Warm-blooded rodents watch out! There are heat-sensing predators on the prowl...

Some snakes are able to detect prey in total darkness without reliance on sight, olfaction or hearing, but with the help of a mysterious ‘sixth sense’ – they can perceive infrared radiation. However, they are not the only animals to have evolved this fascinating sensory modality, as it is also found in vampire bats and several groups of insects (e.g. bed bugs and some beetles). In the snakes, heat-sensitive facial pits have evolved at least twice, once in the modern, aptly named, pit vipers (Crotalinae), which include the rattlesnakes, and probably once in the more ancient boas and pythons. Boas and pythons are closely related, but there is some disagreement regarding their precise taxonomic relationship. While one system unites them in the family Boidae, with the pythons forming the subfamily Pythoninae, another places the pythons in a separate family, the Pythonidae.

The snake infrared-detecting system responds to subtle thermal fluctuations in the environment and allows for an accurate measurement of the distance of a heat source, particularly in the venomous crotalines. In the non-venomous boas and pythons, infrared sensitivity is 5-10 times lower.

Anatomy of the pit organs

The infrared-sensing pits of boids and crotalines are similar with regard to their ultrastructure and electrophysiological function, but differ in number, location and overall morphology. Boas and pythons have a series of simple pits (three or more per side) on their lips, which are lined with a heat-detecting membrane. The single pit pair of crotalines that is found in the loreal region (between eye and nostril) has a more complex morphology. It follows the design of a bolometer (which forms the basis for many artificial heat sensors), consisting of a very thin sensory membrane suspended above a lower air-filled chamber, which serves to insulate the detector.

In both groups of snakes, the heat-detecting membrane, which is sensitive to tiny differences in temperature, is highly vascular, richly endowed with sensory dendrites and packed with mitochondria. The dendrites are formed from terminal masses of the trigeminal nerve (terminal nerve masses, TNMs), which fire constantly at a low rate. An object that exceeds a certain threshold temperature will increase the firing rate of the TNMs, while a colder object will decrease it. In boas and pythons, nerve density is lower than in pit vipers, which probably contributes to the differences in sensitivity. Although the morphology of the pit vasculature differs markedly between the two taxa, the patterns of blood flow in stimulated pit organs are very similar. This is because they function as a heat exchange mechanism that cools down the receptors after stimulation, thus preventing afterimages.

Intriguingly, analogues of these two types of snake infrared receptor are found in two species of beetle that use this sensory modality for the detection of forest fires. The pit organs of boids show anatomical similarities with the heat sensors of Merimna atrata, while Acanthocnemus nigricans has converged on the crotalines.

Neural processing

In all infrared-sensitive snakes, the facial pits are innervated by the trigeminal nerve, but in crotalines, the information is relayed to the optic tectum via the nucleus reticularis caloris in the medulla, which is bypassed in boas and pythons. In the optic tectum, the infrared signals are processed and evidently integrated with visual information - visual and infrared maps of the snakes’ surroundings are somehow overlaid and this combined information is then conveyed to the forebrain.

Indeed, of all the systems of infrared detection, the snakes seem to possess the closest analogue to the eye. Their heat pits are convergent with the pinhole eye (which, of course, has evolved multiple times), as they visualise thermal radiation relying on the same optical principles. Radiation that enters through the hole of the pit will hit the heat-sensing membrane at a particular spot that is dependent on the direction of the heat source. However, it is likely that, similar to a pinhole eye, the resolution is very poor, but there is good reason to assume that the neural processing in the brain leads to a significant sharpening of the thermal image. In the context of prey capture, snakes might furthermore choose colder ambush sites to enhance the contrast of their warm prey and thus the accuracy of their ‘thermal vision’.

Molecular mechanism of infrared detection

Although theoretically infrared receptors could detect photons directly, analogous to the photochemical activation of opsins in the vertebrate retina, an indirect detection of infrared signals through heating of tissue, i.e. through a thermotransduction mechanism, has always been considered more likely. However, the molecular identity of the infrared sensor was long unknown, until a recent study on western diamondback rattlesnakes (Crotalus atrox) provided evidence that the ion channel TRPA1 serves as a specialised infrared detector. The pit membrane seems to transfer thermal energy to the TRPA1 channels, which are located in high numbers on the embedded trigeminal nerve fibres and highly heat-sensitive.

Boas and pythons evidently use the same molecule to detect heat, indicating “that ancient and modern snakes have independently adapted TRPA1 as an infrared sensor through convergent evolution” (Gracheva et al. 2010, Nature, vol. 464, p. 1010). However, the thermal threshold of TRPA1 channels is slightly higher in boids than in rattlesnakes, in accordance with the lower infrared sensitivity of the former. Infrared-insensitive snakes also possess TRPA1 channels, but their activation threshold is so high that they are unsuited as specialised infrared receptors and probably serve to mediate somatic temperature sensation.

TRPA1 channels have been detected in a number of other vertebrate species, including some fish, as well as in invertebrates, such as Drosophila melanogaster. While they contribute to temperature perception in these invertebrates, they mainly function as chemoreceptors in vertebrates other than snakes, thus showing surprising physiological plasticity. In mammals, their primary function is the detection of chemical irritants and inflammatory agents and they are activated by allyl isothiocyanate (AITC), the pungent agent from mustard plants such as wasabi.

Functions of infrared detection

The combination of thermal and visual information in the brain of infrared-sensing snakes allows them to track animals with speed and precision. Pit vipers can detect potential prey at a distance of about 1 m and use their facial pits for orienting and striking towards it. For a long time it was assumed that infrared detection evolved solely for the localisation of ‘warm-blooded’ prey, but now it is considered likely that heat pits may be more general-purpose organs. The ability to sense thermal radiation in the environment could also be used for behavioural thermoregulation and perhaps predator detection or den site selection. Behavioural experiments showed that some snakes indeed made thermoregulatory decisions based on thermal radiation cues, and this was only possible with functional facial pits, but not when their pits were blocked. It has been suggested that thermoregulation may have been the ancestral function of infrared detection in snakes.

Interestingly, the California ground squirrel (Spermophilus beecheyi) that is preyed upon by western rattlesnakes (Crotalus oreganus) has in a way turned the tables on its infrared-sensitive predator. These squirrels have evolved a whole arsenal of anti-predator behaviour, including the so-called tail flagging – waving their erect tail from side to side provokes a defensive response by the snake. Infrared imaging has now shown that the squirrels specifically heat their tail (by flooding it with blood) when encountering a rattlesnake, which makes the predator even more cautious. When confronted with an infrared-insensitive gopher snake (Pituophis melanoleucus), however, they flag their tail without emitting a thermal signal. This is a fascinating case of an infrared signalling system.