The Functional Morphology of Atlantic Deep Water Species of the Families Cuspidariidae and Poromyidae (Bivalvia): An Analysis of the Evolution of the Septibranch Condition
Anatomical studies show that three families, Verticordiidae, Poromyidae and Cuspidariidae, have many features in common. All are carnivores, have similar digestive systems, and have a horizontal septum dividing the mantle into infra- and supraseptal cavities. This partition is developed to different degrees in the different families. In the Verticordiidae the reduced gill is connected by a membrane to the body mantle and intersiphonal septum. The species rely mainly on ciliary currents for respiration and water change. In the Cuspidariidae, there is a thick, muscular sheet which in the most specialized species is pierced by only four pairs of pores. Regular pumping movements change the water in the mantle cavities. Because of their obvious relation, the three families are combined within the suborder Septibranchia, of the order Anomalodesmata (Bivalvia). On the basis of this study the Verticordiidae and Poromyidae are more closely related to one another than either is to the Cuspidariidae. This is demonstrated by the differences in the siphon structure and reproductive systems. The first two families are hermaphrodite, short-siphoned, have a large forward projecting valve at the base of the inhalant siphon, and bear 13 or 15 short tapering tentacles around the siphonal apertures. The Cuspidariidae are dioecious, long-siphoned, the inhalant aperture being sealed internally by a simple vertical sheet pierced by a keyhole slit, and consistently have three dorsal exhalant tentacles and four ventral inhalant tentacles. In the past, the taxonomy of the family Cuspidariidae has been based solely on hinge characteristics. This study, on the basis of gross morphological differences, identifies three genera: Cuspidaria, Halonympha and a new genus, Protocuspidaria. Subdivisions of these genera continue to be based on hinge characters, there being few anatomical differences. Protocuspidaria, Halonympha and Cuspidaria form a series in the development of the septum from a reduced eulamellibranch gill to the typical muscular septum of the genus Cuspidaria. This involves a vast increase in musculature with the development of dorsal attachments of these muscles onto the shell. Associated with this development is a decrease in the size of the palps and an increase in the rostral length of the shell. The septum in both the Poromyidae and Cuspidariidae contains five pairs of muscles; the anterior and posterior septal muscles, the inner and outer longitudinal septal muscles and the lateral septal muscles. These muscles lie between two epithelial layers which are continuous with those of the mantle and the viscera. In the Poromyidae, the septum is already very muscular and pierced by two (Poromya) or three (Cetoconcha) pairs of grouped branchial apertures. In the Cuspidariidae, while there is a progressive increase in the musculature of the septum, the branchial apertures are always set in a single series on either side of the foot. Studies on the comparative morphology of the families, particularly of the nervous systems and musculature, show that the septum is developed mainly from the gill. Except for Cetoconcha, where a few filaments of the outer demibranch persist posteriorly and form the third posterior group of branchial apertures, the openings in the septum are derived from the descending lamella of the inner demibranch. The musculature is mainly derived from that of the inner demibranch. A reduced gill becomes connected via a membrane, laterally to the mantle, anteriorly to the margin of the mouth, posteriorly to the intersiphonal septum and medially to the foot. The anterior septal muscle of the Poromyidae and Cuspidariidae is homologous with the axial muscle of eulamellibranch bivalves. This enlarges, extends forward and, in all but Protocuspidaria, makes an anterior dorsal attachment on the shell. The posterior septal muscle is derived by an increase, fusion and extension of the longitudinal filamentar muscles of several posterior gill filaments of the outer demibranch. This, in all but the more `primitive' genera (Protocuspidaria and Halonympha), also makes a posterior dorsal attachment. The increase and modification of the longitudinal filamentar muscles of the inner demibranch gives rise to the bulk of the septum, forming the lateral septal muscles and the pore-closing mechanism. Pallial muscle along the lateral margin of the septum probably gives rise to the outer longitudinal septal muscle. There is also firm evidence that the inner longitudinal muscle, which provides the seal around the foot, is pedally derived. The Verticordiidae, Poromyidae and Cuspidariidae have a specialized carnivorous habit. In the Verticordiidae food capture is by trapping of passing prey on sticky tentacles, while in the Cuspidariidae feeding involves active use of the muscular pumping septum to suck in the prey detected by the sensory tentacles. In the Poromyidae, however, the seal is incomplete posterior to the foot, and the pumping mechanism is possibly not as efficient as it is in the Cuspidariidae, but neither are the tentacles sticky as they are in the Verticordiidae. It therefore seems likely that they utilize a pumping action that is supplemented by ciliary action for both respiration and drawing in food.