Sexual size dimorphism (SSD), commonly observed in snakes, may arise from a different growth rate between the sexes. This indicates a sex-specific resource intake that is in fact observable in free-living snakes. It is not so well known whether the sexes can express differential feeding rates under conditions unconstrained by spatial accessibility, competition, etc. Here, I studied sex-specific variation in growth, its correlate—moulting frequency, and feeding rate in a captive group of sexually dimorphic banded water snakes (Nerodia fasciata) with access to food unconstrained by predation, competition or space. I showed that the sexes did indeed differ in relative mass growth in that females grew faster than males (p = 0.02), but such differences were not apparent in the moulting rate (p = 0.19). Such differential growth was mirrored in the sex-specific feeding rate, with females ingesting a larger number of meals than males (p = 0.004). Such variation in feeding rate may be governed by an individual’s energy expenditure and can be interpreted as a behavioural tendency that contributes to SSD development, independently of other behavioural characteristics. Sex-specific resource demands may drive the differential effects of increasing resource scarcity on both sexes.
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Abrams PA (1991) Life history and the relationship between food availability and foraging effort. Ecology 72:1242–1252. https://doi.org/10.2307/1941098
Adolph SC, Roughgarden J (1983) Foraging by passerine birds and Anolis lizards on St. Eustatius (Neth. Antilles): implications for interclass competition, and predation. Oecologia 56:313–317. https://doi.org/10.1007/BF00379705
Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509. https://doi.org/10.1093/icb/44.6.498
Autumn K, De Nardo DF (1995) Behavioral thermoregulation increases growth rate in a nocturnal lizard. J Herpetol 29:157–162. https://doi.org/10.2307/1564552
Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368. https://doi.org/10.1016/j.tree.2008.04.003
Blanckenhorn WU (2005) Behavioral causes and consequences of sexual size dimorphism. Ethology 111:977–1016. https://doi.org/10.1111/j.1439-0310.2005.01147.x
Blouin-Demers G, Prior KA, Weatherhead PJ (2002) Comparative demography of black rat snakes (Elaphe obsoleta) in Ontario and Maryland. J Zool 256(1):1–10. https://doi.org/10.1017/S0952836902000018
Brodie ED III, Brodie ED Jr (1990) Tetrodotoxin resistance in garter snakes: an evolutionary response of predators to dangerous prey. Evolution 44(3):651–659. https://doi.org/10.1111/j.1558-5646.1990.tb05945.x
Brown GP, Madsen TR, Shine R (2017) Resource availability and sexual size dimorphism: differential effects of prey abundance on the growth rates of tropical snakes. Funct Ecol 31(8):1592–1599
Bulté G, Blouin-Demers G (2009) Does sexual bimaturation affect the cost of growth and the operational sex ratio in an extremely size-dimorphic reptile? Ecoscience 16:175–182. https://doi.org/10.2980/16-2-3243
Burbrink FT, Futterman I (2019) Female-biased gape and body-size dimorphism in the New World watersnakes (tribe: Thamnophiini) oppose predictions from Rensch’s rule. Ecol Evol 9(17):9624–9633. https://doi.org/10.1002/ece3.5492
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(2):217–218. https://doi.org/10.1093/cz/zoz034
Bury S, Cichoń M, Bauchinger U, Sadowska ET (2018) High oxidative stress despite low energy metabolism and vice versa: insights through temperature acclimation in an ectotherm. J Therm Biol 78:36–41. https://doi.org/10.1016/j.jtherbio.2018.08.003
Cássia Lamonica R, Abrahão-Charles H, de Castro Loguercio MF, Rocha-Barbosa (2007) Growth, shedding and food intake in captive Eunectes murinus (Linnaeus, 1758) (Serpentes: Boidae). Int J Morphol 25(1):103–108
Cliburn JW (1976) Observations of ecdysis in the black pine snake, Pituophis melanoleucus lodingi (Reptilia, Serpentes, Colubridae). J Herpetol 10:299–301. https://doi.org/10.2307/1563066
Cox RM, Skelly SL, John-Alder HB (2003) A comparative test of adaptive hypotheses for sexual size dimorphism in lizards. Evolution 57:1653–1669. https://doi.org/10.1111/j.0014-3820.2003.tb00371.x
Cox RM, Butler MA, John-Alder HB (2007) The evolution of sexual size dimorphism in reptiles. In: Székely T, Lislevand T, Figuerola J, Fairbairn D, Blanckenhorn W (eds) Sex, size and gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, New York, pp 38–49. https://doi.org/10.1093/acprof:oso/9780199208784.003.0005
