Quantitative Analysis of the Structure and Function of the Marsupial Gills of the Freshwater Mussel Anodonta cataracta

Abstract

Gravid females of Anodonta cataracta incubate shelled larvae (glochidia) in the water tubes of their outer demibranchs which, in turn, undergo extensive morphological changes in becoming marsupia. In this study, the brooding gills of A. cataracta were compared to the non-marsupial demibranchs of females and the gills of males. Scanning electron microscopy and video enhanced light microscopy were used, and computer-generated 3D-reconstructions of gill tissue were also prepared from light micrographs of serial histological sections. Marsupial gills possess a tripartite system of water tubes that are not present in non-marsupial gills and include two secondary water channels and one primary water tube (brood chamber) containing glochidia. The lateral dimension (width) of water tubes of the marsupial gills increases nearly 30-fold during brooding, but the anterior-posterior length of the tubes is unaffected. No apparent changes in the morphology of the non-marsupial inner demibranchs were observed. Glochidia are effectively isolated from the surrounding water by secondary septa, positioned between the primary and secondary water tubes. Secondary septa are present during brooding and immediately after larval release, but are not in evidence among females during non-reproductive periods. Quantification by 3D reconstruction revealed that, although secondary water tubes are smaller than the primary water tubes of non-marsupial gills and non-gravid marsupial gills, collectively they provide about the same cross-sectional area as the primary water tubes that are lost to water transport by occlusion with glochidia. However, considering the fluid dynamics of the ciliary gill pump, net water transport through the lumina of marsupial gills is reduced to only about 16% of that in non-gravid marsupial demibranchs.