Evaporative respiratory cooling augments pit organ thermal detection in rattlesnakes

Abstract

Rattlesnakes use their facial pit organs to sense external thermal fluctuations. A temperature decrease in the heat-sensing membrane of the pit organ has the potential to enhance heat flux between their endothermic prey and the thermal sensors, affect the optimal functioning of thermal sensors in the pit membrane and reduce the formation of thermal “afterimages”, improving thermal detection. We examined the potential for respiratory cooling to improve strike behaviour, capture, and consumption of endothermic prey in the South American rattlesnake, as behavioural indicators of thermal detection. Snakes with a higher degree of rostral cooling were more accurate during the strike, attacking warmer regions of their prey, and relocated and consumed their prey faster. These findings reveal that by cooling their pit organs, rattlesnakes increase their ability to detect endothermic prey; disabling the pit organs caused these differences to disappear. Rattlesnakes also modify the degree of rostral cooling by altering their breathing pattern in response to biologically relevant stimuli, such as a mouse odour. Our findings reveal that low humidity increases their ability to detect endothermic prey, suggesting that habitat and ambush site selection in the wild may be influenced by external humidity levels as well as temperature.

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Acknowledgments

This research was supported by grants from the Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Fundação para o Desenvolvimento da Unesp (FUNDUNESP) to DVA, the NSERC of Canada to GJT, and a Journal of Experimental Biologists Travelling Fellowship to VC. Approval to perform the animal studies was issued by the Commission for Ethics in Animal Experimentation from University of São Paulo State (UNESP), SP, Brazil, Protocol Numbers: 03/08-CEEA and 021/2010. We thank Augusto S. Abe for facilitating laboratory logistics, Laura Aedy for assistance with analysis of thermal images, and William Hayes for his critical feedback on the manuscript.

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Correspondence to Glenn J. Tattersall.

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Cadena, V., Andrade, D.V., Bovo, R.P. et al. Evaporative respiratory cooling augments pit organ thermal detection in rattlesnakes. J Comp Physiol A 199, 1093–1104 (2013). https://doi.org/10.1007/s00359-013-0852-4

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Keywords

  • Thermosensation
  • Pit organ
  • Thermal imaging
  • Respiratory cooling
  • Heat detection