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Non-trophic Interactions Control Benthic Producers on Intertidal Flats

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Abstract

The importance of positive effects of ecosystem engineers on associated communities is predicted to increase with environmental stress. However, incorporating such non-trophic interactions into ecological theory is not trivial because facilitation of associated species is conditional on both the type of engineer and the type of abiotic stress. We tested the influence of two allogenic ecosystem engineers (lugworms, Arenicola marina L. and cockles, Cerastoderma edule L.) on the main primary producers (microphytobenthos) of the tidal flats, under different abiotic stresses controlled by reefs of blue mussels (Mytilus edulis L.). We added 25,000 cockles or 2,000 lugworms to 5 × 5 m plots, both in a muddy site with high sedimentation rates located coastward of a mussel bed, and in a sandy site without mussels and characterized by high hydrodynamic stress. After a year, cockles increased algal biomass in the sandy area, but not in the mussel bed site, where high values were measured in all plots. However, lugworms did not affect algal biomass in any of the sites. Field measurements suggest that cockles outweighed negative effects of water currents in the site without mussels by locally increasing sediment stability, whereas mussels overruled the effects of cockles in the wake of the reefs through hydrodynamic stress alleviation and/or biodeposition. Our results suggest that non-trophic interactions by ecosystem engineering bivalves control primary production of intertidal areas, and that the sediment-stabilizing effect of cockles plays a crucial role where the overruling effects of mussel beds are not present.

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References

  • Andersen TJ, Lanuru M, van Bernem C, Pejrup M, Riethmueller R. 2010. Erodibility of a mixed mudflat dominated by microphytobenthos and Cerastoderma edule, East Frisian Wadden Sea, Germany. Estuar Coast Shelf Sci 87:197–206.

    Article  Google Scholar 

  • Banta GT, Holmer M, Jensen MH, Kristensen E. 1999. Effects of two polychaete worms, Nereis diversicolor and Arenicola marina, on aerobic and anaerobic decomposition in a sandy marine sediment. Aquat Microb Ecol 19:189–204.

    Article  Google Scholar 

  • Bertness MD, Callaway R. 1994. Positive interactions in communities. Trends Ecol Evol 9:191–3.

    Article  PubMed  CAS  Google Scholar 

  • Beukema JJ, Dekker R. 2005. Decline of recruitment success in cockles and other bivalves in the Wadden Sea: possible role of climate change, predation on postlarvae and fisheries. Mar Ecol Prog Ser 287:149–67.

    Article  Google Scholar 

  • Beukema JJ, Devlas J. 1979. Population parameters of the lugworm, Arenicola marina, living on tidal flats in the Dutch Wadden Sea. Neth J Sea Res 13:331–53.

    Article  Google Scholar 

  • Blanchard GF, Paterson DM, Stal LJ, Richard P, Galois R, Huet V, Kelly J, Honeywill C, de Brouwer J, Dyer K, Christie M, Seguignes M. 2000. The effect of geomorphological structures on potential biostabilisation by microphytobenthos on intertidal mudflats. Cont Shelf Res 20:1243–56.

    Article  Google Scholar 

  • Bracken MES. 2004. Invertebrate-mediated nutrient loading increases growth of an intertidal macroalga. J Phycol 40:1032–41.

    Article  Google Scholar 

  • Bruno JF, Bertness MD. 2001. Habitat modification and facilitation in benthic marine communities. In: Bertness MD, Gaines SD, Hay ME, Eds. Marine community ecology. Sunderland, MA: Sinauer. p 201–18.

    Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD. 2003. Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–25.

    Article  Google Scholar 

  • Bulleri F, Cristaudo C, Alestra T, Benedetti-Cecchi L. 2011. Crossing gradients of consumer pressure and physical stress on shallow rocky reefs: a test of the stress-gradient hypothesis. J Ecol 99:335–44.

    Article  Google Scholar 

  • Callaway RM. 1997. Positive interactions in plant communities and the individualistic-continuum concept. Oecologia 112:143–9.