Cox RM, Barrett MM, John-Alder HB (2008) Effects of food restriction on growth, energy allocation, and sexual size dimorphism in Yarrow’s spiny lizard, Sceloporus jarrovii. Can J Zool 86(4):268–276. https://doi.org/10.1139/Z08-002
Cox RM, Cox CL, McGlothlin JW, Card DC, Andrew AL, Castoe TA (2017) Hormonally mediated increases in sex-biased gene expression accompany the breakdown of between-sex genetic correlations in a sexually dimorphic lizard. Am Nat 189:315–332. https://doi.org/10.1086/690105
Dmi'el R (1967) Studies on reproduction, growth, and feeding in the snake Spalerosophis cliffordi (Colubridae). Copeia 1967:332–346
Eertmans A, Victoir A, Vansant G, Van den Bergh O (2005) Food-related personality traits, food choice motives and food intake: mediator and moderator relationships. Food Qual Prefer 16:714–726. https://doi.org/10.1016/j.foodqual.2005.04.007
Fry B, Arnold C (1982) Rapid 13 C/12 C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 54(2):200–204
Gifford ME, Clay TA, Careau V (2014) Individual (co) variation in standard metabolic rate, feeding rate, and exploratory behavior in wild-caught semiaquatic salamanders. Physiol Biochem Zool 87:384–396. https://doi.org/10.1086/675974
Gregory PT, Prelypchan CJ (1994) Analysis of variance of first-year growth in captive garter snakes (Thamnophis elegans) by family and sex. J Zool 232(2):313–322
Huey RB, Kingsolver JG (2019) Climate warming, resource availability, and the metabolic meltdown of ectotherms. Am Nat 194(6):E140–E150. https://doi.org/10.1086/705679
Iraeta P, Monasterio C, Salvador A, Díaz JA (2006) Mediterranean hatchling lizards grow faster at higher altitude: a reciprocal transplant experiment. Funct Ecol 20(5):865–872. https://doi.org/10.1111/j.1365-2435.2006.01162.x
John-Alder HB, Cox RM, Taylor EN (2007) Proximate developmental mediators of sexual dimorphism in size: case studies from squamate reptiles. Integr Comp Biol 47:258–271. https://doi.org/10.1093/icb/icm010
Kozłowski J (1992) Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends Ecol Evol 7:15–19. https://doi.org/10.1016/0169-5347(92)90192-E
Lagarde F, Bonnet X, Henen BT, Corbin J, Nagy KA, Naulleau G (2001) Sexual size dimorphism in steppe tortoises (Testudo horsfieldii): growth, maturity, and individual variation. Can J Zool 79:1433–1441. https://doi.org/10.1139/cjz-79-8-1433
Lillywhite HB, Sheehy CM III (2016) Synchrony of ecdysis in snakes. Herpetol Conserv Biol 11(2):286–292
Lourdais O, Guillon M, DeNardo D, Blouin-Demers G (2013) Cold climate specialisation: adaptive covariation between metabolic rate and thermoregulation in pregnant vipers. Physiol Behav 119:149–155. https://doi.org/10.1016/j.physbeh.2013.05.041
Lyman-Henley LP, Burghardt GM (1995) Diet, litter, and sex effects on chemical prey preference, growth, and site selection in two sympatric species of Thamnophis. Herpetol Monogr 9:140–160
Maderson PFA (1985) Some developmental problems of the reptilian integument. In: Gans C, Billett F, Maderson PFA (eds) Biology of the Reptilia, vol 14B. John Wiley & Sons, New York, pp 525–598
Madsen T (1983) Growth rates, maturation and sexual size dimorphism in a population of grass snakes, Natrix natrix, in southern Sweden. Oikos 40:277–282. https://doi.org/10.2307/3544592
Madsen T, Shine R (1993a) Costs of reproduction in a population of European adders. Oecologia 94(4):488–495. https://doi.org/10.1007/BF00566963
Madsen T, Shine R (1993b) Phenotypic plasticity in body sizes and sexual size dimorphism in European grass snakes. Evolution 47(1):321–325. https://doi.org/10.1111/j.1558-5646.1993.tb01222.x
Madsen T, Shine R (2002) Short and chubby or long and slim? Food intake, growth and body condition in free-ranging pythons. Austral Ecol 27:672–680. https://doi.org/10.1046/j.1442-9993.2002.01228.x
Maillet Z, Halliday WD, Blouin-Demers G (2015) Exploratory and defensive behaviours change with sex and body size in eastern garter snakes (Thamnophis sirtalis). J Ethol 33(1):47–54. https://doi.org/10.1007/s10164-014-0416-2
Michelangeli M, Chapple DG, Wong BB (2016) Are behavioural syndromes sex specific? Personality in a widespread lizard species. Behav Ecol Sociobiol 70(11):1911–1919. https://doi.org/10.1007/s00265-016-2197-9
Mushinsky HR, Hebrard JJ, Walley MG (1980) The role of temperature on the behavioral and ecological associations of sympatric water snakes. Copeia 4:744–754. https://doi.org/10.2307/1444453
Nagy KA (1987) Field metabolic rate and food requirement scaling in mammals and birds. Ecol Monogr 57:111–128. https://doi.org/10.2307/1942620
