Sexual dimorphism of tropical green pit viper Trimeresurus (Cryptelytrops) macrops in Northeast Thailand

in Amphibia-Reptilia
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Total body size for arboreal vipers is normally biased toward small males and larger females. We evaluated sexual dimorphism in adult and sub-adult Trimeresurus macrops, a small, arboreal green pit viper commonly found in Southeast Asia, but severely understudied. We evaluated morphological characters of 139 adult T. macrops obtained by active and opportunistic searches at Sakaerat Biosphere Reserve in northeast Thailand, from May 2012 to October 2014. We compared 7 external characters including residual index (Ri) and scaled mass index (SMI) between male and female T. macrops. Body length measurements and mass differed between males and females. Females had greater snout-vent length, body mass and head length and width, while males had greater tail lengths. A postocular stripe was always present on males, but never on females. Male head size was negatively correlated with SMI, which may reveal intersexual competition in T. macrops. Sexually dimorphic characters in T. macrops may have evolved through intraspecific resource partitioning.

Sexual dimorphism of tropical green pit viper Trimeresurus (Cryptelytrops) macrops in Northeast Thailand

in Amphibia-Reptilia

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References

AkaikeH. (1974): A new look at the statistical model identification. IEEE Trans. Automat. Contr. 19: 716-723.

AnderssonM. (1994): Sexual Selection. Princeton University PressPrinceton.

AubretF.BonnetX.ShineR.LourdaisO. (2002): Fat is sexy for females but not males: the influence of body reserves on reproduction in snakes (Vipera aspis). Horm. Behav. 42: 135-147.

BaronJ.P.GalliardJ.F.FerrièreR.TullyT. (2012): Intermittent breeding and the dynamics of resource allocation to reproduction, growth and survival. Funct. Ecol. 27: 173-183.

BonnetX.NaulleauG. (1994): Utilisation d’un indice de condition corporelle (BCI) pour l’étude de la reproduction chez les serpents. C. R. Acad. Sci. Paris 317: 34-41.

BonnetX.NaulleauG.ShineR.LourdaisO. (2000): Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis. Oikos 89: 509-518.

BonnetX.ShineR.NaulleauG.Vacher-VallasM. (1998): Sexual dimorphism in snakes: different reproductive roles favour different body plans. Proc. R. Soc. B 265: 1-5.

BronikowskiA.M. (2000): Experimental evidence for the adaptive evolution of growth rate in the garter snake Thamnophis elegans. Evolution 54: 1760-1767.

BrownD.S.JarmanS.N.SymondsonW.O. (2012): Pyrosequencing of prey DNA in reptile faeces: analysis of earthworm consumption by slow worms. Mol. Ecol. Resour. 12: 259-266.

CoxM.J.HooverM.F.ChanhomeL.ThirakhuptK. (2012): The Snakes of Thailand1st Edition. Sirabutr PrintingBangkok, Thailand.

CoxR.M.BarrettM.M.John-AlderH.B. (2008): Effects of food restriction on growth, energy allocation, and sexual size dimorphism in Yarrow’s Spiny Lizard, Sceloporus jarrovii. Can. J. Zool. 86: 268-276.

CoxR.M.ButlerM.A.John-AlderH.B. (2007): The evolution of sexual size dimorphism in reptiles. In: Sex Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism p.  38-49. FairbairnD.J.BlanckenhornW.U.SzekelyT. Eds Oxford University PressLondon.

CreerS.ChouW.H.MalhotraA.ThorpeR.S. (2002): Offshore insular variation in the diet of the Taiwanese bamboo viper Trimeresurus stejnegeri (Schmidt). Zool. Sci. 19: 907-913.

DasI. (2010): A Field Guide to the Reptiles of South-East Asia. New Holland PublishersLondon.

DudaR.O.HartP.E.StorkD.G. (2001): Pattern Classification2nd Edition. Wiley-Interscience.

DuvallD.BeaupreS.J. (1998): Sexual strategy and size dimorphism in rattlesnakes: integrating proximate and ultimate causation. Am. Zool. 38: 151-164.

FabienA.BonnetX.MaumelatS.BradshawD.SchwanerT. (2004): Diet divergence, jaw size and scale counts in two neighbouring populations of tiger snakes (Notechis scutatus). Amphibia-Reptilia 25: 9-18.

HendryC.R.GuiherT.J.PyronR.A. (2014): Ecological divergence and sexual selection drive sexual size dimorphism in new world pitvipers (Serpentes: Viperidae). J. Evol. Biol. 27: 760-771.

HerrelA.HuygheK.OkovićP.LisičićD.TadićZ. (2011): Fast and furious: effects of body size on strike performance in an arboreal viper Trimeresurus (Cryptelytrops) albolabris. J. Exp. Zool. Part. A. 315: 22-29.

HoustonD.ShineR. (1993): Sexual dimorphism and niche divergence: feeding habits of the Arafura file snake. J. Anim. Ecol.: 737-748.

