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Biogeography and population structure of predominant macrofaunal taxa (Annelida and Isopoda) in abyssal polymetallic nodule fields: implications for conservation and management

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Abstract

Abyssal plains of the Clarion Clipperton Fracture Zone (CCZ) in the NE Pacific Ocean probably harbour one of the world’s most diverse ecosystems. Gaining a basic understanding of the mechanisms underlying the evolution and persistence of CCZ biodiversity in terms of biogeography and connectivity has both scientific merit and informs the development of policy related to potential future deep-sea mining of mineral resources at an early stage in the process. Existing archives of polychaetes and isopods were sorted using a combined molecular and morphological approach, which uses nucleotide sequences (cytochrome c oxidase subunit I (COI)) and morphological information to identify appropriate sample sets for further investigations. Basic patterns of genetic diversity, divergence and demographic history of five polychaete and five isopod species were investigated. Polychaete populations were found to be genetically diverse. Pronounced long- and short-distance dispersal produces large populations that are continuously distributed over large geographic scales. Although analyses of isopod species suggest the same, spatial genetic structuring of populations do imply weak barriers to gene flow. Mining-related, large-scale habitat destruction has the potential to impact the continuity of both isopod and polychaete populations as well as their long-term dispersal patterns, as ecosystem recovery after major impacts is predicted to occur slowly at evolutionary time scales.

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References

  • Aleynik D, Inall ME, Dale A, Vink A (2017) Impact of remotely generated eddies on plume dispersion at abyssal mining sites in the Pacific. Sci Rep 7:16959

  • Amon DJ, Ziegler AF, Dahlgren TG, Glover AG, Goineau A, Gooday AJ, Wiklund H, Smith CR (2016) Insights into the abundance and diversity of abyssal megafauna in a polymetallic-nodule region in the eastern clarion-Clipperton zone. Sci Rep 6(2016)

  • Avise JC, Neigel JE, Ampold J (1984) Demographic influences on mitochondrial DNA lineage survivorship in animal populations. J Mol Evol 20:99–105

    Article  PubMed  CAS  Google Scholar 

  • Banks S, Piggott M, Williamson J, Bové U, Holbrook N et al (2007) Oceanic variability and coastal topography shape genetic structure in a long-dispersing sea urchin. Ecology 88:3055–3064

    Article  PubMed  Google Scholar 

  • Blainville H (1828) Mollusques, Vers et zoophytes. In: Dictionnaire des sciences Naturelles, F.G. Levrault, Strasbourg & Paris. 57: 486

  • Blake J (2006) Spionida. In: Rouse G, Pleijel F (eds) Reproductive biology and phylogeny of Annelida. Science Publishers, Enfield, pp 565–638

    Google Scholar 

  • Bober S, Brix S, Riehl T, Schwentner M, Brandt A (2018) Does the mid-Atlantic ridge affect the distribution of abyssal benthic crustaceans across the Atlantic Ocean? Deep-Sea Res Pt II 148:91–104

    Article  Google Scholar 

  • Böggemann M (2005) Revision of the Goniadidae. Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg NF 39 Goecke & Evers, Keltern-Weiler. Neue Folgen 39:1–354

  • Böggeman M (2009) Polychaetes (Annelida) of the abyssal SE Atlantic. Org Divers Evol 9(4–5):251–428.

    Google Scholar 

  • Bors EK, Rowden AA, Maas EW, Clark MR, Shank TM (2012) Patterns of deep-sea genetic connectivity in the New Zealand region: implications for Management of Benthic Ecosystems. PLoS One 7(11):e49474

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brenke N (2005) A ebibenthic sledge for operations on marine softbottom and bedrock. Mar Technol Soc J 39(2):13–24

    Article  Google Scholar 

  • Brix S, Riehl T, Leese F (2011) First genetic data for species of the genus Haploniscus Richardson, 1908 (Isopoda: Asellota: Haploniscidae) from neighbouring deep-sea basins in the South Atlantic. Zootaxa 2838:84–89

