Advertisement

Hydrobiologia

, Volume 846, Issue 1, pp 193–214 | Cite as

Environmental drivers of nematode abundance and genus composition at two spatial scales on an estuarine intertidal flat

  • Xiuqin WuEmail author
  • Ann Vanreusel
  • Freija Hauquier
  • Tom Moens
Primary Research Paper

Abstract

Estuarine intertidal flats are important ecosystems characterized by high primary production of microphytobenthos and high secondary production of macro- and meiofauna, especially nematodes. However, the link between both ecosystem components (microphytobenthos and faunal communities) is not fully established yet. In this study, spatial patterns and drivers of nematode density and genus composition were investigated at two different spatial scales (i.e. meso- and microscale), with drivers including sediment granulometry, inundation period and food availability as indicated by various phytopigments. Our study has shown that specific food sources, as represented by different pigments and measures of freshness, are important drivers of nematode genus composition and densities at both scales, especially for the surface layers of the sediments. These food sources mainly comprise microphytobenthos, but also deposited phytodetritus and zooplankton faecal pellets, a resource which had hitherto been largely overlooked in intertidal flats. Tidal level and grain size also had a more pronounced structuring effect in the surface layer of the sediment, while their assumed larger importance at the mesoscale was not outspoken. At both scales, vertical heterogeneity in nematode assemblages was larger than horizontal variability, which has repercussions for future studies into the spatial variability of nematode assemblages of tidal flats.

Keywords

Microphytobenthos Sediment granulometry Mesoscale Microscale 

Notes

Acknowledgements

Field samples from the microscale stations were collected in collaboration with NIOZ, which provided the necessary permit for field sampling, issued by the Province of Zeeland, The Netherlands, “Directie Ruimte, Milieu en Water.” Annick Van Kenhove and Guy De Smet provided invaluable support with making slides of nematodes. Dirk Van Gansbeke performed the pigment analyses and Bart Beuselinck completed the sediment granulometry analyses and total organic matter measurements. Niels Viaene is acknowledged for help during field sampling and extraction of nematodes. Renata Mamede da Silva Alves is acknowledged for making sampling maps. Two anonymous reviewers provided valuable feedback that helped to improve the manuscript.

Funding

The first author received a Ph.D. Grant of the Chinese Scholarship Council (2011633060) from November 2011 to November 2015, and received further financial support from the Flemish Science Fund FWO (G0H3817N). Additional support was provided by the special research fund of Ghent University (BOF 01SC3312) from March 2012 to October 2015.

Compliance with ethical standards

Conflict of interest

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.

Supplementary material

10750_2019_4064_MOESM1_ESM.docx (1.8 mb)
Supplementary material 1 (DOCX 1836 kb)

