The evolution of scale sensilla in the transition from land to sea in elapid snakes

Abstract

Scale sensilla are small tactile mechanosensory organs located on the head scales of many squamate reptiles (lizards and snakes). In sea snakes and sea kraits (Elapidae: Hydrophiinae), these scale organs are presumptive scale sensilla that purportedly function as both tactile mechanoreceptors and potentially as hydrodynamic receptors capable of sensing the displacement of water. We combined scanning electron microscopy, silicone casting of the skin and quadrate sampling with a phylogenetic analysis to assess morphological variation in sensilla on the postocular head scale(s) across four terrestrial, 13 fully aquatic and two semi-aquatic species of elapids. Substantial variation exists in the overall coverage of sensilla (0.8–6.5%) among the species sampled and is broadly overlapping in aquatic and terrestrial lineages. However, two observations suggest a divergent, possibly hydrodynamic sensory role of sensilla in sea snake and sea krait species. First, scale sensilla are more protruding (dome-shaped) in aquatic species than in their terrestrial counterparts. Second, exceptionally high overall coverage of sensilla is found only in the fully aquatic sea snakes, and this attribute appears to have evolved multiple times within this group. Our quantification of coverage as a proxy for relative ‘sensitivity’ represents the first analysis of the evolution of sensilla in the transition from terrestrial to marine habitats. However, evidence from physiological and behavioural studies is needed to confirm the functional role of scale sensilla in sea snakes and sea kraits.

Structure and function of skin in the pelagic sea snake, Hydrophis platurus

“…The protuberances and filamentous extensions from the Oberhäutchen are likely to be sensory, given that the former resemble sensory sensilla described in other sea snakes. The former is especially dense in coverage on cephalic scales of the Hydrophis clade of sea snakes, to which H. platurus belongs (Crowe‐Riddell et al, ). Further, each scale that we examined from the body surface is covered by numerous extensions of the epidermis (Figures and ) and, less commonly, elongate filamentous extensions that are hair‐like in appearance (Figure ).…”

Underwater hearing in sea snakes (Hydrophiinae): first evidence of auditory evoked potential thresholds

“…The two different signals may be caused by a response from two different sensory pathways, i.e. the scale mechanoreceptors distributed over the head (Crowe-Riddell et al, 2016, 2019a and the inner ears. Thresholds were successfully determined for both SPL and PAL based on one full protocol completed for one snake and two full protocols repeated after a 1 week interval for the other individual (Fig.…”

“…There is also the possibility that sensory systems in addition to their inner ear contribute to the detection of waterborne vibrations in sea snakes. The cephalic scales of sea snakes are covered in numerous mechanoreceptors known as scale sensillae (Crowe-Riddell et al, 2016;Crowe-Riddell et al, 2019a). Although the sensitivity of these scale mechanoreceptors is not yet known, they may effectively detect low-frequency (<150 Hz) underwater hydrodynamic stimuli produced by swimming fishes, predators or prey items, and thus enhance the auditory sensitivity of sea snakes (Westhoff et al, 2005).…”

Future Directions in the Research and Management of Marine Snakes

“…Marine snakes can provide an insight into how sensory systems have shifted in response to marine environments. For example, vision, chemoreception, and hearing are important senses for terrestrial snakes, but these stimuli have different characteristics underwater, thus altering the selective pressures on sensory systems (Crowe-Riddell et al, 2016). Other sensory organs might compensate for reduced sensory cues in aquatic environments.…”

“…These include understanding how species recognize potential prey, predators, or mates, and how anthropogenic activities and changing environmental conditions may affect sensory cues and systems. Finally, an underexplored avenue of research is the convergent evolution of sensory systems in marine snakes with other aquatic vertebrates, such as a hydrodynamic or 'lateral line' sense (Westhoff et al, 2005;Crowe-Riddell et al, 2016) and cutaneous photoreception (Zimmerman and Heatwole, 1990).…”