    Article  Google Scholar 

  • Brix S, Leese F, Riehl T, Kihara TC (2014a) A new genus and new species of Desmosomatidae Sars, 1897 (Isopoda) from the east South-Atlantic abyss described by means of integrative taxonomy. Mar Biodivers 45(1):7–61

    Article  Google Scholar 

  • Brix S, Svavarsson J, Leese F (2014b) A multi-gene analysis reveals multiple highly divergent lineages of the isopod Chelator insignis (Hansen, 1916) south of Iceland. Pol Polar Res 35:225–242

    Article  Google Scholar 

  • Brökeland W, Gudmundsson G, Svavarsson J (2010) Diet of four species of deep-sea isopods (Crustacea: Malacostraca: Peracarida) in the South Atlantic and the Southern Ocean. Mar Biol 157:177–187

    Article  Google Scholar 

  • Brown RR, Davis CS, Leys SP (2017) Clones or clans: the genetic structure of a deep-sea sponge, Aphrocallistes vastus, in unique sponge reefs of British Columbia, Canada. Mol Ecol 26(4):1045–1059.

    Article  PubMed  CAS  Google Scholar 

  • Bussau C, Schriever G, Thiel H (1995) Evaluation of abyssal metazoan meiofauna from a manganese nodule area of the eastern South Pacific. Vie Milieu 45(1):39–48

  • Borowski C, Thiel H (1998) Deep-sea macrofaunal impacts of a large-scale physical disturbance experiment in the Southeast Pacific. Deep-Sea Res II Top Stud Oceanogr 45:55–81

    Article  Google Scholar 

  • Carson HS, Hentschel BT (2006) Estimating the dispersal potential of polychaete species in the Southern California bight: implications for designing marine reserves. Mar Ecol Prog Ser 316:105–113

    Article  Google Scholar 

  • Chen YJ, Yao R, Xie FA, Yan AQ (2017) Construction of DNA barcode reference library for intertidal polychaetous annelids commonly found in the East China Sea. School of Marine Science, Zhejiang Ocean University, Changzhi Island, Zhou Shan, Zhejiang 316022, China

  • Creasey SS, Rogers AD (1999) Population genetics of bathyal and abyssal organisms. In: Southward AJ, Tyler PA, Young CM (eds) Advances in marine biology, book volume 35. Academic

  • Cronan DS (1980) Underwater minerals, Vol. Academic, London 362p

    Google Scholar 

  • Crow J (1986) Basic concepts in population, quantitative, and evolutionary genetics. Freeman, San Francisco

    Google Scholar 

  • Cowen RK, Gawarkiewicz G, Pineda J, Thorrold SR (2006) Population connectivity in marine systems: an overview. Oceanography 20(3):14–21

    Article  Google Scholar 

  • Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–466

    Article  Google Scholar 

  • Desbruyères D, Almeida A, Biscoito M, Comtet T, Khripounoff A, Le Bris N, Sarradin PM, Segonzac M (2000) A review of the distribution of hydrothermal vent communities along the northern mid-Atlantic ridge: dispersal vs. environmental controls. Hydrobiol 440:201–216

    Article  Google Scholar 

  • De Smet B, Pape E, Riehl T, Bonifácio P, Colson L, Vanreusel A (2017) The community structure of deep-sea macrofauna associated with polymetallic nodules in the eastern part of the clarion-Clipperton fracture zone. Front Mar Sci 4:1–14

    Google Scholar 

  • De Jong MA, Wahlberg N, van Eijk M, Brakefield PM, Zwaan BJ (2011) Mitochondrial DNA signature for range-wide populations of Bicyclus anynana suggests a rapid expansion from recent refugia. PLoS One 6:1–5

    Google Scholar 

  • Duran S, Palacin C, Becerro MA, Turon X, Giribet G (2004) Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol 13(11):3317–3328

    Article  PubMed  CAS  Google Scholar 

  • Elsner N, Golovan O, Malyutina M, Brandt A (2013) Alone in the dark: distribution, population structure and reproductive mode of the dominant isopod Eurycope spinifrons Gurjanova, 1933 (Isopoda: Asellota: Munnopsidae) from bathyal and abyssal depths of the sea of Japan. Deep-Sea Res II Top Stud Oceanogr 87:7