References

  1. Anderson, M. J. & J. Robinson, 2003. Generalized discriminant analysis based on distances. Australian & New Zealand Journal of Statistics 45: 301–318.  https://doi.org/10.1111/1467-842X.00285.CrossRefGoogle Scholar
  2. Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. PRIMER-E Ltd, Plymouth.Google Scholar
  3. Armonies, W. & K. Reise, 2000. Faunal diversity across a sandy shore. Marine Ecology Progress Series 196: 49–57.  https://doi.org/10.3354/meps196049.CrossRefGoogle Scholar
  4. Bezerra, T. et al., 2018. NeMys: world database of free-living marine nematodesGoogle Scholar
  5. Blanchard, G., 1990. Overlapping microscale dispersion patterns of meiofauna and microphytobenthos. Marine Ecology Progress Series 68: 101–111.CrossRefGoogle Scholar
  6. Blome, D., U. Schleier & K. H. von Bernem, 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.  https://doi.org/10.1007/s002270050513.CrossRefGoogle Scholar
  7. Boldina, I., P. G. Beninger & M. Le Coz, 2014. Effect of long-term mechanical perturbation on intertidal soft-bottom meiofaunal community spatial structure. Journal of Sea Research 85: 85–91.  https://doi.org/10.1016/j.seares.2013.10.006.CrossRefGoogle Scholar
  8. Boon, A. & G. Duineveld, 1996. Phytopigments and fatty acids as molecular markers for the quality of near-bottom particulate organic matter in the North Sea. Journal of Sea Research 35: 279–291.  https://doi.org/10.1016/S1385-1101(96)90755-8.CrossRefGoogle Scholar
  9. Boucher, G., 1990. Pattern of nematode species diversity in temperate and tropical subtidal sediments. Marine Ecology 11: 133–146.  https://doi.org/10.1111/j.1439-0485.1990.tb00234.x.CrossRefGoogle Scholar
  10. Braeckman, U., P. Provoost, T. Moens, K. Soetaert, J. J. Middelburg, M. Vincx & J. Vanaverbeke, 2011a. Biological vs. physical mixing effects on benthic food web dynamics. PLoS ONE 6: e18078.  https://doi.org/10.1371/journal.pone.0018078.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Braeckman, U., C. Van Colen, K. Soetaert, M. Vincx & J. Vanaverbeke, 2011b. Contrasting macrobenthic activities differentially affect nematode density and diversity in a shallow subtidal marine sediment. Marine Ecology Progress Series 422: 179–191.  https://doi.org/10.3354/meps08910.CrossRefGoogle Scholar
  12. Carpentier, A., S. Como, C. Dupuy, C. Lefrancois & E. Feunteun, 2014. Feeding ecology of Liza spp. in a tidal flat: evidence of the importance of primary production (biofilm) and associated meiofauna. Journal of Sea Research 92: 86–91.  https://doi.org/10.1016/j.seares.2013.10.007.CrossRefGoogle Scholar
  13. Cibic, T., O. Blasutto & N. Bettoso, 2009. Microalgal–meiofaunal interactions in a sublittoral site of the Gulf of Trieste (northern Adriatic Sea, Italy): a three-year study. Journal of Experimental Marine Biology and Ecology 370: 144–154.  https://doi.org/10.1016/j.jembe.2008.12.006.CrossRefGoogle Scholar
  14. Commito, J. A. & G. Tita, 2002. Differential dispersal rates in an intertidal meiofauna assemblage. Journal of Experimental Marine Biology and Ecology 268: 237–256.  https://doi.org/10.1016/S0022-0981(01)00386-0.CrossRefGoogle Scholar
  15. De Grisse, A., 1965. A labour-saving method for fixing and transferring eelworms to anhydrous glycerin. Landbouw Hogeschool, OpzoekStns—Leerstoel Dierkunde, GentGoogle Scholar
  16. D’Hondt, A.-S., W. Stock, L. Blommaert, T. Moens & K. Sabbe, 2018. Nematodes stimulate biomass production in a multispecies diatom biofilm. Marine Environmental Research 140: 78–89.  https://doi.org/10.1016/j.marenvres.2018.06005.CrossRefPubMedGoogle Scholar