KingR.B. (2000): Analyzing the relationship between clutch size and female body size in reptiles. J. Herpetol. 34: 148-150.

KingR.B. (2002): Predicted and observed maximum prey size-snake size allometry. Funct. Ecol. 16: 766-772.

KissnerK.J.WeatherheadP.J. (2005): Phenotypic effects on survival of neonatal northern watersnakes Nerodia sipedon. J. Anim. Ecol. 74: 259-265.

KramerE. (1977): Zur Schlangenfauna Nepals. Rev. Suisse. Zool. 84: 721-761.

KrasnovB.R.ShenbrotG.I.KhokhlovaI.S.MouillotD.PoulinR. (2008): Latitudinal gradients in niche breadth: empirical evidence from haematophagous ectoparasites. J. Biogeogr. 35: 592-601.

KuchU.GumprechtA.MelaunC. (2007): A new species of Temple Pitviper (Tropidolaemus Wagler, 1830) from Sulawesi, Indonesia (Squamata: Viperidae: Crotalinae). Zootaxa 1446: 1-20.

LabochaM.K.SchutzH.HayesJ.P. (2014): Which body condition index is best? Oikos 123: 111-119.

LourdaisO.BonnetX.DoughtyP. (2002): Costs of anorexia during pregnancy in a viviparous snake (Vipera aspis). J. Exp. Zool. 292: 487-493.

MadsenT. (1988): Reproductive success, mortality and sexual size dimorphism in the adder, Vipera berus. Ecography 11: 77-80.

MadsenT. (2011): Body condition and head size in snakes. Amphibia-Reptilia 32: 565-567.

MalhotraA.ThorpeR.S.StuartB.L. (2004): A morphometric analysis of Trimeresurus vogeli (David, Vidal and Pauwels, 2001), with new data on diagnostic characteristics, distribution and natural history. Herpetol. J. 14: 65-78.

MalhotraA.ThorpeR.S.MrinaliniStuartB.L. (2011): Two new species of pitviper of the genus Cryptelytrops Cope 1860 (Squamata: Viperidae: Crotalinae) from Southeast Asia. Zootaxa 2757: 1-23.

ManjarrezJ.Contreras-GarduñoJ.JanczurM.K. (2014): Sexual size dimorphism, diet, and reproduction in the Mexican garter snake, Thamnophis eques. Herpetol. Conserv. Biol. 9: 163-169.

MitteroeckerP.BooksteinF. (2011): Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol. Biol. 38: 100-114.

NaulleauG.BonnetX. (1995): Reproductive ecology, body fat reserves and foraging mode in females of two contrasted snake species: Vipera aspis (terrestrial, viviparous) and Elaphe longissima (semi-arboreal, oviparous). Amphibia-Reptilia 16: 37-46.

ParkerW.S.PlummerM.V. (1987): Population ecology. In: Snakes: Ecology and Evolutionary Biology p.  253-301. SeigelR.A.CollinsJ.T.NovakS.S. Eds McGraw-HillNew York.

PearsonD.ShineR.HowR. (2002): Sex-specific niche partitioning and sexual size dimorphism in Australian pythons (Morelia spilota imbricata). Biol. J. Linnean Soc. 77: 113-125.

PearsonD.ShineR.WilliamsA. (2002): Geographic variation in sexual size dimorphism within a single snake species (Morelia spilota, Pythonidae). Oecologia 131: 418-426.

PeigJ.GreenA.J. (2009): New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118: 1883-1891.

PierceA.J.PobprasertK. (2007): A portable system for continuous monitoring of bird nests using digital video recorders. J. Field Ornithol. 78: 322-328.

R Development Core Team (2013): R: a Language and Environment for Statistical Computing. R Foundation for Statistical ComputingVienna, Austria. Available at http://www.R-project.org/.

RencherA.C. (2002): Methods of Multivariate Analysis2nd Edition. Wiley-Interscience.

RivasJ.A.BurghardtG.M. (2001): Understanding sexual size dimorphism in snakes: wearing the snake’s shoes. Anim. Behav. 62: 1-6.

SeigelR.FordN. (1987): Reproductive ecology. In: Snakes: Ecology and Evolutionary Biology p.  210-252. SeigelR.A.CollinsJ.T.NovakS. Eds MacMillanNew York.

SetserK. (2007): Use of anesthesia increases precision of snake measurements. Herpetol. Rev. 38: 409-411.

ShettyS.ShineR. (2002): Sexual divergence in diets and morphology in Fijian Sea Snakes Laticauda colubrina (Laticaudinae). Austral. Ecol. 27: 77-84.

ShineR. (1978): Sexual size dimorphism and male combat in snakes. Oecologia 33: 269-277.

ShineR. (1991): Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. Am. Nat. 138: 103-122.

ShineR. (1993): Sexual dimorphism in snakes. In: Snakes: Ecology & Behavior p.  49-86. SeigelR.A.CollinsJ.T. Eds McGraw-HillNew York.

