Abstract
We report observations on spawning and early development in bone-eating worms of the genus Osedax. Individual females of Osedax rubiplumus were observed at 1820 m depth freely spawning hundreds of oocytes, and females of an undescribed species, Osedax “orange collar”, were observed spawning in laboratory aquaria. Cytological and molecular analysis of the spawned oocytes of two Osedax species revealed no evidence for the bacterial endosymbionts that the female worms require for their nutrition, suggesting that the bacteria must be acquired later from the environment, as they are in other siboglinids. Individual O. “orange collar” females released an average of 335 (±130) eggs per day, but the number of oocytes spawned per day varied greatly, suggesting that not all the females spawned daily. Fertilization rates of the spawned oocytes varied from 0 to 100%, though most females showed nearly 100% fertilization rates. Oocytes spawned in the laboratory at 4–6°C were negatively buoyant. If fertilized, these oocytes extruded polar bodies and then after at least four hours cleaved unequally. Subsequent cleavages occurred in a spiral pattern at roughly 2-h intervals, resulting in free-swimming trochophore larvae after 24 h. These lecithotrophic trochophores swam for 9–16 days before settling with several hooked chaetae, similar to those of dwarf Osedax males. The larval life span of the Osedax species studied in the laboratory appears to be shorter than in closely related Vestimentifera. Osedax rubiplumus, on the other hand, has much larger oocytes and so may have greater dispersal potential than these other Osedax species. The high fecundity and apparently continuous reproduction of Osedax boneworms permits the opportunistic exploitation of sunken vertebrate bones.
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References
Bakke T (1976) The early embryos of Siboglinum fiordicum Webb (Pogonophora) reared in the laboratory. Sarsia 60:1–11
Balzer F (1935) Experiments on sex-developments in Bonellia. Collect Net 10:102–108
Braby CE, Rouse GW, Johnson SB, Jones WJ, Vrijenhoek RC (2007) Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California. Deep Sea Res Part I Oceanogr Res Pap 54:1773–1791. doi:https://doi.org/10.1016/j.dsr.2007.05.014
Carey SC, Felbeck H, Holland ND (1989) Observations of the reproductive biology of the hydrothermal vent tube worm Riftia pachyptila. Mar Ecol Prog Ser 52:89–94. doi:https://doi.org/10.3354/meps052089
Dahlgren T, Wiklund H, Kallstrom B, Lundalv T, Smith CR, Glover AG (2006) A shallow-water whale-fall experiment in the north Atlantic. Cah Biol Mar 47:385–389
Fujikura K, Fujiwara Y, Kawato M (2006) A new species of Osedax (Annelida: Siboglinidae) associated with whale carcasses off Kyushu, Japan. Zool Sci 23:733–740. doi:https://doi.org/10.2108/zsj.23.733
Glover AG, Kallstrom B, Smith CR, Dahlgren TG (2005) World-wide whale worms? A new species of Osedax from the shallow north Atlantic. Proc R Soc Ser B 272:2587–2592
Goffredi SK, Johnson S, Vrijenhoek RC (2007) Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms. Appl Environ Microbiol 73:2314–2323. doi:https://doi.org/10.1128/AEM.01986-06
Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T, Turk K, Lee R, Vrijenhoek RC (2005) Evolutionary innovation: a bone-eating marine symbiosis. Environ Microbiol 7:1369–1378. doi:https://doi.org/10.1111/j.1462-2920.2005.00824.x
Grant A (1990) Mode of development and reproductive effort in marine invertebrates: Should there be any relationship? Funct Ecol 4:128–130
Halanych KM, Feldman RA, Vrijenhoek RC (2001) Molecular evidence that Sclerolinum brattstromi is closely related to vestimentiferans, not to frenulate pogonophorans (Siboglinidae, Annelida). Biol Bull 201:65–75. doi:https://doi.org/10.2307/1543527
Hart MW, Byrne M, Smith MJ (1997) Molecular phylogenetic analysis of life-history evolution in asterinid starfish. Evolut Int J Org Evolut 51:1848–1861. doi:https://doi.org/10.2307/2411007
Harvey PH, Pagel M (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford
Hilário A, Young CM, Tyler PA (2005) Sperm storage, internal fertilization, and embryonic dispersal in vent and seep tubeworms (Polychaeta: Siboglinidae: Vestimentifera). Biol Bull 208:20–28. doi:https://doi.org/10.2307/3593097
Jaccarini V, Schembri PJ, Rizzo M (1983) Sex determination and larval sexual interaction in Bonellia viridis Rolando (Echiura: Bonelliidae). J Exp Mar Biol Ecol 66:25–40. doi:https://doi.org/10.1016/0022-0981(83)90025-4
Jones WJ, Johnson SB, Rouse GW, Vrijenhoek RC (2008) Marine worms (genus Osedax) colonize cow bones. Proc R Soc Ser B 275:387–391. doi:https://doi.org/10.1098/rspb.2007.1437
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton
