Fauna of Whale Falls: Systematics and Ecology of a New Polychaete (Annelida: Chrysopetalidae) from the Deep Pacific Ocean$
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ARTICLE IN PRESS Deep-Sea Research I 51 (2004) 1873–1887 www.elsevier.com/locate/dsr Fauna of whale falls: systematics and ecology of a new polychaete (Annelida: Chrysopetalidae) from the deep Pacific Ocean$ Thomas G. Dahlgrena,Ã, Adrian G. Gloverb,c, AmyBaco d, Craig R. Smithb aTja¨rno¨ Marine Biological Laboratory, 452 96 Stro¨mstad, Sweden bDepartment of Oceanography, University of Hawaii, 1000 Pope Rd, Honolulu, HI 96822, USA cZoology Department, The Natural History Museum, Cromwell Rd, London SW7 5BD, UK dWoods Hole Oceanographic Institution, Biology Department, MS 33, Woods Hole, MA 02543, USA Received 29 July2003; received in revised form 26 July2004; accepted 28 July2004 Available online 12 October 2004 Abstract Vigtorniella flokati, a new species of polychaete worm associated with decaying whale remains, is described. Three separate V. flokati populations were sampled using submersibles: two associated with implanted graywhale carcasses in the San Diego Trough (1240 m depth) and the Santa Cruz Basin (1670 m) off California, and one from sperm whale and balaeanopterid bones implanted on the slope of Oahu, Hawaii at 1000 m. Extraordinarilylarge numbers of live specimens were observed and videotaped in situ using submersibles in the San Diego Trough and the Santa Cruz Basin. The populations on the carcass implanted for 4 months in San Diego Trough, and on the bones implanted for 2 years off Oahu, were composed onlyof small sized individuals (including juveniles). V. flokati most closelyresembles the poorlyknown V. zaikai Kiseleva, 1992, described from the Black Sea. Forty-six morphological characters were used in a phylogenetic analysis of selected nereidiform polychaetes. The resulting most-parsimonious trees indicate sister taxon status between V. flokati and V. zaikai, and that this clade is sister to the putativelyancient polychaeteclade Chrysopetalidae. Whale falls, which are intense point sources of organic enrichment at the deep-sea floor, pass through three successional stages. V. flokati appears to colonize the middle, ‘‘enrichment opportunist’’ stage, inhabiting organic- rich bones and sediments 4–24 months after carcass arrival. V. flokati exhibits remarkable behavior, clinging posteriorlyto whale bones or nearbysediments to form a writhing carpet at densities exceeding 8000 m À2. Its extraordinaryabundance on whale falls, and apparent absence from other habitats, suggests it to be a whale-fall specialist. The precise feeding mechanism of the worm remains unknown, but we hypothesize that it may utilize dissolved organic carbon derived from the organic-rich setting of whale falls. The widespread occurrence of V. flokati $The first and second authors contributed equallyto the research and data interpretation. Dahlgren is listed first because he took the lead in writing the paper. ÃCorresponding author. Tel.: +46-526-68682; fax: +46-526-68607. E-mail address: [email protected] (T.G. Dahlgren). 0967-0637/$ - see front matter r 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2004.07.017 ARTICLE IN PRESS 1874 T.G. Dahlgren et al. / Deep-Sea Research I 51 (2004) 1873–1887 on ephemeral, food-rich habitat islands in the Pacific suggests life-historystrategies analogous to those for hydrothermal-vent and cold-seep species. r 2004 Elsevier Ltd. All rights reserved. Keywords: Polychaeta; Chrysopetalidae; Whale fall; Organic enrichment; Opportunist; Succession; Santa Cruz Basin; San Diego Trough; Hawaii; Pacific Ocean; Deep sea 1. Introduction bathymodiolin mussels and vestimentiferan poly- chaetes (Bennett et al., 1994; Baco et al., 1999; The discoveryof a chemoautotrophic faunal Distel et al., 2000; Smith and Baco, 2003). assemblage on a lipid-rich whale skeleton (Smith During both the opportunist and chemoauto- et al., 1989) has spurred the studyof whale falls as trophic stages, whale falls also harbor a number intense point sources of organic enrichment at the of potentiallyendemic species ( Smith and Baco, deep-ocean floor. Recent investigations have 2003). examined their significance in both ecological Although the species diversityof these assem- (Bennett et al., 1994; Naganuma et al., 1996; blages has been well documented using operational Deming et al., 1997; Smith et al., 1998, 2002; Smith taxonomic units (Ampharetidae sp. A, etc.; Baco and Baco, 2003) and evolutionary( Goedert et al., and Smith, 2003; Smith and Baco, 2003), much of 1995; Feldman et al., 1998; Smith and Baco, 1998, the whale-fall fauna remains undescribed, inhibit- 2003; Baco et al., 1999) terms. Ecological research, ing further research into the autecologyand through experimental implantation, indicates that functional significance of the remarkable