88. R Core Team (2023): R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org.
  89. Regnet, R.A., Quintela, F.M., Roedder, D., Loebmann, D. (2022): Attributes of the population structure and ventral polychromatism of Helicops infrataeniatus Jan, 1865 (Serpentes, Colubridae, Dipsadinae) in subtropical Brazil. North-West. J. Zool. 18: 161-167.
  90. Reguera, S., Zamora-Camacho, F. J., & Moreno-Rueda, G. (2014): The lizard Psammodromus algirus (Squamata: Lacertidae) is darker at high altitudes. Biol. J. Linn. Soc. 112: 132-141.
  91. Rivera, X., Arribas, O., Martí, F. (2001): Anomalías pigmentarias en las especies de reptiles presentes en la Península Ibérica, Islas Baleares y Canarias. Butll. Soc. Catalana d’Herpetologia 15: 76-88.
  92. Ruane, S., Myers, E.A., Lo, K., Yuen, S., Welt, R.S., Juman, M., Futterman, I., Nussbaum, R.A., Schneider, G., Burbrink, F.T., Raxworthy, C.J. (2018): Unrecognized species diversity and new insights into colour pattern polymorphism within the widespread Malagasy snake Mimophis (Serpentes: Lamprophiidae). Syst. Biodivers. 16: 229-244.
  93. San-Jose, L.M., Gonzalez-Jimenez, V., Fitze, S. (2008): Frequency and phenotypic differences of a melanistic and normally colored common lizard, Lacerta (Zootoca) vivipara of the Southern Pyrenees (Spain). Herp. Rev. 39: 422-425.
  94. San-Jose, L.M., Roulin, A. (2018): Toward Understanding the Repeated Occurrence of Associations between Melanin-Based Coloration and Multiple Phenotypes. Am. Nat. 192: 111-130.
  95. Santos, X., Azor, J.S., Cortés, S., Rodríguez, E., Larios, J., Pleguezuelos, J.M. (2018): Ecological significance of dorsal polymorphism in a Batesian mimic snake. Curr. Zool. 64: 745-753.
  96. Senczuk, G., Gramolini, L., Avella, I., Mori, E., Menchetti, M., Aloise, G., Castiglia, R. (2021): No association between candidate genes for color determination and color phenotype in Hierophis viridiflavus, and characterization of a contact zone. J. Zool. Syst. Evol. Res. 59: 748-759.
  97. Sherbrooke, W.C., Frost, S.K. (1989): Integumental chromatophores of a color-change, thermoregulating lizard, Phrynosoma modestum (Iguanidae ; Reptilia). Am. Mus. Novit. 2943: 1-14.
  98. Shine, R.G. (1993): Sexual dimorphism in snakes. In: Snakes: Ecology and Behavior, p. 49-86. Seigel, R.A, Collins, J.T, Eds, McGraw-Hill, New York.
  99. Sindaco, R., Razzetti, E. (2021): An updated check-list of Italian amphibians and reptiles. Nat. Hist. Sci. 8: 35-46.
  100. Speybroeck, J., Beukema, W., Bok, B., Van Der Voort, J., Velikov, I. (2016): Field guide to the amphibians & Reptiles of Britain and Europe. Bloomsbury, London, Oxford, New York, New Dehli, Sydney.
  101. Støa, B., Halvorsen, R., Stokland, J.N., Gusarov, V.I. (2019): How much is enough? Influence of number of presence observations on the performance of species distribution models. Sommerfeltia 39: 1-28.
  102. Storniolo, F., Mangiacotti, M., Zuffi, M.A.L., Scali, S., Sacchi, R. (2023): Large scale phenotypic characterisation of Hierophis viridiflavus (Squamata: Serpentes): climatic and environmental drivers suggest the role of evolutionary processes in a polymorphic species. Evol. Ecol. 37: 419-434.
  103. Strugariu, A., Zamfirescu, Ş.R. (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: 457-468.
  104. Tanaka, K. (2009): Does the Thermal Advantage of Melanism Produce Size Differences in Color-dimorphic Snakes? Zool. Sci. 26: 698-703.
  105. Tessa, G. (2016): Preliminary data on distribution of a rare dorsal pattern in Vipera aspis aspis (Ophidia: Viperidae) in the Gran Paradiso National Park. In: Atti XI Congresso Nazionale Della Societas Herpetologica Italica, pp. 22-25. Menegon, M., Rodriguez-Prieto, A., Deflorian, M.C., Eds, Ianieri Edizioni, Pescara.
  106. True, J.R. (2003): Insect melanism: the molecules matter. Trends Ecol. Evol. 18: 640-647.
  107. Turrisi, G.F., Vaccaro, A. (2001): Distribuzione altitudinale di anfibi e rettili sul monte Etna (Sicilia orientale). Pianura, 13: 335-338.
  108. Turrisi, G.F., Vaccaro, A. (2004): Anfibi e rettili del Monte Etna (Sicilia orientale). Boll. Accad. Gioenia Sci. Nat 36: 5-103.
  109. Ursenbacher, S., Conelli, A., Golay, P., Monney, J.-C., Zuffi, M.A.L., Thiery, G., Durand, T., Fumagalli, L. (2006): Phylogeography of the asp viper (Vipera aspis) inferred from mitochondrial DNA sequence data: Evidence for multiple Mediterranean refugial areas. Mol. Phylogenet. Evol. 38: 546-552.
  110. van Proosdij, A.S.J., Sosef, M.S.M., Wieringa, J.J., Raes, N. (2015): Minimum required number of specimen records to develop accurate species distribution models. Ecography 39: 542-552.
  111. Watt, W.B. (1968): Adaptive Significance of Pigment Polymorphisms in Colias Butterflies. I. Variation of Melanin Pigment in Relation to Thermoregulation. Evolution 22: 437.
  112. Wickham, H. (2016): ggplot2: elegant graphics for data analysis. Switzerland, Springer.
  113. Wolf, M., Werner, Y.L. (1994): The striped colour pattern and striped/non-striped polymorphism in snakes (Reptilia: Ophidia). Biol. Rev. 69: 599-610.
  114. Zuffi, M.A.L. (1984): Cenni sulla distribuzione dell ‘ofidiofauna in un ambiente tipo dell ‘Appennino pavese: fasce preferenziali e loro condizioni ecologiche. Natura, Milano 75: 65-68.
  115. Zuffi, M.A.L. (2002): A critique of the systematic position of the asp viper subspecies Vipera aspis aspis (Linnaeus, 1758), Vipera aspis atra Meisner, 1820, Vipera aspis francisciredi Laurenti, 1768, Vipera aspis hugyi Schinz, 1833 and Vipera aspis zinnikeri Kramer, 1958. Amphibia-Reptilia 23: 191-213.
  116. Zuffi, M.A.L. (2006): Vipera aspis (Linnaeus, 1758). In: Atlante Degli Anfibi e Dei Rettili d’Italia, pp. 594-599. Sindaco, R., Doria, G., Razzetti, E., Bernini, F., Eds, Edizioni Polistampa, Firenze.
  117. Zuffi, M.A.L., Gentilli, A., Luiselli, L. (2011): Vipera aspis (Linnaeus, 1758). In: Fauna d’Italia - Vol. XLV - Reptilia, pp. 608-617. Corti, C., Capula, M., Luiselli, L., Razzetti, E., Sindaco, R., Eds, Calderini, Bologna.

Most read articles by the same author(s)