Comparative morphology and ultrastructure of the respiratory system in four species of the Opheliidae family

Abstract

Polychaetes show a remarkable diversity of the respiratory system structures. However, the ultrastructure of gills was studied only in some species from several families. The morphology and ultrastructure of the gills of Ophelia limacina, Ophelina acuminata, Euzonus arcticus, and Travisia forbesii (Opheliidae) were studied using light microscopy, scanning electron microscopy, and transmission electron microscopy. Gills could be interpreted as body wall protrusions containing coelom, blood lacunas, or vessels connected to interepithelial blood sinuses. The blood is separated from the environment by a 1.5-μm thick wall in E. arcticus, 2-μm in O. limacine and T. forbesii, and 3-μm in O. acuminata, which is close to the minimum observed in the polychaetes; it refers to the effective gas exchange. Unlike the other species, the gill surface lacks cilia in T. forbesii. This might be explained by the fact that the body of T. forbesii is covered with a thick layer of mucus making cilia inefficient and leading to their reduction. The cuticle of the gills is thin; its structure in O. acuminata, O. limacina, and E. arcticus resembles the cuticle covering the other part of the body. In T. forbesii, the gills are covered with a protocuticle close to that in larval forms of polychaetes. The epidermal cells of gills are different in form in all four species studied. The epithelial cells in E. arcticus have few organelles, but contain numerous vacuoles, which represent a low level of synthesis. Therefore, they are likely to have a support function. The epithelium in O. limacina, O. acuminata, and E. arcticus has multiple gland cells, while T. forbesii does not have any. The gills of O. acuminata contain glands of two types, while O. limacine and E. arcticus have only one type of gill gland. The epidermal cells in T. forbesii are connected by desmosomes, while in the other three species, they also have dense junctions, and even adhesive belts in O. limacina and E. arcticus. The coelom is lined with mioepithelium, and in E. arcticus, together with podocites. Blood cells of O. limacina, O. acuminata, and E. arcticus were found for the first time, while in O. limacina, amoebocytes form an incomplete endothelium on basal lamina. The gills of T. forbesii differ from those of the other three Opheliid species in anatomy and some ultrastructural features. These data together with the results of recent molecular studies could be one more reason to exclude Travisia from Opheliidae. Furthermore, several common anatomic and ultrastructural features of O. limacina, O. acuminata, and E. arcticus could serve as a synapomorphy of the family Opheliidae. However, further anatomical and ultrastructural investigations are necessary before we can use this character for phylogenetic analysis.