Pollock NB, Feigin S, Drazenovic M, John-Alder HB (2017) Sex hormones and the development of sexual size dimorphism: 5α-dihydrotestosterone inhibits growth in a female-larger lizard (Sceloporus undulatus). J Exp Biol 220:4068–4077. https://doi.org/10.1242/jeb.166553
Rivas JA, Munoz MC, Burghardt GM, Thorbjarnarson JB (2007) Sexual size dimorphism and the mating system of the green anaconda (Eunectes murinus). In: Henderson RW, Powell R (ed) Biology of the Boas and Pythons. Eagle Mountain, Utah: Eagle Mountain Publishing, LC, pp: 312–325
Schudder RM, Burghardt GM (1985) The role of feeding regimens in the growth of neonate broad-banded water snakes, Nerodia fasciata confluens, and possible effects on reproduction. Dev Psychobiol 18:203–214
Schuett GW, Hardy DL, Earley RL, Greene HW (2005) Does prey size induce head skeleton phenotypic plasticity during early ontogeny in the snake Boa constrictor? J Zool 267(4):363–369. https://doi.org/10.1017/S0952836905007624
Sears MW (2005) Resting metabolic expenditure as a potential source of variation in growth rates of the sagebrush lizard. Comp Biochem Physiol A 140:171–177. https://doi.org/10.1016/j.cbpb.2004.12.003
Semlitsch RD, Gibbons JW (1982) Body size dimorphism and sexual selection in two species of water snakes. Copeia 4:974–976. https://doi.org/10.2307/1444113
Shine R (1978) Sexual size dimorphism and male combat in snakes. Oecologia 33:269–277. https://doi.org/10.1007/BF00348113
Shine R (1994) Sexual size dimorphism in snakes revisited. Copeia 2:326–346. https://doi.org/10.2307/1446982
Shine R, Harlow PS, Keogh JS (1998) The influence of sex and body size on food habits of a giant tropical snake, Python reticulatus. Funct Ecol 12:248–258. https://doi.org/10.1046/j.1365-2435.1998.00179.x
Stamps JA (1977) The relationship between resource competition, risk, and aggression in a tropical territorial lizard. Ecology 58:349–358. https://doi.org/10.2307/1935609
Stuginski DR, Mendes GF, Sant’Anna SS, Rubio DT, Vieira SEM, Oitaven LPC, Grego KF (2017) Sexual differences in growth rates of juveniles from a litter ofBothrops fonsecai: the role of feeding conversion in a female-biased SSD species. South Am J Herpetol 12(3):193–199
Swartwout MC, Vogrinc P, Baecher JA, Kross C, Willson JD (2020) Prey size and feeding rate do not influence trophic morphology of juvenile water snakes (Nerodia sipedon). Herpetologica 76(1):53–60. https://doi.org/10.1655/Herpetologica-D-18-00007
Taylor EN, Denardo DF (2005) Sexual size dimorphism and growth plasticity in snakes: an experiment on the western diamond-backed rattlesnake (Crotalus atrox). J Exp Zool A 303(7):598–607. https://doi.org/10.1002/jez.a.189
Tomović LM, Crnobrnja-Isailović JM, Ajtić RD, Aleksić ID, Djordjević SZ (2010) When do meadow vipers (Vipera ursinii) become sexually dimorphic?–ontogenetic patterns of sexual size dimorphisms. J Zool Syst Evol Res 48(3):279–282. https://doi.org/10.1111/j.1439-0469.2009.00556.x
Troncoso-Palacios J, Labra A (2012) Is the exploratory behavior of Liolaemus nitidus modulated by sex? Acta Herp 7(1):69–80. https://doi.org/10.13128/Acta_Herpetol-10481
Ward-Fear G, Brown GP, Pearson DJ, West A, Rollins LA, Shine R (2018) The ecological and life history correlates of boldness in free-ranging lizards. Ecosphere 9(3):e02125. https://doi.org/10.1002/ecs2.2125
Webb JK, Brook BW, Shine R (2003) Does foraging mode influence life history traits? A comparative study of growth, maturation and survival of two species of sympatric snakes from South-Eastern Australia. Austral Ecol 28(6):601–610. https://doi.org/10.1111/j.1442-9993.2003.tb00282.x
Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272. https://doi.org/10.1086/285537
Werner YL, Shapira T (2011) A brief review of morphological variation in Natrix tessellata in Israel: between sides, among individuals, between sexes, and among regions. Turk J Zool 35(4):451–466. https://doi.org/10.3906/zoo-1002-54
I would like to thank Oliver Hawlitschek and one anonymous reviewer for their valuable comments on the manuscript. I also thank Peter Senn for providing linguistic corrections to the manuscript.
The study was supported by a grant from National Science Centre in Poland (grant No. UMO-2016/21/N/NZ8/00959 and UMO-2019/32/T/NZ8/00410) and Jagiellonian University (DS/BW UJ INoS 757).
The study was performed in accordance with the relevant legal requirements in Poland.
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Bury, S. Sex-specific growth is mirrored in feeding rate but not moulting frequency in a sexually dimorphic snake. Sci Nat 108, 6 (2021). https://doi.org/10.1007/s00114-020-01712-y
- Sexual dimorphism
- Food intake
- Feeding rate