    Google Scholar 

  • Etter RJ, Rex MA, Chase MC, Quattro JM (1999) A genetic dimension to deep-sea diversity. Deep-Sea Res Pt I 46:1095–1099

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131(2):479–491

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Fauchald J, Jumars PA (1979) The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar Biol Annu Rev 17:193–284

    Google Scholar 

  • Fogarty MJ, Botsford LW (2007) Population connectivity and spatial management of marine fisheries. Oceanography 20:112–123

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299

    PubMed  CAS  Google Scholar 

  • Glover AG, Smith CR, Paterson GLJ, Wilson GDF, Hawkins L et al (2002) Polychaete species diversity in the Central Pacific abyss:local and regional patterns, and relationships with productivity. Mar Ecol Prog Ser 240:157–170

    Article  Google Scholar 

  • Glover AG, Dahlgren TG, Wiklund H, Mohrbeck I, Smith CR (2016a) An end-to-end DNA taxonomy methodology for benthic biodiversity survey in the clarion-Clipperton zone, Central Pacific abyss. J Mar Sci Eng 4(1):2

    Article  Google Scholar 

  • Glover AG, Dahlgren TG, Taboada S, Patterson G, Wiklund H, Waeschenbach A, Cobley A, Martinez P, Kaiser S, Schnurr S et al (2016b) The London workshop on the biogeography and connectivity of the clarion-Clipperton zone. Workshop Report: Reserach Ideas and Outcomes (RIO) 2:e10528

  • Goineau A, Gooday A (2017) Novel benthic foraminifera are abundant and diverse in an area of the abyssal equatorial Pacific licensed for polymetallic nodule exploration. Sci Rep 7:45288

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gollner S, Stuckas H, Kihara TC, Laurent S, Kodami S, Martinez Arbizu P (2016) Mitochondrial DNA analyses indicate high diversity, expansive population growth and high genetic connectivity of vent copepods (Dirivultidae) acroiss different oceans. Plos One 11(10):e0163776

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Goodall-Copestake WP, Tarling GA, Murphy EJ (2012) On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity 109:50–56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gooday AJ, Holzmann M, Caullec C, Goineau, Kamenskaya O, Weber AAT, Pawlowski J (2017) Giant protists (xenophyophores, Foraminifera) are exceptionally diverse in parts of the abyssal eastern Pacific licensed for polymetallic nodule exploration. Biol Conserv 207:106–116

    Article  Google Scholar 

  • Graf G (1992) Benthic-pelagic coupling: a benthic view. Oceanogr Mar Biol 30:149–190

  • Grantham BA, Eckert GL, Shanks AL (2003) Dispersal potential of marine invertebrates in diverse habitats. Ecol Appl 13(81):108–116

    Article  Google Scholar 

  • Grassle JF (1989) Species diversity in deep-sea communities. Trends Ecol Evol 4(1): 12–15.

    Article  PubMed  CAS  Google Scholar 

  • Grassle JF, Maciolek NJ (1992) Deep-sea species richness: regional and local diversity estimates from quantitative bottom samples. Am Nat 139(2):313–341.

    Article  Google Scholar 

  • Gudmundsson G, von Schmalensee M, Svavarsson J (2000) Are foraminifers (protozoa) important food for small isopods (Crustacea) in the deep sea? Deep-Sea Res I Oceanogr Res Pap 47:2093–2109

    Article  Google Scholar 

  • Gunther C (1992) Dispersal of intertidal invertebrates: a strategy to react to disturbances of different scales? Neth J Sea Res 30:45–56

    Article  Google Scholar 

  • Hannides A, Smith CR (2003) The northeast abyssal Pacific plain. In: Black KB, Shimmield GB (eds) Biogeochemistry of marine systems. CRC Press, Boca Raton

    Google Scholar 

  • Halbach P, Özkara M, Hense J (1975) The influence of metal content on the physical and mineralogical properties of pelagic manganese nodules. Mineral Deposits 10:397–411

    Article  CAS  Google Scholar 

  • Hausdorf B (2011) Progress toward a general species concept. Evolution 65:923–931

