Morphological grounds for the obligate aerial respiration of an aquatic snail: Functional and evolutionary perspectives

RODRIGUEZ, CRISTIAN; PRIETO, GUIDO I.; VEGA, ISRAEL A; CASTRO VAZQUEZ, ALFREDO JUAN

PeerJ

PeerJ, Inc

Año: 2020 vol. 9 p. 10763 - 10763

2167-8359

The freshwater caenogastropod family Ampullariidae is emerging as a model for avariety of studies, among them, the evolution of terrestriality. A common character ofthe family is that they all bear a lung, while they retain the ancestral gill. This ensuresthat many ampullariids are able to inhabit poorly oxygenated waters, to bury inthe mud during estivation, and to temporarily leave the water, in some speciesfor oviposition. To these characters Pomacea canaliculata (Caenogastropoda,Ampullariidae) adds that is, an obligate air-breather. In a recent paper, we showedthe gill epithelium has a set of characteristics that suggest its role for oxygen uptakemay be less significant than its role in ionic/osmotic regulation and immunity.We complement here our morphological investigation on the respiratoryorgans in P. canaliculata by studying the lung of this species at the anatomical(3D reconstructions of the blood system and nerve supply), histological andultrastructural levels. The circulation of the gill and the lung are interconnectedso that the effluence of blood from the gill goes to the lung where it completesoxygenation. Besides that, we found the lung cavity is lined by a pavement epitheliumthat encloses an anastomosing network of small blood spaces resting over afibromuscular layer, which altogether form the respiratory lamina. The pavementcells form a blood-gas barrier that is, 80?150 nm thick and thus fulfils therequirements for an efficient gas exchanger. Tufts of ciliary cells, together withsome microvillar and secretory cells, are interspersed in the respiratory lamina.Rhogocytes, which have been proposed to partake in metal depuration and in thesynthesis of hemocyanin in other gastropods, were found below the respiratorylamina, in close association with the storage cell tissue. In light of these findings,we also discuss the functional role of the lung in P. canaliculata and compare it withthat of other gastropods. Finally, we point to some possible similarities in the patternof evolution of air dependence in this family.