Dataset Information

Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes.

ABSTRACT:

Background

Efficient venom delivery systems are known to occur only in varanoid lizards and advanced colubroidean snakes among squamate reptiles. Although components of these venomous systems might have been present in a common ancestor, the two lineages independently evolved strikingly different venom gland systems. In snakes, venom is produced exclusively by serous glands in the upper jaw. Within the colubroidean radiation, lower jaw seromucous infralabial glands are known only in two distinct lineages-the basal pareatids and the more advanced Neotropical dipsadines known as "goo-eating snakes". Goo-eaters are a highly diversified, ecologically specialized clade that feeds exclusively on invertebrates (e.g., gastropod molluscs and annelids). Their evolutionary success has been attributed to their peculiar feeding strategies, which remain surprisingly poorly understood. More specifically, it has long been thought that the more derived Dipsadini genera Dipsas and Sibynomorphus use glandular toxins secreted by their infralabial glands to extract snails from their shells.

Results

Here, we report the presence in the tribe Dipsadini of a novel lower jaw protein-secreting delivery system effected by a gland that is not functionally related to adjacent teeth, but rather opens loosely on the oral epithelium near the tip of the mandible, suggesting that its secretion is not injected into the prey as a form of envenomation but rather helps control the mucus and assists in the ingestion of their highly viscous preys. A similar protein-secreting system is also present in the goo-eating genus Geophis and may share the same adaptive purpose as that hypothesized for Dipsadini. Our phylogenetic hypothesis suggests that the acquisition of a seromucous infralabial gland represents a uniquely derived trait of the goo-eating clade that evolved independently twice within the group as a functionally complex protein-secreting delivery system.

Conclusions

The acquisition by snail-eating snakes of such a complex protein-secreting system suggests that the secretion from the hypertrophied infralabial glands of goo-eating snakes may have a fundamental role in mucus control and prey transport rather than envenomation of prey. Evolution of a functional secretory system that combines a solution for mucus control and transport of viscous preys is here thought to underlie the successful radiation of goo-eating snakes.

SUBMITTER: Zaher H

PROVIDER: S-EPMC4021269 | biostudies-literature | 2014 Mar

REPOSITORIES: biostudies-literature

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Publications

Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes.

Zaher Hussam H de Oliveira Leonardo L Grazziotin Felipe G FG Campagner Michelle M Jared Carlos C Antoniazzi Marta M MM Prudente Ana L AL

BMC evolutionary biology 20140325

<h4>Background</h4>Efficient venom delivery systems are known to occur only in varanoid lizards and advanced colubroidean snakes among squamate reptiles. Although components of these venomous systems might have been present in a common ancestor, the two lineages independently evolved strikingly different venom gland systems. In snakes, venom is produced exclusively by serous glands in the upper jaw. Within the colubroidean radiation, lower jaw seromucous infralabial glands are known only in two ...[more]

PMID: 24661572

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Project description:Quantifying the performance of animals is a powerful methodology for determining the functional consequences of morphological variation. For example, snakes consume prey whole, and variation in the anatomy of their trophic apparatus directly affects gape and limits maximal prey size. However, for the foraging ecology of snakes and other systems, scant data exist regarding how often maximal capacities are taxed in nature. Hence, we quantified: (1) maximal gape, (2) the size of prey relative to maximal gape, and (3) how the type and relative size of prey affected behavior and prey handling times (HTs) for two species of natricine snakes that primarily eat soft- (Regina septemvittata) or hard-shelled (Liodytes alleni) crayfish. Liodytes alleni had significantly larger maximal gape than R. septemvittata with equal snout-vent length. The percentages of large prey (>60% maximal gape area) consumed in the field were low in both R. septemvittata (22%) and L. alleni (2%). However, R. septemvittata, especially juveniles, ate relatively larger prey than L. alleni. Strategies for dealing with the seasonal scarcity of small crayfish differed as juvenile R. septemvittata commonly removed and ate only chelipeds from crayfish too large to swallow whole, whereas juvenile L. alleni ate many small odonate nymphs. During laboratory trials, unlike R. septemvittata, L. alleni usually used its body to restrain prey with behaviors that depended on relative prey size and prey hardness. Liodytes alleni consumed soft-shelled crayfish significantly faster than R. septemvittata and significantly faster than hard-shelled crayfish. Several of the differences in gape, prey size, and prey HTs and behavior between the crayfish-eating snakes resemble those between two phylogenetically distant species of homalopsid snakes that consume either hard- or soft-shelled crabs. In both groups of crustacean-eating snakes, the decreased capture success in captivity and the rare consumption of relatively large hard-shelled crustaceans in the field suggest that the ability to capture this type of prey constrains prey size more commonly than maximal gape. Based on data integrating snake size and gape with the relative mass of intact prey, the predicted potential feeding performance R. septemvittata consuming intact prey exceeded that of the other three species.

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Dataset Information

Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes.

Background

Results

Conclusions

Publications

Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes.

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