Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T03:10:59.323Z Has data issue: false hasContentIssue false
  • English
  • Français

Simple harpacticoid composition observed at deep hydrothermal vent sites on sea knoll calderas in the North-west Pacific

Published online by Cambridge University Press:  07 January 2022

Futa Nakasugi ,
Motohiro Shimanaga Open the ORCID record for Motohiro Shimanaga [Opens in a new window] ,
Hidetaka Nomaki ,
Hiromi Kayama Watanabe Open the ORCID record for Hiromi Kayama Watanabe [Opens in a new window] ,
Tomo Kitahashi Open the ORCID record for Tomo Kitahashi [Opens in a new window] ,
Yusuke Motomura  and
Koki Iseda
Futa Nakasugi
Affiliation:
Graduate School of Science and Technology, Kumamoto University, 39-1, Kurokami 2-chome, Chuo-ku, Kumamoto 860-8555, Japan
Motohiro Shimanaga*
Affiliation:
Center for Water Cycle, Marine Environment and Disaster Management, Kumamoto University, 39-1, Kurokami 2-chome, Chuo-ku, Kumamoto 860-8555, Japan
Hidetaka Nomaki
Affiliation:
X-star, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
Hiromi Kayama Watanabe
Affiliation:
X-star, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
Tomo Kitahashi
Affiliation:
RIGC, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan
Yusuke Motomura
Affiliation:
Graduate School of Science and Technology, Kumamoto University, 39-1, Kurokami 2-chome, Chuo-ku, Kumamoto 860-8555, Japan
Koki Iseda
Affiliation:
Graduate School of Science and Technology, Kumamoto University, 39-1, Kurokami 2-chome, Chuo-ku, Kumamoto 860-8555, Japan
*
Author for correspondence: Motohiro Shimanaga, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Dirivultid copepods (Siphonostomatoida), one of the most successful meiobenthic organisms found at deep-sea hydrothermal vents, have been the focus of most previous ecological studies among meiofauna in these habitats. The ecology of Harpacticoida, a major benthic copepod group in typical deep-sea floor, however, is not well understood in terms of variations in community structure and controlling factors at venting sites. The spatial heterogeneities in benthic harpacticoid composition and their association with environmental parameters were investigated at hydrothermal vent chimney structures in the calderas of three neighbouring sea knolls (Bayonnaise Knoll, Myojin Knoll and Myojin-sho Caldera) in the western North Pacific. While a previous study had reported the distribution of dirivultids was strongly associated with spatial differences in stable carbon isotopic signatures (δ13C) of organic matter in the detritus on active chimneys in the field, multivariate analyses detected no significant corelation between the parameter and harpacticoid composition in this study. Instead, high associations of the harpacticoid composition with differences in water depth and total organic carbon (TOC) concentration were detected. Ectinosomatidae dominated at vent sites with lower TOC values in the shallowest Bayonnaise Knoll, while they were less prevalent at deeper vent fields in the other knolls, where Miraciidae was the most abundant family. This study indicated the availability of vent chemoautotrophic carbon is not a primary factor controlling the composition of harpacticoids even in the habitats on the hydrothermal vents, but instead by the food amount, regardless of its resources (including marine snow from the sea surface), in the study area.

Keywords

Chemosynthesischimneycommunity compositioncopepoddeep seameiofauna
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 101 , Issue 6 , September 2021 , pp. 947 - 956
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, MJ, Gorley, RN and Clarke, KR (2008) PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. Plymouth: PRIMER-E.Google Scholar
Back, J, Huys, R and Lee, W (2010) A new species of the genus Tegastes (Copepoda: Harpacticoida: Tegastidae) from hydrothermal vents in the Okinawa Trough. Zoological Science 27, 678–688.CrossRefGoogle ScholarPubMed
