Sexual dimorphism and allometry in the head and body size of two viperid snakes (genus Vipera)

Bartosz Borczyk; Przemysław Puszkiewicz; Stanisław Bury

doi:10.26496/bjz.2024.117

Authors

Bartosz Borczyk Department of Evolutionary Biology and Conservation of Vertebrates, University of Wrocław, Poland
Przemysław Puszkiewicz Department of Evolutionary Biology and Conservation of Vertebrates, University of Wrocław, Poland
Stanisław Bury Department of Comparative Anatomy, Institute of Zoology and Biomedical Research, Jagiellonian University Gronostajowa 9, 30-387 Cracow, Poland

DOI:

https://doi.org/10.26496/bjz.2024.117

Keywords:

allometry, head size, head shape, morphology, sexual dimorphism

Abstract

Sexual dimorphism in the size and shape of the body and head is the result of manifold selective pressures acting on organisms. In snakes, sexual size dimorphism is common and has been well-studied. However, intersexual differences in relative head size and shape have attracted far less attention. Similarly, the allometric properties of head shape and size in snakes are poorly known. Here, we analyse sexual dimorphism in two viperid species: European adder Vipera berus (Linnaeus, 1758) and Steppe viper Vipera renardi (Christoph, 1861). We measured body length, tail length and several head characteristics: head length, head width, head height, pileus length, interorbital distance and internarial distance. Our findings were that males and females of both species did not differ in body length (SVL), but that males tended to have significantly longer tails; there were also significant differences in head characteristics – males tended to have higher heads, and larger internarial and interorbital distances. The head dimensions displayed negative allometry when compared against SVL but when scaled against head length, dimensions like head height and head width exhibited positive allometry. We argue that these differences may be related to sexual selection and that the wider heads may also serve as antipredatory signal.

References

Andjelković M., Tomović L. & Ivanović A. (2016). Variation in skull size and shape of two species (Natrix natrix and Natrix tessellata). Zoomorphology 135: 243–253. https://doi.org/10.1007/s00435-016-0301-3

Andrén C. (1982). The role of the vomeronasal organs in the reproductive behavior of the adder Vipera berus. Copeia 1982: 148–157.

Arnold S. J. (1993). Foraging theory ad prey-size—predator-size relations in snakes. In: Seigel R.A. & Collins J.T. (eds) Snakes. Ecology and Behavior: 87–115. McGraw-Hill, New York.

Bohonak A.J. & van der Linde K. (2004). RMA: Software for Reduced Major Axis regression, Java version. Available from http://www.kimvdlinde.com/professional/rma.html [accessed 5 February 2024].

Bonnet X., Shine R., Naulleau G. & Vacher-Vallas M. (1998). Sexual dimorphism in snakes: different reproductive roles favour different body plans. Proceedings of the Royal Society of London B 265: 179–183. https://doi.org/10.1098/rspb.1998.0280

Bonnet X., Naulleau G., Shine R. & Lourdais O. (2000). Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis. Oikos 89: 509–518. https://doi.org/10.1034/j.1600-0706.2000.890310.x

Borczyk B. (2015). Allometry of head size and shape dimorphism in the grass snake (Natrix natrix L.). Turkish Journal of Zoology 39: 340–343. https://doi.org/10.3906/zoo-1402-9

Borczyk B. (2023). Sexual dimorphism in skull size and shape of Laticauda colubrina (Serpentes: Elapidae). PeerJ 11: e16266. https://doi.org/10.7717/peerj.16266

Borczyk B., Kusznierz J., Paśko Ł. & Turniak E. (2014). Scaling of the sexual size and shape skull dimorphism in the sand lizard (Lacerta agilis L.). Vertebrate Zoology 64: 221–227.

Borczyk B., Paśko Ł., Kusznierz J. & Bury S. (2021). Sexual dimorphism and skull size and shape in the highly specialized snake species, Aipysurus eydouxii (Elapidae: Hydrophiinae) PeerJ 9: e11311 https://doi.org/10.7717/peerj.11311

Bury S. (2021). Sex-specific growth is mirrored in feeding rate but not moulting frequency in a sexually dimorphic snake. Science of Nature 108: 6. https://doi.org/10.1007/s00114-020-01712-y

Bury S. & Zając B. (2020). The loss of sexual size dimorphism in urban populations of a widespread reptile, the European grass snake Natrix natrix. Current Zoology 66: 217–218. https://doi.org/10.1093/cz/zoz034

Bury S., Cierniak A., Jakóbik J., Sadowska E.T., Cichoń M. & Bauchinger U. (2020). Cellular turnover: a potential metabolic rate-driven mechanism to mitigate accumulation of DNA damage. Physiological Biochemical Zoology 93: 90–96. https://doi.org/10.1086/707506

Camilleri C. & Shine R. (1990). Sexual dimorphism and dietary divergence: differences in trophic morphology between male and female snakes. Copeia 1990: 649–658.

Cliburn J.W. (1976). Observations of ecdysis in the black pine snake, Pituophis melanoleucus lodingi (Reptilia, Serpentes, Colubridae). Journal of Herpetology 10: 299–301. https://doi.org/10.2307/1563066

Darwin C. (1871). The Descent of Man, and Selection in Relation to Sex. J. Murray, London.