  17. Ferreira, R. C., A. B. Nascimento, P. J. P. Santos, M. L. Botter-Carvalho & T. K. Pinto, 2015. Responses of estuarine nematodes to an increase in nutrient supply: an in situ continuous addition experiment. Marine Pollution Bulletin 90: 115–120.  https://doi.org/10.1016/j.marpolbul.2014.11.012.CrossRefPubMedGoogle Scholar
  18. Fonseca, G., P. Hutchings, D. C. Vieira & F. Gallucci, 2011. Meiobenthic community underneath the carcass of a stingray: a snapshot after natural death. Aquatic Biology 13: 27–33.  https://doi.org/10.3354/ab00347.CrossRefGoogle Scholar
  19. Franco, M. A., K. Soetaert, M. J. Costa, M. Vincx & J. Vanaverbeke, 2008. Uptake of phytodetritus by meiobenthos using C13 labelled diatoms and Phaeocystis in two contrasting sediments from the North Sea. Journal of Experimental Marine Biology and Ecology 362: 1–8.  https://doi.org/10.1016/j.jembe.2008.04.010.CrossRefGoogle Scholar
  20. Gallucci, F., M. Steyaert & T. Moens, 2005. Can field distributions of marine predacious nematodes be explained by sediment constraints on their foraging success? Marine Ecology Progress Series 304: 167–178.  https://doi.org/10.3354/meps304167.CrossRefGoogle Scholar
  21. Gallucci, F., G. Fonseca & M. Brustolin, 2019. Hydrodynamic exposure decreases the role of environmental filtering over benthic coastal metacommunities. In Adão, H., C. Vicente, K. Sroczyńska, M. Espada, P. Alvim, M. Costa & S. Vieira (eds), Book of Abstracts, SeventIMCO—Seventeenth International Meiofauna Conference, Portugal, University of Évora: 36Google Scholar
  22. Gheskiere, T., E. Hoste, J. Vanaverbeke, M. Vincx & S. Degraer, 2004. Horizontal zonation patterns and feeding structure of marine nematode assemblages on a macrotidal, ultra-dissipative sandy beach (De Panne, Belgium). Journal of Sea Research 52: 211–226.  https://doi.org/10.1016/j.seares.2004.02.001.CrossRefGoogle Scholar
  23. Giere, O., 2009. Meiobenthology: The Microscopic Motile Fauna of Aquatic Sediments. Springer, Berlin.Google Scholar
  24. Gingold, R., M. Mundo-Ocampo, O. Holovachov & A. Rocha-Olivares, 2010. The role of habitat heterogeneity in structuring the community of intertidal free-living marine nematodes. Marine Biology 157: 1741–1753.  https://doi.org/10.1007/s00227-010-1447-z.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gingold, R., S. E. Ibarra-Obando & A. Rocha-Olivares, 2011. Spatial aggregation patterns of free-living marine nematodes in contrasting sandy beach micro-habitats. Journal of the Marine Biological Association of the United Kingdom 91: 615–622.  https://doi.org/10.1017/S0025315410001128.CrossRefGoogle Scholar
  26. Heip, C., M. Vincx & G. Vranken, 1985. The ecology of marine nematodes. Oceanography and Marine Biology: An Annual Review 23: 399–489.Google Scholar
  27. Heip, C. H. R., N. K. Goosen, P. M. J. Herman, J. Kromkamp, J. J. Middelburg & J. Soetaert, 1995. Production and consumption of biological particles in temperate tidal estuaries. Oceanography and Marine Biology: an Annual Review 33: 1–149.Google Scholar
  28. Herman, P., J. Middelburg, J. Van de Koppel & C. Heip, 1999. Ecology of estuarine macrobenthos. Advances in Ecological Research 29: 195–240.CrossRefGoogle Scholar
  29. Herman, P. M., J. J. Middelburg & C. H. Heip, 2001. Benthic community structure and sediment processes on an intertidal flat: results from the ECOFLAT project. Continental Shelf Research 21: 2055–2071.  https://doi.org/10.1016/S0278-4343(01)00042-5.CrossRefGoogle Scholar
