Skip to main content
Log in

Phylogenetic analysis of standard metabolic rate of snakes: a new proposal for the understanding of interspecific variation in feeding behavior

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

The current proposal about the variation of standard metabolic rates (SMR) in snakes predicts that SMR is influenced by the feeding frequency (frequent or infrequent feeders). However, feeding frequency in snakes is poorly studied and hard to quantify under natural conditions. Alternatively, foraging strategy was studied for a large number of species and is usually related to the feeding frequency. In this work, we performed a meta-analysis on the SMR of compiled data from 74 species of snakes obtained from the literature and five more different species of lanceheads (genus Bothrops), after categorization according to the foraging mode (ambush or active foraging) and regarding their phylogenetic history. We tested the hypothesis that foraging mode (FM) is a determinant factor on the interspecific variation of SMR despite the phylogenetic relationship among species. We demonstrated that FM predicted SMR, but there is also a partial phylogenetic structuration of SMR in snakes. We also detected that evolution rates of SMR in active foragers seem to be higher than ambush-hunting snakes. We suggested that foraging mode has a major effect over the evolution of SMR in snakes, which could represent an ecophysiological co-adaptation, since ambush hunters (with low feeding rates) present a lower maintenance energetic cost (SMR) when compared to active foragers. The higher SMR evolution rates for active foraging snakes could be related to a higher heterogeny in the degree of activity during hunting by active foragers when compared to ambush-hunting snakes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abe AS, Mendes EG (1980) Effect of body size and temperature on oxygen uptake in the water snakes Helicops modestus and Liophis miliaris (COLUBRIDAE). Comp Biochem Physiol A 65(3):367–370. doi:10.1016/0300-9629(80)90045-6

    Article  Google Scholar 

  • Alexander GJ, Brooks R (1999) Circannual rhythms of appetite and ecdysis in the elapid snake, Hemachatus haemachatus, appear to be endogenous. Copeia 1999(1):146–152. doi:10.2307/1447395

    Article  Google Scholar 

  • Alsadoon MK (1991) Metabolic rate-temperature curves of the horned viper, Cerastes cerastes gasperetti, the moila snake, Malpolon moilensis, and the adder, Vipera berus. Comp Biochem Physiol A 99(1–2):119–122. doi:10.1016/0300-9629(91)90245-8

    Article  Google Scholar 

  • Andrews RM, Pough FH (1985) Metabolism of squamate reptiles—allometric and ecological relationships. Physiol Zool 58(2):214–231

    Article  Google Scholar 

  • Beaupre SJ (1993) An ecological study of oxygen consumption in the mottled rock rattlesnake, Crotalus lepidus lepidus, and the black-tailed rattlesnake, Crotalus molossus molossus, from 2 populations. Physiol Zool 66(3):437–454

    Article  Google Scholar 

  • Beaupre SJ, Duvall D (1998) Variation in oxygen consumption of the western diamondback rattlesnake (Crotalus atrox): implications for sexual size dimorphism. J Comp Physiol B 168(7):497–506. doi:10.1007/s003600050170

    Article  Google Scholar 

  • Beaupre SJ, Zaidan F (2001) Scaling of CO2 production in the timber rattlesnake (Crotalus horridus), with comments on cost of growth in neonates and comparative patterns. Physiol Biochem Zool 74(5):757–768. doi:10.1086/322965

    Article  CAS  PubMed  Google Scholar 

  • Bedford GS, Christian KA (1998) Standard metabolic rate and preferred body temperatures in some Australian pythons. Aust J Zool 46(4):317–328. doi:10.1071/zo98019

    Article  Google Scholar 

  • Bessler SM, Stubblefield MC, Ultsch GR, Secor SM (2010) Determinants and modeling of specific dynamic action for the Common Garter Snake (Thamnophis sirtalis). Can J Zool 88(8):808–820. doi:10.1139/z10-045

    Article  CAS  Google Scholar 

  • Blomberg SP, Garland T (2002) Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J Evol Biol 15(6):899–910. doi:10.1046/j.1420-9101.2002.00472.x

    Article  Google Scholar 

  • Blomberg SP, Ives AR, Garland T (2001) Detecting phylogenetic signal in comparative data. Am Zool 41(6):1395–1395

    Google Scholar 

  • Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evol Int J Org Evol 57(4):717–745. doi:10.1111/j.0014-3820.2003.tb00285.x

    Article  Google Scholar 

  • Brischoux F, Lillywhite HB (2013) Trophic consequences of pelagic life-style in yellow-bellied sea snakes. Mar Ecol Prog Ser 478:231–238. doi:10.3354/meps10177

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Castoe TA, Jiang ZJ, Gu W, Wang ZO, Pollock DD (2008) Adaptive evolution and functional redesign of core metabolic proteins in snakes. Plos One 3(5):e2201

