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Sexual Dimorphism in the Growth of Rattlesnake Crotalus ravus (Cope, 1865)

Mixtli Crisóstomo-Pérez, Gissele Islas-López, Candelario Jiménez-Olivares, Verónica Mitsui Saito-Quezada, Isaías Hazarmabeth Salgado-Ugarte

Abstract


Age estimation and growth modelling are important biological characteristics to understand sexual differences in organisms with continuous growth. In this research, to find sexual differences in adult organisms covering a wide size range, we evaluated sexual dimorphism by comparing individual growth curves for each sex of the rattlesnake Crotalus ravus. For snakes age estimation, we employed skeletochronology techniques on the snakes’ midbody ribs and fitted Logistic, Gompertz and von Bertalanffy growth functions to the resulting age-size data and estimated longevity per sex. We found von Bertalanffy was the best model and the growth curves showed significant differences between sexes (Hotelling’s T2), with males growing faster and attaining longer sizes than females; at the same age males are longer than females but females have greater longevity. This dimorphism can be attributed to reproduction costs.

Keywords


age; Viperidae; von Bertalanffy; skeletochronology

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References


Bauwens D. and Thoen C. (1981), «Escape tactics and vulnerability to predation associated with reproduction in the lizard Lacerta vivipara», J. Anim. Ecol., 50(3), 733 – 743.

Bernard D. R. (1981), «Multivariate analysis as a means of comparing growth in fish», Can. J. Fish. Aquat. Sci., 38(2), 233 – 236.

Beverton R. J. H. and Holt S. J. (1957), «On the dynamics exploited fish populations», Fish. Invest. Minst. Agric. Fish. Food. (G. B.) Ser. II. Sea fish, 19.

Bonnet X. S. L., Shine R., Naulleau G., and Vacher-Vallas M. (1998), «Sexual dimorphism in snakes: different reproductive roles favour different body plans», Proc. R. Soc. Lond. B. Biol. Sci., 265(1392), 179 – 183.

Blouin-Demers G., Prior, K. A., and Weatherhead P. J. (2002), «Comparative demography of black rat snakes (Elaphe obsoleta) in Ontario and Maryland», J. Zool. Lond., 256(2002), 1 – 10.

Brito J. C. and Rebelo R. (2003), «Differential growth and mortality affect sexual size dimorphism in Vipera latastei», Copeia, 4(2003), 865 – 871.

Campbell J. A. and Lamar W. W. (1989), The Venomous Reptiles of Latin America, Cornell Univ. Press, Ithaca, NY.

Campbell J. A. and Lamar W. W. (2004), The Venomous Reptiles of the Western Hemisphere. Vol. II, Cornell Univ. Press, Ithaca, NY.

Castanet J. (1994), «Age estimation and longevity in reptiles», Gerontology, 40(2-4), 174 – 192.

Chen C. H. and Fassois S. D. (1992), «Maximum likelihood identification of stochastic Weiner – Hammerstein-type non-linear systems», Mech. Syst. Signal Process, 6(2), 135 – 153.

Cooper W. E. Jr., Vitt L. J., Hedges R., and Huey R. (1990), «Locomotor impairment and defence in gravid lizards (Eumeces laticeps): behavioural shift in activity may offset costs of reproduction in an active forager», Behav. Ecol. Sociobiol., 27(3), 153 – 157.

Cope E. D. (1865), «Third contribution to the herpetology of tropical America», Proc. Acad. Nat. Sci. Philadelphia, 17(4), 185 – 198.

Cox R. M., Butler M. A., and John-Alder H. B. (2007), «The evolution of sexual size dimorphism in reptiles» in: D. J. Fairbairn, T. Szekely, and W. U. Blanckenhorn (eds.), Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism, Oxford Univ. Press, Oxford, pp. 38 – 49.

Cox R. M., Skelly S. L., and John-Alder H. B. (2003), «A comparative test of adaptive hypotheses for sexual size dimorphism in lizards», Evolution, 57(7), 1653 – 1669.

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

Dick D. C. and Mebert K. (2017), «Between housing and deep forest: long-term population biology and dispersal of suburban Smooth snakes (Coronella austriaca)», Zool. Anz., 270(2017), 98 – 106.