Faiman R., Abergil D., Babocsay G., Razzetti E., Seligmann H. & Werner Y. (2018). A review of sexual dimorphism of eye size in Colubroidea snakes. Vertebrate Zoology 68: 91–108.

Frosman A. (1991a). Adaptive variation in head size in Vipera berus L. populations. Biological Journal of the Linnean Society 43: 281–296. https://doi.org/10.1111/j.1095-8312.1991.tb00600.x

Frosman A. (1991b). Variation in sexual size dimorphism and maximum body size among adder populations: effects of prey size. Journal of Animal Ecology 60: 253–267.

Gentili A., Scali S. & Sacchi R. (2006). Morphometric differences between extant and extinct Italian populations of the adder, Vipera berus (Linnaeus, 1758). Acta Herpetologica 1: 65–71. https://doi.org/10.13128/Acta_Herpetol-1251

Gibson A.R. & Falls B.B. (1979). Thermal biology of the common garter snake Thamnophis sirtalis. Oecologia 43: 79–97. https://doi.org/10.1007/BF00346675

Greene H.W. (1997). Snakes. Evolution of Mystery in Nature. University of California Press. Berkeley, Los Angeles, London.

Hampton P.M. & Moon B.R. 2013. Gape size, its morphological basis, and the validity of gape indices in Western Diamond-backed Rattlesnakes (Crotalus atrox). Journal of Morphology 274: 194–202. https://doi.org/10.1002/jmor.20087

Hedges B.S. (2008). At the lower size limit in snakes: two new species of threadsnakes (Squamata: Leptotyphlopidae: Leptotyphlops) from the Lesser Antilles. Zootaxa 1841: 1–30. https://doi.org/10.11646/zootaxa.1841.1.1

Henao-Duque A.M. & Ceballos C.P. (2013). Sex-related head size and shape dimorphism in Mapaná snakes (Bothrops asper) kept in captivity. Revista Colombiana de Ciencias Pecuarias 26: 201–210.

Iraeta P., Monasterio C., Salvador A. & Díaz J.A. (2006). Mediterranean hatchling lizards grow faster at higher altitude: a reciprocal transplant experiment. Functional Ecology 20: 865–872. https://doi.org/10.1111/j.1365-2435.2006.01162.x

King R.B. (1989). Sexual dimorphism in snake tail length: sexual selection, or morphological constraint? Biological Journal of the Linnean Society 38: 133–154. https://doi.org/10.1111/j.1095-8312.1989.tb01570.x

King R.B., Bittner T.D., Queral-Regil A. & Cline J.H. (1999). Sexual dimorphism in neonate and adult snakes. Journal of Zoology (London) 247: 19–28. https://doi.org/10.1111/j.1469-7998.1999.tb00189.x

Kozłowski J. (1992). Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends in Ecology and Evolution 7: 15–19. https://doi.org/10.1016/0169-5347(92)90192-E

Kratochvil L., Fokt M., Rehak I. & Frynta D. (2003). Misinterpretation of character scaling: a tale of sexual dimorphism in body shape of common lizards. Canadian Journal of Zoology 81: 1112–1117. https://doi.org/10.1139/z03-078

Loebens L., Hendges C.D., Almeida-Santos S.M. & Cechin S.Z. (2019). Morphological variation and sexual dimorphism in two sympatric dipsadine snakes from Southern Brazil. Zoologischer Anzeiger, 280: 42–51. https://doi.org/10.1016/j.jcz.2019.03.004

López M.S., Manzano A.S. & Prieto Y.A. (2013). Ontogenetic variation in head morphology and diet in two sympatric snakes (Viperidae) from Northeastern Argentina. Journal of Herpetology 47: 406–412. https://doi.org/10.1670/12-007

Madsen T. (1988). Reproductive success, mortality and sexual size dimorphism in the adder, Vipera berus. Ecography 11: 77–80. https://doi.org/10.1111/j.1600-0587.1988.tb00783.x

Madsen T. & Shine R. (1993). Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes. American Naturalist 141: 167–171.

Madsen T. & Shine R. (2002). Short and chubby or long and slim? Food intake, growth and body condition in free-ranging pythons. Australian Ecology 27: 672–680. https://doi.org/10.1046/j.1442-9993.2002.01228.x

Murta-Fonseca R.A., Machado A., Lopes R.T. & Fernandes D.S. (2019). Sexual dimorphism in Xenodon neuwiedii skull revealed by geometric morphometrics (Serpentes; Dipsadidae). Amphibia-Reptilia 40: 461–474. https://doi.org/10.1163/15685381-20191147

Nilson G. & Andren C. (2001). The Meadow and Steppe vipers of Europe and Asia – the Vipera (Acridophaga) ursinii complex. Acta Zoologica Academiae Scientiarum Hungaricae 47: 87–267.