  30. Higgins, R. P. & H. Thiel, 1988. Introduction to the Study of Meiofauna. Smithsonian Institution Press, Washington, DC: 488.Google Scholar
  31. Hodda, M., 1990. Variation in estuarine littoral nematode populations over three spatial scales. Estuarine, Coastal and Shelf Science 30: 325–340.  https://doi.org/10.1016/0272-7714(90)90001-8.CrossRefGoogle Scholar
  32. Hooper, D. U., et al., 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75: 3–35.  https://doi.org/10.1890/04-0922.CrossRefGoogle Scholar
  33. Hubas, C., C. Sachidhanandam, H. Rybarczyk, H. V. Lubarsky, A. Rigaux, T. Moens & D. M. Paterson, 2010. Bacterivorous nematodes stimulate microbial growth and exopolymer production in marine sediment microcosms. Marine Ecology Progress Series 419: 85–94.  https://doi.org/10.3354/meps08851.CrossRefGoogle Scholar
  34. Joint, I. R., J. M. Gee & R. M. Warwick, 1982. Determination of fine-scale vertical-distribution of microbes and meiofauna in an intertidal sediment. Marine Biology 72: 157–164.  https://doi.org/10.1007/BF00396916.CrossRefGoogle Scholar
  35. Kromkamp, J. C., J. F. C. de Brouwer, G. F. Blanchard, R. M. Forster & V. Creach, 2006. Functioning of Microphytobenthos in Estuaries: Proceedings of the Colloquium, Amsterdam, 21–23 August 2003. Royal Netherlands Academy of Arts and Sciences, AmsterdamGoogle Scholar
  36. Le Hir, P., W. Roberts, O. Cazaillet, M. Christie, P. Bassoullet & C. Bacher, 2000. Characterization of intertidal flat hydrodynamics. Continental Shelf Research 20: 1433–1459.  https://doi.org/10.1016/S0278-4343(00)00031-5.CrossRefGoogle Scholar
  37. Lucas, C. H., J. Widdows, M. D. Brinsley, P. N. Salkeld & P. M. J. Herman, 2000. Benthic-pelagic exchange of microalgaeat a tidal flat. 1. Pigment analysis. Marine Ecology Progress Series 196: 59–73.  https://doi.org/10.3354/meps196059.CrossRefGoogle Scholar
  38. MacIntyre, H. L., R. J. Geider & D. C. Miller, 1996. Microphytobenthos: the ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 19: 186–201.  https://doi.org/10.2307/1352224.CrossRefGoogle Scholar
  39. Maria, T. F., J. Vanaverbeke, R. Gingold, A. M. Esteves & A. Vanreusel, 2013. Tidal exposure or microhabitats: what determines sandy-beach nematode zonation? a case study of a macrotidal ridge-and-runnel sandy beach in Belgium. Marine Ecology 34: 207–217.  https://doi.org/10.1111/maec.12008.CrossRefGoogle Scholar
  40. McLachlan, A. & E. Jaramillo, 1996. Zonation on sandy beaches. Oceanographic Literature Review 12: 1247.Google Scholar
  41. Meire, P., T. Ysebaert, S. V. Damme, E Vd Bergh, T. Maris & E. Struyf, 2005. The Scheldt estuary: a description of a changing ecosystem. Hydrobiologia 540: 1–11.  https://doi.org/10.1007/s10750-005-0896-8.CrossRefGoogle Scholar
  42. Middelburg, J. J., C. Barranguet, H. T. S. Boschker, P. M. J. Herman, T. Moens & C. H. R. Heip, 2000. The fate of intertidal microphytobenthos carbon: an in situ C13-labeling study. Limnology and Oceanography 45(6): 1224–1234.  https://doi.org/10.4319/lo.2000.45.6.1224.CrossRefGoogle Scholar
  43. Moens, T. & P. G. Beninger, 2018. Meiofauna: an inconspicuous but important player in mudflat ecology. In Beninger, P. G. (ed.), Mudflat Ecology. Springer, Berlin: 91–148.CrossRefGoogle Scholar
  44. Moens, T. & M. Vincx, 1997. Observations on the feeding ecology of estuarine nematodes. Journal of the Marine Biological Association of the United Kingdom 77: 211–227.  https://doi.org/10.1017/S0025315400033889.CrossRefGoogle Scholar