    Article  Google Scholar 

  • Callaway RM, Walker LR. 1997. Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–65.

    Article  Google Scholar 

  • Choler P, Michalet R, Callaway RM. 2001. Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–308.

    Article  Google Scholar 

  • Ciutat A, Widdows J, Readman JW. 2006. Influence of cockle Cerastoderma edule bioturbation and tidal-current cycles on resuspension of sediment and polycyclic aromatic hydrocarbons. Mar Ecol Prog Ser 328:51–64.

    Article  CAS  Google Scholar 

  • Ciutat A, Widdows J, Pope ND. 2007. Effect of Cerastoderma edule density on near-bed hydrodynamics and stability of cohesive muddy sediments. J Exp Mar Biol Ecol 346:114–26.

    Article  Google Scholar 

  • Crain CM, Bertness ND. 2005. Community impacts of a tussock sedge: is ecosystem engineering important in benign habitats? Ecology 86:2695–704.

    Article  Google Scholar 

  • Crain CM, Bertness MD. 2006. Ecosystem engineering across environmental gradients: implications for conservation and management. Bioscience 56:211–18.

    Article  Google Scholar 

  • Daleo P, Iribarne O. 2009. Beyond competition: the stress-gradient hypothesis tested in plant–herbivore interactions. Ecology 90:2368–74.

    Article  PubMed  Google Scholar 

  • Dayton PK. 1972. Toward an understanding of community resilience and the potential effects of enrichments to the benthos at McMurdo Sound, Antarctica. In: Proceedings of the colloquium on conservation problems in Antarctica. Lawrence, KS: Allen Press. pp 81–95.

  • de Jong DJ, de Jonge VN. 1995. Dynamics and distribution of microphytobenthic chlorophyll a in the Western Scheldt Estuary (SW Netherlands). Hydrobiologia 311:21–30.

    Article  Google Scholar 

  • de Jonge VN, van Beusekom JEE. 1995. Wind-induced and tide-induced resuspension of sediment and microphytobenthos from tidal flats in the Ems Estuary. Limnol Oceanogr 40:766–78.

    Article  Google Scholar 

  • Donadi S, van der Heide T, van der Zee EM, Eklöf JS, van de Koppel J, Weerman EJ, Piersma T, Olff H, Eriksson BK. 2013. Cross-habitat interactions among bivalve species control community structure on intertidal flats. Ecology 94:489–98.

    Article  PubMed  Google Scholar 

  • Eriksson BK, van der Heide T, van de Koppel J, Piersma T, van der Veer HW, Olff H. 2010. Major changes in the ecology of the Wadden Sea: human impacts, ecosystem engineering and sediment dynamics. Ecosystems 13:752–64.

    Article  CAS  Google Scholar 

  • Filgueira R, Castro BG. 2011. Study of the trophic web of San Simon Bay (Ria de Vigo) by using stable isotopes. Cont Shelf Res 31:476–87.

    Article  Google Scholar 

  • Flach EC. 1996. The influence of the cockle, Cerastoderma edule, on the macrozoobenthic community of tidal flats in the Wadden Sea. Mar Ecol 17:87–98.

    Article  Google Scholar 

  • Graf G, Rosenberg R. 1997. Bioresuspension and biodeposition: a review. J Mar Syst 11:269–78.

    Article  Google Scholar 

  • Herman PMJ, Middelburg JJ, Heip CHR. 2001. Benthic community structure and sediment processes on an intertidal flat: results from the ECOFLAT project. Cont Shelf Res 21:2055–71.

    Article  Google Scholar 

  • Jeffrey SW, Humphrey GF. 1975. New spectrophotometric equation for determining chlorophyll a, b, c 1 and c 2 . Biochem Physiol Pflanz 167:194–204.

    Google Scholar 

  • Jensen KT. 1992. Dynamics and growth of the cockle, Cerastoderma edule, on an intertidal mud-flat in the Danish Wadden sea: effects of submersion time and density. Neth J Sea Res 28:335–45.