Baldrighi, E, Zeppilli, D, Crespin, R, Chauvaud, P, Pradillon, F and Sarrazin, J (2017) Colonization of synthetic sponges at the deep-sea lucky strike hydrothermal vent field (Mid-Atlantic Ridge): a first insight. Marine Biodiversity 48, 89–103.CrossRefGoogle Scholar
Boxshall, GA and Halsey, SA (2004) An Introduction to Copepod Diversity. London: The Ray Society.Google Scholar
Clarke, KR and Warwick, RM (2001) Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd Edn. Plymouth: PRIMER-E.Google Scholar
Copley, JTP, Flint, HC, Ferrero, TJ and Van Dover, CL (2007) Diversity of meiofauna and free-living nematodes in hydrothermal vent mussel beds on the northern and southern East Pacific Rise. Journal of the Marine Biological Association of the United Kingdom 87, 1141–1152.CrossRefGoogle Scholar
Cuvelier, D, Beesau, J, Ivanenko, V, Zeppilli, D, Sarradin, PM and Sarrazin, J (2014) First insights into macro- and meiofaunal colonisation patterns on paired wood/slate substrata at Atlantic deep-sea hydrothermal vents. Deep-Sea Research Part I 87, 70–81.CrossRefGoogle Scholar
Degen, R, Riavitz, L, Gollner, S, Vanreusel, A, Plum, C and Bright, M (2012) Community study of tubeworm-associated epizooic meiobenthos from deep-sea cold seeps and hot vents. Marine Ecology Progress Series 468, 135–148.CrossRefGoogle Scholar
Dinet, A, Grassle, F and Tunnicliffe, V (1988) Premières observations sur la méiofaune des hydrothermaux de la dorsale Est-Pacifique (Guaymas, 21°N) et de l'Explorer Ridge (First observations on the meiofauna from hydrothermal vents of the East Pacifie Rise [Guaymas, 21°N] and Explorer Ridge). Oceanologica Acta 85, 7–14. [In French with English abstract].Google Scholar
Dubilier, N, Bergin, C and Lott, C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Reviews Microbiology 6, 725–740.CrossRefGoogle ScholarPubMed
Flint, HC, Copley, JTP, Ferrero, TJ and Van Dover, CL (2006) Patterns of nematode diversity at hydrothermal vents on the East Pacific Rise. Cahiers de Biologie Marine 47, 365–370.Google Scholar
Gollner, S, Zekely, J, Van Dover, CL, Govenar, B, Le Bris, N, Nemeschkal, HL and Bright, M (2006) Benthic copepod communities associated with tubeworm and mussel aggregations on the East Pacific Rise. Cahiers de Biologie Marine 47, 397–402.Google Scholar
Gollner, S, Zekely, J, Govenar, B, Le Bris, N, Nemeschkal, HL, Fisher, CR and Bright, M (2007) Tubeworm-associated permanent meiobenthic communities from two chemically different hydrothermal vent sites on the East Pacific Rise. Marine Ecology Progress Series 337, 39–49.CrossRefGoogle Scholar
Gollner, S, Riemer, B, Arbizu, PM, Le Bris, N and Bright, M (2010 a) Diversity of meiofauna from the 9°50′N East Pacific Rise across a gradient of hydrothermal fluid emissions. PLoS ONE 5, e12321.CrossRefGoogle ScholarPubMed
Gollner, S, Ivanenko, VN, Arbizu, PM and Bright, M (2010 b) Advances in taxonomy, ecology, and biogeography of Dirivultidae (Copepoda) associated with chemosynthetic environments in the deep sea. PLoS ONE 5, e9801.CrossRefGoogle ScholarPubMed
Gollner, S, Govenar, B, Fisher, CR and Bright, M (2015 a) Size matters at deep-sea hydrothermal vents: different diversity and habitat fidelity patterns of meio- and macrofauna. Marine Ecology Progress Series 520, 57–66.CrossRefGoogle ScholarPubMed
Gollner, S, Govenar, B, Martinez Arbizu, P, Mills, S, Le Bris, N, Weinbauer, M, Shank, TM and Bright, M (2015 b) Differences in recovery between deep-sea hydrothermal vent and vent-proximate communities after a volcanic eruption. Deep-Sea Research Part I 106, 167–182.CrossRefGoogle Scholar
Gollner, S, Govenar, B, Martinez Arbizu, P, Mullineaux, LS, Mills, S, Le Bris, N, Weinbauer, M, Shank, TM and Bright, M (2020) Animal community dynamics at senescent and active vents at the 9°N east pacific rise after a volcanic eruption. Fronters in Marine Science 6, 832.CrossRefGoogle Scholar
Hicks, GRF and Coull, BC (1983) The ecology of marine meiobenthic harpacticoid copepods. Oceanography and Marine Biology, an Annual Review 21, 67–175.Google Scholar
Huys, R, Gee, JM, Moore, CG and Hamond, R (1996) Marine and Brackish Water Harpacticoid Copepods, Part 1. Shrewsbury: Field Studies Council.Google Scholar
