Skip to main content

Advertisement

SpringerLink
Log in

Do free-ranging rattlesnakes use thermal cues to evaluate prey?

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

Abstract

Rattlesnakes use infrared radiation to detect prey animals such as small mammals and lizards. Because ectotherm locomotor performance depends on temperature, rattlesnakes could use prey temperature to evaluate the potential of lizards to evade attacks. Here, we tested whether hunting rattlesnakes use infrared information to (1) detect and (2) evaluate prey before attack. We expected thermal contrast between prey and background to be the best predictor of predatory behaviour under the prey detection hypothesis, and absolute prey temperature under the prey evaluation hypothesis. We presented lizard carcasses of varying temperatures to free-ranging sidewinder rattlesnakes (Crotalus cerastes) and scored behavioural responses as a function of thermal contrast, absolute lizard temperature, and light level. Thermal contrast and light level were the most salient predictors of snake behaviour. Snakes were more likely to respond to lizards and/or respond at greater distances at night and when thermal contrast was high, supporting the known prey detection function of infrared sensing. Absolute lizard temperature was not an important predictor of snake behaviour; thus, we found no evidence for temperature-based prey evaluation. Infrared sensing is still poorly understood in ecologically relevant contexts; future research will test whether rattlesnakes learn to evaluate prey based on temperature with experience.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268

    Article  Google Scholar 

  • Angilletta MJ, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240

    Article  Google Scholar 

  • Bakken GS, Krochmal AR (2007) The imaging properties and sensitivity of the facial pits of pitvipers as determined by optical and heat-transfer analysis. J Exp Biol 210:2801–2810

    Article  PubMed  Google Scholar 

  • BartoÅ„ K (2016) MuMIn: Multi-model inference. R package version 1.15.6. https://CRAN.R-project.org/package=MuMIn

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bradbury JW, Vehrencamp SL (2011) Principles of animal communication. Sinauer Associates, Sunderland

    Google Scholar 

  • Burnham K, Anderson D (2002) Model selection and multimodel inference: A practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Cadena V, Andrade DV, Bovo RP, Tattersall GJ (2013) Evaporative respiratory cooling augments pit organ thermal detection in rattlesnakes. J Comp Phys A 199:1093–1104

    Article  CAS  Google Scholar 

  • Campbell JA, Lamar WW (2004) Venomous reptiles of the western hemisphere, vol 2. Cornell University Press, Ithaca

    Google Scholar 

  • Chen Q, Deng H, Brauth SE, Ding L, Tang Y (2012) Reduced performance of prey targeting in pit vipers with contralaterally occluded infrared and visual senses. PLoS One 7:e34989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Kang D, Xu J, Lake M, Hogan JO, Sun C, Walter K, Yao B, Kim D (2013) Species differences and molecular determinant of TRPA1 cold sensitivity. Nat Commun 4:2501

    PubMed  PubMed Central  Google Scholar 

  • Chen Q, Liu Y, Brauth SE, Fang G, Tang Y (2017) The thermal background determines how the infrared and visual systems interact in pit vipers. J Exp Biol 220:3103–3109

    Article  PubMed  Google Scholar 

  • Clark R (2004) Timber rattlesnakes (Crotalus horridus) use chemical cues to select ambush sites. J Chem Ecol 30:607–617

    Article  CAS  PubMed  Google Scholar 

  • Clark R (2005) Pursuit-deterrent communication between prey animals and timber rattlesnakes (Crotalus horridus): the response of snakes to harassment displays. Behav Ecol Sociobiol 59:258–261

    Article  Google Scholar 

  • Clark R, Tangco S, Barbour M (2012) Field video recordings reveal factors influencing predatory strike success of free-ranging rattlesnakes (Crotalus spp.). Anim Behav 84:183–190

    Article  Google Scholar 

  • Clark RW, Dorr SW, Whitford MD, Freymiller GA, Putman BJ (2016) Activity cycles and foraging behaviors of free-ranging sidewinder rattlesnakes (Crotalus cerastes): the ontogeny of hunting in a precocial vertebrate. Zoology 119:196–206

