Mandibular sawing in a snail-eating snake

We found that operculate snails were more abundant than were non-operculate snails: 34 and 22 individuals were encountered, respectively. Among snails of moderate size (shell width, 10–20 mm), which were often consumed by A. boa, operculate snails were more than 10 times as abundant as were non-operculate snails (25 and 2 individuals were encountered, respectively).

Individuals of A. boa (n = 8) readily preyed upon Leptopoma sp. (n = 30) in our feeding trials. Upon capture, the snakes immediately inserted their mandibles into the aperture of the shell and then extracted the operculate soft body using the mandibles. After extraction, the snakes regurgitated the extracted snail and precisely repositioned it so that the operculum protruded out of the mouth and the junction of the operculum and the soft body came to lie along the mandible on the right (n = 24, 80%) or the left (n = 6, 20%) side. From this position, the snakes moved the side of the relevant mandible backward and forward, while the snail was held in the stable position by the upper jaws and the mandible on the other side. These mandibular movements were especially vigorous when the mandible was being retracted. Six to 51 (median, 14) strokes of these sliding movements resulted in the removal of the operculum (Fig. 1, Supplementary Information, Videos S1, S2). Snakes consumed solely the soft part of the snails, while discarding the shell and the operculum (n = 30, 100%). Discarded opercula retained little soft tissue. The duration of extraction, repositioning, and sawing processes ranged 36–274 (median, 96), 9–459 (median, 66), and 15–428 (median, 30) seconds, respectively (Supplementary Information, Table S1). Thus, the snakes spent considerable time for handling of the extracted snail (reposition and sawing). The sequence of feeding was highly consistent among all cases, and the routine operculum-removing behaviour presumably allows A. boa to regularly consume the otherwise hazardous prey, which is abundant in its habitat.

The feeding apparatus of A. boa is illustrated in Fig. 2. Aplopeltura boa exhibits a set of derived morphological features known in other pareids and dipsadines, including short snout, short pterygoids, reduced supratemporals, long mandibles, and comb-like mandibular teeth. The skull of A. boa is short and tall, in which the snout is very short, and the orbits are exceptionally large. The pterygoids are greatly shortened, and their posterior ends are completely detached from the quadrato-mandibular joint. The quadrates are remarkably long and stout, extending ventrally rather than ventrolaterally. The mandibles are long and carry dense teeth, which are more robust than the maxillary teeth. The size and interval of mandibular teeth gradually change along the mandible; the anterior teeth are larger and sparser. The lower jaw unit (the mandible and the quadrate) is L-shaped, and the mandible travels anteroposteriorly when the quadrate swings backward and forward, as anticipated or observed in other pareids or dipsadines. This mechanism enables independent, substantial anteroposterior excursions of the mandible (Fig. 3), which is used for the extraction and the sawing processes during feeding on the operculate snails. The elongated quadrates are likely to contribute to long mandibular excursion¹⁸.

Most of > 3,700 species of snakes swallow their prey whole, and prey-breaking behaviours are known only from a few species that feed either on crabs^20,21,22,23 or termites^24,25,26, which may be relatively easily broken into segments. These snakes grasp their arthropod prey with their jaws and break it apart usually using the movements of the head or the trunk. In contrast, A. boa cuts its mollusk prey using independent movements of the lower jaw. The mandibular sawing is, therefore, a surprising evolutionary solution for the limbless animals to utilize new food. This dexterous behaviour is especially surprising given that few other vertebrates, if any, are able to sever food in the mouth using unilateral sliding movements of a jaw element like A. boa. The evolutionary invention of sawing was evidently made possible by the unique feeding mechanism in the snail-eating snakes. Extensive mobility of the mandibles is a convergent trait in the two distinct lineages of snakes (pareids and dipsadines) that feed on slugs or snails, suggesting it is an adaptation to feeding on their slippery prey^4,5,6,7,8,9. It is likely that acquisition of the free mandibular apparatus promoted the subsequent evolution of the novel behaviour and has resulted in functional versatility of the free-moving jaw elements.

Most pareids and some dipsadines have a larger number of teeth on the right mandible than on the left as feeding specialization to extract dextral (clockwise-coiled) snails^13,15. There is a cline in the degree of the dentitional asymmetry in correlation with diets, where snail-specialist species have highly asymmetrical mandibles, whereas slug-specialist species have symmetrical mandibles^13,15. However, A. boa is an exception of this pattern because individuals exhibit only weak mandibular asymmetry despite its snail diet¹³. In the phylogeny, A. boa is nested within the derived clade with mandibular asymmetry²⁷, suggesting the presence of additional selective forces toward the mandibular symmetry in this species. By showing the additional role of its mandibles (cutting the prey), our results suggest functional trade-offs in A. boa (typical comb-like teeth in snail-eating snakes are expected to facilitate extraction by providing a firm grip on the prey but probably are not optimal to cut the prey tissue), highlighting the importance of behavioural studies to understand selective forces on functional units.