Ivanenko, VN (1998) Deep-sea hydrothermal vent Copepoda (Siphonostomatoida, Dirivultidae) in plankton over the Mid-Atlantic Ridge (29°N), morphology of their first copepodid stage. Zoologicheskii Zhurnal 77, 1249–1256. [In Russian with English abstract.]Google Scholar
Ivanenko, VN, Martínez Arbizu, P and Stecher, J (2007) Lecithotrophic nauplius of the family Dirivultidae (Copepoda; Siphonostomatoida) hatched on board over the Mid-Atlantic Ridge (5°S). Marine Ecology 28, 49–53.CrossRefGoogle Scholar
Ivanenko, VN, Ferrari, FD, Defaye, D and Sarradin, PM (2011) Description, distribution and microhabitats of a new species of Tisbe (Copepoda: Harpacticoida: Tisbidae) from a deep-sea hydrothermal vent field at the Mid-Atlantic Ridge (37°N, Lucky Strike). Cahiers de Biologie Marine 52, 89–106.Google Scholar
Ivanenko, VN, Corgosinho, PHC, Ferrari, F, Sarradin, PM and Sarrazin, J (2012) Microhabitat distribution of Smacigastes micheli (Copepoda: Harpacticoida: Tegastidae) from deep-sea hydrothermal vents at the Mid-Atlantic Ridge, 37°N (Lucky Strike), with a morphological description of its nauplius. Marine Ecology 33, 246–256.CrossRefGoogle Scholar
Kouris, A, Limén, H, Stevens, CJ and Juniper, SK (2010) Blue mats: faunal composition and food web structure in colonial ciliate (Folliculinopsis sp.) mats at Northeast Pacific hydrothermal vents. Marine Ecology Progress Series 412, 93–101.CrossRefGoogle Scholar
Lee, W and Huys, R (2000) New Aegisthidae (Copepoda: Harpacticoida) from western Pacific cold seeps and hydrothermal vents. Zoological Journal of the Linnean Society 129, 1–71.CrossRefGoogle Scholar
Limén, H, Levesque, C and Juniper, SK (2007) POM in macro-/meiofaunal food webs associated with three flow regimes at deep-sea hydrothermal vents on Axial Volcano, Juan de Fuca Ridge. Marine Biology 153, 129–139.CrossRefGoogle Scholar
Lorenzo, CDR, ter Bruggen, D, Luther, GWIII and Gartman, GS (2021) Copepod assemblages along a hydrothermal stress gradient at diffuse flow habitats within the ABE vent site (Eastern Lau Spreading Center, Southwest Pacific). Deep-Sea Research I 173, 103532.CrossRefGoogle Scholar
Nomaki, H, Uejima, Y, Ogawa, NO, Yamane, M, Watanabe, HK, Senokuchi, R, Bernhard, JM, Kitahashi, T, Miyairi, Y, Yokoyama, Y, Ohkouchi, N and Shimanaga, M (2019) Nutritional sources of meio- and macrofauna at hydrothermal vents and adjacent areas: natural-abundance radiocarbon and stable isotope analyses. Marine Ecology Progress Series 622, 49–65.CrossRefGoogle Scholar
Plum, C, Pradillon, F, Fujiwara, Y and Sarrazin, J (2017) Copepod colonization of organic and inorganic substrata at a deep-sea hydrothermal vent site on the Mid-Atlantic Ridge. Deep-Sea Research Part II 137, 335–348.CrossRefGoogle Scholar
Sarrazin, J, Legendre, P, De Busserolles, F, Fabri, MC, Guilini, K, Ivanenko, VN, Morineaux, M, Vanreusel, A and Sarradin, PM (2015) Biodiversity patterns, environmental drivers and indicator species on a high-temperature hydrothermal edifice, mid-Atlantic ridge. Deep-Sea Research Part II 121, 177–192.CrossRefGoogle Scholar
Senokuchi, R, Nomaki, H, Watanabe, HK, Kitahashi, T, Ogawa, NO and Shimanaga, M (2018) Chemoautotrophic food availability influences copepod assemblage composition at deep hydrothermal vent sites within sea knoll calderas in the northwestern Pacific. Marine Ecology Progress Series 607, 37–51.CrossRefGoogle Scholar
Setoguchi, Y, Nomaki, H, Kitahashi, T, Watanabe, H, Inoue, K, Ogawa, NO and Shimanaga, M (2014) Nematode community composition in hydrothermal vent and adjacent non-vent fields around Myojin Knoll, a seamount on the Izu-Ogasawara Arc in the western North Pacific Ocean. Marine Biology 161, 1775–1785.CrossRefGoogle Scholar
Shimanaga, M, Kitahashi, T and Kawamura, K (2019) First insight of bathymetric patterns among deep-sea harpacticoid diversity and composition on landward slopes of subduction zones along the Japanese island arc. Journal of Oceanography 75, 475–484.CrossRefGoogle Scholar