Duvall D. and Beaupre S. J. (1998)», Sexual strategy and size dimorphism in rattlesnakes: integrating proximate and ultimate causation», Am. Zool., 38(1998), 152 – 165.

Ford E. (1933), «An account of the herring investigations conducted at Plymouth during the years from 1924 – 1933», J. Mar. Biol. Assoc., 19(1), 305 – 384.

Gibbons J. W. (1972), «Reproduction, growth, and sexual dimorphism in the canebrake rattlesnake (Crotalus horridus atricaudatus)», Copeia, 2(1972), 222 – 226.

Gómez-Márquez J. L., Cervantes-Sandoval A., Salgado-Ugarte I. H., Peña-Mendoza B., Alejo-Plata Ma. del C., Guzmán-Santiago J. L., Mendoza-Vallejo E., and Machuca-Rodríguez C. (2016), Temas Selectos de Biología Pesquera, DGAPA and FES Zaragoza, UNAM, México

Griebeler E. M., Klein N., and Sander P. M. (2013), «Aging, maturation and growth of sauropodomorph dinosaurs as deduced from growth curves using long bone histological data: an assessment of methodological constraints and solutions», PLOS One, 8(6), e67012.

Gulland J. A. (1983), Fish Stock Assessment. A Manual of Basic Methods, Wiley Series, Chichester.

García-Grajales J., Buenrostro-Silva A., and Charruau P. (2012), «Growth and age of juvenile American crocodiles (Crocodylus acutus) in La Ventanilla estuary, Oaxaca, Mexico», Herpetol. Conserv. Biol., 7(3), 330 – 338.

Guarino F. M., Di Maio A., and Caputo V. (2004), «Age estimation by phalangeal skeletochronology of Caretta caretta from the Mediterranean Sea», Ital. J. Zool., 71(S2), 175 – 179.

Guarino F. M., Di Gia I., and Sindaco R. (2010), «Age and growth of the sand lizards. (Lacerta agilis) from a high Alpine population of north-western Italy», Acta Herpetol., 5(1), 23 – 29.

James C. D. (1991), «Growth rates and ages at maturity of sympatric scincid lizards (Ctenotus) in Central Australia», J. Herpetol., 25(3), 284 – 295.

Jenkins C. L., Peterson C. R., Doering S. C., and Cobb V. A. (2009), «Microgeographic variation in reproductive characteristics among western rattlesnake (Crotalus oreganus) populations», Copeia, 4(2009), 774 – 780.

Karkach A. S. (2006), «Trajectories and models of individual growth», DemRes, 15(12), 347 – 400.

Kimura D. K. (1980), «Likelihood methods for the von Bertalanffy growth curve» Fishery Bull., 77(4), 765 – 776.

King R. B. (1989), «Sexual dimorphism in snake tail length: sexual selection, natural selection, or morphological constraint?» Biol. J. Linn. Soc., 38(2), 133 – 154.

Kirkwood P. (1983), «Estimation of von Bertalanffy growth curve parameters using both length increment and age-length data», Can. J. Fish. Aquat. Sci., 40(9), 1405 – 1411.

Madsen T. and Shine R. (1993), «Costs of reproduction in a population of European adders», Oecologia, 94(4), 488 – 495.

Madsen T. and Shine R. (1994), «Cost of reproduction influence the evolution of sexual size dimorphism in snakes», Evolution, 48(4), 1389 – 1397.

McCreary B., Pearl C. A., and Adams M. J. (2008), A Protocol for Aging Anurans Using Skeletochronology, U.S. Geological Survey Open-File Report, 2008-1209.

Ogle D. H. (2015), Introductory Fisheries Analyses with R, CRC Press, Boca Raton, FL.

Qualls C. P. and Shine R. (1998), «Costs of reproduction in conspecific oviparous and viviparous lizards, Lerista bougainvillii», Oikos, 82(3), 539 – 551.

Ralls K. and Mesnick S. (2009), «Sexual Dimorphism», in: W. F. Perrin, B. Wuersig, and J. G. M. Thewissen (eds.), Encyclopedia of Marine Mammals. Second Edition, Acad. Press, Amsterdam – Boston, pp. 1005 – 1011.