    Article  PubMed  PubMed Central  Google Scholar 

  • Chappell MA, Ellis TM (1987) Resting metabolic rates in boid snakes—allometric relationships and temperature effects. J Comp Physiol B 157(2):227–235. doi:10.1007/bf00692367

    Article  CAS  PubMed  Google Scholar 

  • Cooper N, Thomas GH, Venditti C, Meade A, Freckleton RP (2016) A cautionary note on the use of Ornstein Uhlenbeck models in macroevolutionary studies. Biol J Linn Soc 118(1):64–77. doi:10.1111/bij.12701

    Article  Google Scholar 

  • Cox CL, Secor SM (2010) Integrated postprandial responses of the diamondback watersnake, Nerodia rhombifer. Physiol Biochem Zool 83:618–631

    Article  PubMed  Google Scholar 

  • Cruzneto AP, Abe AS (Serpentes, Viperidae (1994) Ontogenic variation of oxygen-uptake in the pitviper Bothrops moojeni. Comp Biochem Physiol A 108(4):549–554. doi:10.1016/0300-9629(94)90339-5

    Article  Google Scholar 

  • Dejours P (1981) Principles of comparative respiratory physiology. 2 edn. Elsevier/North-Holland Biomedical Press, Amsterdam

    Google Scholar 

  • Dlugosz EM, Chappell MA, Meek TH, Szafranska P, Zub K, Konarzewski M, Jones JH, Bicudo E, Garland T (2009) Phylogenetic analysis of mammalian maximal oxygen consumption. Integr Comp Biol 49:E48-E48

    Google Scholar 

  • Dorcas ME, Hopkins WA, Roe JH (2004) Effects of body mass and temperature on standard metabolic rate in the eastern diamondback rattlesnake (Crotalus adamanteus). Copeia 1:145–151

    Article  Google Scholar 

  • Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971. doi:10.1016/j.anbehav.2005.01.016

    Article  Google Scholar 

  • Enok S, Simonsen LS, Wang T (2013) The contribution of gastric digestion and ingestion of amino acids on the postprandial rise in oxygen consumption, heart rate and growth of visceral organs in pythons. Comp Biochem Physiol A 165(1):46–53. doi:10.1016/j.cbpa.2013.01.022

    Article  CAS  Google Scholar 

  • Eskew EA, Willson JD, Winne CT (2009) Ambush site selection and ontogenetic shifts in foraging strategy in a semi-aquatic pit viper, the Eastern cottonmouth. J Zool 277(2):179–186. doi:10.1111/j.1469-7998.2008.00527.x

    Article  Google Scholar 

  • Farrell TM, May PG, Andreadis PT (2011) Experimental manipulation of tail color does not affect foraging success in a caudal luring rattlesnake. J Herpetol 45(3):291–293

    Article  Google Scholar 

  • Fathinia B, Rastegar-Pouyani N, Rastegar-Pouyani E, Todehdehghan F, Amiri F (2015) Avian deception using an elaborate caudal lure in Pseudocerastes urarachnoides (Serpentes: Viperidae). Amphibia Reptilia 36(3):223–231. doi:10.1163/15685381-00002997

    Article  Google Scholar 

  • Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160(6):712–726. doi:10.1086/343873

    Article  CAS  PubMed  Google Scholar 

  • Garland T, Bennett AF, Rezende EL (2005) Phylogenetic approaches in comparative physiology. J Exp Biol 208(16):3015–3035. doi:10.1242/jeb.01745

    Article  PubMed  Google Scholar 

  • Gavira RSB, Andrade DV (2013a) Meal size effects on the postprandial metabolic response of Bothrops alternatus (Serpentes: Viperidae). Zoologia 30(3):291–295. doi:10.1590/s1984-46702013000300005

    Article  Google Scholar 

  • Gavira RSB, Andrade DV (2013b) Temperature and thermal regime effects on the specific dynamic action of Bothrops alternatus (Serpentes, Viperidae). Amphibia Reptilia 34(4):483–491. doi:10.1163/15685381-00002903

    Article  Google Scholar 

  • Glaudas X, Alexander GJ (2017) A lure at both ends: aggressive visual mimicry signals and prey-specific luring behaviour in an ambush-foraging snake. Behav Ecol Sociobiol. doi:10.1007/s00265-016-2244-6

    Google Scholar 

  • Greene S, McConnachie S, Secor S, Perrin M (2013) The effects of body temperature and mass on the postprandial metabolic responses of the African egg-eating snakes Dasypeltis scabra and Dasypeltis inornata. Comp Biochem Physiol A 165(2):97–105. doi:10.1016/j.cbpa.2013.02.023

