Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-28T19:42:07.907Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of biofilm resuspension on mesozooplankton in a shallow coastal ecosystem characterized by a bare intertidal mudflat

Published online by Cambridge University Press:  29 April 2016

Valérie David ,
Hans Hartmann ,
Alexandre Barnett ,
Martine Bréret ,
Hélène Montanié ,
Francis Orvain  and
Christine Dupuy
Valérie David*
Affiliation:
Université de la Rochelle-CNRS, UMR 7266, Littoral Environnement et Sociétés (LIENSs), Institut du Littoral et de l'Environnement, 2 rue Olympe de Gouges, F-17000 La Rochelle, France
Hans Hartmann
Affiliation:
Université de la Rochelle-CNRS, UMR 7266, Littoral Environnement et Sociétés (LIENSs), Institut du Littoral et de l'Environnement, 2 rue Olympe de Gouges, F-17000 La Rochelle, France
Alexandre Barnett
Affiliation:
Université de la Rochelle-CNRS, UMR 7266, Littoral Environnement et Sociétés (LIENSs), Institut du Littoral et de l'Environnement, 2 rue Olympe de Gouges, F-17000 La Rochelle, France
Martine Bréret
Affiliation:
Université de la Rochelle-CNRS, UMR 7266, Littoral Environnement et Sociétés (LIENSs), Institut du Littoral et de l'Environnement, 2 rue Olympe de Gouges, F-17000 La Rochelle, France
Hélène Montanié
Affiliation:
Université de la Rochelle-CNRS, UMR 7266, Littoral Environnement et Sociétés (LIENSs), Institut du Littoral et de l'Environnement, 2 rue Olympe de Gouges, F-17000 La Rochelle, France
Francis Orvain
Affiliation:
Université de Caen Basse-Normandie, UMR BOREA (MNHN, UPMC, UCBN, CNRS-7208, IRD-207), esplanade de la Paix, 14032 Caen, France
Christine Dupuy
Affiliation:
Université de la Rochelle-CNRS, UMR 7266, Littoral Environnement et Sociétés (LIENSs), Institut du Littoral et de l'Environnement, 2 rue Olympe de Gouges, F-17000 La Rochelle, France
*
Correspondence should be addressed to:V. David, Université de la Rochelle-CNRS, UMR 7266, Littoral Environnement et Sociétés (LIENSs), Institut du Littoral et de l'Environnement, 2 rue Olympe de Gouges, F-17000 La Rochelle, France email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

A prey–predator experimental setup was conducted in a shallow coastal ecosystem characterized by a bare intertidal mudflat to test if benthic biofilm resuspension causing microalgae inputs and carbon export toward nanoflagellates would favour the highest planktonic trophic level (i.e. mesozooplankton) when nutrient concentrations are high in the water column. Mesozooplankton predation and somatic production were studied by comparing the evolution of the prey assemblage (diversity and abundances) in the presence and absence of these predators during 24 h experiments. The results were then statistically analysed according to the cross-calculation method. Biofilm resuspension caused (i) a direct input of benthic microorganisms that had changed prey structure in term of diversity and/or size and (ii) a differential growth ability between prey taxa. Both reasons implied a bottom-up control on both micro- and mesozooplankton. The carbon export toward heterotrophic nanoflagellates favoured pelagic ciliate growth while mesozooplankton benefited from largest diatoms with high growth rates, both benthic and R-strategist pelagic species. Even if these microbial and herbivorous pathways are controlled by benthic inputs, they seemed to be totally disconnected since ciliates represented only a small part of mesozooplankton diet. The sensitivity of mesozooplankton production appeared species-dependent with the most tolerant taxa dominating the zooplankton assemblages. This suggests a role of the intensities and the frequencies of biofilm resuspension on the spatio-temporal structuring of mesozooplankton in macrotidal coastal ecosystems.

