Extensive spatial impacts of oyster reefs on an intertidal mudflat community via predator facilitation.


Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
22 03 2022
Historique:
received: 18 05 2021
accepted: 24 02 2022
entrez: 23 3 2022
pubmed: 24 3 2022
medline: 13 4 2022
Statut: epublish

Résumé

Habitat engineers make strong and far-reaching imprints on ecosystem processes. In intertidal mudflats, the dominant primary producer, microphytobenthos (MPB), often forms high biomass patches around oyster reefs. We evaluate multiple hypotheses linking MPB with oyster reefs, including oyster biodeposition, meiofaunal grazing, and abiotic factors, aiming to help predict effects of reef removal or proliferation. We quantify spatial patterns of an Atlantic mudflat community and its environment around two large Crassostrea reefs before experimentally sacrificing one reef via burning. MPB biomass was enriched surrounding living oyster reefs although infaunal biomass and individual sizes were low. Structural equation modelling best supported the hypothesis that crab predation intensity, which decayed with distance from the reefs, locally freed MPB from grazing. Our results suggest that Crassostrea reef expansion may enrich local MPB patches and redirect trophic energy flows away from mudflat infauna, with potential implications for the sustainability of local fisheries and bird conservation.

Identifiants

pubmed: 35318453
doi: 10.1038/s42003-022-03192-4
pii: 10.1038/s42003-022-03192-4
pmc: PMC8940938
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

250

Informations de copyright

© 2022. The Author(s).

