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A comparison of epiphytic nematode diversity and assemblages in Corallina turves on British and South Korean coasts across hierarchical spatial scales

Published online by Cambridge University Press:  26 June 2019

Hyeong-Gi Kim ,
Lawrence E. Hawkins ,
Jasmin A. Godbold ,
Moira Maclean ,
Chul-Woong Oh ,
Hyun Soo Rho  and
Stephen J. Hawkins
Hyeong-Gi Kim*
Affiliation:
Ocean and Earth Science, National Oceanography Centre Southampton, University of Southampton, Southampton SO14 3ZH, UK School of Earth and Environmental Sciences and Research Institute of Oceanography, Seoul National University, Seoul, R. Korea, 08826
Lawrence E. Hawkins
Affiliation:
Ocean and Earth Science, National Oceanography Centre Southampton, University of Southampton, Southampton SO14 3ZH, UK
Jasmin A. Godbold
Affiliation:
Ocean and Earth Science, National Oceanography Centre Southampton, University of Southampton, Southampton SO14 3ZH, UK
Moira Maclean
Affiliation:
Ocean and Earth Science, National Oceanography Centre Southampton, University of Southampton, Southampton SO14 3ZH, UK
Chul-Woong Oh
Affiliation:
Department of Marine Biology, Pukyoung National University, Busan, R. Korea, 48513
Hyun Soo Rho
Affiliation:
Korea Institute of Ocean Science and Technology, Gyeongbuk, R. Korea, 36315
Stephen J. Hawkins
Affiliation:
Ocean and Earth Science, National Oceanography Centre Southampton, University of Southampton, Southampton SO14 3ZH, UK Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, PL1 2PB, UK
*
Author for correspondence: Hyeong-Gi Kim, E-mail: [email protected]
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Abstract

Cosmopolitan habitat-forming taxa of algae such as the genus Corallina provide an opportunity to compare patterns of biodiversity over wide geographic scales. Nematode assemblages inhabiting Corallina turves were compared between the south coasts of the British Isles and South Korea. A fully nested design was used with three regions in each country, two shores in each region and replicate samples taken from three patches on each shore to compare differences in the taxonomic and biological trait composition of nematode assemblages across scales. A biological traits approach, based on functional diversity of nematodes, was used to make comparisons between countries, among regions, between shores and among patches. The taxonomic and biological trait compositions of nematode assemblages were significantly different across all spatial scales (patches, shores, regions and countries). There is greater variation amongst nematode assemblages at the scale of shore than at other spatial scales. Nematode assemblage structure and functional traits are influenced by the local environmental factors on each shore including sea-surface temperature, the amount of sediment trapped in Corallina spp. and tidal range. The sea-surface temperature and the amount of sediment trapped in Corallina spp. were the predominant factors determining nematode abundance and composition of assemblages and their functional diversity.

