Occurrence of a bivalve-inhabiting marine hydrozoan (Hydrozoa: Hydroidolina: Leptothecata) in the amber pen-shell Pinna carnea Gmelin, 1791 (Bivalvia: Pteriomorphia: Pinnidae) from Bocas del Toro, Panama

Abstract

Hydroidomedusan polyps are involved in associations ranging from simple epibiosis to strict symbiosis (mutualism and parasitism) with organisms belonging to many animal phyla, including sponges, cnidarians, molluscs, annelids, arthropods (crustaceans), bryozoans, echinoderms, tunicates and vertebrates (fishes) (Gili & Hughes, 1995).Many known symbiotic hydroids are found on mollusc shells, as are the cases of Neoturris pileata (Forsskal, 1775) on Nucula spp. (see Edwards, 1965); Hydractinia angusta Hartlaub, 1904 on Adamussium colbecki (E. A. Smith, 1902) (Cerrano et al., 2000, 2001);Zanclea costata Gegenbaur, 1857 on the three bivalve species Chamelea gallina (Linnaeus, 1758), Cardium sp. and Spisula subtruncata (da Costa, 1778) (Gravili, Boero & Bouillon, 1996; Cerrano, Amoretti & Bavestrello, 1997) and Monobrachium parasitum Mereschkowsky, 1877 on the shells of some Antarctic bivalves (Jarms M both in Leptothecata, Eirenidae (Brinckmann-voss, 1973; Bouillon, 1985; Kubota, 1985, 1992). Polyps of these hydroids attach to soft body parts of the host bivalves (mainly the mantle) and reproduce asexually by budding (Kubota, 1983, 2012; Piraino et al., 1994). The polyp of Eutima releases a medusa with immature gonads, but with a well-developed feeding apparatus comprising long tentacles and a well-differentiated manubrium (Kubota, 1983, 2012). In contrast, the polyp of Eugymnanthea releases a reproductively mature medusoid with a reduced feeding apparatus that has no tentacles and a reduced manubrium (Kubota, 1979). As far as it is known these hydroids do not show strict host specificity, but they do display a certain host preference like Mytilus galloprovincialis Lamarck, 1819, Crenomytilus grayanus (Dunker, 1853) (Cerruti, 1941; Crowell, 1957; Kubota, 1983, 1992; Kubota & Larson, 1990; Rayyan, Photis & Chintiroglou, 2004), Crassostrea gigas (Thunberg, 1793), C. virginica (Gmelin, 1791), C. rhizophorae (Guilding, 1828) (Kubota, 1979, 1983, 2012; Kubota & Larson, 1990), Tivela mactroides (Born, 1778) (Narchi & Hebling, 1975; Migotto, Caobelli & Kubota, 2004), Acanthocardia tuberculata (Linnaeus, 1758), Cerastoderma glaucum (Bruguiere, 1789), Cardites antiquata (Linnaeus, 1758), Ruditapes decussatus (Linnaeus, 1758), Venus verrucosa Linnaeus, 1758 and Arca noae Linnaeus, 1758 (Kubota, 1979, 1983; Piraino et al., 1994). Details of these hydroid-bivalve associations have been reviewed in Kubota (1983, 1987) and Piraino et al. (1994). Although the hydroid-bivalve interaction has been described as parasitic (Cerruti, 1941) it is now thought to be commensalistic (Mattox & Crowell, 1951; Kubota, 1983) or even mutualistic (Rees, 1967; Piraino et al., 1994). The hydroids inhabiting the bivalve mantle cavity benefit from a sheltered environment and from the food transported by the mollusc inner current in exchange for protection against intruders (Rees, 1967). In fact, Piraino et al. (1994) suggest that polyps can feed on trematode sporocysts that infest the bivalve host, causing parasitic castration. However, some species have been associated with deleterious or harmful consequences on commercial shellfish species, i.e. decreased growth and fertility and reduced condition index (i.e. measurement of shellfish overall quality) induced by Eutima japonica Uchida, 1925 in Mizuhopecten yessoensis (Jay, 1857) (Baba et al., 2007) and by Eugymnanthea inquilina Palombi, 1935 in Mytilus galloprovincialis (Rayyan et al., 2004; Mladineo et al., 2012). As a consequence, the occurrence, life cycle and evolution of these symbiotic hydroids have been studied in detail (Kubota, 2000; Bouillon et al., 2004; Migotto et al., 2004; Govindarajan et al., 2005; Cartwright et al., 2008). Nevertheless, to our knowledge, there is no report of these hydroids occurring in the large bivalves of the family Pinnidae. During a field trip conducted to the archipelago of Bocas del Toro, Panama, in March 2012, we observed prevalent occurrence of a hydroid on the gills of an amber penshell, Pinna carnea Gmelin, 1791 (from a total sample of 25 P. carnea; Fig. 1A, B), a common bivalve species in the bays of the archipelago of Bocas del Toro, the Caribbean and nearby Atlantic. These large bivalves are commonly found half or completely buried in mud or sand in seagrass beds (Turner & Rosewater, 1958; Rosewater, 1961; Schultz & Huber, 2013) where they are often encountered with the valves open while they filter feed. Our infected specimen had a thick and large shell, typical of an old individual and it was found semi-buried in coarse sand in a seagrass meadow at a depth of 3 m in Managuar Cay (9.290328–82.189838). The particular large shell of these bivalves allows them to often be used as a substrate for epibionts, including algae, cnidarians, tunicates, sponges, corals, sedentary polychaetes, or other molluscs (bivalves, chitons, gastropods). Many species in the family Pinnidae are also known to host symbionts within their pallial