Ramirez M. D., Popovska T., and Babcock E. A. (2021), «Global synthesis of sea turtle von Bertalanffy growth parameters through Bayesian hierarchical modelling», Mar. Ecol. Prog. Ser., 657(2021), 191 – 207.

R Core Team (2020), R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org.

Ricker W. E. (1968), Methods for the Assessment of Fish Production in Freshwaters. I. P. B. Handbook 3, Blackwell Scientific Publications, Oxford.

Rivas J. A., and Burghardt G. M. (2001), «Understanding sexual size dimorphism in snakes: wearing the snakeґs shoes», Anim. Behav., 62(3), F1 – F6.

Roff D. A. (2006), Introduction to Computer-Intensive Methods of Data Analysis in Biology, Cambridge Univ. Press, New York, NY.

Salgado-Ugarte I. H. and Saito-Quezada V. M. (2020), Métodos cuantitativos computarizados para biología pesquera, DGAPA and FES-Zaragoza, UNAM, México

Salgado-Ugarte I. H., Gómez-Márquez J. L., and Peña-Mendoza B. (2005), Métodos actualizados para análisis de datos biológico-pesqueros, DGAPA and FES-Zaragoza, UNAM. México.

Schaefer W. F. (1934), «Diagnosis of Sex in Snakes», Copeia, 4(1934), 181.

Schneider C. A., Rasband W. S., and Eliceiri K. W. (2012), «NIH Image to ImageJ: 25 years of image analysis», Nat. Methods, 9(2012), 671 – 675.

Shine R. (1978), «Sexual size dimorphism and male combat in snakes», Oecologia, 33(3), 269 – 278.

Shine R. (1980), «’Cost’ of reproductions in reptiles», Oecologica, 46(1), 92 – 100.

Shine R. (1988), «The evolution of large body size in females: a critique of Darwin’s ‘fecundity advantage’ model», Am. Naturalist, 131(1), 124 – 131.

Shine R. (1994), «Sexual size dimorphism in snakes revisited», Copeia, 1(1994), 326 – 346.

Shine R. and Charnov E. L. (1992), «Patterns of survival, growth, and maturation in snakes and lizards», Am. Naturalist, 139(6), 1257 – 1269.

Sinervo B., Hedges R., and Adolph S. C. (1991), «Decreased sprint speed as a cost of reproduction in the lizard Sceloporus occidentalis: variation among populations», J. Exp. Biol., 155(1), 323 – 336.

Smirina E. M. (1985), «Some results of the studies of growth in Anura» in: Zbyněk Roček (ed.), Studies in Herpetology. Proc. of the European Herpetological Meeting. 3rd Ordinary General Meeting of the Soc. Eur. Herpetol., Charles University, Prague, pp. 263 – 266.

StataCorp (2016), Stata Statistical Software: Release 16, StataCorp LLC, College Station, TX.

Tjørve K. M. C. and Tjørve E. (2017), «The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family», PLoS One; 12(6), e0178691.

Tucker A. D., Limpus C. J., McDonald K. R., and McCallum H. I. (2007), «Growth dynamics of freshwater crocodiles (Crocodylus johnstoni) in the Lynd River», Aust. J. Zool., 54(6), 409 – 415.

Uribe-Peña Z., Ramírez-Bautista A., and Casas-Andreu G. (1999), Anfibios y reptiles de las serranías del Distrito Federal, México, Cuadernos del Instituto de Biología UNAM México.

van Devender R. W. (1978), «Growth ecology of a Tropical lizard, Basiliscus basiliscus», Ecology, 59(5), 1031 – 1038.

von Bertalanffy L. (1938), «A quantitative theory of organic growth (inquires on growth laws. II)», Human Biol., 10(2), 181 – 213.

Vrieze S. I. (2012), «Model selection and psychological theory: a discussion of the differences between the Akaike information criterion (AIC) and the Bayesian information criterion. (BIC)», Psychol. Methods, 17(2), 228 – 243.

Walford L. A. (1946), «A new graphic method of describing the growth of animals», Biol. Bull. Rev., 90(2), 141 – 147.

Waye H. L. and Gregory P. T. (1998), «Determining the age of garter snakes (Thamnophis spp.) by means of skeletochronology», Can. J. Zool., 76(2), 288 – 294.




DOI: https://doi.org/10.30906/1026-2296-2026-33-1-33-38

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