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Osedax: Bone-Eating Marine Worms with Dwarf Males

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Science  30 Jul 2004:
Vol. 305, Issue 5684, pp. 668-671
DOI: 10.1126/science.1098650

Abstract

We describe a new genus, Osedax, and two new species of annelids with females that consume the bones of dead whales via ramifying roots. Molecular and morphological evidence revealed that Osedax belongs to the Siboglinidae, which includes pogonophoran and vestimentiferan worms from deep-sea vents, seeps, and anoxic basins. Osedax has skewed sex ratios with numerous dwarf (paedomorphic) males that live in the tubes of females. DNA sequences reveal that the two Osedax species diverged about 42 million years ago and currently maintain large populations ranging from 105 to 106 adult females.

Deep-sea exploration continues to reveal biological novelties (1) such as whale fall communities (2). Here, we describe remarkable polychaete annelids, Osedax gen. nov. (nov.), discovered in January 2002 on the bones of a gray whale carcass at 2891 m depth in Monterey Bay, California (3). Their conspicuous red plumes extended from most exposed portions of the whale bones (Figs. 1A and 2A). Colonies of these worms comprised two species, Osedax rubiplumus sp. nov. and O. frankpressi sp. nov., that we describe along with the new genus. Nucleotide sequence analysis revealed that the two Osedax species differed by 17.28 ± 0.21% ( ± SD) for mitochondrial COI, by 7.63 ± 0.46% for mitochondrial 16S rRNA, and by 4.09 ± 0.04% for nuclear 18S rRNA (4). On the basis of a molecular clock calibrated for COI in deep-sea annelids (5), O. rubiplumus and O. frankpressi diverged about 42 million years ago (Ma) (4), in the late Eocene, when their ancestor may have exploited the bones of archeocete whales such as Basilosaurus (6). Phylogenetic analysis (Fig. 3) placed Osedax in the family Siboglinidae (7, 8), which includes frenulate and vestimentiferan tubeworms that also lack digestive systems (9, 10).

Fig. 1.

O. rubiplumus. (A) Bones in situ with emergent worms (arrows). (B) Whale rib with female worms. (C) Female, tube removed, dissected from bone. (D) Anterior of oviduct with eggs. (E) Dorsal crown-trunk junction. (F) Lateraltrunk base with oviduct emerging from ovisac (arrow). (G) Transverse section of anterior trunk. Male sits on oviduct (arrow). (H) Lateral ovisac and roots of holotype. (I) Dwarf males (arrows) in tube with female. (J) Transmission electron micrograph (TEM) of root tissue with bacteriocytes. (K) Dwarf male with sperm duct (arrow) and spermatids. (L) Scanning electron micrograph (SEM) of male anterior. (M) Longitudinal section (LS) through male anterior. (N) Longitudinal TEM section through posterior of sperm head. (O) SEM of posterior hooks (arrows) on male. (P) LS through hook. (Q) SEM of hook with subrostral teeth (arrow). b, bone; ba bacteria; c, collar; cm, circular muscle; dbv, dorsal blood vessel; od, oviduct; lm longitudinal muscle; m, male; op, ovisac projection; os, ovisac; p, palps; pl, plaques; pr, prototroch; r, roots; sd, sperm duct; st, spermatids; t, trunk; tu, tube; and vbv, ventral blood vessel.

Fig. 2.

O. frankpressi. (A) Whale rib in situ with emergent worms. (B) Retracted worms. (C) Female partly dissected from bone; note fluid-filled ovisac. (D) Female dissected from bone. (E) Crown-trunk junction. (F) Ovisac with green sheath cut to reveal ovary and blood vessels. (G) Dwarf males in female tube. (H) Male hooks. (I) Male showing prototroch, developing sperm, and yolk. bv, blood vessel; y, yolk; otherwise as for Fig. 1.

Fig. 3.

Osedax as member of Siboglinidae. Bayesian analyses of 2088 molecular characters from combined 16S and 18S rDNA (22). Posterior probability values of 100% indicated by asterisks.