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M. 1994. Organisms as ecosystem engineers. Oikos 69:373–86.

    Article  Google Scholar 

  • Kawai T, Tokeshi M. 2007. Testing the facilitation-competition paradigm under the stress-gradient hypothesis: decoupling multiple stress factors. Proc R Soc B Biol Sci 274:2503–8.

    Article  Google Scholar 

  • Kefi S, Berlow EL, Wieters EA, Navarrete SA, Petchey OL, Wood SA, Boit A, Joppa LN, Lafferty KD, Williams RJ, Martinez ND, Menge BA, Blanchette CA, Iles AC, Brose U. 2012. More than a meal…integrating non-feeding interactions into food webs. Ecol Lett 15:291–300.

    Article  Google Scholar 

  • Kraan C, Dekinga A, Piersma T. 2011. Now an empty mudflat: past and present benthic abundances in the western Dutch Wadden Sea. Helgol Mar Res 65:51–8.

    Article  Google Scholar 

  • Lebreton B, Richard P, Galois R, Radenac G, Pfleger C, Guillou G, Mornet F, Blanchard GF. 2011. Trophic importance of diatoms in an intertidal Zostera noltii seagrass bed: evidence from stable isotope and fatty acid analyses. Estuar Coast Shelf Sci 92:140–53.

    Article  CAS  Google Scholar 

  • Legendre P, Legendre L. 1998. Numerical ecology. In: Developments in environmental modelling, vol 20, 2nd edn. Amsterdam: Elsevier, ISBN-9780444538680.

  • Lohrer AM, Thrush SF, Gibbs MM. 2004. Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431:1092–5.

    Article  PubMed  CAS  Google Scholar 

  • Lohrer AM, Halliday NJ, Thrush SF, Hewitt JE, Rodil IF. 2010. Ecosystem functioning in a disturbance-recovery context: contribution of macrofauna to primary production and nutrient release on intertidal sandflats. J Exp Mar Biol Ecol 390:6–13.

    Article  Google Scholar 

  • Lotze HK, Reise K, Worm B, van Beusekom J, Busch M, Ehlers A, Heinrich D, Hoffmann RC, Holm P, Jensen C, Knottnerus OS, Langhanki N, Prummel W, Vollmer M, Wolff WJ. 2005. Human transformations of the Wadden Sea ecosystem through time: a synthesis. Helgol Mar Res 59:84–95.

    Article  Google Scholar 

  • Maestre FT, Callaway RM, Valladares F, Lortie CJ. 2009. Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205.

    Article  Google Scholar 

  • Montserrat F, Van Colen C, Provoost P, Milla M, Ponti M, Van den Meersche K, Ysebaert T, Herman PMJ. 2009. Sediment segregation by biodiffusing bivalves. Estuar Coast Shelf Sci 83:379–91.

    Article  CAS  Google Scholar 

  • Nacken N, Reise K. 2000. Effects of herbivorous birds on intertidal seagrass beds in the northern Wadden Sea. Helgol Mar Res 54:87–94.

    Article  Google Scholar 

  • Needham HR, Pilditch CA, Lohrer AM, Thrush SF. 2011. Context-specific bioturbation mediates changes to ecosystem functioning. Ecosystems 14:1096–109.

    Article  CAS  Google Scholar 

  • Neumeier U, Lucas CH, Collins M. 2006. Erodibility and erosion patterns of mudflat sediments investigated using an annular flume. Aquat Ecol 40:543–54.

    Article  CAS  Google Scholar 

  • Newell RIE, Koch EW. 2004. Modeling seagrass density and distribution in response to changes in turbidity stemming from bivalve filtration and seagrass sediment stabilization. Estuaries 27:793–806.

    Article  Google Scholar 

  • Olff H, Alonso D, Berg MP, Eriksson BK, Loreau M, Piersma T, Rooney N. 2009. Parallel ecological networks in ecosystems. Philos Trans R Soc B Biol Sci 364:1755–79.