  45. Moens, T. & M. Vincx, 2000. Temperature, salinity and food thresholds in two brackish-water bacterivorous nematode species: assessing niches from food absorption and respiration experiments. Journal of Experimental Marine Biology and Ecology 243: 137–154.  https://doi.org/10.1016/S0022-0981(99)00114-8.CrossRefGoogle Scholar
  46. Moens, T., D. Van Gansbeke & M. Vincx, 1999. Linking estuarine nematodes to their suspected food. A case study from the Westerschelde Estuary (south-west Netherlands). Journal of the Marine Biological Association of the United Kingdom 79: 1017–1027.  https://doi.org/10.1017/s0025315499001253.CrossRefGoogle Scholar
  47. Moens, T., P. Herman, L. Verbeeck, M. Steyaert & M. Vincx, 2000. Predation rates and prey selectivity in two predacious estuarine nematode species. Marine Ecology Progress Series 205: 185–193.  https://doi.org/10.3354/meps205185.CrossRefGoogle Scholar
  48. Moens, T., C. Luyten, J. J. Middelburg, P. M. J. Herman & M. Vincx, 2002. Tracing organic matter sources of estuarine tidal flat nematodes with stable carbon isotopes. Marine Ecology Progress Series 234: 127–137.  https://doi.org/10.3354/meps234127.CrossRefGoogle Scholar
  49. Moens, T., S. Bouillon & F. Gallucci, 2005. Dual stable isotope abundances unravel trophic position of estuarine nematodes. Journal of the Marine Biological Association of the United Kingdom 85: 1401–1407.  https://doi.org/10.1017/S0025315405012580.CrossRefGoogle Scholar
  50. Moens, T., S. Vanhove, I. De Mesel, B. Kelemen, T. Janssens, A. Dewicke & A. Vanreusel, 2007. Carbon sources of Antarctic nematodes as revealed by natural carbon isotope ratios and a pulse-chase experiment. Polar Biology 31: 1–13.  https://doi.org/10.1007/s00300-007-0323-x.CrossRefGoogle Scholar
  51. Moens, T., et al., 2013. Ecology of free-living marine nematodes. In Schmidt-Rhaesa, A. (ed.), Handbook of Zoology. De Gruyter, Berlin: 109–152.Google Scholar
  52. Moens, T., A.-M. Vafeiadou, E. De Geyter, P. Vanormelingen, K. Sabbe & M. De Troch, 2014. Diatom feeding across trophic guilds in tidal flat nematodes, and the importance of diatom cell size. Journal of Sea Research 92: 125–133.  https://doi.org/10.1016/j.seares.2013.08.007.CrossRefGoogle Scholar
  53. Montagna, P. A., B. C. Coull, T. L. Herring & B. W. Dudley, 1983. The relationship between abundances of meiofauna and their suspected microbial food (diatoms and bacteria). Estuarine, Coastal and Shelf Science 17: 381–394.  https://doi.org/10.1016/0272-7714(83)90124-5.CrossRefGoogle Scholar
  54. Netto, S. A. & A. Meneghel, 2014. Pulse of marine subsidies: the role of surf diatom Asterionellopsis glacialis accumulations in structuring the meiofauna of sandy beaches. Marine Biodiversity 44: 445–457.  https://doi.org/10.1007/s12526-014-0253-0.CrossRefGoogle Scholar
  55. Nicholas, W. L. & M. Hodda, 1999. The free-living nematodes of a temperate, high energy, sandy beach: faunal composition and variation over space and time. Hydrobiologia 394: 113–127.  https://doi.org/10.1023/a:1003544115600.CrossRefGoogle Scholar
  56. Peters, K., C. Walters & J. Moldowan, 2005. The Biomarker Guide. Cambridge University Press, Cambridge, UK.Google Scholar
  57. Pinckney, J. & R. Sandulli, 1990. Spatial autocorrelation analysis of meiofaunal and microalgal populations on an intertidal sandflat: scale linkage between consumers and resources. Estuarine, Coastal and Shelf Science 30: 341–353.  https://doi.org/10.1016/0272-7714(90)90002-9.CrossRefGoogle Scholar