    Article  CAS  Google Scholar 

  • Hagman M, Phillips BL, Shine R (2008) Tails of enticement: caudal luring by an ambush-foraging snake (Acanthophis praelongus, Elapidae). Funct Ecol 22(6):1134–1139. doi:10.1111/j.1365-2435.2008.01466.x

    Article  Google Scholar 

  • Hopkins WA, Roe JH, Philippi T, Congdon JD (2004) Standard and digestive metabolism in the banded water snake, Nerodia fasciata fasciata. Comp Biochem Physiol A 137(1):141–149. doi:10.1016/j.cbpb.2003.09.017

    Article  CAS  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50(3):346–363. doi:10.1002/bimj.200810425

    Article  Google Scholar 

  • Huey RB, Pianka ER (1981) Ecological consequences of foraging mode. Ecology 62(4):991–999. doi:10.2307/1936998

    Article  Google Scholar 

  • Klaczko J, Sherratt E, Setz EZF (2016) Are diet preferences associated to skulls shape diversification in xenodontine snakes?. Plos One. doi:10.1371/journal.pone.0148375

    PubMed  PubMed Central  Google Scholar 

  • Lighton JRB (2008) Measuring metabolic rates—a manual for scientists. Oxford University Press, Oxford

    Book  Google Scholar 

  • Lourdais O, Guillon M, DeNardo D, Blouin-Demers G (2013) Cold climate specialization: adaptive covariation between metabolic rate and thermoregulation in pregnant vipers. Physiol Behav 119:149–155. doi:10.1016/j.physbeh.2013.05.041

    Article  CAS  PubMed  Google Scholar 

  • Lourdais O, Gartner GEA, Brischoux F (2014) Ambush or active life: foraging mode influences haematocrit levels in snakes. Biol J Linn Soc 111(3):636–645. doi:10.1111/bij.12223

    Article  Google Scholar 

  • Marques OAV, Martins M, Develey PF, Macarrao A, Sazima I (2012) The golden lancehead Bothrops insularis (Serpentes: Viperidae) relies on two seasonally plentiful bird species visiting its island habitat. J Nat Hist 46(13–14):885–895. doi:10.1080/00222933.2011.654278

    Article  Google Scholar 

  • Martins M, Marques OAV, Sazima I (2002) Ecological and phylogenetic correlates of feeding habits in Neotropical pitvipers (genus Bothrops). In: Schuett GW, Hoggren M, Douglas ME, Greene HW (eds) Biology of the vipers. Eagle Mountain Publishing, Eagle Mountain

    Google Scholar 

  • McCue MD (2006) Specific dynamic action: a century of investigation. Comp Biochem Physiol A 144(4):381–394. doi:10.1016/j.cbpa.2006.03.011

    Article  CAS  Google Scholar 

  • McCue MD, Lillywhite HB (2002) Oxygen consumption and the energetics of island-dwelling Florida cottonmouth snakes. Physiol Biochem Zool 75(2):165–178. doi:10.1086/339390

    Article  PubMed  Google Scholar 

  • Nelson XJ, Garnett DT, Evans CS (2010) Receiver psychology and the design of the deceptive caudal luring signal of the death adder. Anim Behav 79(3):555–561. doi:10.1016/j.anbehav.2009.12.011

    Article  Google Scholar 

  • O’Meara BC, Ane C, Sanderson MJ, Wainwright PC (2006) Testing for different rates of continuous trait evolution using likelihood. Evol Int J Org Evol 60(5):922–933

    Article  Google Scholar 

  • Ott BD, Secor SM (2007) Adaptive regulation of digestive performance in the genus Python. J Exp Biol 210(2):340–356. doi:10.1242/jeb.02626

    Article  PubMed  Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401(6756):877–884. doi:10.1038/44766

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20(2):289–290. doi:10.1093/bioinformatics/btg412

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) _nlme: Linear and Nonlinear Mixed Effects Models_. R package version 3.1–128. http://CRAN.R-project.org/package=nlme&gt

  • Rabatsky AM, Waterman JM (2005) Ontogenetic shifts and sex differences in caudal luring in the dusky pygmy rattlesnake, Sistrurus miliarius barbouri. Herpetologica 61(2):87–91. doi:10.1655/04-22

    Article  Google Scholar 

  • Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3(2):217–223. doi:10.1111/j.2041-210X.2011.00169.x

    Article  Google Scholar 

  • Roe JH, Hopkins WA, Snodgrass JW, Congdon JD (2004) The influence of circadian rhythms on pre- and post-prandial metabolism in the snake Lamprophis fuliginosus. Comp Biochem Physiol A 139(2):159–168. doi:10.1016/j.cbpb.2004.08.005

    Article  CAS  Google Scholar 

  • Sazima I (1991) Caudal luring in 2 neotropical pitvipers, Bothrops jararaca and B. jararacussu. Copeia 1:245–248

