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Variation of geochemical environments associated with whale-fall biomass mineralization processes in the sediment during the mobile scavenger, enrichment opportunist, and sulfophilic stages

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Abstract

The succession of faunal composition of a whale-fall community is believed to depend on the progress of decomposition of the whale carcass, which itself is dependent on microbial activity in the sediment around the carcass. This means that the faunal succession could be reflected in the variation of the geochemical environment. In this study, we examined sperm whale carcasses placed in two areas of Japanese waters. In Sagami Bay at a depth of ca. 500 m, dive surveys were performed 2 weeks, 2 months, and 9 months after implantation, when mobile scavengers and Osedax worms were observed. Off Cape Nomamisaki, 12 carcasses were implanted at a depth of 200–300 m, and dive surveys were performed there 17, 29, and 41 months after implantation, and abundant chemosynthesis-based mussels were observed at these times. The recovered sediment cores from beneath and around the carcasses in Sagami Bay showed increases in 15N-enriched ammonium and 34S-depleted sulfide and decreases in 34S-enriched sulfate during the 9 months following implantation, and their stoichiometric relationship suggested that proteinaceous matter from the carcass was decomposed preferentially followed by active bacterial sulfate reduction. In comparison, relatively low ammonium but high sulfide concentrations after 41 months off Cape Nomamisaki suggest that primarily lipids from the almost skeletonized carcasses were decomposed in the sediment during bacterial sulfate reduction. Such variation of decomposed organic substrates and geochemical environments result from interaction with the animals inhabiting in and on the sediments adjacent the whale carcasses. It is possible that evolution of the geochemical environment plays an important role in faunal succession, from the enrichment opportunist to sulfophilic stages.

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References

  • Allison PA, Smith CR, Kukert H, Deming JW, Bennett BA (1991) Deep-water taphonomy of vertebrate carcasses: a whale skeleton in the bathyal Santa Barbara Basin. Paleobiology 17(1):78–89

    Article  Google Scholar 

  • Amon DJ, Glover AG, Wiklund H, Marsh L, Linse K, Rogers AD, Copley JT (2013) The discovery of a natural whale fall in the Antarctic deep sea. Deep-Sea Res Pt II 92:87–96. https://doi.org/10.1016/j.dsr2.2013.01.028

    Article  Google Scholar 

  • Bennett BA, Smith CR, Glaser B, Maybaum HL (1994) Faunal community structure of a chemotrophic assemblage on whale bones in the deep northeast Pacific Ocean. Mar Ecol Prog Ser 108:205–223

    Article  Google Scholar 

  • Bowen HJM (1979) Environmental chemistry of the elements. Academic, London

    Google Scholar 

  • Brooks JM, Kennicutt MC II, Fisher CR, Macko SA, Cole K, Childress JJ, Bidigare RR, Vetter RD (1987) Deep-sea hydrocarbon seep communities: evidence for energy and nutritional carbon sources. Science 238:1138–1142

    Article  CAS  PubMed  Google Scholar 

  • Canfield DE, Teske A (1996) Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382:127–132

    Article  CAS  PubMed  Google Scholar 

  • Deines P (1980) The isotopic composition of reduced organic carbon. In: Fritz P, Fontes JCh (eds) Handbook of environmental isotope geochemistry, vol 1. Elsevier, Amsterdam, pp 329–406

    Google Scholar 

  • Deming JW, Reysenbach AL, Macko SA, Smith CR (1997) Evidence for the microbial basis of chemoautotrophic invertebrate community at a whale fall on the deep seafloor. Microsc Res Tech 37:162–170

    Article  CAS  PubMed  Google Scholar 

  • Durmaz B, Sani FD (2001) Effect of carbon to nitrogen ratio on the composition of microbial extracellular polymers in activated sludge. Water Sci Technol 44(10):221–229

    Article  CAS  PubMed  Google Scholar 

  • Froelich PN, Klinkhammer GP, Bender ML, Luedtke NA, Heath GR, Cullen D, Dauphin P (1979) Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis. Geochim Cosmochim Acta 43:1075–1090

    Article  CAS  Google Scholar 

  • Fujiwara Y, Kawato M, Yamamoto T, Yamanaka T, Sato-Okoshi W, Noda C, Tsuchida S, Komai T, Cubelio SS, Sasaki T, Jacobsen K, Kubokawa K, Fujikura K, Maruyama T, Furushima Y, Okoshi K, Miyake H, Miyazaki M, Nogi Y, Yatabe A, Okutani T (2007) Three-year investigations into sperm whale-fall ecosystems in Japan. Mar Ecol 28:219–232

    Article  Google Scholar 

  • Fujiwara Y, Okutani T, Yamanaka T, Kawato M, Mizota C, Fujikura K, Yamamoto T, Okoshi K (2009) Solemya pervernicosa lives in sediment underneath submerged whale carcasses: its biological significance. Venus 68(1–2):27–37