Keywords

Biodiversitybroad-scale comparisonCorallinahabitat provisionnematodes
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 7 , November 2019 , pp. 1481 - 1493
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

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References

Anderson, M, Gorley, RN and Clarke, RK (2008) Permanova + for Primer: Guide to Software and Statistical Methods. Plymouth: Primer-E Ltd.Google Scholar
Andrew, N and Mapstone, B (1987) Sampling and the description of spatial pattern in marine ecology. Oceanography and Marine Biology 25, 39–90.Google Scholar
Armenteros, M, Ruiz-Abierno, A, Fernández-Garcés, R, Pérez-García, JA, Díaz-Asencio, L, Vincx, M and Decraemer, W (2009) Biodiversity patterns of free-living marine nematodes in a tropical bay: Cienfuegos, Caribbean Sea. Estuarine, Coastal and Shelf Science 85, 179–189.Google Scholar
Bell, SS and Coen, LD (1982) Investigations on epibenthic meiofauna. Influence of microhabitat and macroalgae on abundance of small invertebrates on Diopatra cuprea (Bosc) (Polychaeta: Onuphidae) tube-caps in Virginia. Journal of Experimental Marine Biology and Ecology 61, 175–188.Google Scholar
Blome, D, Schleier, U and van Bernem, K-H (1999) Analysis of the small-scale spatial patterns of free-living marine nematodes from tidal flats in the East Frisian Wadden Sea. Marine Biology 133, 717–726.Google Scholar
Bongers, T (1999) The maturity index, the evolution of nematode life history traits, adaptive radiation and cp-scaling. Plant and Soil 212, 13–22.Google Scholar
Bongers, T, Alkemade, R and Yeates, G (1991) Interpretation of disturbance-induced maturity decrease in marine nematode assemblages by means of the Maturity Index. Marine Ecology Progress Series 76, 135–142.Google Scholar
Bracken, ME, Gonzalez-Dorantes, CA and Stachowicz, JJ (2007) Whole-community mutualism: associated invertebrates facilitate a dominant habitat-forming seaweed. Ecology 88, 2211–2219.Google Scholar
Brauko, KM, de Souza, FM, Muniz, P, de Camargo, MG and da Cunha Lana, P (2015) Spatial variability of three benthic indices for marine quality assessment in a subtropical estuary of Southern Brazil. Marine Pollution Bulletin 91, 454–460.Google Scholar
Bremner, J, Rogers, S and Frid, C (2003) Assessing functional diversity in marine benthic ecosystems: a comparison of approaches. Marine Ecology Progress Series 254, 11–25.Google Scholar
Cardinale, BJ, Duffy, JE, Gonzalez, A, Hooper, DU, Perrings, C, Venail, P, Narwani, A, Mace, GM, Tilman, D and Wardle, DA (2012) Biodiversity loss and its impact on humanity. Nature 486, 59–67.Google Scholar
Clarke, K and Gorley, RN (2006) V6: User Manual/Tutorial. Plymouth: Primer-E Ltd.Google Scholar
Coleman, RA, Underwood, AJ, Benedetti-Cecchi, L, Åberg, P, Arenas, F, Arrontes, J, Castro, J, Hartnoll, RG, Jenkins, SR and Paula, J (2006) A continental scale evaluation of the role of limpet grazing on rocky shores. Oecologia 147, 556–564.Google Scholar
Da Rocha, C, Venekey, V, Bezerra, T and Souza, J (2006) Phytal marine nematode assemblages and their relation with the macrophytes structural complexity in a Brazilian tropical rocky beach. Hydrobiologia 553, 219–230.Google Scholar
Danovaro, R and Gambi, C (2002) Biodiversity and trophic structure of nematode assemblages in seagrass systems: evidence for a coupling with changes in food availability. Marine Biology 141, 667–677.Google Scholar
De Oliveira, DA, Derycke, S, Da Rocha, CM, Barbosa, DF, Decraemer, W and Dos Santos, GA (2016) Spatiotemporal variation and sediment retention effects on nematode communities associated with Halimeda opuntia (Linnaeus) Lamouroux (1816) and Sargassum polyceratium Montagne (1837) seaweeds in a tropical phytal ecosystem. Marine Biology 163, 1–13.Google Scholar