Références

Jones, C. G., Lawton, J. H. & Shachak, M. Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78, 1946–1957 (1997).
doi: 10.1890/0012-9658(1997)078[1946:PANEOO]2.0.CO;2
Bateman, D. & Bishop, M. The environmental context and traits of habitat‑forming bivalves influence the magnitude of their ecosystem engineering. Mar. Ecol. Prog. Ser. 563, 95–110 (2017).
doi: 10.3354/meps11959
Koppel, J. Van De. et al. Long-distance interactions regulate the structure and resilience of coastal ecosystems. Ann. Rev. Mar. Sci. 7, 139–158 (2015).
doi: 10.1146/annurev-marine-010814-015805
van der Zee, E. M. et al. Spatially extended habitat modification by intertidal reef-building bivalves has implications for consumer-resource interactions. Ecosystems 15, 664–673 (2012).
doi: 10.1007/s10021-012-9538-y
Daggers, T. D., Oevelen, D., Herman, P. M. J., Boschker, H. T. S. & Wal, D. Spatial variability in macrofaunal diet composition and grazing pressure on microphytobenthos in intertidal areas. Limnol. Oceanogr. 65, 2819–2834 (2020).
doi: 10.1002/lno.11554
Ruesink, J. L. et al. Introduction of non-native oysters: ecosystem effects and restoration implications. Annu. Rev. Ecol. Evol. Syst. 36, 643–689 (2005).
doi: 10.1146/annurev.ecolsys.36.102003.152638
Markert, A., Esser, W., Frank, D., Wehrmann, A. & Exo, K. M. Habitat change by the formation of alien crassostrea-reefs in the wadden sea and its role as feeding sites for waterbirds. Estuar. Coast. Shelf Sci. 131, 41–51 (2013).
doi: 10.1016/j.ecss.2013.08.003
Troost, K. Causes and effects of a highly successful marine invasion: case-study of the introduced Pacific oyster Crassostrea gigas in continental NW European estuaries. J. Sea Res. 64, 145–165 (2010).
doi: 10.1016/j.seares.2010.02.004
Boogert, N. J., Paterson, D. M. & Laland, K. N. The implications of niche construction and ecosytem engineering for conservation biology. Bioscience 56, 570 (2006).
doi: 10.1641/0006-3568(2006)56[570:TIONCA]2.0.CO;2
Barbier, E. B. E. B. et al. The value of estuarine and coastal ecosystem services. Ecol. Monogr. 81, 169–193 (2011).
doi: 10.1890/10-1510.1
Molnar, J. L., Gamboa, R. L., Revenga, C. & Spalding, M. D. Assessing the global threat of invasive species to marine biodiversity. Front. Ecol. Environ. 6, 485–492 (2008).
doi: 10.1890/070064
Lejart, M. & Hily, C. Differential response of benthic macrofauna to the formation of novel oyster reefs (Crassostrea gigas, Thunberg) on soft and rocky substrate in the intertidal of the Bay of Brest, France. J. Sea Res. 65, 84–93 (2011).
doi: 10.1016/j.seares.2010.07.004
Morris, R. L. et al. The application of oyster reefs in shoreline protection: are we over‐engineering for an ecosystem engineer? J. Appl. Ecol. 56, 1703–1711 (2019).
doi: 10.1111/1365-2664.13390
Guarini, J. M. et al. Dynamics of spatial patterns of microphytobenthic biomass: inferences from a geostatistical analyisis of two comprenhensive surveys in Marennes-Oléron Bay (France). Mar. Ecol. Prog. Ser. 166, 131–141 (1998).
doi: 10.3354/meps166131
Orvain, F. et al. Spatial and temporal interaction between sediment and microphytobenthos in a temperate estuarine macro-intertidal bay. Mar. Ecol. Prog. Ser. 458, 53–68 (2012).
doi: 10.3354/meps09698
Echappé, C. et al. Satellite remote sensing reveals a positive impact of living oyster reefs on microalgal biofilm development. Biogeosciences 15, 905–918 (2018).
doi: 10.5194/bg-15-905-2018
Le Bris, A. et al. Hyperspectral remote sensing of wild oyster reefs. Estuar. Coast. Shelf Sci. 172, 1–12 (2016).
doi: 10.1016/j.ecss.2016.01.039
Méléder, V., Launeau, P., Barillé, L. & Rincé, Y. Microphytobenthos assemblage mapping by spatial visible-infrared remote sensing in a shellfish ecosystem. C. R. Biol. 326, 377–389 (2003).
pubmed: 12876890 doi: 10.1016/S1631-0691(03)00125-2