Unlike other siboglinids, female Osedax lack a discrete trophosome, the organ housing symbiotic bacteria in vestimentiferans and pogonophorans. Instead, Osedax possess a bulbous posterior ovisac covered by a sheath of green-colored tissue that branches into a vascularized “root” system and invades the bone marrow (Figs. 1, C and H, and 2, C, D, and F). This branching root system is histologically distinct and not homologous with the singular chitinous root tube found in some Lamellibrachia vestimentiferans (11). Microscopic and molecular analyses (12) of this sheath revealed bacteriocytes (Fig. 1J) containing large rod-shaped bacteria of the microbial order Oceanospirillales, known for heterotrophic degradation of complex organic compounds. Analyses of stable isotopes and fatty acids (12) revealed that the endosymbionts are responsible for the nutrition of this worm. This heterotrophic symbiosis differs markedly from the chemolitho-autotrophic symbioses found in other deep-sea annelids and mollusks that rely on sulfide- or methane-oxidizing bacterial endosymbionts (13). This finding of an endosymbiosis involving heterotrophic degradation in Osedax suggests that the evolutionary history of bacterial symbioses among the Siboglinidae is more varied than previously suspected (14). Reliance on the bones of marine mammals, hydrocarbon degradation, and the unusual morphology of the symbiont-bearing ovisac and root system of these worms make this particular symbiotic association unique in the animal kingdom.

All Osedax visible to the eye were females that ranged from 0.2 to 0.5 mm in trunk width, suggesting ongoing recruitment. Females as small as 0.3 mm wide produced eggs (Figs. 1, D and F, and 2F). The tubes of individual females contain numerous microscopic males (Figs. 1, K to O, and 2G) that were filled with developing sperm (Fig. 1N) and often contained yolk droplets (Fig. 2I). These paedomorphic males retain morphological traits typical of siboglinid trochophore larvae (15), including a ciliary band that appears to be a putative prototroch (Figs. 1L and 2I) and opisthosomal chaetae (Figs. 1O and 2H). The tubes of larger females contained up to 111 males each, with a male-to-female sex ratio of 17:1. Females either accumulate males over time or attract more when larger, because the number of males is correlated (r = 0.899, P < 0.01) with female size in O. rubiplumus (16). We hypothesize that sex may be environmentally determined in Osedax, with larvae settling on exposed bones maturing as females and those landing on females becoming males. Environmental sex determination is known in the echiuran Bonellia (17), now regarded as a polychaete (18).

Amounts of mitochondrial COI diversity (θ) suggest that the effective female population sizes [Ne(f)] range from 5 × 105 in O. rubiplumus to 9 × 105 in O. frankpressi. These numbers are of the same magnitude as estimates of Ne(f) (range of 105 to 106 females) inferred for deep-sea annelids (4) and consistent with estimates of Ne(f) from other invertebrates (19). The large female population sizes estimated for these Osedax species suggest they are common on whale falls. These numbers also suggest that the frequency of whale falls has historically been great, which is consistent with estimates of large whale populations before modern whaling (2, 20). Their abundance suggests that these worms might play a substantial role in the cycling of large organic inputs into the surrounding deep-sea communities.

Systematic description. Annelida, Lamarck 1809; Canalipalpata, Rouse and Fauchald 1997; Siboglinidae Caullery, 1914. Osedax gen. nov. Diagnosis. Polychaete worms with females having a discrete red crown, contractile trunk, bulbous ovisac, and branching roots. Crown and trunk within transparent tube emergent from whale bone (Figs. 1, A and B, and 2, A to C). Crown composed of cylindrical oviduct (Figs. 1D and 2E) plus four pinnule-bearing palps (Figs. 1C and 2, D and E). No mouth or obvious gut. Cylindrical trunk composed mostly of longitudinal muscles and glands. Dorsal heart lies at anterior region of trunk; major dorsal and ventral blood vessels present (Fig. 1G). Oviduct parallels trunk surface into posterior ovisac (Figs. 1, C and F to G, and 2D) filled with numerous white oocytes. Ovisac enclosed by green sheath (Fig. 2F) composed of epidermis and bacteriocytes containing bacteria (Fig. 1J). Ovisac sheath continuous with variably branching posterior roots (Figs. 1, C and H, and 2D). Vascularized roots and ovisac (Fig. 2F). No chaetae or segmentation apparent in females. Paedomorphic males cluster around oviduct in female tubes (Figs. 1, I and K, and 2G). Males with anterior prototroch (Figs. 1L and 2I) and posterior hooked chaetae (Figs. 1O and 2H) arranged in two rows of four pairs (Fig. 1O). Hooks, lacking rostrum, comprise capitium with curved teeth over subrostral process (Figs. 1, P and Q, and 2H). Internally, males contain spermatids and sperm in anterior duct (Fig. 1, K and M, and 2I). Etymology. From Latin os, bone, and edax, devouring; gender masculine. Type species. Osedax rubiplumus sp. nov. by present designation.

