Cooler snakes respond more strongly to infrared stimuli, but we have no idea why

Abstract

The pit organ defining pit vipers (Crotalinae) contains a membrane covered with temperature receptors that detect thermal radiation from environmental surfaces. Temperature is both the environmental parameter being sensed and the mechanism by which the pit membrane detects the signal. As snakes are ectotherms, temperature also has a strong influence on neurological and locomotor responses to the signal. This study of Pacific rattlesnakes () systematically examined the effect of body, target and background temperatures on response to a moving target. We presented each snake with a moving pendulum bob regulated at a series of six temperatures against a uniform background regulated at one of three temperatures. Snake body temperatures varied from 18 to 36°C. As expected, we found stronger responses to positive contrasts (target warmer than background) than to negative contrasts, and stronger responses to greater contrasts. However, the effect of body temperature was contrary to expectations based on studies of the TRPA1 ion channel (believed to be the molecular basis for pit membrane temperature receptors) and typical thermal reaction norms for neural and motor performance. These predict (1) no response below the threshold where the TRPA1 channel opens, (2) response increasing as temperature increases, peaking near preferred body temperature, and (3) declining thereafter. Remarkably, this behavioral response decreased as body temperature increased from 18 to 36°C, with no threshold or peak in this range. We review various possible physiological mechanisms related to body temperature proposed in the literature, but find none that can satisfactorily explain this result.

The impacts of heat stress on animal cognition: Implications for adaptation to a changing climate

“…Similarly, a higher metabolic rate induced by increased temperatures can cause a higher feeding rate in response to hunger level (Frances & McCauley, 2018; Walker et al, 2020). Finally, the functioning of sensory receptors can also be temperature‐dependent, and therefore modify the quality of the information acquired from the environment and the following behavioral response, even if the underlying cognitive processes remain unchanged (Bakken et al, 2018). 2 Separating these mechanistic effects of temperature on perception from cognitive effects is likely to require controlled laboratory studies to complement field results.…”

Thermoconforming rays of the star-nosed mole

“…Taken together, these observations suggest that evolutionary reductions in thermosensing ion channels may be a specialization for somatosensory organs that must operate well below core body temperatures. Curiously, an enhanced sensory response has been observed in the rattlesnake pit organ when cold, as it responds more strongly to stimuli at cooler temperatures than at warm temperatures (Bakken et al, 2018; Cadena et al, 2013).…”

Infrared-sensing snakes select ambush orientation based on thermal backgrounds

“…2) 25 . Also, laboratory studies have reported robust behavioural responses 14,15,26 and higher strike success 15 when thermal contrast between target and background was large and positive (target warmer than background). This preference for positive thermal contrast might be related to observations of antiphase tracking of moving pendulum targets with negative contrast 14,27 , which should be inimical to strike success.…”

“…The models included a random intercept for snake ID to statistically account for the non-independence of repeated measurements from the same snake. Snakes respond to positive and negative thermal contrast, though response to negative contrast is typically weaker 14,15,26 . We therefore analysed absolute contrast values.…”