    Article  PubMed  Google Scholar 

  • Hartman O, Fauchald K (1971) Deep-water benthic Polychaetous annelids of New England to Bermuda and other North Atlantic areas. Part II, 6, Los Angeles

  • Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66(4):591–600

    PubMed  CAS  Google Scholar 

  • Hein JR, Koschinsky A (2014) Deep-ocean ferromanganese crusts and nodules. In: Holland HD, Turekian KK (eds) Treatise on geochemistry, Edition: Second, Chapter: Volume 13, Chapter 11. Elsevier, pp 273–291

  • Hessler RR, Sanders HL (1967) Faunal diversity in the deep-sea. Deep-Sea Res 14:65–78.

    Google Scholar 

  • Hessler RR, Jumars PA (1974) Abyssal community analysis from replicate cores in the central North Pacific. Deep-Sea Res 21:185–209

    Article  Google Scholar 

  • Hessler RR, Wilson GDF, Thistle D (1979) The deep-sea isopods: a biogeographic and phylogenetic overview. Sarsia 64:67–75

    Article  Google Scholar 

  • Hessler RR, Wilson GDF (1983) The origin and biogeography of malacostracan crustaceans in the deep sea. In: Sims RW, Price JH, Whalley PES (ed) Evolution, time and space: the emergence of the biosphere. Academic press. London and New York, pp. 227–254.

    Google Scholar 

  • Hessler RR, Strömberg JO (1989) Behavior of janiroidean isopods (Asellota), with special reference to deep sea genera. Sarsia 74:145–159

    Article  Google Scholar 

  • Hilário A, Gaudron SM, Metaxas A, Howell KL, Mercier A, Mestre NC, Ross RE, Thurnherr AM, Young C (2015) Estimating dispersal distance in the deep sea: challenges and applications to marine reserves. Front Mar Sci 2:6

    Article  Google Scholar 

  • Hurtado LA, Lutz RA, Vrijenhoek RC (2004) Distinct patterns of genetic differentiation among annelids of eastern Pacific hydrothermal vents. Mol Ecol 13:2603–2615

    Article  PubMed  CAS  Google Scholar 

  • Janssen A, Kaiser S, Meissner K, Brenke N, Menot L, Martinez Arbizu P (2015) A reverse taxonomic approach to assess macrofaunal distribution patterns in abyssal pacific polymetallic nodule fields. PLoS One 10(2):e0117790

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jeong KS, Kang JK, LeeKY JHS, Chi SB, Ahn SJ (1996) Formation and distribution of manganese nodule deposit in the northestern margin of clarion Clipperton fracture zones, northeast equatorial Pacific. Geo-Mar Lett 16:123–131

    Article  CAS  Google Scholar 

  • Johnson SB, Young CR, Jones WJ, Waren A, Vrijenhoek RC (2006) Migration, isolation, and speciation of hydrothermal vent limpets (Gastropoda; Lepetodrilidae) across the Blanco transform fault. Biol Bull 210:140–157

    Article  PubMed  Google Scholar 

  • Jones DOB, Kaiser S, Sweetman AK, Smith CR, Menot L, Vink A, Trueblood D, Greinert J, Billett DSM, Martinez Arbizu P, Radziejewska T, Singh R, Ingole B, Stratmann T, Simon-Lledo E, Durden JM, Clark MR (2017) Biological responses to disturbance from simulated deep-sea polymetallic nodule mining. PLOSOne 12(2)

  • Kersken D, Janussen D, Martínez Arbizu P (2018) Deep-sea glass sponges (Hexactinellida) from polymetallic nodule fields in the Clarion-Clipperton Fracture Zone (CCFZ), northeastern Pacific: Part I–Amphidiscophora. Mar Biodivers 48:545–573

    Article  Google Scholar 

  • Kimura M (1980) A simple methode for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216

    Article  Google Scholar 

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiol 420:73–90

    Article  CAS  Google Scholar 

  • Kussakin OG (1965) On the fauna of Desmosomatidae (Crustacea, Isopoda) of the far-eastern seas of the U.S.S.R. (in Russian). Akademiya Nauk SSSR, zoological institute. Exploration of the Fauna of the seas III (XI). Fauna seas NW Pacific 115-144