    Article  Google Scholar 

  • Piersma T, Koolhaas A, Dekinga A, Beukema JJ, Dekker R, Essink K. 2001. Long-term indirect effects of mechanical cockle-dredging on intertidal bivalve stocks in the Wadden Sea. J Appl Ecol 38:976–90.

    Article  Google Scholar 

  • Reise K. 2002. Sediment mediated species interactions in coastal waters. J Sea Res 48:127–41.

    Article  Google Scholar 

  • Sauriau PG, Kang CK. 2000. Stable isotope evidence of benthic microalgae-based growth and secondary production in the suspension feeder Cerastoderma edule (Mollusca, Bivalvia) in the Marennes-Oleron Bay. Hydrobiologia 440:317–29.

    Article  Google Scholar 

  • Swanberg IL. 1991. The influence of the filter-feeding bivalve Cerastoderma edule L. on microphytobenthos—a laboratory study. J Exp Mar Biol Ecol 151:93–111.

    Article  Google Scholar 

  • Thompson TL, Glenn EP. 1994. Plaster standards to measure water motion. Limnol Oceanogr 39:1768–79.

    Article  Google Scholar 

  • Thrush SF, Whitlatch RB, Pridmore RD, Hewitt JE, Cummings VJ, Wilkinson MR. 1996. Scale-dependent recolonization: the role of sediment stability in a dynamic sandflat habitat. Ecology 77:2472–87.

    Article  Google Scholar 

  • Thrush SF, Hewitt JE, Gibbs M, Lundquist C, Norkko A. 2006. Functional role of large organisms in intertidal communities: community effects and ecosystem function. Ecosystems 9:1029–40.

    Article  Google Scholar 

  • Tolhurst TJ, Black KS, Shayler SA, Mather S, Black I, Baker K, Paterson DM. 1999. Measuring the in situ erosion shear stress of intertidal sediments with the cohesive strength meter (CSM). Estuar Coast Shelf Sci 49:281–94.

    Article  Google Scholar 

  • Van De Koppel J, Herman PMJ, Thoolen P, Heip CHR. 2001. Do alternate stable states occur in natural ecosystems? Evidence from a tidal flat. Ecology 82:3449–61.

    Article  Google Scholar 

  • van der Heide T, van Nes EH, Geerling GW, Smolders AJP, Bouma TJ, van Katwijk MM. 2007. Positive feedbacks in seagrass ecosystems—implications for success in conservation and restoration. Ecosystems 10:1311–22.

    Article  Google Scholar 

  • van der Wal D, Wielemaker-van den Dool A, Herman PMJ. 2010. Spatial synchrony in intertidal benthic algal biomass in temperate coastal and estuarine ecosystems. Ecosystems 13:338–51.

    Article  Google Scholar 

  • van der Zee EM, van der Heide T, Donadi S, Eklof JS, Eriksson BK, Olff H, van der Veer HW, Piersma T. 2012. Spatially extended habitat modification by intertidal reef-building bivalves has implications for consumer–resource interactions. Ecosystems 15:664–73.

    Article  CAS  Google Scholar 

  • Volkenborn N, Hedtkamp SIC, van Beusekom JEE, Reise K. 2007. Effects of bioturbation and bioirrigation by lugworms (Arenicola marina) on physical and chemical sediment properties and implications for intertidal habitat succession. Estuar Coast Shelf Sci 74:331–43.

    Article  Google Scholar 

  • Weerman EJ, van de Koppel J, Eppinga MB, Montserrat F, Liu QX, Herman PMJ. 2010. Spatial self-organization on intertidal mudflats through biophysical stress divergence. Am Nat 176:E15–32.

    Article  PubMed  Google Scholar 

  • Widdows J, Brinsley M. 2002. Impact of biotic and abiotic processes on sediment dynamics and the consequences to the structure and functioning of the intertidal zone. J Sea Res 48:143–56.

