Abstract
Bone-eating Osedax worms can quickly colonize exposed bones and are important ecosystem engineers in whale fall communities, contributing to cause of bone degradation. This study shows that the deep SW Atlantic margin harbors many Osedax species. Using DNA barcoding, we found four putative new lineages as well as O. frankpressi Rouse, Goffredi, and Vrijenhoek, 2004 and O. braziliensis Fujiwara, Jimi, Sumida, Kawato, & Kitazato, 2019, with assemblages varying with depth. It is probable that the bathymetric distributions of these species are controlled by different water masses and their directions of flow. The haplotype network of Atlantic and Pacific O. frankpressi populations suggests segregation between populations, as is also seen in the high FST. However, the low p distance between both populations and the few substitution sites separating haplogroups from both regions (Atlantic and Pacific) could be evidence that populations of both basins are somehow close to each other. It is likely that whale fall habitats exist between both populations analyzed, connecting both basins.
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References
Alfaro-Lucas JM, Shimabukuro M, Ferreira GD, Kitazato H, Fujiwara Y, Sumida PY (2017) Bone-eating Osedax worms (Annelida: Siboglinidae) regulate biodiversity of deep-sea whale-fall communities. Deep-Sea Res II 146:4–12. https://doi.org/10.1016/j.dsr2.2017.04.011
Amon DJ, Wiklund H, Dahlgren TG, Copley JT, Smith CR, Jamieson AJ, Glover AG (2014) Molecular taxonomy of Osedax (Annelida: Siboglinidae) in the Southern Ocean. Zool Scr 43(4):405–417. https://doi.org/10.1111/zsc.12057
Audzijonyte A, Vrijenhoek RC (2010) When gaps really are gaps: statistical phylogeography of hydrothermal vent invertebrates. Evolution 64(8):2369–2384. https://doi.org/10.1111/j.1558-5646.2010.00987.x
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 I 54:1773–1791. https://doi.org/10.1016/j.dsr.2007.05.014
Breaker LC, Broenkow WW (1994) The circulation of Monterey Bay and related processes. Oceanogr Mar Biol Annu Rev 32:1–64 ISSN: 0078-3218
Campos EJD, Miller JL, Müller TJ, Peterson RG (1995) Physical oceanography of the Southwest Atlantic Ocean. Oceanography 8(3):87–91. https://doi.org/10.5670/oceanog.1995.03
Clement MP, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. https://doi.org/10.1046/j.1365-294x.2000.01020.x
De Madron XD, Weatherly G (1994) Circulation, transport and bottom boundary layers of the deep currents in Brazil Basin. J Mar Res 52:583–638. https://doi.org/10.1357/0022240943076975
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10(3):564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Fujikura K, Fujiwara Y, Kawato M (2006) A new species of Osedax (Annelida: Siboglinidae) associated with whale carcasses off Kyushu, Japan. Zool Sci 23(8):733–740. https://doi.org/10.2108/zsj.23.733
Fujiwara Y, Jimi N, Sumida PYG, Kawato M, Kitazato H (2019) New species of bone-eating worm Osedax from the abyssal South Atlantic Ocean (Annelida, Siboglinidae). ZooKeys 814:53–69. https://doi.org/10.3897/zookeys.814.28869
Glover AG, Källström B, Smith CR, Dahlgren TG (2005) World-wide whale worms? A new species of Osedax from the shallow north Atlantic. Proc R Soc 272:2587–2592. https://doi.org/10.1098/rspb.2005.3275
Glover AG, Wiklund H, Taboada S, Avila C, Cristobo J, Smith CR, Kemp KM, Jamieson AJ, Dahlgren TG (2013) Bone-eating worms from the Antarctic: the contrasting fate of whale and wood remains on the Southern Ocean seafloor. Proc R Soc B 280:20131390. https://doi.org/10.1098/rspb.2013.1390
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. https://doi.org/10.1111/j.1462-2920.2005.00824.x
Goffredi SK, Johnson SB, 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. https://doi.org/10.1128/AEM.01986-06
Higgs ND, Little CTS, Glover AG (2011) Bones as biofuel: a review of whale bone composition with implications for deep-sea biology and paleoanthropology. Proc R Soc B 278(1702):9–17. https://doi.org/10.1098/rspb.2010.1267
Hogg NG, Owens B (1999) Direct measurement of the deep circulation within the Brazil Basin. Deep-Sea Res II 46:335–353. https://doi.org/10.1016/S0967-0645(98)00097-6
Jones WJ, Johnson SB, Rouse GW, Vrijenhoek RC (2008) Marine worms (genus Osedax) colonize cow bones. Proc R Soc B 275:387–391. https://doi.org/10.1098/rspb.2007.1437