  • Kvist S (2014) Does a global DNA barcoding gap exist in Annelida? Mitochondr DNA 27(3):2241–2252

  • Lee SH, Kim KH (2004) Side-scan sonar characteristics and manganese nodule abundance in the clarion-Clipperton fracture zones, NE equatorial Pacific. Mar Georesour Geotec 22:103–114

    Article  CAS  Google Scholar 

  • Leese F, Agrawal S, Held C (2010) Long-distance island hopping without dispersal stages: transportation across major zoogeographic barriers in a Southern Ocean isopod. Naturwissenschaften 97(6):583–594

    Article  PubMed  CAS  Google Scholar 

  • Leigh JW, Bryant D (2015) Popart:full-feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116

    Article  Google Scholar 

  • Lowe WH, Allendorf FW (2010) What can genetic tell us about population connectivity? Mol Ecol 19:3038–3051

    Article  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lim S-C, Wiklund H, Glover AG, Dahlgren TG, Tan K-S (2017) A new genus and species of abyssal sponge commonly encrusting polymetallic nodules in the Clarion-Clipperton Zone, east Pacific Ocean. Syst Biodivers 15(6):507–519.

    Article  Google Scholar 

  • Mallett J (1995) A species definition for the modern synthesis. Trends Ecol Evol 10:294–299

    Article  Google Scholar 

  • McClain CR, Hardy SM (2010) The dynamics of biogeographic ranges in the deep sea. Proc R Soc B Biol Sci

  • Maggs CA, Castilho R, Foltz D, Henzler C, Jolly MT, Kelly J, Olsen J, Perez KE, Stam W, Väinölä R, Viard F, Wares J (2008) Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89(11):S108-S122

    Article  PubMed  Google Scholar 

  • Markhaseva EL, Mohrbeck I, Renz J (2017) Description of Pseudeuchaeta vulgaris n. sp (Copepoda: Calanoida), a new aetideid species from the deep Pacific Ocean with notes on the biogeography of benthopelagic aetideid calanoids. Mar Biodivers 47(2):289–297

    Article  Google Scholar 

  • Miljutin DM, Miljutina MA, Arbizu PM, Galéron J (2011) Deep-sea nematode assemblage has not recovered 26 years after experimental mining of polymetallic nodules (Clarion-Clipperton Fracture Zone, Tropical Eastern Pacific). Deep-Sea Res I Oceanogr Res Pap 58:885–897

    Article  Google Scholar 

  • Molotdsova TN, Opresko DM (2017) Black corals (Anthozoa:Antipatharia) of the clarion Clipperton fracture zone. Mar Biodivers 47(2):349–365

    Article  Google Scholar 

  • Mullineaux LS (1987) Vertical distributions of the epifauna on manganese nodules: implications for settlement and feeding. Limnol Oceanogr 34(7):1247–1262

    Article  Google Scholar 

  • Paterson GLJ, Wilson GDF, Cosson N, Lamont PA (1998) Hessler and Jumars (1974) revisited: abyssal polychaete assemblages from the Atlantic and Pacific. Deep Sea Res II 45:225–251

    Article  Google Scholar 

  • Pfenninger M, Schwenk K (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographic regions. BMC Evol Biol 7:121

    Article  PubMed  PubMed Central  Google Scholar 

  • Pineda J, Hare JA, Sponaugle S (2007) Transport and dispersal in the coastal oceans and consequences for population connectivity. Oceanography 20(3):22–39

    Article  Google Scholar 

  • Plouviez S, Shank TM, Faure B et al (2009) Comparative phylogeography among hydrothermal vent species along the East Pacific rise reveals vicariant processes and population expansion in the south. Mol Ecol 18:3903–3917

    Article  PubMed  CAS  Google Scholar 

  • Purser A, Marcon Y, Hoving HJT, Piatkowski U, Vecchione M, Eason D, Bluhm H, Boetius A (2016) Association of deep-sea incirate octopods with manganese crusts and nodule fields in the Pacific Ocean. Curr Biol 26(24):R1247–R1271