    Google Scholar 

  • Fujiwara Y, Kawato M, Noda C, Kinoshita G, Yamanaka T, Fujita Y, Uematsu K, Miyazaki JI (2010) Extracellular and mixotrophic symbiosis in the whale-fall mussel Adipicola pacifica: a trend in evolution from extra- to intracellular symbiosis. PLoS One 5(7):e11808. https://doi.org/10.1371/journal.pone.0011808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujiwara Y, Kawato M, Miyazaki M, Florence P, Nagahori A, Shinozaki A, Yatabe A, Maruyama T (2012) Early succession of whale-fall ecosystems in Japanese waters. In: Proceedings of 13th deep-sea biology symposium

  • Fujiwara Y, Kawato M, Furushima Y, Aguzzi J, Bodenmann A, Thornton B (2013) A detailed observation of a whale carcass deployed in Sagami Bay, Japan. In: Proceedings of 5th international symposium on chemosynthesis-based ecosystems

  • Gieskes JM, Gamo T, Brumsack H (1991) Chemical methods for interstitial water analysis on JOIDES RESOLUTION. ODP technical note 15, p 60

  • Goffredi SK, Orphan VJ (2010) Bacterial community shifts in taxa and diversity in response to localized organic loading in the deep sea. Environ Microbiol 12(2):344–363. https://doi.org/10.1111/j.1462-2920.2009.02072.x

    Article  CAS  PubMed  Google Scholar 

  • Goffredi SK, Wilpiszeski R, Lee R, Orphan VJ (2008) Temporal evolution of methane cycling and phylogenetic diversity of archaea in sediments from a deep-sea whale-fall in Monterey Canyon, California. ISME J 2(2):204–220

    Article  CAS  PubMed  Google Scholar 

  • Higgs ND, Little CTS, Glover AG (2011) Bones as biofuel: a review of whale bone composition with implications for deep-sea biology and palaeoanthropology. Proc R Soc B 278:9–17. https://doi.org/10.1098/rspb.2010.1267

    Article  PubMed  Google Scholar 

  • Kaplan IR, Rittenberg SC (1964) Microbiological fractionation of sulphur isotopes. J Gen Microbiol 34:195–212

    Article  CAS  PubMed  Google Scholar 

  • Leavitt WD, Bradley AS, Santos AA, Pereira IAC, Johnston DT (2015) Sulfur isotope effects of dissimilatory sulfite reductase. Front Microbiol 6:1392. https://doi.org/10.3389/fmicb.2015.01392

    Article  PubMed  PubMed Central  Google Scholar 

  • Lockyer C (1976) Body weights of some species of large whales. ICES J Mar Sci 36:259–273

    Article  Google Scholar 

  • Lundsten L, Paul CK, Schlining KL, McGann M, Usser WIII (2010) Biological characterization of a whale fall near Vancouver Island, British Columbia, Canada. Deep-Sea Res Pt I 57:918–922. https://doi.org/10.1016/j.dsr.2010.04.006

    Article  Google Scholar 

  • Marschall C, Frenzel P, Cypionka H (1993) Influence of oxygen on sulfate reduction and growth of sulfate-reducing bacteria. Arch Microbiol 159:168–173

    Article  CAS  Google Scholar 

  • Meyers PA, Ishiwatari R (1993) Lacustrine organic geochemistry—an overview of indicators of organic matter sources and diagenesis in lake sediments. Org Geochem 20(7):867–900

    Article  CAS  Google Scholar 

  • Mizota C, Shimoyama S, Yamanaka T (1999) An isotopic characterization of sulfur uptake by benthic animals from Tsuyazaki inlet, northern Kyushu. Benthos Res 54(2):81–85

    Article  Google Scholar 

  • Mizota C, Sasaki M, Yamanaka T (2007) Temporal variation in the concentration and nitrogen isotopic ratios of inorganic nitrogen from soils under Cormorant and Heron colonies. Jpn J Ornithol 56:115–130 (in Japanese with English abstract)

    Article  Google Scholar 

  • Naganuma T, Wada H, Fujioka K (1996) Biological community and sediment fatty acids associated with the deep-sea whale skeleton at the Torishima Seamount. J Oceanogr 52:1–15

    Article  CAS  Google Scholar 

  • Nakaseama M, Ishibashi J, Ogawa K, Hamasaki H, Fujino K, Yamanaka T (2008) Fluid sediment interaction in a marine shallow-water hydrothermal system in the Wakamiko submarine crater, South Kyushu, Japan. Resour Geol 58(3):289–300. https://doi.org/10.1111/j.1751-3928.2008.00062.x

    Article  CAS  Google Scholar 

  • Nelson DC, Fisher CR (1995) Chemoautotrophic and methanotrophic endosymbiotic bacteria at deep-sea vents and seeps. In: Karl DM (ed) The microbiology of deep-sea hydrothermal vents. CRC, Boca Raton, pp 125–167

    Google Scholar 

  • Parsons TR, Stephens K, Strickland JDH (1961) On the chemical composition of eleven species of marine phytoplankton. J Fish Res Board Can 18:1001–1016

    Article  CAS  Google Scholar 

  • Rau GH, Sweeney RE, Kaplan IP (1982) Plankton 13C:12C ratio change with latitude: differences between northern and southern oceans. Deep-Sea Res 29:1035–1039