Thomas, Y. et al. Global change and climate-driven invasion of the Pacific oyster (Crassostrea gigas) along European coasts: a bioenergetics modelling approach. J. Biogeogr. 43, 568–579 (2016).
doi: 10.1111/jbi.12665
Hope, J. A., Paterson, D. M. & Thrush, S. F. The role of microphytobenthos in soft‐sediment ecological networks and their contribution to the delivery of multiple ecosystem services. J. Ecol. 108, 815–830 (2020).
doi: 10.1111/1365-2745.13322
Leguerrier, D., Degré, D. & Niquil, N. Network analysis and inter-ecosystem comparison of two intertidal mudflat food webs (Brouage Mudflat and Aiguillon Cove, SW France). Estuar. Coast. Shelf Sci. 74, 403–418 (2007).
doi: 10.1016/j.ecss.2007.04.014
Le Pape, O. et al. Sources of organic matter for flatfish juveniles in coastal and estuarine nursery grounds: a meta-analysis for the common sole (Solea solea) in contrasted systems of Western Europe. J. Sea Res. 75, 85–95 (2013).
doi: 10.1016/j.seares.2012.05.003
Miller, D. C., Geider, R. J. & MacIntyre, H. L. Microphytobenthos: the ecological role of the ‘secret garden’ of unvegetated, shallow-water marine habitats. II. Role in sediment stability and shallow-water food webs. Estuaries 19, 202–212 (1996).
doi: 10.2307/1352225
Underwood, G. & Kromkamp, J. Primary production by phytoplankton and microphytobenthos in estuaries. Adv. Ecol. Res. 29, 93–153 (1999).
doi: 10.1016/S0065-2504(08)60192-0
Frankenbach, S. et al. Synoptic spatio-temporal variability of the photosynthetic productivity of microphytobenthos and phytoplankton in a tidal estuary. Front. Mar. Sci. 7, 170 (2020).
doi: 10.3389/fmars.2020.00170
Méléder, V. et al. Mapping the intertidal microphytobenthos gross primary production part I: coupling multispectral remote sensing and physical modeling. Front. Mar. Sci. 7, 520 (2020).
doi: 10.3389/fmars.2020.00520
Jesus, B. et al. Adaptations of microphytobenthos assemblages to sediment type and tidal position. Cont. Shelf Res. 29, 1624–1634 (2009).
doi: 10.1016/j.csr.2009.05.006
Méléder, V. et al. Spatio-temporal changes in microphytobenthos structure analysed by pigment composition in a macrotidal flat (Bourgneuf Bay, France). Mar. Ecol. Prog. Ser. 297, 83–99 (2005).
doi: 10.3354/meps297083
Colden, A. M., Fall, K. A., Cartwright, G. M. & Friedrichs, C. T. Sediment suspension and deposition across restored oyster reefs of varying orientation to flow: implications for restoration. Estuaries Coasts 39, 1435–1448 (2016).
doi: 10.1007/s12237-016-0096-y
Engel, F. G. et al. Mussel beds are biological power stations on intertidal flats. Estuar. Coast. Shelf Sci. 191, 21–27 (2017).
doi: 10.1016/j.ecss.2017.04.003
Pinckney, J. & Sandulli, R. Spatial autocorrelation analysis of meiofaunal and microalgal populations on an intertidal sandflat: Scale linkage between consumers and resources. Estuar. Coast. Shelf Sci. 30, 341–353 (1990).
doi: 10.1016/0272-7714(90)90002-9
Al-Zaidan, A. S. Y., Kennedy, H., Jones, D. & Al-Mohanna, S. Y. Role of microbial mats in Sulaibikhat Bay (Kuwait) mudflat food webs: evidence from δ 13 C analysis. Mar. Ecol. Prog. Ser. 308, 27–36 (2006).
doi: 10.3354/meps308027
Kang, C. K. et al. Linking intertidal and subtidal food webs: consumer-mediated transport of intertidal benthic microalgal carbon. PLoS One 10, 1–26 (2015).
doi: 10.1371/journal.pone.0139802
Middelburg, J. J. et al. The fate of intertidal microphytobenthos carbon: an in situ 13C-labeling study. Limnol. Oceanogr. 45, 1224–1234 (2000).
doi: 10.4319/lo.2000.45.6.1224
van der Wal, D. et al. Distribution and dynamics of intertidal macrobenthos predicted from remote sensing: Response to microphytobenthos and environment. Mar. Ecol. Prog. Ser. 367, 57–72 (2008).
doi: 10.3354/meps07535
Cognie, B. & Barillé, L. Does bivalve mucus favour the growth of their main food source, microalgae? Oceanol. Acta 22, 441–450 (1999).