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780. https://doi.org/10.1093/molbev/mst010
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34(3):772–773. https://doi.org/10.1093/molbev/msw260
Leigh JW, Bryant D (2015) Popart: full-feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116. https://doi.org/10.1111/2041-210X.12410
Li Y, Kocot KM, Schander C, Santos SR, Thornhill DJ, Halanych KM (2015) Mitogenomics reveals phylogeny and repeated motifs in control regions of the deep-sea family Siboglinidae (Annelida). Mol Phylogenet Evol 85:221–229. https://doi.org/10.1016/j.ympev.2015.02.008
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Lösekann T, Robador A, Niemann H, Knittel K, Boetius A, Dubilier N (2008) Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic Cold Seep (Haakon Mosby Mud Volcano, Barents Sea). Environmental Microbiology 10 (12):3237–3254 https://doi.org/10.1111/j.1462-2920.2008.01712.x
Lundsten L, Schlining KL, Frasier K, Johnson SB, Kuhnz LA, Harvey JBJ, Clague G, Vrijenhoek RC (2010) Times-series analysis of six whale-fall communities in Monterey canyon, California, USA. Deep Sea Res I 57:1573–1584. https://doi.org/10.1016/j.dsr.2010.09.003
McCartney MS (1993) Crossing of the equator by the deep west boundary current in the western Atlantic Ocean. J Phys Oceanogr 23:1953–1974. https://doi.org/10.1175/1520-0485(1993)023<1953:COTEBT>2.0.CO;2
McMullin ER, Hourdez S, Schaeffer, SW and Fisher CR (2003) Phylogeny and biogeography of deep sea vestimentiferan tubeworms and their bacterial symbionts. Symbiosis 34, 1–41.
Miyamoto N, Yamamoto T, Yusa Y, Fujiwara Y (2013) Postembryonic development of the bone-eating worm Osedax japonicus. Naturwissenschaften 100:285–289. https://doi.org/10.1007/s00114-013-1024-7
Müller TJ, Ikeda Y, Zangenberg N, Nonato LV (1998) Direct measurements of western boundary currents off Brazil between 20°S and 28°S. J Geophys Res 103(C3):5429–5437. https://doi.org/10.1029/97JC03529
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes v. 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Rouse GW, Goffredi SK, Vrijenhoek RC (2004) Osedax: bone-eating marine worms with dwarf males. Science 30:668–671. 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. (Siboglinida; Annelida). Biol Bull 214:67–82. https://doi.org/10.2307/25066661
Rouse GW, Wilson NG, Goffredi SK, Johnson SB, Smart T, Widmer C, Young CM, Vrijenhoek RC (2009) Spawning and development in Osedax boneworms (Siboglinidae, Annelida). Mar Biol 156:395–405. https://doi.org/10.1007/s00227-008-1091-z
Rouse GW, Wilson NG, Worsaae K, Vrijenhoek RC (2015) A dwarf male reversal in bone-eating worms. Curr Biol 25:1–6. https://doi.org/10.1016/j.cub.2014.11.032
Rouse GW, Goffredi SK, Johnson SB, Vrijenhoek RC (2018) An inordinate fondness for Osedax (Siboglinidae: Annelida): fourteen new species of bone worms from California. Zootaxa 4377(4):451–489. https://doi.org/10.11646/zootaxa.4377.4.1
Saeedi H, Bernardino AF, Shimabukuro M, Falchetto G, Sumida PYG (2019) Macrofaunal community structure and biodiversity patterns based on a wood-fall experiment in the deep South-west Atlantic. Deep Sea Res I 145:73–82. https://doi.org/10.1016/j.dsr.2019.01.008
Salathé RM, Vrijenhoek RC (2012) Temporal variation and lack of host specificity among bacterial endosymbionts of Osedax bone worms (Polychaeta: Siboglinidae). BMC Evol Biol 12:189. https://doi.org/10.1186/1471.2148.12.189
Santos MCO, Siciliano S, Vicente AFC, Alvarenga FS, Zampirolli E, Souza SP, Maranho A (2010) Cetacean records along São Paulo state coast southeastern Brazil. Braz J Oceanogr 58(2):123–142. https://doi.org/10.1590/S1679-87592010000200004
Silveira ICA, Schmidt ACK, Campos EJD, Godoi SS, Ikeda Y (2000) A corrente do Brazil ao largo da costa leste Brasileira. Rev Bras Oceanogr 48(2):171–183. https://doi.org/10.1590/S1413-77392000000200008
Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanogr Mar Biol Annu Rev 41:311–354 ISSN: 0078-3218
Smith CR, Glover AG, Treude T, Higgs ND, Amon DJ (2015) Whale-fall ecosystems: recent insights into ecology, paleoecology, and evolution. Annu Rev Mar Sci 7:10.1–10.6. https://doi.org/10.1146/annurev-marine-010213-135144