Keywords

biofilm resuspensionmesozooplanktongrowthgrazingsomatic productionplanktonic trophic pathwaysmicrophytobenthos
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 6 , September 2016 , pp. 1319 - 1329
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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

REFERENCES

Alves-de-Souza, C., Gonzalez, M.T. and Iriarte, J.L. (2008) Functional groups in marine phytoplankton assemblages dominated by diatoms in fjords of southern Chile. Journal of Plankton Research 30, 1233–1243.Google Scholar
Aminot, A. and Kérouel, R. (2004) Hydrologie des écosystèmes marins. Paramètres et analyses. France: Ifremer Edition.Google Scholar
Azémar, F., Boulêtreau, S., Lionard, M., Muylaert, K., Vyverman, W., Meire, P. and Tackx, M. (2007) Looking for general trends in trophic interactions among estuarine micro- and mesozooplankton. Journal of Plankton Research 29, i135–i147.Google Scholar
Bassoullet, P., Le Hir, P., Gouleau, R. and Robert, S. (2000) Sediment transport over an intertidal mudflat: field investigations and estimation of fluxes within the “Baie de Marennes-Oleron”. Continental Shelf Research 20, 1635–1653.Google Scholar
Blanchard, G.F., Guarini, J.M., Orvain, F. and Sauriau, P.G. (2001) Dynamic behaviour of benthic microalgal biomass in intertidal mudflats. Journal of Experimental Marine Biology and Ecology 264, 85–100.Google Scholar
Cariou-Le Gall, V. and Blanchard, G. (1995) Monthly HPLC measurements of pigment concentration from an intertidal muddy sediment of Marennes-Oléron Bay, France. Marine Ecology Progress Series 121, 171–179.CrossRefGoogle Scholar
Ceballos, S. and Ianora, A. (2003) Different diatoms induce contrasting effects on the reproductive success of the copepod Temora stylifera . Journal of Experimental Marine Biology and Ecology 294, 189–202.Google Scholar
De Jonge, V.N. and Van Beusekom, J.E.E. (1992) Contribution of resuspended microphytobenthos to total phytoplankton in the EMS estuary and its possible role for grazers. Netherlands Journal of Sea Research 30, 91–105.Google Scholar
De Jonge, V.N. and Van Beusekom, J.E.E. (1995) Wind- and tide-induced resuspension of sediment and microphytobenthos from tidal flats in the Ems estuary. Limnology and Oceanography 40, 766–778.Google Scholar
Dupuy, C., Mallet, C., Guizien, K., Montanie, H., Bréret, M., Mornet, F., Fontaine, C., Nérot, C. and Orvain, F. (2014) Sequential resuspension of biofilm components (viruses, prokaryotes and protists) as measured by erodimetry experiments in the Brouage mudflat (French Atlantic coast). Journal of Sea Research 92, 56–65.Google Scholar
Frontier, S. (1972) Calcul de l'erreur sur un comptage de zooplancton. Journal of Experimental Marine Biology and Ecology 8, 121–132.Google Scholar
Frost, B. (1972) Effects of size concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus . Limnology and Oceanography 17, 805–815.Google Scholar
Gaonkar, C.A. and Chandrashekar Anil, A. (2010) What do barnacle larvae feed on? Implications in biofouling ecology. Journal of the Marine Biological Association of the United Kingdom 90, 1241–1247.Google Scholar
Garstecki, T., Wickham, S.A. and Arndt, H. (2002) Effects of experimental sediment resuspension on a coastal planktonic microbial food web. Estuarine, Coastal and Shelf Science 55, 751–762.Google Scholar
Guarini, J.M., Gros, P., Blanchard, G., Richard, P. and Fillon, A. (2004) Benthic contribution to pelagic microalgal communities in two semi-enclosed, European-type littoral ecosystems (Marennes-Oléron Bay and Aiguillon Bay, France). Journal of Sea Research 52, 241–258.Google Scholar