    Article  PubMed  Google Scholar 

  • Combes SA, Rundle DE, Iwasaki JM, Crall JD (2012) Linking biomechanics and ecology through predator–prey interactions: flight performance of dragonflies and their prey. J Exp Biol 215:903–913

    Article  CAS  PubMed  Google Scholar 

  • de Cock Buning T (1983) Thermal sensitivity as a specialization for prey capture and feeding in snakes. Am Zool 23:363–375

    Article  Google Scholar 

  • de Cock Buning T, Terashima S, Goris RC (1981) Crotaline pit organs analyzed as warm receptors. Cell Mol Neurobiol 1:69–85

    Article  PubMed  Google Scholar 

  • Ebert J, Westhoff G (2006) Behavioural examination of the infrared sensitivity of rattlesnakes (Crotalus atrox). J Comp Physiol A 192:941–947

    Article  CAS  Google Scholar 

  • Fitzgibbon CD (1994) The costs and benefits of predator inspection behaviour in Thomson’s gazelles. Behav Ecol Sociobiol 34:139–148

    Article  Google Scholar 

  • Garamszegi LZ, Calhim S, Dochtermann N, Hegyi G, Hurd PL, Jørgensen C, Kutsukake N, Lajeunesse MJ, Pollard KA, Schielzeth H, Symonds MR (2009) Changing philosophies and tools for statistical inferences in behavioural ecology. Behav Ecol 20:1363–1375

    Article  Google Scholar 

  • Goris RC (2011) Infrared organs of snakes: an integral part of vision. J Herpetol 45:2–14

    Article  Google Scholar 

  • Gracheva EO, Ingolia NT, Kelly YM. Cordero-Morales JF, Hollopeter G, Chesler AT, Sánchez EE, Perez JC, Weissman JS, Julius D (2010) Molecular basis of infrared detection by snakes. Nature 464:1006–1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartline PH, Kass L, Loop MS (1978) Merging of modalities in the optic tectum: infrared and visual integration in rattlesnakes. Science 199:1225–1229

    Article  CAS  PubMed  Google Scholar 

  • Haverly JE, Kardong KV (1996) Sensory deprivation effects on the predatory behavior of the rattlesnake, Crotalus viridis oreganus. Copeia 1996:419–428

  • Hayes WK, Duvall D (1991) A field study of praire rattlesnake predatory strikes. Herpetologica 47:78–81

    Google Scholar 

  • Huey RB (1982) Temperature, physiology, and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of the reptilia, vol 12. Academic Press, New York, pp 25–74

    Google Scholar 

  • Kang K (2016) Exceptionally high thermal sensitivity of rattlesnake TRPA1 correlates with peak current amplitude. BBA Biomembranes 1858:318–325

    Article  CAS  PubMed  Google Scholar 

  • Kardong KV, Smith TL (2002) Proximate factors involved in rattlesnake predatory behavior: a review. In: Schuett GW, Hoggren M, Douglas ME, Greene HW (eds) Biology of the vipers. Eagle Mountain Publishing, Eagle Mountain, pp 253–266

    Google Scholar 

  • Khan JJ, Richardson JM, Tattersall GJ (2010) Thermoregulation and aggregation in neonatal bearded dragons (Pogona vitticeps). Physiol Behav 100:180–186

    Article  CAS  PubMed  Google Scholar 

  • Klauber LM, McClung KH (1982) Rattlesnakes, their habits, life histories, and influence on mankind. University of California Press, Berkeley

    Google Scholar 

  • Moiseenkova V, Bell B, Motamedi M, Wozniak E, Christensen B (2003) Wide-band spectral tuning of heat receptors in the pit organ of the copperhead snake (Crotalinae). Am J Physiol Regul Integr Comp Physiol 284:598–606

    Article  Google Scholar 

  • Mosauer W (1933) Locomotion and diurnal range of Sonora occipitalis, Crotalus cerastes, and Crotalus atrox as seen from their tracks. Copeia 1933:14–16