Niskansen M. & Mappes J. (2005). Significance of the dorsal zigzag pattern of Vipera latastei gaditana against avian predators. Journal of Animal Ecology 74: 1091–1101. https://doi.org/10.1111/j.1365-2656.2005.01008.x

Pearson D., Shine R. & Williams A. (2002). Geographic variation in sexual size dimorphism within a single snake species (Morelia spilota, Pythonidae). Oecologia 131: 418–426. https://doi.org/10.1007/s00442-002-0917-5

Saint-Girons H. (1957). Croissance et fécondité de Vipera aspis. Vie et Milieu 8: 265–286.

Scali S. & Gentili A. (1998). Morphometric analysis and sexual dimorphism of extinct adders (Vipera berus) of the Po Plaine (Northern Italy). In: Miaud C. & Guyetant R. (eds) Current Studies in Herpetology. Proceedings of the 9th Ordinary General Meeting of the SEH: 391–396. Societas Europaea Herpetologica, Le Bourget du Lac.

Seigel R.A. & Ford N.B. (1987). Reproductive Ecology. In: Seigel R.A., Collins J.T. & Novak S.S. (eds) Snakes: Ecology and Evolutionary Biology: 210–252. McGraw-Hill Publishing Company, New York.

Shetty S. & Shine R. (2002). Sexual divergence in diets and morphology in Fijian sea snakes Laticauda colubrina (Laticaudinae). Australian Ecology 27: 77–84. https://doi.org/10.1046/j.1442-9993.2002.01161.x

Shine R. (1978). Sexual dimorphism and male combat in snakes. Oecologia 33: 269–277. https://doi.org/10.1007/BF00348113

Shine R. (1991). Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. American Naturalist 138: 103–122. https://doi.org/10.1086/285207

Shine R. (1993). Sexual dimorphism. In: Seigel R. & Collins J. (eds) Snakes: Ecology and Behavior: 49–86. McGraw-Hill, New York.

Shine R. (1994). Sexual size dimorphism in snakes revisited. Copeia 1994: 326–346.

Shine R. (2005). All at sea: aquatic life modifies mate-recognition modalities in sea snakes (Emydocephalus annulatus, Hydrophiidae). Behavioral Ecology and Sociobiology 57: 591–598. https://doi.org/10.1007/s00265-004-0897-z

Shine R., Olsson M., Moore I.T., LeMaster M.P. & Mason R.T. (1999). Why do male snakes have longer tails than females? Proceedings of the Royal Society London B 266: 2147–2151. https://doi.org/10.1098/rspb.1999.0901

Smith C.F., Schwenk K., Earley R.L. & Schuett G.W. (2008). Sexual size dimorphism of the tongue in a North American pitviper. Journal of Zoology (London) 274: 367–374. https://doi.org/10.1111/j.1469-7998.2007.00396.x

Sokal R.R. & Rohlf F.J. (1995). Biometry. The Principles and Practice of Statistics in Biological Research. 3rd Edition. W.H. Freeman and Co., New York

Steward J. (1971). The Snakes of Europe. Newton Abbot, London.

Strugariu A., Zamfirescu S.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? Animal Biology 61: 457–468. https://doi.org/10.1163/157075511X597601

Strugariu A., Zamfirescu S.R., Gherghel I., Sahlean T.C., Moraru V. & Zamfirescu O. (2011). A preliminary study on population characteristics and ecology of the critically endangered meadow viper Vipera ursinii in the Romanian Danube Delta. Biologia 66: 175–180. https://doi.org/10.2478/s11756-010-0146-z

Tamagnini D., Stephenson J., Brown R.P. & Meloro C. (2018). Geometric morphometric analyses of sexual dimorphism and allometry in two sympatric snakes: Natrix helvetica (Natricidae) and Vipera berus (Viperidae). Zoology 129: 25–34. https://doi.org/10.1016/j.zool.2018.05.008

Tomović L.M., Radojicic J., Dzukic G. & Kalezic M.L. (2002). Sexual dimorphism of the sand viper (Vipera ammodytes L.) from the central part of Balkan Peninsula. Russian Journal of Herpetology 9: 69–76.

Tomović L.M., Crnobrnija-Islanović J.M., Ajtić R.D., Aleksić I.D. & Djordević S.Z. (2009). When do meadow vipers (Vipera ursinii) become sexually dimorphic? - ontogenetic patterns of sexual size dimorphism. Journal of the Zoological Systematics and Evolutionary Research 48: 279–282. https://doi.org/10.1111/j.1439-0469.2009.00556.x

Valkonen J.K., Nokelainen O. & Mappes J. (2011). Antipredatory function of head shape for vipers and their mimics. PLoS ONE 6(7): e22272. https://doi.org/10.1371/journal.pone.0022272

Vincent S.E., Herrel A. & Irschick D.J. (2004). Sexual dimorphism in head shape and diet in the cottonmouth snake (Agkistrodon piscivorous). Journal of Zoology (London) 264: 53–59. https://doi.org/10.1017/S0952836904005503

Vincent S.E., Moon B.R., Herrel A. & Kley N.J. (2007). Are ontogenetic shifts in diet linked to shifts in feeding mechanics? Scaling of the feeding apparatus in the banded watersnake Nerodia fasciata. Journal of Experimental Biology 210: 2057–2069. https://doi.org/10.1242/jeb.02779