doi: 10.1016/S0399-1784(00)88727-7
Leguerrier, D. et al. Numerical analysis of the food web of an intertidal mudflat ecosystem on the Atlantic coast of France. Mar. Ecol. Prog. Ser. 246, 17–37 (2003).
doi: 10.3354/meps246017
Passarelli, C., Olivier, F., Paterson, D. M. & Hubas, C. Impacts of biogenic structures on benthic assemblages: microbes, meiofauna, macrofauna and related ecosystem functions. Mar. Ecol. Prog. Ser. 465, 85–97 (2012).
doi: 10.3354/meps09915
Downie, R. A., Babcock, R. C., Thomson, D. P. & Vanderklift, M. A. Density of herbivorous fish and intensity of herbivory are influenced by proximity to coral reefs. Mar. Ecol. Prog. Ser. 482, 217–225 (2013).
doi: 10.3354/meps10250
Markert, A., Wehrmann, A. & Kröncke, I. Recently established Crassostrea-reefs versus native Mytilus-beds: differences in ecosystem engineering affects the macrofaunal communities (Wadden Sea of Lower Saxony, southern German Bight). Biol. Invasions 12, 15–32 (2010).
doi: 10.1007/s10530-009-9425-4
Savelli, R. et al. On biotic and abiotic drivers of the microphytobenthos seasonal cycle in a temperate intertidal mudflat: a modelling study. Biogeosciences 15, 7243–7271 (2018).
doi: 10.5194/bg-15-7243-2018
Morrisey, D. J. Differences in effects of grazing by deposit-feeders Hydrobia ulvae (Pennant) (Gastropoda: Prosobranchia) and Corophium arenarium Crawford (Amphipoda) on sediment microalgal populations. II. Quantitative effects. J. Exp. Mar. Bio. Ecol. 118, 43–53 (1988).
doi: 10.1016/0022-0981(88)90121-9
Riera, P. et al. Determination of food sources for benthic invertebrates in a salt marsh (Aiguillon Bay, France) by carbon and nitrogen stable isotopes: importance of locally produced sources. Mar. Ecol. Prog. Ser. 187, 301–307 (1999).
doi: 10.3354/meps187301
Stafford, R. & Davies, M. S. Spatial patchiness of epilithic biofilm caused by refuge-inhabiting high shore gastropods. Hydrobiologia 545, 279–287 (2005).
doi: 10.1007/s10750-005-3320-5
Silliman, B. R. & Bertness, M. D. A trophic cascade regulates salt marsh primary production. Proc. Natl Acad. Sci. USA 99, 10500–10505 (2002).
pubmed: 12149475 pmcid: 124954 doi: 10.1073/pnas.162366599
Reynolds, P. L. & Bruno, J. F. Multiple predator species alter prey behavior, population growth, and a trophic cascade in a model estuarine food web. Ecol. Monogr. 83, 119–132 (2013).
doi: 10.1890/11-2284.1
Raffaelli, D., Conacher, A., McLachlan, H. & Emes, C. The role of epibenthic crustacean predators in an estuarine food web. Estuar. Coast. Shelf Sci. 28, 149–160 (1989).
doi: 10.1016/0272-7714(89)90062-0
Eggleston, D. B., Lipcius, R. N. & Hines, A. H. Density-dependent predation by blue crabs upon infaunal clam species with contrasting distribution and abundance patterns. Mar. Ecol. Prog. Ser. 85, 55–68 (1992).
doi: 10.3354/meps085055
Raffaelli, D. & Milne, H. An experimental investigation of the effects of shorebird and flatfish predation on estuarine invertebrates. Estuar. Coast. Shelf Sci. 24, 1–13 (1987).
doi: 10.1016/0272-7714(87)90002-3
Moksnes, P., Pihl, L. & van Montfrans, J. Predation on postlarvae and juveniles of the shore crab Carcinus maenas:importance of shelter, size and cannibalism. Mar. Ecol. Prog. Ser. 166, 211–225 (1998).
doi: 10.3354/meps166211
McAfee, D. & Bishop, M. J. The mechanisms by which oysters facilitate invertebrates vary across environmental gradients. Oecologia 189, 1095–1106 (2019).
pubmed: 30826868 doi: 10.1007/s00442-019-04359-3
Lindström Swanberg, I. The influence of the filter-feeding bivalve Cerastoderma edule L. on microphytobenthos: a laboratory study. J. Exp. Mar. Bio. Ecol. 151, 93–111 (1991).
doi: 10.1016/0022-0981(91)90018-R
Donadi, S. et al. Multi-scale habitat modification by coexisting ecosystem engineers drives spatial separation of macrobenthic functional groups. Oikos 124, 1502–1510 (2015).