Dray, S,Pélissier, R, Couteron, P, Fortin, M-J, Legendre, P, Peres-Neto, P, Bellier, E, Bivand, R, Blanchet, FG and De Cáceres, M (2012) Community ecology in the age of multivariate multiscale spatial analysis. Ecological Monographs 82, 257–275.Google Scholar
Eckman, JE and Thistle, D (1988) Small-scale spatial pattern in meiobenthos in the San Diego Trough. Deep Sea Research Part A. Oceanographic Research Papers 35, 1565–1578.Google Scholar
Fonseca, G, Soltwedel, T, Vanreusel, A and Lindegarth, M (2010) Variation in nematode assemblages over multiple spatial scales and environmental conditions in Arctic deep seas. Progress in Oceanography 84, 174–184.Google Scholar
Frey, MA (2010) The relative importance of geography and ecology in species diversification: evidence from a tropical marine intertidal snail (Nerita). Journal of Biogeography 37, 1515–1528.Google Scholar
Galéron, J, Sibuet, M, Mahaut, M-L and Dinet, A (2000) Variation in structure and biomass of the benthic communities at three contrasting sites in the tropical Northeast Atlantic. Marine Ecology Progress Series 167, 121–137.Google Scholar
Gee, J and Warwick, R (1994 a) Metazoan community structure in relation to the fractal dimensions of marine macroalgae. Marine Ecology Progress Series 103, 141–150.Google Scholar
Gee, JM and Warwick, RM (1994 b) Body-size distribution in a marine metazoan community and the fractal dimensions of macroalgae. Journal of Experimental Marine Biology and Ecology 178, 247–259.Google Scholar
Gering, JC and Crist, TO (2002) The alpha–beta–regional relationship: providing new insights into local–regional patterns of species richness and scale dependence of diversity components. Ecology Letters 5, 433–444.Google Scholar
Gestoso, I, Olabarria, C and Troncoso, JS (2010) Variability of epifaunal assemblages associated with native and invasive macroalgae. Marine and Freshwater Research 61, 724–731.Google Scholar
Gibbons, M (1988) The impact of wave exposure on the meiofauna of Gelidium pristoides (Turner) Kuetzing (Gelidiales: Rhodophyta). Estuarine, Coastal and Shelf Science 27, 581–593.Google Scholar
Giere, O (2009) Meiobenthology: The Microscopic Motile Fauna of Aquatic Sediments. Berlin: Springer.Google Scholar
Gobin, JF and Warwick, RM (2006) Geographical variation in species diversity: a comparison of marine polychaetes and nematodes. Journal of Experimental Marine Biology and Ecology 330, 234–244.Google Scholar
Heip, C, Vincx, M and Vranken, G (1985) The ecology of marine nematodes. Oceanography and Marine Biology: An Annual Review 23, 399–489.Google Scholar
Hewitt, JE, Thrush, SF, Halliday, J and Duffy, C (2005) The importance of small-scale habitat structure for maintaining beta diversity. Ecology 86, 1619–1626.Google Scholar
Hill, MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432.Google Scholar
Hooper, DU, et al. (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75, 3–35.Google Scholar
Horner-Devine, MC, Carney, KM and Bohannan, BJ (2004) An ecological perspective on bacterial biodiversity. Proceedings of the Royal Society of London B: Biological Sciences 271, 113–122.Google Scholar
Huff, TM and Jarett, JK (2007) Sand addition alters the invertebrate community of intertidal coralline turf. Marine Ecology Progress Series 345, 75–82.Google Scholar
Huh, OK (1982) Spring season flow of the Tsushima Current and its separation from the Kuroshio: satellite evidence. Journal of Geophysical Research: Oceans 87(C12), 9687–9693.Google Scholar
Ingels, J and Vanreusel, A (2013) The importance of different spatial scales in determining structural and functional characteristics of deep-sea infauna communities. Biogeosciences (Online) 10, 4547–4563.Google Scholar
Isbell, F, Calcagno, V, Hector, A, Connoly, J, Harpole, WS, Reich, PB, Scherer-Lorezen, M, Schmid, B, Tilman, D, Van Ruijven, J, Weigelt, A, Wilsey, BJ, Zavaleta, ES and Loreau, M (2011) High plant diversity is needed to maintain ecosystem services. Nature 477, 199–202.Google Scholar