Guiry, M.D. and Guiry, G.M. (2015) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway (taxonomic information republished from AlgaeBase with permission of M.D. Guiry). Accessed through: World Register of Marine Species http://www.marinespecies.org/aphia.php?p=taxdetails&id=163646 on 2015-04-29.Google Scholar
Guizien, K., Dupuy, C., Ory, P., Montanié, H., Hartmann, H., Chatelain, M. and Karpytchev, M. (2014) Microorganism dynamics during a rising tide: disentangling effects of resuspension and mixing with offshore waters above an intertidal mudflat. Journal of Marine Systems 129, 178–188.Google Scholar
Haubois, A.G., Sylvestre, F., Guarini, J.M., Richard, P. and Blanchard, G.F. (2005) Spatio-temporal structure of the epipelic diatom assemblage from an intertidal mudflat in Marennes-Oléron Bay, France. Estuarine, Coastal and Shelf Science 64, 385–394.Google Scholar
Herlory, O., Guarini, J.M. and Blanchard, G. (2004) Microstructure of microphytobenthic biofilm and its spatio-temporal dynamics in an intertidal mudflat (Aiguillon Bay, France). Marine Ecology Progress Series 282, 33–44.Google Scholar
Hillebrand, H., Dürselen, C.D., Kirschtel, D., Pollingher, U. and Zohary, T. (1999) Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35, 403–424.Google Scholar
Irigoien, X. and Castel, J. (1997) Light limitation and distribution of chlorophyll pigments in a highly turbid estuary: the Gironde estuary (SW France). Estuarine, Coastal and Shelf Science 44, 507–517.Google Scholar
Kerambrun, P., Thessalou-Legaki, M. and Verriopoulos, G. (1993) Comparative effects of environmental conditions, in eutrophic polluted and oligotrophic non-polluted areas of the Saronikos Gulf (Greece), on the physiology of the copepod Acartia clausi . Comparative Biochemistry and Physiology Part C: Comparative Pharmacology 105, 415–420.CrossRefGoogle Scholar
Kimmerer, W.J. and McKinnon, A.D. (1987) Growth, mortality, and secondary production of the copepod Acartia tranteri in Westernport Bay, Australia. Limnology and Oceanography 32, 14–28.Google Scholar
Kumlu, M. (1999) Feeding and digestion in larval decapod crustaceans. Journal of Biology 23, 215–229.Google Scholar
Lohmann, H. (1908) Untersuchungen zur Feststellung des Vollständigen Gehaltes des Meeres an Plankton. Wissenschaftliche Meeresuntersuchungen Abt. Kiel, N. F 10, 129–370.Google Scholar
Mazzocchi, M., Buffoni, G.G., Carotenuto, Y., Pasquali, S. and Ribera d'Alcalà, M. (2006) Effects of food conditions on the development of the population of Temora stylifera: a modeling approach. Journal of Marine Systems 62, 71–84.Google Scholar
Montanié, H., Ory, P., Orvain, F., Delmas, D., Dupuy, C. and Hartmann, H.J. (2014) Microbial interactions in marine water amended by eroded benthic biofilm: a case study from an intertidal mudflat. Journal of Sea Research 92, 74–85.Google Scholar
Orvain, F., Guizien, K., Lefebvre, S., Bréret, M. and Dupuy, C. (2014) Relevance of macrozoobenthic grazers to understand the dynamic behaviour of sediment erodibility and microphytobenthos resuspension in sunny summer conditions. Journal of Sea Research 92, 46–55.Google Scholar
Orvain, F., Sauriau, P.G., Sygut, A., Joassard, L. and Le Hir, P. (2004) Roles of Hydrobia ulvae bioturbation and the physiological stage of microphytobenthic mats in resuspended sediment and pigment fluxes. Marine Ecology Progress Series 278, 205–223.Google Scholar
