A Vermetid Gastropod with Complex Intracapsular Cannibalism of Nurse Eggs and Sibling Larvae and a High Potential for Invasion

A vermetid gastropod, previously unreported from the Pacific Ocean, was found at O‘ahu, Hawai‘i, in aquariums at the Kewalo Marine Laboratory, in fouling communities on docks, and on intertidal and shallow subtidal coral rubble. It also occurs on coral rubble in Florida. Eggs, or nurse eggs, and early embryos are about 100 mm in diameter. Young are brooded in 1–13 stalked capsules attached inside the tubular shell. Intracapsular development involves an unusual complex adelphophagy (sibling cannibalism). Most eggs are nondeveloping nurse eggs. Ten to 20 eggs develop into apparently normal small veligers. Of these most arrest as small veligers, but a few grow to hatch as large pediveligers or juveniles. The species has a high potential for invasion and establishment following maritime transport or natural rafting. Protected intracapsular development ends with the release of crawling hatchlings that also produce mucous threads on which they can drift. Juveniles settle readily on hard substrata. An apparent rarity or absence of males suggests long-term sperm storage, hermaphroditism, or parthenogenesis, any of which could aid colonization. Adults and juveniles occur in fouling communities and can survive extended periods in still seawater and at low food levels. The species’ global distribution and history of invasions are unknown. We predict widespread distribution and invasions in warm waters. The small vermetid gastropod described here was recognized in 1970 on the walls of outdoor aquariums at the Kewalo Marine Laboratory in Honolulu (M. Hadfield, pers. comm.). They were very small specimens that were brooding capsules attached to the inside of the tube. Hadfield noted that the developmental mode differed from any described for gastropods in that more than one size of veliger was present in the capsules. Here we describe this unusual form of adelphophagy (sibling cannibalism), which involves intracapsular feeding on both nurse eggs and small but well-formed sibling veligers. Many animals have encapsulated larvae that feed on nurse eggs (ova or arrested embryos) or abnormal embryos, but it is extremely rare for capsules to include nondeveloping nurse eggs, well-formed larvae arrested at an early stage, and siblings that complete development. A similar mix of undeveloped nurse eggs and arrested but normal siblings has been described from encapsulated development of some spionid annelids (Blake and Kudenov 1981, Gibson 1997, Duchene 2000, Gibson and Gibson 2004). To our knowledge, such development is previously unreported for gastropods. The species is also of interest because it possesses traits that confer a high potential for invasion by maritime transport and subsequent establishment of populations. We found small vermetid specimens with identical adult morphology and reproductive traits on the Atlantic coast of Florida. The species may be widespread in warm marine waters. We therefore include here a description of traits Pacific Science (2006), vol. 60, no. 1:97–108 : 2006 by University of Hawai‘i Press All rights reserved 1 This research was supported by NSF grant IBN0113603 to R.R.S., ONR Award N00014-03-1-0078 to M. G. Hadfield, the Kewalo Marine Laboratory, the Smithsonian Marine Station, and the Friday Harbor Laboratories. Manuscript accepted 28 February 2005. 2 Friday Harbor Laboratories, University of Washington, 620 University Road, Friday Harbor, Washington 98250. (Correspondence to R. R. Strathmann, email: [email protected]). visible in live adults that will aid recognition of the species wherever it is found. We could not assign this vermetid to a known species with certainty, though it resembles a species that Bieler (1995) found in the Azores, which in turn resembles Thylaeodus rugulosus (Monterosato, 1878), a species originally described from the Mediterranean. Assignment to a genus is also uncertain because of ongoing taxonomic revisions concerning vermetids (R. Bieler and T. Rawlings, pers. comm.). In the meantime, we refer to this gastropod as Hadfield’s vermetid, because M. Hadfield (pers. comm.) first recognized its unusual adelphophagy. materials and methods Specimens were collected on O‘ahu, Hawai‘i, from aquariums at Kewalo Marine Laboratory (KML), situated at the channel opening of Kewalo Basin (February to March 1995 and January to March 2002), from racks submerged for a fouling study at Ford Island in Pearl Harbor (February to March 2002 and March 2003), from floating docks at Rainbow Marina in East Loch of Pearl Harbor (March 2003), and from intertidal and shallow subtidal coral rubble at the base of a seawall at Kewalo Park, Honolulu, and shoreward of a reef opening at Kualoa Park at the north end of Kāne‘ohe Bay (March 2003). We examined more than 150 living specimens from O‘ahu during spring months. Colleagues examined additional specimens for reproductive state in August and November 2002. We also collected two brooding adults on shallow rubble at Peanut Island, Florida, in May 2003. Adult snails were freed from their tubes by breaking the shell and severing the columellar muscle. Some voucher specimens were relaxed with MgCl2, transferred to 4% formaldehyde (10% V/V formalin in filtered seawater), then transferred to 70% ethanol. Other voucher specimens were preserved directly in 80 to 100% ethanol. Voucher specimens (collected at Ford Island, Pearl Harbor, Hawai‘i) are at the Bernice P. Bishop Museum, Honolulu, Hawai‘i. One whole specimen (Accession No. 2002.053, bpbm catalog no. 264015) has the underside of one whorl broken open; the living specimen visible inside had typical mantle coloration and possibly a dorsal mantle cleft. A brooding adult specimen (bpbm cat. no. 264016) was removed from its shell and preserved with three of the five capsules of the brood. Other specimens were deposited as bpbm catalog numbers 264017 to 264031. From a few specimens, opercula and radulae were excised, cleaned of soft tissue by brief treatment with 3% sodium hypochlorite followed by a distilled water rinse, and mounted in water on slides for microscopy or photography. For observation of in vitro development, brood capsules, some with the stalk attached to a piece of shell, were transferred to small plastic petri dishes containing seawater that had been filtered (0.5 mm), microwave-heated to just below boiling, cooled overnight, and aerated by swirling. Water was changed daily.