Jenkins, SR, Aberg, P, Cervin, G, Coleman, RA, Delany, J, Della Santina, P, Hawkin, SJ, LaCroix, E, Myers, AA, Lindegarth, M, Power, AM, Roberts, MF and Hartnoll, RG (2000) Spatial and temporal variation in settlement and recruitment of the intertidal barnacle Semibalanus balanoides (L.) (Crustacea: Cirripedia) over a European scale. Journal of Experimental Marine Biology and Ecology 243, 209–225.Google Scholar
Jenkins, S, Coleman, R, Della Santina, P, Hawkins, S, Burrows, M and Hartnoll, R (2005) Regional scale differences in the determinism of grazing effects in the rocky intertidal. Marine Ecology Progress Series 287, 77–86.Google Scholar
Kelaher, B, Chapman, M and Underwood, A (2001) Spatial patterns of diverse macrofaunal assemblages in coralline turf and their associations with environmental variables. Journal of the Marine Biological Association of the United Kingdom 81, 917–930.Google Scholar
Kelaher, BP, Castilla, JC and Seed, R (2004) Intercontinental test of generality for spatial patterns among diverse molluscan assemblages in coralline algal turf. Marine Ecology Progress Series 271, 221–231.Google Scholar
Kim, HG, Hawkins, LE, Godbold, JA, Oh, CW, Rho, HS and Hawkins, SJ (2019) Comparison of nematode assemblages associated with Sargassum muticum in its native range in South Korea and as an invasive species in the English Channel. Marine Ecology Progress Series 611, 95–110.Google Scholar
Liuzzi, MG and López Gappa, J (2011) Algae as hosts for epifaunal bryozoans: role of functional groups and taxonomic relatedness. Journal of Sea Research 65, 28–32.Google Scholar
Mayr, E (1942) Systematics and the Origin of Species, From the Viewpoint of a Zoologist. New York, NY: Columbia University Press.Google Scholar
McEwen, GF, Johnson, MW and Folsom, TR (1954) A statistical analysis of the performance of the Folsom plankton sample splitter, based upon test observations. Archiv für Meteorologie, Geophysik und Bioklimatologie, Serie A 7, 502–527.Google Scholar
Moens, T, Braeckman, U, Derycke, S, Fonseca, G, Gallucci, F, Gingold, R, Guilini, K, Ingels, J, Leduc, D, Vanaverbeke, J, Colen, CV, Vanreusel, A and Vincx, M (2013) Ecology of free-living marine nematodes. In Schmidt-Rhaesa, A (ed.), Handbook of Zoology: Gastrotricha, Cycloneuralia and Gnathifera, vol. 2, Nematoda. Berlin: de Gruyter, pp. 109–152.Google Scholar
Mouillot, D, Mason, WN, Dumay, O and Wilson, JB (2005) Functional regularity: a neglected aspect of functional diversity. Oecologia 142, 353–359.Google Scholar
Muniz, P, Hutton, M, Kandratavicius, N, Lanfranconi, A, Brugnoli, E, Venturini, N and Giménez, L (2012) Performance of biotic indices in naturally stressed estuarine environments on the Southwestern Atlantic coast (Uruguay): a multiple scale approach. Ecological Indicators 19, 89–97.Google Scholar
Murphy, R, Tolhurst, T, Chapman, M and Underwood, A (2009) Seasonal distribution of chlorophyll on mudflats in New South Wales, Australia measured by field spectrometry and PAM fluorometry. Estuarine, Coastal and Shelf Science 84, 108–118.Google Scholar
Noss, RF (1990) Indicators for monitoring biodiversity: a hierarchical approach. Conservation Biology 4, 355–364.Google Scholar
Pérez-García, J, Ruiz-Abierno, A and Armenteros, M (2015) Does morphology of host marine macroalgae drive the ecological structure of epiphytic meiofauna? Journal of Marine Biology & Oceanography 4(1), 1–7.Google Scholar
Petchey, OL and Gaston, KJ (2002) Functional diversity (FD), species richness and community composition. Ecology Letters 5, 402–411.Google Scholar
Petchey, OL and Gaston, KJ (2006) Functional diversity: back to basics and looking forward. Ecology Letters 9, 741–758.Google Scholar
Pingree, R and Griffiths, D (1980) Currents driven by a steady uniform wind stress on the shelf seas around the British Isles. Oceanologica Acta 3, 227–236.Google Scholar