    Article  CAS  Google Scholar 

  • Ramirez-Llodra E, Tyler PA, Baker MC, Bergstad OA, Clark MR, Escobar E, Levin LA, Menot L, Rowden AA, Smith CR, Van Dover CL (2011) Man and the last great wilderness: human impact on the deep sea. PLoS ONE 6(8):e22588

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19(12):2092–2100

    Article  PubMed  CAS  Google Scholar 

  • Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86

    Article  PubMed  CAS  Google Scholar 

  • Rengaiyan P, Ingole BS, Meena RR (2017) A new species of the Perinereis auriculaexpando (Nereididae: Polychaeta) from Goa, the west coast of India biological oceanography division, national. Institute of Oceanography, Dona Paula, Panaji, Goa 403 004, India

  • Riehl T, Kaiser S (2012) Conquered from the deep sea? A new deep-sea isopod species from the Antarctic shelf shows pattern of recent colonization. PLoS ONE 7(11):E49354

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Riehl T, Wilson GDF, Malyutina MV (2014) Urstylidae – a new family of deep-sea isopods and its phylogenetic implications. Zool J Linnean Soc 170:245–296

  • Ritchie H, Jamieson AJ, Piertney SB (2017) Population genetic structure of two congeneric deep-sea amphipod species from geographically isolated hadal trenches in the Pacific Ocean. Deep Sea Res PT I 119:50–57.

    Article  Google Scholar 

  • Rouse G, Pleijel F (2001) Polychaetes. Oxford University Press, London

    Google Scholar 

  • Rokop FJ (1977) Patterns of reproduction in the deep-sea benthic crustaceans: a re-evaluation. Deep-Sea Res 24(7):683-691

    Article  Google Scholar 

  • Sars GO (1864) Om en anomal Gruppe af Isopoder. Forhandlinger i Videnskaps-selskabet i Christiania 1863:205–221

    Google Scholar 

  • Scheltema RS (1971) Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic marine gastropods. Biol Bull 140:284–322

    Article  Google Scholar 

  • Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152(3):1079–1089

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schnurr S, Brix S (2012) A new species from the South Atlantic Ocean:Eugerdella huberti sp. nov. Mar Biodivers 42(1):13–24

    Article  Google Scholar 

  • Schüller M (2011) Evidence for a role of bathymetry and emergence in speciation in the genus Glycera (Glyceridae, Polychaeta) from the deep eastern Weddell Sea. Polar Biol 34:549–564

    Article  Google Scholar 

  • Sites J, Marshall J (2004) Operational criteria for delimiting species. Annu Rev Ecol Syst 35:199–227

    Article  Google Scholar 

  • Smith CR, Demopoulos AWJ (eds) (2003) Ecology of the deep Pacific Ocean floor. Elsevier, Amsterdam 569p

    Google Scholar 

  • Smith CR, Paterson G, Lambshead J, Glover A, Rogers A, et al (2008a) Biodiversity, species ranges, and gene flow in the abyssal Pacific nodule province: predicting and managing the impacts of deep seabed mining. ISA technical study, international seabed authority, Kingston, Jamaica no. 3

  • Smith CR, Gaines S, Watling S, Friedlander A, Morgan C, Thurnherr A, Mincks S, Rogers A, Clark M, Baco-Tyler A, Bernardino A, De Leo F, Dutrieux P, Riesner A, Kittinger J, Padilla-Gamino J, Prescott R, Srsen P (2008b) Rationale and recommendations for the estaplishment of preservation reference areas for nodule mining in the clarion-Clipperton zone. Legal and Technical Commission, Kingston

    Google Scholar 

  • Struck TH, Purschke G, Halanych KM (2005) A scaleless scale worm? Molecular evidence for the phylogenetic placement of Pisione remota (Pisionidae, Annelida). Mar Biol Res 1:243–253

    Article  Google Scholar 

  • Taboada S, Riesgo A, Wiklund H, Paterson GLJ, Koutsouveli V, Santodomingo N, Dale A, Smith CR, Jones DOB, Dahlgreen TG, Glover AG (2018) Implications of population connectivity studies for the design of marine protected areas in the deep sea: An example of a demosponge from the Clarion-Clipperton Zone. Mol Ecol 27:4657–4679.