    Article  Google Scholar 

  • Widdows J, Brinsley MD, Bowley N, Barrett C. 1998. A benthic annular flume for in situ measurement of suspension feeding/biodeposition rates and erosion potential of intertidal cohesive sediments. Estuar Coast Shelf Sci 46:27–38.

    Article  Google Scholar 

  • Widdows J, Blauw A, Heip CHR, Herman PMJ, Lucas CH, Middelburg JJ, Schmidt S, Brinsley MD, Twisk F, Verbeek H. 2004. Role of physical and biological processes in sediment dynamics of a tidal flat in Westerschelde Estuary, SW Netherlands. Mar Ecol Prog Ser 274:41–56.

    Article  Google Scholar 

  • Winterwerp JC, Van Kesteren WGM. 2004. Introduction to the physics of cohesive sediment in the marine environment. In: van Loon T, Ed. Developments in sedimentology. Amsterdam: Elsevier.

    Google Scholar 

  • Ysebaert T, Hart M, Herman PMJ. 2009. Impacts of bottom and suspended cultures of mussels Mytilus spp. on the surrounding sedimentary environment and macrobenthic biodiversity. Helgol Mar Res 63:59–74.

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM, Eds. 2009. Mixed effects models and extensions in ecology with R. New York: Springer.

    Google Scholar 

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Acknowledgments

We thank Imke Gerwen, Marc Bartelds, Judith Westveer, Jeroen Kuypers, Tim Ruiter, Jim de Fouw, Karin de Boer, Stefania Gemignani, Nicola Stefani, Katrin Sieben, Guus Diepenmaat, and Maria van Leeuwe for help in the field; Johan Eklöf for advise on the experimental design; and three anonymous reviewers who greatly contributed to improve our manuscript. We are grateful to Vereniging Natuurmonumenten for granting us permission for the field work on the tidal flats. This study was financed by a grant from the ZKO program of the Netherlands Organization of Scientific Research (NWO) to BKE (Grant No. 839.08.310).

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Authors and Affiliations

  1. Department of Marine Benthic Ecology and Evolution, Centre for Ecological and Evolutionary Studies (CEES), University of Groningen, P.O. Box 11103, 9700 CC, Groningen, The Netherlands

    Serena Donadi, Joëlle Westra & Britas Klemens Eriksson

  2. Community and Conservation Ecology Group, Centre for Ecological and Evolutionary Studies (CEES), University of Groningen, P.O. Box 11103, 9700 CC, Groningen, The Netherlands

    Ellen J. Weerman, Tjisse van der Heide, Johan van de Koppel & Han Olff

  3. Animal Ecology Group, Centre for Ecological and Evolutionary Studies (CEES), University of Groningen, P.O. Box 11103, 9700 CC, Groningen, The Netherlands

    Els M. van der Zee & Theunis Piersma

  4. Department of Marine Ecology, Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, 1790 AB, Den Burg, Texel, The Netherlands

    Els M. van der Zee, Theunis Piersma & Henk W. van der Veer

  5. Spatial Ecology Department, Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 140, 4400 AC, Yerseke, The Netherlands

    Johan van de Koppel

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  1. Serena Donadi
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  2. Joëlle Westra
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  3. Ellen J. Weerman
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Correspondence to Serena Donadi.

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Author contributions

BKE, SD, TvdH, EMvdZ, HO, JvdK, TP, and HWvdV have conceived and designed the experiments. SD, JW, EMvdZ, EJW, TvdH, and BKE have performed the experiments. SD and BKE have analyzed the data. SD, BKE, JvdK, EJW, EvdZ, HO, and TP wrote the paper.

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Donadi, S., Westra, J., Weerman, E.J. et al. Non-trophic Interactions Control Benthic Producers on Intertidal Flats. Ecosystems 16, 1325–1335 (2013). https://doi.org/10.1007/s10021-013-9686-8

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