    Article  CAS  Google Scholar 

  • Rees CE, Jenkins WJ, Monster J (1978) The sulphur isotopic composition of ocean water sulphate. Geochim Cosmochim Acta 42:377–381

    Article  CAS  Google Scholar 

  • Ruby EG, Jannasch HW, Deuser WG (1987) Fractionation of stable carbon isotopes during chemoautotrophic growth of sulfur-oxdizing bacteria. Appl Environ Microbiol 53(8):1940–1943

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saka K (2015) Study on distribution of the dissolved methane concentration in the ocean. MS Thesis, Okayama University (in Japanese with English abstract)

  • Schoell M (1983) Genetic characterization of natural gases. AAPG Bull 67:2225–2228

    CAS  Google Scholar 

  • Sim MS, Bosak T, Ono S (2011) Large sulfur isotope fractionation does not require disproportionation. Science 333:74–77

    Article  CAS  PubMed  Google Scholar 

  • Smith CR (1992) Whale falls: chemosynthesis on the deep seafloor. Oceanus 35(3):74–78

    Google Scholar 

  • Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanogr Mar Biol 41:311–354

    Google Scholar 

  • Smith CR, Kukert H, Wheatcroft RA, Jumars PA, Deming JW (1989) Vent fauna on whale remains. Nature 341:17–18

    Article  Google Scholar 

  • Smith CR, Baco AR, Glover AG (2002) Faunal succession on replicate deep-sea whale falls: time scales and vent-seep affinities. Cah Biol Mar 43:293–297

    Google Scholar 

  • Smith CR, Bernardino AF, Baco A, Hannides AK, Altamira I (2014) The seven-year enrichment: macrofaunal succession in deep-sea sediments around a 30-ton whale fall in the Northeast Pacific. Mar Ecol Prog Ser 515:133–149. https://doi.org/10.3354/meps10955

    Article  Google Scholar 

  • 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 7:571–596. https://doi.org/10.1146/annurev-marine-010213-135144

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tsunogai U, Yoshida N, Ishibashi J, Gamo T (2000) Carbon isotopic distribution of methane in deep-sea hydrothermal plume, Myojin Knoll Caldera, Izu-Bonin arc: implications for microbial methane oxidation in the oceans and applications to heat flux estimation. Geochim Cosmochim Acta 64:2439–2452. https://doi.org/10.1016/S0016-7037(00)00374-4

    Article  CAS  Google Scholar 

  • Turner GL, Bergersen FJ, Tantala H (1983) Natural enrichment of 15N during decomposition of plant material in soil. Soil Biol Biochem 15:495–497

    Article  CAS  Google Scholar 

  • Wada E, Kadonaga T, Matsuo S (1975) 15N abundance in nitrogen of naturally occurring substances and global assessment of denitrification from isotope viewpoint. Geochem J 9:139–148

    Article  CAS  Google Scholar 

  • Weston NB, Porubsky WP, Samarkin VA, Erickson M, Macavoy SE, Joye SB (2006) Porewater stoichiometry of terminal metabolic products, sulfate, and dissolved organic carbon and nitrogen in estuarine intertidal creek-bank sediments. Biogeochem 77:375–408. https://doi.org/10.1007/s10533-005-1640-1

    Article  CAS  Google Scholar 

  • Yamanaka T, Mizota C (2001) Sulfur nutrition of gastropods and bivalves relevant to the mangrove forests: a case study from central Sumatra, Indonesia. Venus 60:71–78

    Google Scholar 

  • Yamanaka T, Murae T, Chiba H (1999) Isotopic fractionation of sulfur in micro zones of tidal flat sediments. Geochem J 33(2):89–99

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to H. Iwasaki and Y. Yuki of NHK who promoted this project. We are grateful to Professor H. Chiba and Dr. C. Mizota who provided very useful comments on an early version of the manuscript. We appreciate to Dr. A. Cronin who provided very useful comments and checked English of this manuscript. We are also grateful to Professor H. Tsutsumi, Kumamoto Prefectural University, for providing facilities for TOC, TN, and CN isotope measurement. Dr. T. Yamamoto and Mr. M. Kawato helped us during the cruises. All of the sediment, bottom, and pore water samples and whale soft tissues were obtained through the cooperative efforts of the team that operated the remotely operated vehicle HyperDolphin and the captain and crew of the support ship R/V Natsushima, to whom we extend our heartfelt thanks. We appreciate the valuable comments given by two anonymous reviewers and editorial handling by Dr. U. Sommer, Academic Editor of this journal. This research was partially supported by the Ministry of Education, Culture, Sports, Science and Technology of Japan through the Special Coordination Fund ‘TAIGA’ project (20109005; T. Y.).

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Correspondence to Yuji Onishi.

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Funding was provided to TY by MEXT Japan and the authors have no conflict of interest.

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Responsible Editor: U. Sommer.

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Onishi, Y., Shimamura, S., Yamanaka, T. et al. Variation of geochemical environments associated with whale-fall biomass mineralization processes in the sediment during the mobile scavenger, enrichment opportunist, and sulfophilic stages. Mar Biol 165, 141 (2018). https://doi.org/10.1007/s00227-018-3398-8

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