whale- fresh whale falls pass through a series of succes- fall endemics. Here we present both the systema- sional stages (Smith et al., 2002; Smith and Baco, tics and ecologyof a dominant new species of 2003). Evolutionaryresearch, using both morpho- polychaete from the opportunistic successional logical and molecular methods, indicates that stage. Perhaps atypically for a deep-sea poly- whale bones could have acted as sulfide-rich chaete, both in situ observations and fixed samples ‘‘stepping stones’’ for the dispersal of sulfide are available for the description. ‘‘loving’’ fauna across the deep ocean basins, and Chrysopetalid polychaetes are a diverse group from shallow-water into deep-sea habitats (Smith of marine worms inhabiting most seas and et al., 1989; Bennett et al., 1994; Baco et al., 1999; substrates, including arctic, temporal and tropical Smith and Baco, 2003). littoral habitats, as well as decaying wood and soft Studies of whale carcasses implanted at bathyal sediments in the deep sea (Dahlgren, 2000; Watson depths off California for less than 1.5 months have Russell, 2000). Most intertidal and shallow sub- revealed largelyintact carcasses, with soft tissue tidal chrysopetalids possess flattened notochaetae, predominantlyscavenged byhagfish, Eptatretus called paleae, covering the dorsum in a roofing-tile deani, sleeper sharks, Somniosus pacificus,and like pattern. Manyof the deep-sea forms, however, lysianassid amphipods (Smith and Baco, 2003). lack the paleae and instead carryerect spines that Carcasses at the seafloor for 4–18 months still are rounded in cross section. Further, close attracted hagfish, but (depending on carcass size) examination of newlycollected material of known were essentiallystripped of soft tissue and but poorlydescribed species indicates a wider primarilysupported invertebrate opportunists on diversityof chaetal morphologywithin the group bones and in organicallyenriched sediments than has been previouslysuggested ( Dahlgren, (Smith et al., 1998, 2003). The bones of carcasses 1996, 2000, in press; Aguirrezabalaga et al., 1999). at the seafloor for 4.5 to 415 years were colonized Based on structural similarities to Cambrian bychemoautotrophic microbial mats and macro- annelid fossil taxa, it has been argued that faunal invertebrates, including some taxa known chrysopetalids represent a basal group within the from vents and seeps, such as vesicomyid clams, Annelida (Butterfield, 1990, 1994; Westheide and ARTICLE IN PRESS T.G. Dahlgren et al. / Deep-Sea Research I 51 (2004) 1873–1887 1875 Watson Russell, 1992; Dahlgren, 2000; Rouse and 2. Material and methods Pleijel, 2001). Chrysopetalidae has traditionally been treated as an aberrant familywithin the order Specimens of Vigtorniella flokati sp. n. were Phyllodocida (e.g. Pettibone, 1982). Perkins (1985) collected using manned and remotelyoperated and Glasby(1993) emphasized the close relation- submersible vehicles from whale-bone habitats at ships between the Hesionidae, Nereididae, and three different locations in the Northern Pacific Chrysopetalidae within the order Phyllodocida, a Ocean. Two of the whale falls are located off the hypothesis further supported by cladistic analyses coast of California in the San Diego Trough of morphological and molecular data (Pleijel and (SDT) and Santa Cruz Basin (SCrB), and the third Dahlgren, 1998; Dahlgren et al., 2000). is located off Oahu, Hawaii (Fig. 1). Details of The new whale-fall chrysopetalid most closely collection methods, locations, and depths are resembles the poorlyknown Vigtorniella zaikai provided in Table 1. All specimens for morpholo- (Kiseleva, 1992). V. zaikai was described from gical analyses were initially fixed in a 4% pelagic polychaete larvae that were raised to formaldehyde solution in seawater and subse- supposedlyadult stage in the laboratory( Kiseleva, quentlytransferred to 70% ethanol. In addition, 1992). The original name Victoriella Kiseleva, 1992 four specimens from SCrB were fixed directlyin was found to be pre-occupied and subsequently EtOH for subsequent DNA extraction. replaced with Vigtorniella Kiseleva, 1996. Larvae of this form were first reported from Black Sea 2.1. Imaging plankton tows by Kiseleva (1959), and can occur in large numbers throughout the year (Murina, Formalin-fixed specimens were examined using 1997). The larvae were also described in detail by dissecting and compound light microscopes and Murina (1986) who misidentified them as the larvae digitallyimaged. The digital images were con- of Pelagobia serrata Southern, 1909 (Phyllodocidae). verted to halftones and contrast enhanced using In 1994, live adults were first recorded from Adobe Photoshop 6.0. For size measurements, sediments at 117–151 m depths at the oxic-anoxic batches of specimens were placed under the boundaryof the Black Sea floor ( Sergeeva et al., dissecting