ShineR. (1994): Sexual size dimorphism in snakes revisited. Copeia 2: 326-346.

ShineR.OlssonM.M.MooreI.T.LeMasterM.P.MasonR.T. (1999): Why do male snakes have longer tails than females? Proc. R. Soc. London Ser. B 266: 2147-2151.

ShineR.SunL.X. (2003): Attack strategy of an ambush predator: which attributes of the prey trigger a pit-viper’s strike? Funct. Ecol. 17: 340-348.

ShineR.SunL.X.ZhaoE.BonnetX. (2002): A review of 30 years of ecological research on the Shedao pitviper, Gloydius shedaoensis. Herpetol. Nat. Hist. 9: 1-14.

SlatyerR.A.HirstM.SextonJ.P. (2013): Niche breadth predicts geographic range size: a general ecological pattern. Ecol. Lett. 16: 1104-1114.

SoogarunS.ChoewbamrungkiatM.WiwanitkitV.SuwansaksriJ.NotpanityaW.PradniwatP.PalasuwanA.ChanprasertS.JangprasertP.NetsupunP.SirisapsombatW. (2006): The effect of green pit viper (Trimeresurus albolabris) venom on platelet morphology by electron microscopy. Southeast Asian J. Trop. Med. Public Health 37: 937-939.

SparkmanA.M.ArnoldS.J.BronikowskiA.M. (2007): An empirical test of evolutionary theories for reproductive senescence and reproductive effort in the garter snake Thamnophis elegans. Proc. R. Soc. London Ser. B 274: 943-950.

StrineC.BarnesC.SilvaI.NadolskiB.ArtchawakomT.HillJ.SuwanwareeP. (2015): The first record of ritualized male combat in wild Malayan Pit Viper (Calloselasma rhodostoma). Asian Herpetol. Res. (in press).

StuartB.Chan-ArdT.ThyN. (2012): Cryptelytrops macrops. The IUCN red list of threatened species. Version 2015.1. www.iucnredlist.org. Downloaded on 05 June 2015.

TaylorE.N.DenardoD.F. (2005): Sexual size dimorphism and growth plasticity in snakes: an experiment on the Western Diamond-backed Rattlesnake (Crotalus atrox). J. Exp. Zool. A. Comp. Exp. Biol. 303: 598-607.

TemelesE.J.MillerJ.S.RifkinJ.C. (2010): Evolution of sexual dimorphism in bill size and shape of hermit hummingbirds (Phaethornithinae): a role for ecological causation. Philos. T. Roy. Soc. B 365: 1053-1063.

TsaiT.S.TuM.C. (1998): Sexual dimorphism of Chinese green tree viper Trimeresurus stejnegeri stejnegeri. Biol. Bull. Natl. Taiwan Norm. Univ. 33: 13-22.

TuM.C.WangS.LinY.C. (2000): No divergence of habitat selection between male and female arboreal snakes, Trimeresurus s. stejnegeri. Zool. Stud. 39: 91-98.

VincentS.E.HerrelA.IrschickD.J. (2004): Sexual dimorphism in head shape and diet in the cottonmouth snake (Agkistrodon piscivorus). J. Zool. 264: 53-59.

ViravanC.LooareesuwanS.KosakarnW.WuthiekanunV.McCarthyC.J.StimsonA.F.BunnagD.WarrellD.A. (1992): A national hospital-based survey of snakes responsible for bites in Thailand. Trans. R. Soc. Trop. Med. Hyg. 866: 100-106.

VogelG.DavidP.SidikI. (2014): On Trimeresurus sumatranus (Raffles, 1822), with the designation of a neotype and the description of a new species of pit viper from Sumatra (Squamata: Viperidae: Crotalinae). Amphib. Reptile Conserv. 8: 1-29.

WinneC.T.WillsonJ.D.AndrewsK.M.ReedR.N. (2006): Efficacy of marking snakes with disposable medical cautery units. Herpetol. Rev. 37: 52-54.

YorkD.S. (1984): The combat ritual of the Malayan Pit Viper (Calloselasma rhodostoma). Copeia 3: 770-772.

Figures

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    Adult male T. macrops (A) with a visible post ocular stripe and adult female T. macrops (B) with no visible post ocular stripe. Photo credit: Andrew Brown. This figure is published in color in the online version.

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    The relationship between (A) SVL and HL of male (n=42) and female (n=51), and between (B) SVL and HW of male (n=42) and female (n=51) T. macrops. Linear regression fits and associated r2 values are displayed in each sub-figure.

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    The relationship between (A) SMI and HL of male (n=42) and female (n=51), and between (B) SMI and HW of male (n=42) and female (n=51) T. macrops. Linear regression fits and associated r2 values are displayed in each sub-figure.

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    Biplot of (A) first and second and (B) second and third principal component axes for males (M) and females (F), with their explained proportion of variance, showing the intersex variation of morphometric variables.

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