Report of a cohesive gelatinous egg mass produced by a tropical marine bivalve

Gelatinous egg masses are common in a number of animal phyla. However, they are virtually unknown in marine bivalves, with structures that could be thought of as gelatinous egg masses being reported for only five species. We describe the gelatinous egg mass and intracapsular development in the tropical lucinid Phacoides pectinatus. The embryos developed within individual capsules embedded in a large flimsy, spherical mass. Swimming veligers hatch at 198mm shell length. They did not feed, settled within several days of hatching, and metamorphosis was completed within 2 weeks of hatching. Gelatinous egg masses might be detected in members of more lucinid species if studies of development included field or in vivo observations of reproduction in addition to producing embryos by stripping the gonads. Additional key words: Bivalvia, Lucinidae, development, Caribbean, Heterodonta Gelatinous egg masses are thought to confer a number of advantages in aquatic environments. They can provide protection either mechanically; via embedded chemical defenses (Ebel et al. 1999), antibacterial compounds (Benkendorff et al. 2001), or sunscreens (Przeslawski et al. 2004); and from desiccation (Pechenik 1979). In addition, the gel and spacing increases oxygen diffusion between embryos in comparison with clusters of eggs that lack gel (Chaffee & Strathmann 1984; Moran & Woods 2007). The utility of gelatinous egg masses is supported by the fact that they have evolved multiple times among a diversity of animals including arenicolid, nereid, sabellid, and maldanid polychaetes (Strathmann & Strathmann 1989), several families of fishes (Breder & Rosen 1966), and various insects with aquatic development. Gelatinous egg masses are particularly common in molluscs, and are almost ubiquitous among cephalopods and opisthobranch gastropods, in addition to occurring in trochids and members of the caenogastropod littorinid genera Lacuna TURTON, 1827, and Littorina FÉRUSSAC, 1822. In contrast, gelatinous egg masses are rare, if ever, observed in marine bivalves (Miyazaki 1938; Sastry 1979). In most bivalve species, eggs and sperm are released into the water column for external fertilization and embryonic development (Morton et al. 1998), although a number of species brood their developing embryos within the mantle cavity (reviewed in Sastry 1979). In an extensive review of marine bivalve development, Sastry (1979; see also Sellmer 1967) listed eight species that have been shown to produce eggs with gelatinous coverings or external capsules, and a few additional records are available in the literature. These can be broken down into two categories: those that release eggs with individual gelatinous coverings, which may or may not stick together, and those that form more cohesive masses. Eggs with gelatinous egg coverings are not uncommon among bivalves, and seem to be most common at high latitudes. Ockelmann (1958) listed eight species of marine bivalves from Greenland, whose members produce eggs with a mucous covering and an adhesive membrane. He mentioned the possibility that these bivalves attach the eggs to the substrate, but it is doubtful that they result in the production of any kind of cohesive mass. These species belong to the families Astartidae [Astarte borealis (SCHUMACHER, 1817), Astarte crenata (GRAY, 1824), Astarte elliptica (BROWN, 1827), Astarte montagui (DILLWYN, 1817), Astarte sulcata (DA COSTA, 1778)] and Tellinidae [Macoma loveni (JENSEN, 1905), Macoma moesta DESHAYES, 1855, Macoma torelli (JENSEN, 1905)]. Egg membranes of some thickness have also been reported for the cardiid species Ciliatocardium ciliatum (O. FABRICIUS, 1780) and several anomalodesmatans, Invertebrate Biology 129(2): 165–171. 2010, No claim to U.S. government works Journal compilation r 2010, The American Microscopical Society, Inc. DOI: 10.1111/j.1744-7410.2010.00188.x Author for correspondence. E-mail: [email protected] including the laternulid Laternula elliptica (KING & BRODERIP, 1831) (Ansell & Harvey 1997), although these are not thought to attach to the substrate. Likewise, the typical ‘‘veneracean’’ eggs, described by Ockelmann (1964) as possessing a well-developed gelatinous envelope around a vitellus, are not reported to adhere to each other or to the substrate. In two cases, however, Musculus discors (LINNAEUS, 1767) and Musculus niger (J.E. GRAY, 1824) adults were reported to spawn gelatinous egg strings that attach to the substrate (Ockelmann 1958:238–239; Thorson 1935). Finally, the protobranchs Solemya velum SAY, 1822, and Solemya reidi BERNARD, 1980, produce individual adhesive capsules that are deposited on the substrate (Gustafson & Reid 1986; Gustafson & Lutz 1992). External egg masses have only been reported for five species of marine bivalves. The special egg sac in the protobranch Nucula delphinodonta MIGHELS & C.B. ADAMS, 1842 is composed of a mucus-like material, probably secreted by the hypobranchial gland, mixed with foreign bodies, and attached to the posterior ends of the valves of the shell (Drew 1901). So far, no other protobranchiate bivalves have been reported to reproduce in this manner (Zardus 2002). In Turtonia minuta (FABRICIUS, 1780), the mantle margin secretes an egg capsule attached to the byssus, containing ten to 20 eggs (Oldfield 1955; Jeffreys 1863; Ockelmann 1964). Other authors have reported the same species producing two to six eggs in each capsule, which is then attached to stones and algae (Matveeva 1953). In addition, Ockelmann (1964) observed 13 females that each had one to four egg capsules attached to the byssus, and each capsule contained one to 16 embryos. Lovén (1848) reported the spawning in the cardiid Parvicardium exiguum (GMELIN, 1791) in the summer months near the coast of Bohuslän (Sweden). The eggs are laid enclosed in a ‘‘thick gelatinous mantle,’’ within which the development progresses until the shell-bearing veliger has attained a length of 90mm (J^rgensen 1946). An egg capsule has also been reported for the lucinid Loripes lacteus (LINNAEUS, 1758) (Pelseneer 1926; Lebour 1938). Pelseneer (1926) reports that this species deposits stalked egg capsules on the sand and these are figured to contain numerous eggs. However, Miyazaki (1938) claims that Guiart suggests, contrary to Pelseneer’s report, that the egg mass is cast freely into the water column and not deposited onto a substratum. Finally, the semelid Abra tenuis (MONTAGU, 1803) produces eggs enclosed in sticky gelatinous envelopes, which are laid in a gelatinous mass within the sediment (Gibbs 1984: fig. 4C). It seems that in this case, fertilization may occur in the mantle cavity of the female, followed by extrusion of the eggs in an external mass. The few accounts of egg masses in marine bivalves suggest that this is a rare form of reproduction in the group. The details of the reported cases remain vague as most reports were incidental and only one report of a gelatinous mass from a bivalve has been published since the 1960s. Here, we provide details on the first known cohesive gelatinous egg mass, produced by a tropical lucinid.