Ory, P., Hartmann, H.J., Jude, F., Dupuy, C., Del Amo, Y., Catala, P., Mornet, F., Huet, V., Jan, B., Vincent, D., Sautour, B. and Montanié, H. (2010) Pelagic food web patterns: do they modulate virus and nanoflagellate effects on picoplankton during the phytoplankton spring bloom? Environmental Microbiology 12, 2755–2772.Google Scholar
Pagano, M., Sagarra, P.B., Champalbert, G., Bouvy, M., Dupuy, C., Thomas, Y. and Charpy, L. (2012) Metazooplankton communities in the Ahe atoll lagoon (Tuamotu Archipelago, French Polynesia): spatiotemporal variations and trophic relationships. Marine Pollution Bulletin 65, 538–548.Google Scholar
Pierce, R.W. and Turner, J.T. (1992) Ecology of planktonic ciliates in marine food webs. Reviews in Aquatic Sciences 6, 139–181.Google Scholar
Pommier, J., Frenette, J.J. and Glémet, H. (2010) Relating RNA:DNA in Eurytemora affinis to seston fatty acids in a highly dynamic environment. Marine Ecology Progress Series 400, 143–154.Google Scholar
Porter, E.T., Mason, R.P. and Sanford, L.P. (2010) Effect of tidal resuspension on benthic-pelagic coupling in an experimental ecosystem study. Marine Ecology Progress Series 413, 33–53.Google Scholar
Reynolds, C.S. (2006) Ecology of phytoplankton. Cambridge: Cambridge University Press.Google Scholar
Saint-Béat, B. (2012) Modélisation du rôle du biofilm dans le fonctionnement du réseau trophique de la vasière de Brouage (Bassin de Marennes-Oléron): influence sur les flux de carbone et conséquences sur la stabilité. PhD thesis, Université de La Rochelle, La Rochelle, France.Google Scholar
Saint-Béat, B., Dupuy, C., Agogué, H., Carpentier, A., Chalumeau, J., Como, S., David, V., de Crignis, M., Duchêne, J.C., Fontaine, C., Feunteun, E., Guizien, K., Hartmann, H., Lavaud, J., Lefebvre, S., Lefrancois, C., Mallet, C., Montanié, H., Mouget, J., Orvain, F., Ory, P., Pascal, P., Radenac, G., Richard, P., Vezina, A. and Niquil, N. (2014) How does resuspension of the biofilm alter the functioning of the benthos-pelagos coupled food web of a bare mudflat in Marennes-Oléron Bay (NE Atlantic)? Journal of Sea Research 92, 144–155.Google Scholar
Sakka Hlaili, A., Niquil, N. and Legendre, L. (2014) Planktonic food webs revisited: reanalysis of results from the linear inverse approach. Progress in Oceanography 120, 216–229.Google Scholar
Sautour, B. and Castel, J. (1993) Distribution of zooplankton populations in Marennes-Oleron Bay (France), structure and grazing impact of copepod communities. Oceanologica Acta 16, 279–290.Google Scholar
Sherr, E.B., Caron, D.A. and Sherr, B.F. (1994) Staining of heterotrophic protists for visualisation via epifluorescence microscopy. In Kemp, P.F., Sherr, B.F., Sherr, E.B. and Cole, J.J. (eds) Handbook of methods in aquatic microbial ecology. Boca Raton, FL: Lewis Publisher, pp. 213–227.Google Scholar
Ubertini, M., Lefebvre, S., Gangnery, A., Grangeré, K., Le Gendre, R. and Orvain, F. (2012) Spatial variability of benthic-pelagic coupling in an estuary ecosystem: consequences for microphytobenthos resuspension phenomenon. PLoS ONE 7, e44155.Google Scholar
Underwood, N. and Kromkamp, J. (1999) Primary production by phytoplankton and microphytobenthos in estuaries. In Nedwell, D.R. (ed.) Estuaries. London: Academic Press, pp. 93–153.Google Scholar
Walter, T.C. and Boxshall, G. (2015) World of Copepods database. Accessed through World Register of Marine Species. http://www.marinespecies.org/aphia.php?p=taxdetails&id=104685 on 2015-04-29.Google Scholar
Warren, A. (2015) World Ciliophora database. Accessed through World Register of Marine Species. http://marinespecies.org/aphia.php?p=taxdetails&id=101287 on 2015-04-29.Google Scholar