  58. Pinckney, J. L., K. R. Carman, S. E. Lumsden & S. N. Hymel, 2003. Microalgal-meiofaunal trophic relationships in muddy intertidal estuarine sediments. Aquatic Microbial Ecology 31: 99–108.  https://doi.org/10.3354/ame031099.CrossRefGoogle Scholar
  59. Platt, H. M. & R. M. Warwick, 1983. A Synopsis of the Freeliving Marine Nematodes. Part 1: British Enoplids. Cambridge University Press, Cambridge.Google Scholar
  60. R Core Team, 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Viennva, Austria. http://www.R-project.org/
  61. Rzeznik Orignac, J., G. Boucher, D. Fichet & P. Richard, 2008. Stable isotope analysis position of intertidal of food source and trophic nematodes and copepods. Marine Ecology Progress Series 359: 145–150.  https://doi.org/10.3354/meps07328.CrossRefGoogle Scholar
  62. Sahraean, N., T. C. Bezerra, K. E. Khanaghah, H. Mosallanejad, E. Van Ranst & T. Moens, 2017. Effects of pollution on nematode assemblage structure and diversity on beaches of the northern Persian Gulf. Hydrobiologia 799: 349–369.  https://doi.org/10.1007/s10750-017-3234-z.CrossRefGoogle Scholar
  63. Saidi, I., N. Essid, F. Boufahja, A. Nasri, A. Hannachi, B. Nefzi & H. Beyrem, 2017. The effects of raw effluents from pulp and paper industry from Tunisia on marine nematodes: a microcosm bioassay. Cahiers De Biologie Marine 58: 387–395.  https://doi.org/10.21411/cbm.a.c942a02d.CrossRefGoogle Scholar
  64. Schratzberger, & J. Ingels, 2018. Meiofauna matters: the roles of meiofauna in benthic ecosystems. Journal of Experimental Marine Biology and Ecology 502: 12–25.  https://doi.org/10.1016/j.jembe.2017.01.007.CrossRefGoogle Scholar
  65. Seinhorst, J., 1959. A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica 4: 67–69.CrossRefGoogle Scholar
  66. Semprucci, F., P. Colantoni, G. Baldelli, M. Rocchi & M. Balsamo, 2010. The distribution of meiofauna on back-reef sandy platforms in the Maldives (Indian Ocean). Marine Ecology-an Evolutionary Perspective 31: 592–607.  https://doi.org/10.1111/j.1439-0485.2010.00383.x.CrossRefGoogle Scholar
  67. Semprucci, F., M. Balsamo & R. Sandulli, 2016. Assessment of the ecological quality (EcoQ) of the Venice lagoon using the structure and biodiversity of the meiofaunal assemblages. Ecological Indicators 67: 451–457.  https://doi.org/10.1016/j.ecolind.2016.03.014.CrossRefGoogle Scholar
  68. Somerfield, P. J., S. L. Dashfield & R. M. Warwick, 2007. Three-dimensional spatial structure: nematodes in a sandy tidal flat. Marine Ecology Progress Series 336: 177–186.  https://doi.org/10.3354/meps336177.CrossRefGoogle Scholar
  69. Steyaert, M., N. Garner, D. van Gansbeke & M. Vincx, 1999. Nematode communities from the North Sea: environmental controls on species diversity and vertical distribution within the sediment. Journal of the Marine Biological Association of the United Kingdom 79: 253–264.  https://doi.org/10.1017/S0025315498000289.CrossRefGoogle Scholar
  70. Steyaert, M., P. M. J. Herman, T. Moens, J. Widdows & M. Vincx, 2001. Tidal migration of nematodes on an estuarine tidal flat (the Molenplaat, Schelde Estuary, SW Netherlands). Marine Ecology Progress Series 224: 299–304.  https://doi.org/10.3354/meps224299.CrossRefGoogle Scholar