doi: 10.1111/oik.02100
Pearson, T. H. & Rosenberg, R. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr. Mar. Biol. Annu. Rev. 16, 229–311 (1978).
Jones, A. G., Dubois, S. F., Desroy, N. & Fournier, J. Interplay between abiotic factors and species assemblages mediated by the ecosystem engineer Sabellaria alveolata (Annelida: Polychaeta). Estuar. Coast. Shelf Sci. 200, 1–18 (2018).
doi: 10.1016/j.ecss.2017.10.001
Leguerrier, D., Niquil, N., Petiau, A. & Bodoy, A. Modeling the impact of oyster culture on a mudflat food web in Marennes-Oléron Bay (France). Mar. Ecol. Prog. Ser. 273, 147–161 (2004).
doi: 10.3354/meps273147
Callaway, R. Tube worms promote community change. Mar. Ecol. Prog. Ser. 308, 49–60 (2006).
doi: 10.3354/meps308049
Zwerschke, N., Emmerson, M. C., Roberts, D. & O’Connor, N. E. Benthic assemblages associated with native and non-native oysters are similar. Mar. Pollut. Bull. 111, 305–310 (2016).
pubmed: 27377003 doi: 10.1016/j.marpolbul.2016.06.094
Heiman, K. W. & Micheli, F. Non-native ecosystem engineer alters estuarine communities. In: Integrative and Comparative Biology vol. 50 226–236 (Oxford Academic, 2010).
Bertness, M. D. & Leonard, G. H. The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78, 1976–1989 (2012).
doi: 10.1890/0012-9658(1997)078[1976:TROPII]2.0.CO;2
Passarelli, C., Olivier, F., Paterson, D. M., Meziane, T. & Hubas, C. Organisms as cooperative ecosystem engineers in intertidal flats. J. Sea Res. 92, 92–101 (2014).
doi: 10.1016/j.seares.2013.07.010
Lenihan, H. S. Physical-biological coupling on oyster reefs: How habitat structure influences individual performance. Ecol. Monogr. 69, 251–275 (1999).
De Jonge, V. N. & Van Beuselom, J. E. E. Contribution of resuspended microphytobenthos to total phytoplankton in the EMS estuary and its possible role for grazers. Neth. J. Sea Res. 30, 91–105 (1992).
doi: 10.1016/0077-7579(92)90049-K
Decottignies, P., Beninger, P., Rincé, Y., Robins, R. & Riera, P. Exploitation of natural food sources by two sympatric, invasive suspension-feeders: Crassostrea gigas and Crepidula fornicata. Mar. Ecol. Prog. Ser. 334, 179–192 (2007).
doi: 10.3354/meps334179
Cognie, B., Haure, J. & Barillé, L. Spatial distribution in a temperate coastal ecosystem of the wild stock of the farmed oyster Crassostrea gigas (Thunberg). Aquaculture 259, 249–259 (2006).
doi: 10.1016/j.aquaculture.2006.05.037
Underwood, A. J. The analysis of stress in natural populations. Biol. J. Linn. Soc. 37, 51–78 (1989).
doi: 10.1111/j.1095-8312.1989.tb02005.x
Brito, A. C. et al. Seasonality of microphytobenthos revealed by remote-sensing in a South European estuary. Cont. Shelf Res. 66, 83–91 (2013).
doi: 10.1016/j.csr.2013.07.004
Ricciardi, A. & Bourget, E. Weight-to-weight conversion factors for marine benthic macroinvertebrates. Mar. Ecol. Prog. Ser. 163, 245–251 (1998).
doi: 10.3354/meps163245
Dutilleul, P., Clifford, P., Richardson, S. & Hemon, D. Modifying the T test for assessing the correlation between two spatial processes. Biometrics 49, 305–314 (1993).
doi: 10.2307/2532625
Grace, J. B. Structural equation modeling for observational studies. J. Wildl. Manag. 72, 14–22 (2008).
doi: 10.2193/2007-307
Rosseel, Y. Lavaan: An R package for structural equation modeling. J. Stat. Softw. 48, 1–36 (2012).
doi: 10.18637/jss.v048.i02
Pebesma, E. J. Multivariable geostatistics in S: the gstat package. Comput. Geosci. 30, 683–691 (2004).
doi: 10.1016/j.cageo.2004.03.012
R Development Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2021).
Reddin C. J., et al. Data from: Extensive spatial impacts of oyster reefs on an intertidal mudflat community via predator facilitation. Zenodo. https://doi.org/10.5281/zenodo.5902388 (2022).