    Article  Google Scholar 

  • Secor SM (1995) Ecological aspects of foraging mode for the snakes Crotalus cerastes and Masticophis flagellum. Herpetol Monogr 9:169–186

    Article  Google Scholar 

  • Secor SM (2003) Gastric function and its contribution to the postprandial metabolic response of the Burmese python Python molurus. J Exp Biol 206(10):1621–1630. doi:10.1242/jeb.00300

    Article  PubMed  Google Scholar 

  • Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179(1):1–56. doi:10.1007/s00360-008-0283-7

    Article  PubMed  Google Scholar 

  • Secor SM, Diamond J (1997) Determinants of the postfeeding metabolic response of Burmese pythons, Python molurus. Physiol Zool 70(2):202–212

    Article  CAS  PubMed  Google Scholar 

  • Secor SM, Diamond J (1998) A vertebrate model of extreme physiological regulation. Nature 395(6703):659–662. doi:10.1038/27131

    Article  CAS  PubMed  Google Scholar 

  • Secor SM, Diamond JM (2000) Evolution of regulatory responses to feeding in snakes. Physiol Biochem Zool 73(2):123–141. doi:10.1086/316734

    Article  CAS  PubMed  Google Scholar 

  • Secor SM, Nagy KA (1994) Bioenergetic correlates of foraging mode for the snakes Crotalus cerastes and Masticophis flagellum. Ecology 75(6):1600–1614. doi:10.2307/1939621

    Article  Google Scholar 

  • Secor SM, Taylor JR, Grosell M (2012) Selected regulation of gastrointestinal acid-base secretion and tissue metabolism for the diamondback water snake and Burmese python. J Exp Biol 215:185–196

    Article  CAS  PubMed  Google Scholar 

  • Shine R (1980) Ecology of the australian death adder Acanthophis antarcticus (elapidae)—evidence for convergence with the viperidae. Herpetologica 36(4):281–289

    Google Scholar 

  • Shine R, Sun LX (2002) Arboreal ambush site selection by pit-vipers Gloydius shedaoensis. Anim Behav 63:565–576. doi:10.1006/anbe.2001.1928

    Article  Google Scholar 

  • Smith MT, Ortega J, Beaupre SJ (2014) Metabolic cost of venom replenishment by Prairie Rattlesnakes (Crotalus viridis viridis). Toxicon 86:1–7. doi:10.1016/j.toxicon.2014.04.013

    Article  CAS  PubMed  Google Scholar 

  • Tsai TS, Lee HJ, Tu MC (2008) Specific dynamic action, apparent assimilation efficiency, and digestive rate in an arboreal pitviper, Trimeresurus stejnegeri stejnegeri. Can J Zool 86(10):1139–1151. doi:10.1139/z08-090

    Article  Google Scholar 

  • Wall M, Thompson MB, Shine R (2013) Does foraging mode affect metabolic responses to feeding? A study of pygopodid lizards. Curr Zool 59(5):618–625

    Article  Google Scholar 

  • Wang T, Abe AS (1994) Oxygen-uptake in snakes—is there a reduction in fossorial species. Comp Biochem Physiol A 107(3):483–485

    Article  Google Scholar 

  • Webber MM, Jezkova T, Rodriguez-Robles JA (2016) Feeding ecology of sidewinder rattlesnakes, Crotalus cerastes (Viperidae). Herpetologica 72(4):324–330

    Article  Google Scholar 

  • Zaidan F, Beaupre SJ (2003) Effects of body mass, meal size, fast length, and temperature on specific dynamic action in the timber rattlesnake (Crotalus horridus). Physiol Biochem Zool 76(4):447–458. doi:10.1086/375661

    Article  PubMed  Google Scholar 

  • Zheng YC, Wiens JJ (2016) Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol Phylogenet Evol 94:537–547. doi:10.1016/j.ympev.2015.10.009

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

DRS and JEC were supported by FAPESP (Proc.09/53202-4) and by the INCT Fisiologia Comparada (FAPESP/CNPq/MCT Proc.08/57712-4). CAN was supported by PFPMCG/PRONEX FAPES (Proc.08/57687-0). FC is supported by PNPD-CAPES. AC was supported by FAPESP 12/15754-8. KGF was supported by INCT-Tox (Proc.08/57898-0). We also like to thank Stephen Secor for SMR data provided and Diogo Provete for the analysis advices.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel Rodrigues Stuginski.

Additional information

Communicated by G. Heldmaier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 77 KB)

Supplementary material 2 (DOCX 22 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stuginski, D.R., Navas, C.A., de Barros, F.C. et al. Phylogenetic analysis of standard metabolic rate of snakes: a new proposal for the understanding of interspecific variation in feeding behavior. J Comp Physiol B 188, 315–323 (2018). https://doi.org/10.1007/s00360-017-1128-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-017-1128-z

Keywords

Navigation