Environmental drivers of nematode abundance and genus composition at two spatial scales on an estuarine intertidal flat
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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.
KeywordsMicrophytobenthos Sediment granulometry Mesoscale Microscale
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.
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.
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.
- 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
- Bezerra, T. et al., 2018. NeMys: world database of free-living marine nematodesGoogle Scholar
- 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
- 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
- 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
- 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
- De Grisse, A., 1965. A labour-saving method for fixing and transferring eelworms to anhydrous glycerin. Landbouw Hogeschool, OpzoekStns—Leerstoel Dierkunde, GentGoogle Scholar
- 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
- 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
- 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
- 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
- Giere, O., 2009. Meiobenthology: The Microscopic Motile Fauna of Aquatic Sediments. Springer, Berlin.Google Scholar
- 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
- Heip, C., M. Vincx & G. Vranken, 1985. The ecology of marine nematodes. Oceanography and Marine Biology: An Annual Review 23: 399–489.Google Scholar
- 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
- Higgins, R. P. & H. Thiel, 1988. Introduction to the Study of Meiofauna. Smithsonian Institution Press, Washington, DC: 488.Google Scholar
- 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
- 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
- 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
- McLachlan, A. & E. Jaramillo, 1996. Zonation on sandy beaches. Oceanographic Literature Review 12: 1247.Google Scholar
- 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
- 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
- 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
- Peters, K., C. Walters & J. Moldowan, 2005. The Biomarker Guide. Cambridge University Press, Cambridge, UK.Google Scholar
- Platt, H. M. & R. M. Warwick, 1983. A Synopsis of the Freeliving Marine Nematodes. Part 1: British Enoplids. Cambridge University Press, Cambridge.Google Scholar
- R Core Team, 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Viennva, Austria. http://www.R-project.org/
- 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
- 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
- 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
- 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
- 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
- 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