Abstract

Ampullariids are freshwater gastropods bearing a gill and a lung, thus showing different degrees of amphibiousness. In particular, Pomacea canaliculata (Caenogastropoda, Ampullariidae) is an obligate air-breather that relies mainly or solely on the lung for dwelling in poorly oxygenated water, for avoiding predators, while burying in the mud during aestivation, and for oviposition above water level. In this paper, we studied the morphological peculiarities of the gill in this species. We found (1) the gill and lung vasculature and innervation are intimately related, allowing alternation between water and air respiration; (2) the gill epithelium has features typical of a transporting rather than a respiratory epithelium; and (3) the gill has resident granulocytes within intraepithelial spaces that may serve a role for immune defence. Thus, the role in oxygen uptake may be less significant than the roles in ionic/osmotic regulation and immunity. Also, our results provide a morphological background to understand the dependence on aerial respiration of Pomacea canaliculata. Finally, we consider these findings from a functional perspective in the light of the evolution of amphibiousness in the Ampullariidae, and discuss that master regulators may explain the phenotypic convergence of gill structures amongst this molluscan species and those in other phyla.

Highlights

  • Respiratory organs are identified as either gills or lungs, whether they are formed as protrusions or as invaginations of the respiratory mucosae

  • We present a thorough description of the gill of Pomacea canaliculata at the anatomical (3D rendering of its blood system) and ultrastructural levels

  • In Pomacea canaliculata, we found a bundle of thick longitudinal muscle fibres embedded in a dense collagen matrix, which runs along the efferent margin of each gill leaflet.it is a fibromuscular contractile structure and not a skeletal rod as has been suggested by earlier authors

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Summary

Introduction

Respiratory organs are identified as either gills or lungs, whether they are formed as protrusions or as invaginations of the respiratory mucosae. Gills are almost always used for aquatic respiration while lungs are for aerial respiration, but in addition to respiration, these organs may serve other functions (Maina, 2000a, 2002b). In bimodal breathers (i.e. aquatic animals that have retained a gill while developing a respiratory organ for breathing air), the gill may partially lose the respiratory role while. In such cases, the respiratory function is supplied mainly by the air-breathing organ. In bimodal crustaceans and fishes, for example, the dependence on water comes in grades, the lesser water-dependent species having well-developed lungs that take up oxygen from the air and reduced or modified gills for ionic/osmotic regulation and CO2 excretion (Farrelly & Greenaway, 1987; Graham, Lee & Wegner, 2007; Hughes & Morgan, 1973; Innes & Taylor, 1986; Low, Lane & Ip, 1988)

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