  71. Steyaert, M., J. Vanaverbeke, A. Vanreusel, C. Barranguet, C. Lucas & M. Vincx, 2003. The importance of fine-scale, vertical profiles in characterising nematode community structure. Estuarine, Coastal and Shelf Science 58: 353–366.  https://doi.org/10.1016/S0272-7714(03)00086-6.CrossRefGoogle Scholar
  72. Thomas, M. C. & P. C. Lana, 2011. A new look into the small-scale dispersal of free-living marine nematodes. Zoologia 28: 449–456.  https://doi.org/10.1590/S1984-46702011000400006.CrossRefGoogle Scholar
  73. Underwood, G. & J. Kromkamp, 1999. Primary production by phytoplankton and microphytobenthos in estuaries. Advances in Ecological Research 29: 93–153.CrossRefGoogle Scholar
  74. Underwood, A., M. Chapman & S. Connell, 2000. Observations in ecology: you can’t make progress on processes without understanding the patterns. Journal of Experimental Marine Biology and Ecology 250: 97–115.  https://doi.org/10.1016/S0022-0981(00)00187-7.CrossRefPubMedGoogle Scholar
  75. Urban-Malinga, B. & T. Moens, 2006. Fate of organic matter in Arctic intertidal sediments: is utilisation by meiofauna important? Journal of Sea Research 56: 239–248.  https://doi.org/10.1016/j.seares.2006.05.003.CrossRefGoogle Scholar
  76. Urkmez, D., M. L. Brennan, M. Sezgin & L. Bat, 2015. A brief look at the free-living Nematoda of the oxic/anoxic interface with a new genus record (Trefusia) for the Black Sea. Oceanological and Hydrobiological Studies 44: 539–551.  https://doi.org/10.1515/ohs-2015-0051.CrossRefGoogle Scholar
  77. Vafeiadou, A.-M., P. Materatski, H. Adão, M. De Troch & T. Moens, 2014. Resource utilization and trophic position of nematodes and harpacticoid copepods in and adjacent to Zostera noltii beds. Biogeosciences 11: 4001–4014.  https://doi.org/10.5194/bg-11-4001-2014.CrossRefGoogle Scholar
  78. Vanaverbeke, J., T. Gheskiere, M. Steyaert & M. Vincx, 2002. Nematode assemblages from subtidal sandbanks in the Southern Bight of the North Sea: effect of small sedimentological differences. Journal of Sea Research 48: 197–207.  https://doi.org/10.1016/S1385-1101(02)00165-X.CrossRefGoogle Scholar
  79. Vanaverbeke, J., M. Franco, D. van Oevelen, L. Moodley, P. Provoost, et al., 2008. Benthic responses to sedimentation of phytoplankton on the Belgian Continental Shelf. In Rousseau, V., C. Lancelot & D. Cox (eds), Current Status of Eutrophication in the Belgian Coastal Zone. Presses Universitaires de Bruxelles, Brussels: 73–90.Google Scholar
  80. Vieira, D. C. & G. Fonseca, 2013. The importance of vertical and horizontal dimensions of the sediment matrix in structuring nematodes across spatial scales. PLoS ONE 8: e77704.  https://doi.org/10.1371/journal.pone.0077704.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Warwick, R. M., H. M. Platt & P. J. Somerfield, 1998. Freeliving marine nematodes: part III. Monhysterida. Synopses of the British Fauna No. 53. Field Studies Council, ShrewsburyGoogle Scholar
  82. Wentworth, C. K., 1922. A scale of grade and class terms for clastic sediments. The Journal of Geology 30: 377–392.CrossRefGoogle Scholar
  83. Wright, S. & S. Jeffrey, 1997. High-resolution HPLC system for chlorophylls and carotenoids of marine phytoplankton. In Jeffrey, S. W., R. F. C. Mantoura & S. W. Wright (eds), Phytoplankton Pigments in Oceanography: Guidelines to Moder Methods. UNESCO, Paris.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Xiuqin Wu
    • 1
    Email author
  • Ann Vanreusel
    • 1
  • Freija Hauquier
    • 1
  • Tom Moens
    • 1
  1. 1.Marine Biological Laboratory, Biology DepartmentGhent UniversityGhentBelgium

Personalised recommendations