Unusual modes of oogenesis and brooding in bivalves: the case of Gaimardia trapesina (Mollusca: Gaimardiidae)

Abstract

Abstract. I describe an unusual case of follicular oogenesis in a bivalve, Gaimardia trapesina, a common marine bivalve from the Magellan Region and adjacent Sub‐Antarctic waters, whose members brood their developing larvae. The gonad in G. trapesina is an acinus organ that infiltrates the perivisceral connective tissue; the walls of the acini are formed by tall, slender cells with distal nuclei, supported by a thin conjunctive tissue layer. At the onset of vitellogenesis, each developing oocyte becomes surrounded by a one‐cell‐thick layer of follicle cells, which may originate from the wall of the acinus. The cells form a follicle that completely encompasses single oocytes, except at the basal zone, where oocytes are in contact with the acinus wall. The follicle persists beyond the end of vitellogenesis and spawning. After gamete release, the persistent follicle participates in the attachment of ova and developing embryos to the interfilamental junctions of the inner and outer demibranchs of the gill, where embryos are incubated until hatching as late‐stage pediveliger larvae. Ripe eggs are large (∼250 μm diameter), suggesting that development is entirely lecithotrophic. The follicle cells that mediate connections between developing embryos and the maternal individual probably have a mechanical role only, providing support and possibly facilitating the accommodation of a large number of embryos to maximize the branchial space available for brooding.

Embryo brooding and its effect on feeding in the bivalve Gaimardia bahamondei Osorio & Arnaud, 1984

“…The large size of the oocytes of G. bahamondei and the lack of evidence for microalgae ingestion by embryos indicate that development in this species is lecithotrophic. In the congeneric species G. trapezina there is a cell layer that envelops the entire oocyte and also gives rise to the peduncle which attaches the embryo to the gill tissue [22]. This layer remains in place throughout the entire incubation period and appears to form a barrier to the entry and ingestion of exogenous food particles.…”

“…Each embryo is attached to the abfrontal region of the branchial filament by means of a peduncle [13,22]. The gill is homorhabdic and the inner demibranch is larger than the external one; embryos are attached to both [13].…”

“…In bivalves, the brooding habit is usually associated with low fecundity and large eggs [27] and the embryos are confined within the pallial cavity of the brooding adult, usually in the branchial region, e.g. Neogaimardia finlayi [32], Nutricola tantilla (=Transennella tantilla) [24,25], Kingiella chilenica [17], Sphaerium striatinum [5], Gaimardia trapezina [22], Adacnarca nitens [21], Mysella charcoti and M. narchii [38], Neolepton salmoneum [33]. In some species, the embryos can move freely within the female's mantle cavity during brooding [29,34].…”

Reproductive strategy of the semelparous clam Gaimardia bahamondei (Bivalvia, Gaimardiidae)

“…In certain bivalve species, the embryos being brooded can move freely between the mother's branchial lamellae (Nelson 1946;Chaparro et al 1993). In many cases, the embryos being brooded are restricted to enclosed areas, specialized structures, brooded in masses, or attached to maternal tissue while they develop, hindering their mobility during this phase (Morton 1977;Bartlett 1979;Richardson 1979;Mackie 1984;Beauchamp 1986;Russell & Huelsenbeck 1989;Richard et al 1991;Tankersley & Dimock 1992;Schwartz & Dimock 2001;Ituarte 2009).…”

“…In certain species of bivalve molluscs, brooding occurs in the mother's infrabranchial region (e.g., Ostrea chilensis PHILIPPI 1845: Chaparro et al 1999;Ostrea edulis LINNAEUS 1758: Waller 1981Ostrea circumpicta PILSBRY 1904: Kang et al 2004. However, there are many cases in which embryos are brooded within the suprabranchial region or the interior of the tubes through which the water circulates (Silverman et al 1987;Tankersley & Dimock 1992;Schwartz & Dimock 2001;Ituarte 2009;Passos & Domaneschi 2009). Despite the potential benefit of oxygen availability to embryos, internal brooding may impose various costs to the mother, from a reduction in feeding activities and an increase in the use of refuge (Chaparro & Thompson 1998;Pardo & Johnson 2006) to the adoption of drastic reproductive strategies such as semelparity, which has been identified in some brooding microbivalves (e.g., Kingiella chilenica SOOT RYEN 1959: Gallardo 1993; Nutricola tantilla (GOULD 1853): Kabat 1985; Pisidium sp.…”