Protodrilidae (Annelida: Polychaeta) from the Hawaiian Islands and Comparison with Specimens from French Polynesia

Three species of Protodrilidae were collected from the islands of O‘ahu and Ni‘ihau in the Hawaiian chain, including specimens closely resembling Parenterodrilus taenioides ( Jouin, 1979), described from Mo‘orea (French Polynesia). Others are probably an undescribed species of Parenterodrilus that was found in fine sand substrate collected off Wai‘anae, O‘ahu. A third species, Protodrilus albicans Jouin, 1970, described from Banyuls-sur-Mer (Mediterranean Sea) and recorded from Mo‘orea and Tahiti as well, was also collected from O‘ahu. Depths and habitat characteristics are given for these new records to the Hawaiian fauna. It is suggested that the wide geographical distribution of the different ‘‘cosmopolitan species’’ of Protodrilidae is related both to the dispersal by free-swimming larvae and to the ancient origin of this interstitial fauna. Protodrilidae have long been considered a family of ‘‘Archiannelida’’ due to their small size, ventral ciliary gliding, ventral pharyngeal organ, and lack of conspicuous external segmental structures. Interstitial polychaetes previously called ‘‘archiannelids’’ are now regarded as specialized as opposed to primitive from an evolutionary perspective for Protodrilidae, Protodriloididae, Saccocirridae, Polygordiidae, Nerillidae, Dinophilidae, and Diurodrilidae (Westheide 1985, Purschke and Jouin-Toulmond 1988, Bailey-Brock 1999, Bailey-Brock et al. 2003). Protodrilidae have well-developed sensory structures (Purschke 1990a,b,c, 1993), epidermal glands, epidermal ciliation, and a medioventral ciliary field. In Protodrilidae, Parenterodrilus Jouin, 1992 (Astomus is a synonym), living in coral sands, is unique in having a vestigial nonfunctioning gut, no mouth, no symbiotic bacteria, and a peculiar body shape ( Jouin 1979). The ultrastructure of the cephalic sense organs and central nervous system demonstrates the sister-group relationship to Protodrilus and the derived position of Parenterodrilus (Purschke and JouinToulmond 1993, 1994). The ultrastructure of the ciliated epidermis suggests transepidermal absorption of nutrients ( Jouin 1992). Experiments made on living animals, with ferritin added to the seawater in contact with the animals, demonstrated that after 30 min the epidermis has few subcuticular coated vesicles containing ferritin, this substance being already concentrated in endosomes in the apical part of epidermal cells and in secondary lysosomes more basally ( Jouin-Toulmond 1994). The males of Parenterodrilus taenioides ( Jouin 1979), like Protodrilus species, have lateral organs and sperm ducts, and the ultrastructure of the spermatozoa is basically the same in the two genera ( Jouin-Toulmond and Purschke 2004). Adaptations that facilitate reproduction in Protodrilus include transfer of sperm by spermatophores deposited in Pacific Science (2010), vol. 64, no. 3:463–472 doi: 10.2984/64.3.463 : 2010 by University of Hawai‘i Press All rights reserved 1 Funding for J.H.B.-B. and R.E.B. provided in part by the U.S. Environmental Protection Agency, Environmental Monitoring and Assessment Program for the Hawaiian Islands, 2002–2004. Manuscript accepted 21 August 2009. 2 Zoology Department, University of Hawai‘i at Mānoa, 2538 McCarthy Mall, Honolulu, Hawai‘i 96822. 3 Université Pierre et Marie Curie-Paris 6, CNRSUMR 7144 AD2M Station Biologique, BP 74 29682 Roscoff Cedex, France. 4 Water Resources Research Center, University of Hawai‘i at Mānoa, Honolulu, Hawai‘i 96822. 5 Corresponding author. the external milieu and then collected by the female epidermis and internal fertilization ( Jägersten 1952, Jouin 1970, von Nordheim 1989, 1991a,b, Purschke 2006). The eggs are spawned and attached on sand grains; the larvae have a pelagic life, and metamorphosis depends on the availability of suitable habitat substratum ( Jägersten 1952). Previous records from the Hawaiian Islands include Protodrilus sp. (Bailey-Brock 1987) from the southeast shore of O‘ahu. In this paper, we discuss Protodrilus spp. that were collected on O‘ahu from sewage outfall sites and live specimens from Kawainui Beach Park that were examined briefly in the laboratory but did not survive in aerated shallow containers of sand. Collections of coral sands and reef rubble were made during an extensive coastal Estuarine Monitoring Program (EMAP) initiated by the U.S. Environmental Protection Agency. For comparison, previously unpublished data on specimens collected in French Polynesia ( by C.J.-T.) are presented. materials and methods Sand cores (11 cm diameter, 5 cm deep) were collected by divers, fixed in 10% formalin for 24 hr or longer and elutriated over 0.5 mm and 0.25 mm sieves to extract the infauna. Protodrilids and other polychaetes were retained on the sieves and transferred to ethanol for storage. Parenterodrilus specimens were placed on slides with two drops of glycerol and examined microscopically. Protodrilus specimens were stained with Carmalum and mounted in gelatin-glycerol or in Canada balsam after dehydration. Illustrations were made with the aid of a compound microscope and drawing tube. Only fixed, unrelaxed specimens of Hawaiian material were examined. Hawaiian localities where sand cores containing protodrilids were collected by divers are as follows: Ni‘ihau: Station 1, 21 57.913 0 N, 160 7.428 0 W, located in Keawanui Bay just seaward of a sand beach on the northwestern section of the coast of Ni‘ihau (sediment comprised 50%–60% carbonate sands of medium grain size), collected by EMAP divers on 18 June 2002, at 4.85 m depth. O‘ahu: Two sites were investigated: (1) sewage outfall monitoring stations at Wai‘anae, off the west coast of O‘ahu (sediments comprised mediumto fine-grain carbonate sands), sampled 7–9 June 2004 at depths of 27–33.5 m; (2) Kūhiō Beach, part of an extensive sand beach at Waikı̄kı̄ on the south coast of O‘ahu (clean mediumto fine-grain sands), collected 12 October 2006 and February 2007 at 5 m depth. In French Polynesia, live mature specimens of Protodrilus albicans were collected in coarse sand near the water’s edge of beaches in Mo‘orea (Irioa) and Tahiti (Vairao). They were examined for reproduction: spermatophores, sperm transfer, spawning, and young larvae were observed microscopically in Mo‘orea in July 1981. Specimens studied have been deposited in the Muséum National d’Histoire Naturelle (mnhn) and in J.B.-B.’s personal collection at the University of Hawai‘i.