    Article  PubMed  Google Scholar 

  • Tajima F (1989) Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tajima F (1996) Infinite-allele model and infinite-site model in population genetics. J Genet 75:27

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2725–2729

    Article  CAS  Google Scholar 

  • Taylor ML, Roterman CN (2017) Invertebrate population genetics across earth’s largest habitat: the deep-sea floor. Mol Ecol 26:4872–4896

    Article  PubMed  CAS  Google Scholar 

  • Teixera S, Cambon-Bonavita MA, Serrao EA, Desbruéres D, Arnaud-Haond S (2011) Recent population expansion and connectivity in the hydrothermal shrimp Rimicaris exoculata along the mid-Atlantic ridge. J Biogeogr 38(3):564–574

    Article  Google Scholar 

  • Thiel H, Schriever G, Bussau C, Borowski C (1993) Manganese nodule crevice fauna. Deep-Sea Res Pt I 40:419–423

    Article  Google Scholar 

  • Thiel H, Schriever G, Ahnert A, Bluhm H, Borowski C et al (2001) The large-scale environmental impact experiment DISCOL—reflection and foresight. Deep Sea Res II 48:3869–3882

    Article  Google Scholar 

  • Thistle D, Wilson GDF (1996) Is the HEBBLE isopod fauna hydrodynamically modified? A second test. Deep-Sea Res I 43:545–554

    Article  Google Scholar 

  • Tilot V, Ormond R, Moreno Navas J, Catalá TS (2018) The benthic Megafaunal assemblages of the CCZ (eastern Pacific) and an approach to their Management in the Face of threatened anthropogenic impacts. Front Mar Sci 5

  • Wedding LM, Friedlander AM, Kittinger JN, Watling L, Gaines SD, Bennett M, Hardy SM, Smith CR (2013) From principles to practices: a spatial approach to systematic conservation planning in the deep sea. Proc Biol Sci 280(1773):20131684

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wilson G (1987) Crustacean communities of the manganese Nodule Province. NOAA report on contract no. NA-84-ABH_0030

  • Wilson W (1991) Sexual reproductive modes in polychaetes: classification and diversity. Bull Mar Sci 48:1–16

    Google Scholar 

  • Ying H, Beifang N, Ying G, Limin F, Weizhong L (2010) CD-HIT: suite: a web server for clustering and comparing biological sequences. Bioinformatics 26:680–682

    Article  CAS  Google Scholar 

  • Van Dover CL (2000) The ecology of deep-sea hydrothermal vents. Princeton University Press, Princeton

    Book  Google Scholar 

  • Van Soosten C, Schmidt H, Westheide W (1998) Genetic variability and relationship among geographically widely seperated populations of Petitia amphophtalma (Polychaeta: Syllidae). Results from RAPD-PCR investigations. Mar Biol 131:659–669

    Article  Google Scholar 

  • Vanreusel A, Hilario A, Ribeiro PA, Menot L, Martínez Arbizu P (2016) Threatened by mining, polymetallic nodules are required to preserve abyssal epifauna. Sci Rep 6:26808

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Veillette J, Sarrazin J, Gooday AJ, Galeron J, Caprais JC, Vangriesheim A et al (2007) Ferromanganese nodule fauna in the Tropical North Pacific ocean: species richness, faunal cover and spatial distribution. Deep Sea Res I Oceanogr Res Pap 54:1912–1935

    Article  Google Scholar 

  • Von Stackelberg U (1984) Significance of benthic organisms for the growth and movement of manganese nodules, equatorial North Pacific. Geo-Mar Lett 4:37–42

    Article  Google Scholar 

  • Vriejenhoek RC (2010) Genetic diversity and connectivity of deep-sea hydrothermal vent metapopulations. Mol Ecol 19:4391–4411

    Article  Google Scholar 

  • Zhang Y, Pham NK, Zhang H, Lin J, Lin Q (2014) Genetic variations in two seahorse species Hippocampus mohnikei and Hippocampus trimaculatus: evidence for middle pleistocene population expansion. PLoS One 9:1–10