Osedax rubiplumus sp. nov. Type material. (21) Monterey Bay, California, Tiburon dive T486, 36°36.8'N, 122°26.0'W, 2891 m, 8 February 2002: holotype, mature adult female (CASIZ 170238); allotypes, 38 males from tube of holotype (CASIZ 170240); paratypes, 10 females and numerous males (CASIZ 170239), 10 females and numerous males (LACM-AHF POLY 02146), and 31 females and numerous males (SAM E3376). Diagnosis. Holotype, emergent body in cylindrical tube, walls 1 mm thick. Contracted crown plumes 2.1 cm long. Oviduct, filled with ellipsoid eggs (mean diameters 151 μm by 121 μm, n = 30). Oviduct extends between palps, 1.8 cm from trunk. Palps red in living worms, pinnules on outer margins. Collar with brown plaques dorsally (Fig. 1E). Trunk 3.8 cm long, 2 mm wide at collar. Ovisac, 8 mm by 4 mm by 0.3 mm, with paired anterolateral projections (Fig. 1C) and four discrete roots posteriorly. Roots with spherical lobes (Fig. 1H). Allotypes 0.4- to 1.1-mm-long males. Putative prototroch incomplete (Fig. 1L). Posteriorly, 16 hooks with capitium teeth emergent; handles 18 to 23 μm (Fig. 1P). Capitium with six to eight teeth; two smaller subrostrumal teeth (Fig. 1Q). Etymology. From Latin rubi, red, and pluma, feather.

Osedax frankpressi sp. nov. Type material. (21) Monterey Bay, California, Tiburon dive T610, 36°36.8'N, 122°26.0'W, 2891 m, 7 August 2002: holotype, mature adult female (CASIZ 170235); allotypes, 80 males from tube of holotype (CASIZ 170237); paratypes, three females (CASIZ 170236), three females (LACM-AHF POLY 02147), three females (SAM E3377). Diagnosis. Holotype, emergent body in gelatinous hemispherical tube, 7-mm diameter. Contracted crown plumes 0.95 cm long. Oviduct filled with ellipsoid eggs (mean diameters 146 μm by 117 μm; n = 15), Oviduct convoluted upon contraction, extending between palps, 3 mm from trunk (Fig. 2, D and E). Palps red with two longitudinal white stripes in living worms (Fig. 2A); pinnules on inner margins. Trunk 4.5 mm long, 0.9 mm wide, and marked by white thickened tissue at anterior (Fig. 2E). Green, bacteriocyte-filled sheath forms trunk-ovisac junction 1.2 mm long, 1 mm wide (Fig. 2D). Lobulate ovisac, 6.5 mm by 5 mm by 3 mm (Fig. 2F). Ovisac and roots inflated with clear fluid in situ in bone (Fig. 2C); fluid lost on extraction. Allotypes, 0.15- to 0.25-mm-long males (Fig. 2, G and I). Chaetae with hooks and handles 15 to 21 μm (Fig. 2H). Capitium with five teeth; no subrostral teeth (Fig. 2H). Etymology. In honor of Dr. Frank Press, former U.S. presidential science advisor, president of the U.S. National Academy of Sciences, and chair of the MBARI Board of Directors, for his distinguished service to science.

Remarks. Females of the two new species are easily distinguished by the lengths of their tubes and palp coloration. O. rubiplumus tubes have a uniform diameter and maintain shape when removed from the water, whereas O. frankpressi tubes are gelatinous and collapse in air. The white-striped O. frankpressi palps contrast with the uniform red palps of O. rubiplumus. Females of the two species differ in the trunk-ovisac junction, ovisac shape, and ramification of roots. Males of O. frankpressi are less than one-third the size of O. rubiplumus males. Male chaetae of O. rubiplumus have subrostral teeth and more capitium teeth.

Supporting Online Material

www.sciencemag.org/cgi/content/full/305/5684/668/DC1

Materials and Methods

Fig. S1

Tables S1 to S3

References and Notes

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