MacDonald IR, Tunnicliffe V, Southward EC (2002) Detection of sperm transfer and synchronous fertilization in Ridgeia piscesae at Endeavour Segment, Juan de Fuca Ridge. Cah Biol Mar 43:395–398
Marsh AG, Mullineaux LS, Young CM, Manahan DT (2001) Larval dispersal potential of the tubeworm Riftia pachyptila at deep-sea hydrothermal vents. Nature 411:77–80. doi:https://doi.org/10.1038/35075063
McHugh D, Rouse GW (1998) Life history evolution of marine invertebrates—new views from phylogenetic systematics. Trends Ecol Evol 13:182–186. doi:https://doi.org/10.1016/S0169-5347(97)01285-8
Miyake H, Tsukahara J, Hashimoto J, Uematsu K, Maruyama T (2006) Rearing and observation methods of vestimentiferan tubeworm and its early development at atmospheric pressure. Cah Biol Mar 47:471–475
Nussbaumer AD, Fisher CR, Bright M (2006) Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441:345–348. doi:https://doi.org/10.1038/nature04793
Olive PJW (1985) Covariability of reproductive traits in marine invertebrates: implications for the phylogeny of the lower invertebrates. In: Conway Morris S, George D, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates. Clarendon Press, Oxford, pp 42–59
Ramirez-Llodra E (2002) Fecundity and life-history strategies in marine invertebrates. Adv Mar Biol 43:87–170. doi:https://doi.org/10.1016/S0065-2881(02)43004-0
Rouse GW (2001) A cladistic analysis of Siboglinidae Caullery, 1914 (Polychaeta, Annelida): formerly the phyla Pogonophora and Vestimentifera. Zool J Linn Soc 132:55–80. doi:https://doi.org/10.1111/j.1096-3642.2001.tb02271.x
Rouse GW, Fitzhugh K (1994) Broadcasting fables: is external fertilization really primitive? Sex, size and larvae in sabellid polychaetes. Zool Scr 23:271–312. doi:https://doi.org/10.1111/j.1463-6409.1994.tb00390.x
Rouse GW, Goffredi SK, Vrijenhoek RC (2004) Osedax: bone-eating marine worms with dwarf males. Science 305:668–671. doi:https://doi.org/10.1126/science.1098650
Rouse GW, Worsaae K, Johnson SB, Jones WJ, Vrijenhoek RC (2008) Acquisition of dwarf male ‘harems’ by recently settled females of Osedax roseus n. sp. (Siboglinidae; Annelida). Biol Bull 214:67–82
Smith CR, Baco AR (2003) Ecology of whale falls at the deep sea floor. Oceanogr Mar Biol 41:311–354
Southward EC (1999) Development of Perviata and Vestimentifera (Pogonophora). Hydrobiologia 402:185–202
Southward EC, Coates KA (1989) Sperm masses and sperm transfer in a Vestimentiferan, Ridgeia piscesae Jones 1985 (Pogonophora Obturata). Can J Zool 67:2776–2781
Southward EC, Schulze A, Gardiner SL (2005) Pogonophora (Annelida): form and function. Hydrobiologia 535–536:227–251. doi:https://doi.org/10.1007/s10750-004-4401-6
Staver JM, Strathmann RR (2002) Evolution of fast development of planktonic embryos to early swimming. Biol Bull 203:58–69. doi:https://doi.org/10.2307/1543458
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Van Dover CL (1994) In situ spawning of hydrothermal vent tubeworms (Riftia pachyptila). Biol Bull 186:134–135. doi:https://doi.org/10.2307/1542043
Vrijenhoek RC, Collins PC, Van Dover CL (2008a) Bone-eating marine worms: habitat specialists or generalists? Proc R Soc Lond B Biol Sci 275:1963–1964. doi:https://doi.org/10.1098/rspb.2008.0350
Vrijenhoek RC, Johnson SB, Rouse GW (2008b) Bone-eating Osedax females and their harems of dwarf males are recruited from a common larval pool. Mol Ecol 17:4535–4544. doi:https://doi.org/10.1111/j.1365-294X.2008.03937.x
Young CM (2003) Reproduction, development and life history traits. In: Tyler PA (ed) Ecosystems of the World, vol 28. Ecosystems of the Deep Oceans Elsevier, Amsterdam
Young CM, Vásquez E, Metaxas A, Tyler PA (1996) Embryology of vestimentiferan tube worms from deep-sea methane/sulphide seeps. Nature 381:514–516. doi:https://doi.org/10.1038/381514a0
Acknowledgments
Thanks to the pilots of ROV Tiburon and ROV Ventana and crews of RV Western Flyer and RV Point Lobos. We also thank Eddie Kisfaludy (SIO) for essential aquarium facilities, Lonny Lundsten (MBARI) for edited videos, Evelyn York (SIO) for SEM assistance, and Larry Chlebeck (SIO) and Shawn Arellano (OIMB) for laboratory assistance. We thank Victoria J. Orphan at the California Institute of Technology for use of FISH microscopy facilities. Funding was provided by The David and Lucille Packard Foundation (to MBARI), by Scripps Institution of Oceanography (to GWR), and by NSF (OCE-0118733 and OCE-0527139 to CMY). Work carried out in this study complies with the current laws in the USA.
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Communicated by M. Byrne.
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Rouse, G.W., Wilson, N.G., Goffredi, S.K. et al. Spawning and development in Osedax boneworms (Siboglinidae, Annelida). Mar Biol 156, 395–405 (2009). https://doi.org/10.1007/s00227-008-1091-z
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DOI: https://doi.org/10.1007/s00227-008-1091-z