  • Newman EA, Hartline PH (1981) Integration of visual and infrared information in bimodal neurons of the rattlesnake optic tectum. Science 213:789–791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Putman BJ, Clark RW (2017) Behavioral thermal tolerances of free-ranging rattlesnakes (Crotalus oreganus) during the summer foraging season. J Therm Biol 65:8–15

    Article  PubMed  Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/

  • Randall J, Boltas King D (2001) Assessment and defence of solitary kangaroo rats under risk of predation by snakes. Anim Behav 61:579–587

    Article  Google Scholar 

  • Reiserer RS (2001) Evolution of life histories in rattlesnakes. Dissertation, University of California, Berkeley

  • Rundus AS, Owings DH, Joshi SS, Chinn E, Giannini N (2007) Ground squirrels use an infrared signal to deter rattlesnake predation. Proc Natl Acad Sci USA 104:14372–14376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Secor SM (1994) Ecological significance of movements and activity range for the sidewinder, Crotalus cerastes. Copeia 1994:631–645

    Article  Google Scholar 

  • Shine R, Sun L-X (2003) Attack strategy of an ambush predator: which attributes of the prey trigger a pit-viper’s strike? Funct Ecol 17:340–348

    Article  Google Scholar 

  • Shine R, Sun L, Kearney M, Fitzgerald M (2002) Thermal correlates of foraging-site selection by Chinese pit-vipers (Gloydius shedaoensis, Viperidae). J Therm Biol 27:405–412

    Article  Google Scholar 

  • Tattersall GJ (2016) Infrared thermography: a non-invasive window into thermal physiology. Comput Biochem Phys A 202:78–98

    Article  CAS  Google Scholar 

  • Theodoratus DH, Chiszar D, Smith HM (1997) Rattlesnake orientation to prey as a function of thermal backgrounds and edges. Psychol Rec 47:461–472

    Article  Google Scholar 

  • Van Dyke JU, Grace MS (2010) The role of thermal contrast in infrared-based defensive targeting by the copperhead, Agkistrodon contortrix. Anim Behav 79:993–999

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Young BA (2010) How a heavy-bodied snake strikes quickly: high-power axial musculature in the puff adder (Bitis arietans). J Exp Zool Part A 313:114–121

    Google Scholar 

  • Zajitschek SRK, Zajitschek F, Miles DB, Clobert J (2012) The effect of coloration and temperature on sprint performance in male and female wall lizards. Biol J Linn Soc 107:573–582

    Article  Google Scholar 

Download references

Acknowledgements

We thank Abigail Rosenberg and the Marine Corps Air Station Yuma for logistical support and providing access to field sites and housing. Jessica Tingle, Jessica Ryan, Drew Steele, Malachi Whitford, Grace Freymiller, and Katherine Phillips provided field support. Shannon Whelan, George Bakken, and two anonymous reviewers offered valuable comments on earlier versions of this manuscript. The San Diego State University Institutional Animal Care and Use Committee approved all methods (APF 16-08-014C). This study was funded by San Diego State University, the Animal Behavior Society, and the San Diego Chapter of the Explorer’s Club.

Author information

Authors and Affiliations

  1. Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, CA, 92182, USA

    Hannes A. Schraft & Rulon W. Clark

  2. Graduate Group in Ecology, Department of Neurobiology, Physiology, and Behavior, University of California, Davis, CA, USA

    Hannes A. Schraft

  3. Environmental Science and Policy Program, University of Maryland, College Park, MD, USA

    Colin Goodman

Authors
  1. Hannes A. Schraft
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Colin Goodman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rulon W. Clark
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hannes A. Schraft.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 2170 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schraft, H.A., Goodman, C. & Clark, R.W. Do free-ranging rattlesnakes use thermal cues to evaluate prey?. J Comp Physiol A 204, 295–303 (2018). https://doi.org/10.1007/s00359-017-1239-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-017-1239-8

Keywords

Search

Navigation