Srivathsan A, Meier R (2012) On the inappropriate use of Kimura-2-parameter (K2P) divergences in the DNA-barcoding literature. Cladistics 28(2):190–194. https://doi.org/10.1111/j.1096-0031.2011.00370.x
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stramma L, England M (1999) On the water masses and mean circulation of the South Atlantic Ocean. J Geophys Res 104(C9):20,863–20,883. https://doi.org/10.1029/1999JC900139
Sumida PYG, Alfaro-Lucas JM, Shimabukuro M, Kitazato H, Perez JAA, Soares-Gomes A, Toyofuku T, Lima AOS, Ara K, Fujiwara Y (2016) Deep-sea whale fall fauna from the Atlantic resembles that of the Pacific Ocean. Sci Rep 6:22139. https://doi.org/10.1038/srep22139
Taboada S, Riego A, Bas M, Arnedo MA, Cristobo J, Rouse GW, Avila C (2015) Bone-eating worms spread: insights into shallow-water Osedax (Annelida, Siboglinidae) from Antarctic, Subantarctic, and Mediterranean waters. PLoS One 10(11):e0140341. https://doi.org/10.1371/journal.pone.0140341
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595 ISSN: 0016-6731
Treude T, Smith CR, Wenzhöfer F, Carney E, Bernardino AF, Hannides AK, Krüger M, Boetius A (2009) Biogeochemistry of a deep-sea whale fall: sulfate reduction, sulfide efflux and methanogenesis. Mar Ecol Prog Ser 382:1–21. https://doi.org/10.3354/meps07972
Vrijenhoek RC, Johnson SB, Rouse GW (2008) Bone-eating Osedax females and their “harems” of dwarf males are recruited from a common larval pool. Mol Ecol 17:4535–4544. https://doi.org/10.1111/j.1365-294X.2008.03937.x
Vrijenhoek RC, Johnson SB, Rouse GW (2009) A remarkable diversity of bone-eating worms (Osedax; Siboglinidae; Annelida). BMC Biol 7(1):74. https://doi.org/10.1186/1741-7007-7-74
Wedekin LL, Rossi-Santos MR, Baracho C, Cypriano-Souza AL, Simões-Lopes PC (2014) Cetacean records along a coastal-offshore gradient in the Vitória-Trindade Chain, western South Atlantic Ocean. Braz JBiol 74(1):137–144. https://doi.org/10.1590/1519-6984.21812
Worsaae K, Rouse GW (2010) The simplicity of males: dwarf males of four species of Osedax (Siboglinidae: Annelida) investigated by confocal laser scanning microscopy. J Morphol 271:127–142. https://doi.org/10.1002/jmor.10786
Xia X (2017) DAMBE6: new tools for microbial genomics, phylogenetics, and molecular evolution. J Hered 108(4):431–437. https://doi.org/10.1093/jhered/esx033
Zerbini AN, Secchi ER, Siciliano S, Simões-Lopes PC (1997) A review of the occurrence and distribution of whales of the genus Balaenoptera along the Brazilian coast. Report International Whaling Commission 47:407–417 Available at: https://archive.iwc.int/pages/search.php?search=!collection33&bc_from=themes. Accessed 14 Aug 2017
Zerbini AN, Andriolo A, Heide-Jørgensen MP, Pizzorno JL, Maia YG, VanBlaricom GR, DeMaster DP, Simões-Lopes P, Moreira S, Bethlem C (2006) Satellite-monitored movements of humpback whales Megaptera novaeangliae in the Southwest Atlantic Ocean. Mar Ecol Prog Ser 313:295–304. https://doi.org/10.3354/meps313295
Acknowledgments
We would like to thank the Masters and crews of R/V Alpha Crucis and R/V Alpha Delphini from IOUSP during the deployment and the recovering of SP-1500 lander. We are also indebted to the Brazilian Navy and the Master and crew of PRV Almirante Maximiano for the help during the recovering of the other landers. We also thank the editor, Dr. Craig R. Smith, and the two anonymous reviewers for the comments on the manuscript. MS was supported by CAPES/Proex PhD scholarship.
Funding
This study was funded by São Paulo Research Foundation (FAPESP) into the Research Program on Biodiversity Characterization, Conservation, Restoration and Sustainable Use (BIOTA Program)—grant number 2011/50185-1.
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All data generated or analysed during this study are included in this published article and its supplementary information files. All new COI sequences of Osedax were deposited in GenBank and the accession numbers are detailed in Table 2.
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Shimabukuro, M., Sumida, P.Y.G. Diversity of bone-eating Osedax worms on the deep Atlantic whale falls—bathymetric variation and inter-basin distributions. Mar. Biodivers. 49, 2587–2599 (2019). https://doi.org/10.1007/s12526-019-00988-2
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DOI: https://doi.org/10.1007/s12526-019-00988-2