Shirayama, Y (1992) Studies of meiofauna collected from the Iheya Ridge during the dive 541 of the SHINKAI 2000. Proceedings JAMSTEC Symposium Deep Sea Research 1992, 287–290. [In Japanese with English abstract.]Google Scholar
Thistle, D, Sedlacek, L, Carman, KR, Fleeger, JW and Barry, JP (2007) Emergence in the deep sea: evidence from harpacticoid copepods. Deep Sea Research Part I 54, 1008–1014.CrossRefGoogle Scholar
Tsurumi, M, de Graaf, RC and Tunnicliffe, V (2003) Distributional and biological aspects of copepods at hydrothermal vents on the Juan de Fuca Ridge, northeast Pacific Ocean. Journal of the Marine Biological Association of the United Kingdom 83, 469–477.CrossRefGoogle Scholar
Uejima, Y, Nomaki, H, Senokuchi, R, Setoguchi, Y, Kitahashi, T, Watanabe, HK and Shimanaga, M (2017) Meiofaunal communities in hydrothermal vent and proximate non-vent habitats around neighboring seamounts on the Izu-Ogasawara Arc, western North Pacific Ocean. Marine Biology 164, 183.CrossRefGoogle Scholar
Uyeno, D, Watanabe, HK and Shimanaga, M (2018) A new dirivultid copepod (Siphonostomatoida) from hydrothermal vent fields of the Izu-Bonin Arc in the North Pacific Ocean. Zootaxa 4415, 381–389.CrossRefGoogle ScholarPubMed
Van Dover, CL (2000) The Ecology of Deep-sea Hydrothermal Vents. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Vanreusel, A, Bossche, IV and Thiermann, F (1997) Free-living marine nematodes from hydrothermal sediments: similarities with communities from diverse reduced habitats. Marine Ecology Progress Series 157, 207–219.CrossRefGoogle Scholar
Vanreusel, A, De Groote, A, Gollner, S and Bright, M (2010) Ecology and biogeography of free-living nematodes associated with chemosynthetic environments in the deep sea: a review. PLoS ONE 5, e12449.CrossRefGoogle ScholarPubMed
Walter, TC and Boxshall, G (2021) World of Copepods Database. http://www.marinespecies.org/copepoda doi:10.14284/356. Accessed online 23 March 2021.CrossRefGoogle Scholar
Watanabe, H and Kojima, S (2015) Vent fauna in the Okinawa trough. In Ishibashi, J, Okino, K and Sunamura, M (eds), Subseafloor Biosphere Linked to Global Hydrothermal Systems. TAIGA Concept. Tokyo: Springer, pp. 449–459.Google Scholar
Watanabe, H, Fujikura, K, Kojima, S, Miyazaki, J and Fujiwara, Y (2010) Japan: vent and seeps in close proximity. In Kiel, S (ed.), The Vent and Seep Biota. New York, NY: Springer, pp. 379–402.CrossRefGoogle Scholar
Watanabe, H, Senokuchi, R, Nomaki, H, Kitahashi, T, Uyeno, D and Shimanaga, M (2021) Distribution and genetic divergence of deep-sea hydrothermal vent copepods (Dirivultidae: Siphonostomatoida: Copepoda) in the northwestern Pacific. Zoological Science 38, 223–230.CrossRefGoogle Scholar
Wells, JBJ (2007) An Annotated Checklist and Keys to the Species of Copepoda Harpacticoida (Crustacea). Auckland: Magnolia Press.CrossRefGoogle Scholar
Zekely, J, Gollner, S, Van Dover, CL, Govenar, B, Bris, NL, Nemeschkal, HL and Bright, M (2006 a) Nematode communities associated with tubeworm and mussel aggregations on the East Pacific Rise. Cahiers de Biologie Marine 47, 477–482.Google Scholar
Zekely, J, Van Dover, CL, Nemeschkal, HL and Bright, M (2006 b) Hydrothermal vent meiobenthos associated with mytilid mussel aggregations from the mid-Atlantic Ridge and the East Pacific Rise. Deep-Sea Research Part Ι 53, 1363–1378.CrossRefGoogle Scholar
Zeppilli, D, Vanreusel, A, Pradillon, F, Fuchs, S, Mandon, P, James, T and Sarrazin, J (2015) Rapid colonisation by nematodes on organic and inorganic substrata deployed at the deep-sea Lucky Strike hydrothermal vent field (Mid-Atlantic Ridge). Marine Biodiversity 45, 489–504.CrossRefGoogle Scholar
Zeppilli, D, Leduc, D, Fontanier, C, Fontaneto, D, Fuchs, S, Gooday, AJ, Goineau, A, Ingels, J, Ivanenko, VN, Kristensen, RM, Neves, RC, Sanchez, N, Sandulli, R, Sarrazin, J, Sørensen, MV, Tasiemski, A, Vanreusel, A, Autret, M, Bourdonnay, L, Claireaux, M, Coquillé, V, de Wever, L, Durand, R, Marchant, J, Toomey, L and Fernandes, D (2018) Characteristics of meiofauna in extreme marine ecosystems: a review. Marine Biodiversity 48, 35–71.CrossRefGoogle Scholar