    Google Scholar 

  • Zinssmeister C, Wilke T, Hoppenrath M (2016) Species diversity of dinophysid dinoflagellates in the Clarion-Clipperton Fracture Zone, eastern Pacific. Mar Biodivers 47(2):1–17

    Google Scholar 

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Acknowledgements

We thank the captains and the crews of RV ‘Sonne’, ‘L’Atalante’ and ‘Kilo Moana’ for their skilled help in sampling the material during the MANGAN 2010, 2013 and 2014 and Bionod 2012 cruises. We also thank Stefanie Kaiser, Nils Brenke and Karin Meissner (Research Institute Senckenberg am Meer; German Center for Marine Biodiversity (DZMB, Wilhelmshaven and Hamburg)) for their help in determining the morpho-species of isopods and polychaetes. Additionally we would like to thank Uwe Raschka (Research Institute Senckenberg am Meer; DZMB, Wilhelmshaven) for assistance with DNA sequencing. The authors thank the anonymous reviewers for providing helpful comments and suggestions on earlier versions of the manuscript.

Funding

Annika Janssen was financially supported by the Federal Ministry of Education and Research (BMBF, Germany, grant 03G0205D), the Federal Institute of Geosciences and Natural Resources (BGR, Germany), and the French Research Institute for Exploitation of the Sea (IFREMER, France). Heiko Stuckas and Pedro Martínez Arbizu received funding from the European Union Seventh Framework Programme (FP7/2007-2013) under the MIDAS project, grant agreement no. 603418. Pedro Martínez Arbizu received financial support from the Federal Ministry of Education and Research (BMBF, Germany, grant 03F0707E) under the JPI Oceans MiningImpact project.

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Correspondence to Annika Janssen or Heiko Stuckas.

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The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable.

Data availability

All sequences newly obtained in this study have been deposited in GenBank under accession numbers KX226464 - KX227103.

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Communicated by S. Kaiser

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Electronic supplementary material

ESM 1

Haplotype networks (Minimum-Spanning-Trees) for polychaete species based on sampling years. a. Paralacydonia cf. weberi (MOTU 0); b. Sigalionidae sp. 1 (MOTU 1); c. Lumbrineris sp. 1 (MOTU 2); d. Bathyglycinde cf. profunda (MOTU 3); e. Sigalionidae sp. 2 (MOTU 4). (PNG 1111 kb)

High resolution image (TIFF 1035 kb)

ESM 2

Haplotype networks (Minimum-Spanning-Trees) for isopod species based on sampling years. a. Macrostylis sp. 1 (MOTU 0); b. Macrostylis sp. 2 (MOTU 1); c. Desmosomatidae sp. 1 (MOTU 2); d. Eugerdella sp. 1 (MOTU 3); e. Eugerdella sp. 2 (MOTU 4). (PNG 642 kb)

High resolution image (TIFF 605 kb)

ESM 3

Polychaete and isopod specimens used in this study including species name, MOTU assignment, sequence ID, Genbank accession numbers, expedition and sample location (DOCX 66 kb)

ESM 4

Diversity and demography parameters for each polychaete population (≥ 4 specimens). NSeq = number of sequences, NHap = number of haplotypes, Hd = haplotype diversity, π = nucleotide diversity, ns = not significant, SSD = Sums of Squares Deviation (refers to expansion model based on mismatch distribution), r = Raggedness index. (DOCX 41 kb)

ESM 5

Diversity and demography parameters for each isopod population (≥ 4 specimens). NSeq = number of sequences, NHap = number of haplotypes, Hd = haplotype diversity, π = nucleotide diversity, ns = not significant; SSD = Sums of Squares Deviation (refers to expansion model based on mismatch distribution), r = Raggedness index. (DOCX 31 kb)

ESM 6

(DOCX 15 kb)

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Janssen, A., Stuckas, H., Vink, A. et al. Biogeography and population structure of predominant macrofaunal taxa (Annelida and Isopoda) in abyssal polymetallic nodule fields: implications for conservation and management. Mar. Biodivers. 49, 2641–2658 (2019). https://doi.org/10.1007/s12526-019-00997-1

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