Auteurs

Carl J Reddin (CJ)

Université de Nantes, Département des Sciences de la Vie, EA 2160 Mer - Molécules - Santé 2, Rue de la Houssinière, 44322, Nantes, France. Carl.reddin@mfn.berlin.
Museum für Naturkunde - Leibniz Institute for Research on Evolution and Biodiversity, Invalidenstr. 43, 10115, Berlin, Germany. Carl.reddin@mfn.berlin.

Priscilla Decottignies (P)

Université de Nantes, Département des Sciences de la Vie, EA 2160 Mer - Molécules - Santé 2, Rue de la Houssinière, 44322, Nantes, France.

Lise Bacouillard (L)

French Research Institute for the Exploration of the Sea (IFREMER), DYNECO-LEBCO, Centre de Bretagne, ZI de la pointe du Diable, CS 10070, 29280, Plouzané, France.

Laurent Barillé (L)

Université de Nantes, Département des Sciences de la Vie, EA 2160 Mer - Molécules - Santé 2, Rue de la Houssinière, 44322, Nantes, France.

Stanislas F Dubois (SF)

French Research Institute for the Exploration of the Sea (IFREMER), DYNECO-LEBCO, Centre de Bretagne, ZI de la pointe du Diable, CS 10070, 29280, Plouzané, France.

Caroline Echappé (C)

Université de Nantes, Département des Sciences de la Vie, EA 2160 Mer - Molécules - Santé 2, Rue de la Houssinière, 44322, Nantes, France.

Pierre Gernez (P)

Université de Nantes, Département des Sciences de la Vie, EA 2160 Mer - Molécules - Santé 2, Rue de la Houssinière, 44322, Nantes, France.

Bruno Jesus (B)

Université de Nantes, Département des Sciences de la Vie, EA 2160 Mer - Molécules - Santé 2, Rue de la Houssinière, 44322, Nantes, France.

Vona Méléder (V)

Université de Nantes, Département des Sciences de la Vie, EA 2160 Mer - Molécules - Santé 2, Rue de la Houssinière, 44322, Nantes, France.

Paulina S Nätscher (PS)

GeoZentrum Nordbayern, Department of Geography and Geosciences, Universität Erlangen-Nürnberg, Erlangen, Germany.

Vincent Turpin (V)

Université de Nantes, Département des Sciences de la Vie, EA 2160 Mer - Molécules - Santé 2, Rue de la Houssinière, 44322, Nantes, France.

Daniela Zeppilli (D)

French Research Institute for the Exploration of the Sea (IFREMER), REM-EEP-LEP, Centre de Bretagne, ZI de la pointe du diable, CS10070, 29280, Plouzané, France.

Nadescha Zwerschke (N)

Joint Nature Conservation Committee, Inverdee House, Baxter Street, Aberdeen, AB11 9QA, UK.

Anik Brind'Amour (A)

French Research Institute for the Exploration of the Sea (IFREMER), PDG-RBE-EMH, Rue de l'Ile d'Yeu, BP 21105, 44311, Nantes, France.

Bruno Cognie (B)

Université de Nantes, Département des Sciences de la Vie, EA 2160 Mer - Molécules - Santé 2, Rue de la Houssinière, 44322, Nantes, France.

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