Divergent Shell Shape as an Antipredator Adaptation in Tropical Land Snails

Abstract

Although many land snails exhibit amazingly divergent shell shapes in the tropics, the functions of these remain obscure. Here we show that a modified aperture shape acts as an impediment specifically to predation by a snail-eating snake. Pareas iwasakii (Colubridae: Pareatinae) uses a unique method to feed on land snails: the snake extracts the soft body from the shell through the aperture by alternately retracting its mandibles. The snail Satsuma caliginosa (Camaenidae: Camaeninae) has apertural variation in regard to the presence of snail-eating snakes. Our experiments demonstrated that the distorted aperture mechanically impeded predation by this gape-limited predator, interrupting the mandibular movements. In contrast, congeneric snails with round apertures did not escape predation by snakes. The paleobiogeography of the focal area indicates that the subspecies Satsuma caliginosa picta, which does not have apertural modification, was derived from a defensive ancestor after the extinction of snail-eating snakes. Our study suggests a possibility that snail-eating snakes are responsible for divergent shell shapes in a variety of tropical land snails.

A speciation gene for left–right reversal in snails results in anti-predator adaptation

“…Therefore, our results are consistent with the hypothesis that 'right-handed' snake predation drives snail speciation by left–right reversal. Further experimental studies may be desired to examine the effect of shell shape on the snake's predation success27.…”

“…As a test case, we examined the molecular phylogeny of the genus Satsuma , which includes multiple dextral and sinistral species in the snake range. In natural conditions, P. iwasakii preys on dextral species of Satsuma 28, which exhibit defensive aperture morphology against snake predation27. Thus, Satsuma snails have probably been subject to severe snake predation.…”

Cost of autotomy drives ontogenetic switching of anti-predator mechanisms under developmental constraints in a land snail

“…Together with the field observations of mature snails with a regenerated foot, capability of autotomy probably contributes to higher fitness after being attacked by the snakes. Snake predation is an important selective agent for shell traits of the snail genus Satsuma [37], especially of S. c. caliginosa [12]. Thus, the capacity for autotomy by S. c. caliginosa is probably a product of adaptive evolution against snake predation.…”

“…To mechanically impede the enemies' attacks, some snails enclose or thicken their apertures by modifying the growth pattern of their shells [4,11,12]. However, especially in terrestrial pulmonates except a few taxa such as Streptaxidae, modified apertures are available as anti-predator devices only when the snails are mature [13], because of the developmental constraints from the additive growth of the shells.…”

Reclassification of Oligodon ningshaanensis Yuan, 1983 (Ophidia: Colubridae) into a New Genus, Stichophanes gen. nov. with Description on Its Malacophagous Behavior

“…Although all genera mentioned above include species able to hunt slugs, preying on snails is not handled by all of them. The exclusive snail-eater Pareas developed high specialization on extracting the snail from the gastropod helical shell (Gotz, 2002;Hoso and Hori, 2008;Hoso et al, 2007). In the Dipsadinae, inserting mandibles are also employed by Dipsas (Gans, 1975;Peters, 1960;Sazima, 1989) and Sibynomorphus (Agudo-Padrón, 2013;LaportaFerreira and Salomão, 2004), but the morphological and behavioral asymmetry in Pareatidae for efficient handling dextral shell has not been documented.…”