Piot, A, Nozais, C and Archambault, P (2013) Meiofauna affect the macrobenthic biodiversity–ecosystem functioning relationship. Oikos 123, 203–213.Google Scholar
Platt, HM and Warwick, RM (1983) Freeliving Marine Nematodes. Part 1: British Enoplids. Pictorial Key to World Genera and Notes for the Identification of British Species. Cambridge: Cambridge University Press.Google Scholar
Rex, MA, Stuart, CT, Hessler, RR, Allen, JA, Sanders, HL and Wilson, GD (1993) Global-scale latitudinal patterns of species diversity in the deep-sea benthos. Nature 365, 636–639.Google Scholar
Sanders, HL (1968) Marine benthic diversity: a comparative study. American Naturalist 102, 243–282.Google Scholar
Schaff, T and Levin, L (1994) Spatial heterogeneity of benthos associated with biogenic structures on the North Carolina continental slope. Deep Sea Research Part II: Topical Studies in Oceanography 41, 901–918.Google Scholar
Schmidt-Rhaesa, A (ed) (2014) Handbook of Zoology. Gastrotricha, Cycloneuralia, Gnathifera, vol. 2. Nematoda. Berlin: de Gruyter.Google Scholar
Schratzberger, M, Warr, K and Rogers, S (2007) Functional diversity of nematode communities in the southwestern North Sea. Marine Environmental Research 63, 368–389.Google Scholar
Shirayama, Y, Kaku, T and Higgins, RP (1993) Double-sided microscopic observation of meiofauna using an HS-slide. Benthos Research 1993, 41–44.Google Scholar
Snelgrove, PV, Grassle, J and Petrecca, R (1992) The role of food patches in maintaining high deep-sea diversity: field experiments with hydrodynamically unbiased colonization trays. Limnology and Oceanography 37, 1543–1550.Google Scholar
Thistle, D and Sherman, KM (1985) The nematode fauna of a deep-sea site exposed to strong near-bottom currents. Deep-Sea Research Part I: Oceanographic Research Papers 32, 1077–1088.Google Scholar
Thistle, D, Lambshead, P and Sherman, K (1995) Nematode tail-shape groups respond to environmental differences in the deep sea. Vie et Milieu 45, 107–116.Google Scholar
Underwood, AJ (1997) Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance. Cambridge: Cambridge University Press.Google Scholar
Vanreusel, A, Vincx, M, Bett, BJ and Rice, AL (1995) Nematode biomass spectra at two abyssal sites in the NE Atlantic with a contrasting food supply. International Review of Hydrobiology 80, 287–296.Google Scholar
Veiga, P, Sousa-Pinto, I and Rubal, M (2016) Meiofaunal assemblages associated with native and non-indigenous macroalgae. Continental Shelf Research 123, 1–8.Google Scholar
Walker, B, Kinzig, A and Langridge, J (1999) Plant attribute diversity, resilience, and ecosystem function: the nature and significance of dominant and minor species. Ecosystems 2, 95–113.Google Scholar
Walker, RH, Brodie, J, Russell, S, Irvine, LM and Orfanidis, S (2009) Biodiversity of coralline algae in the north eastern Atlantic including Corallina caespitosa sp. nov. (Corallinoideae, Rhodophyta). Journal of Phycology 45, 287–297.Google Scholar
Wieser, W (1953) Die Beziehung zwischen Mundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebenden marinen Nematoden: eine ökologisch-morphologische Studie. Arkiv für Zoologie 2, 439–484.Google Scholar
Wieser, W (1959) The effect of grain size on the distribution of small invertebrates inhabiting the beaches of Puget Sound. Limnology and Oceanography 4, 181–194.Google Scholar
Witman, JD, Etter, RJ and Smith, F (2004) The relationship between regional and local species diversity in marine benthic communities: a global perspective. Proceedings of the National Academy of Sciences USA 101, 15664–15669.Google Scholar
WoRMS Editorial Board (2019) World Register of Marine Species. Available at http://www.marinespecies.org at VLIZ. (Accessed 31 March 2019). doi: 10.14284/170.Google Scholar
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