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Regional-Scale Differences in Eutrophication Effects on Eelgrass-Associated (Zostera marina) Macrofauna

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Abstract

Eutrophication has caused strong shifts from perennial seagrass to opportunistic macroalgae and phytoplankton in many coastal ecosystems worldwide, yet responses of the primary-producer assemblage can vary with regional environmental and nutrient-loading conditions. The wider consequences of this variable primary-producer response on the associated animal community are little known. We used large-scale field surveys across 12 study sites with low or high eutrophication levels in two geographic provinces in Atlantic Canada to examine region-specific responses of macrofauna associated with eelgrass beds. In both regions, abundances of all groups increased with eutrophication, but species richness of mobile fishes and invertebrates decreased. Generally, filter feeders, epibenthic detritivores and some herbivores increased, while more hypoxia sensitive species declined. Small fishes and invertebrate predators increased with eutrophication mirrored by decreases in their prey. Despite similar general trends, our results show distinct shifts in species composition in each geographic region associated with differences in food availability and predation refuge offered by phytoplankton and opportunistic epiphytic or benthic macroalgae as well as tolerance to an increasingly hostile physico-chemical environment. So far, the continued persistence of eelgrass beds at our “highly” eutrophied sites indicates intermediate eutrophication levels with short-term benefits for some species. However, the loss of sensitive species and decrease in species richness highlight that eutrophication has already changed seagrass ecosystems in Atlantic Canada. Our work suggests that mitigating these changes will require regional-scale management.

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References

  • Anderson, M.J., R.N. Gorley, and R.K. Clarke. 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: PRIMER-E Ltd..

    Google Scholar 

  • Bachelet, G., X. de Montaudouin, I. Auby, and P.J. Labourg. 2000. Seasonal changes in macrophyte and macrozoobenthos assemblages in three coastal lagoons under varying degrees of eutrophication. ICES Journal of Marine Science 57: 1495–1506.

    Article  Google Scholar 

  • Baden, S., C. Boström, S. Tobiasson, H. Arponen, and P.-O. Moksnes. 2010. Relative importance of trophic interactions and nutrient enrichment in seagrass ecosystems: a broad-scale field experiment in the Baltic-Skagerrak area. Limnology and Oceanography 55: 1435.

    Article  CAS  Google Scholar 

  • Baden, S., A. Emanuelsson, L. Pihl, C.-J. Svensson, and P. Åberg. 2012. Shift in seagrass food web structure over decades is linked to overfishing. Marine Ecology Progress Series 451: 61–73.

    Article  Google Scholar 

  • Bonsdorff, E., E.M. Blomqvist, J. Mattila, and A. Norkko. 1997. Long-term changes and coastal eutrophication. Examples from the Hand Islands and the Archipelago Sea, northern Baltic Sea. Oceanologica Acta 20: 319–329.

    Google Scholar 

  • Borum, J., K. Sand-Jensen, T. Binzer, O. Pedersen, and T.M. Greve. 2006. Oxygen movement in seagrasses. In Seagrasses: biology, ecology and conservation, ed. A.W.D. Larkum, R. Orth, and C.M. Duarte, 255–270. Dordrecht: Springer.

    Google Scholar 

  • Boström, C., E. Bonsdorff, P. Kangas, and A. Norkko. 2002. Long-term changes of a brackish-water eelgrass (Zostera marina L.) community indicate effects of coastal eutrophication. Estuarine Coastal and Shelf Science 55: 795–804.

    Article  Google Scholar 

  • Bugden, G., Y. Jiang, M. van den Heuvel, H. Vandermeulen, K. MacQuarrie, C. Crane, and B. Raymond. 2014. Nitrogen loading criteria for estuaries in Prince Edward Island: Fisheries and Oceans Canada.

  • Cardoso, P., M. Pardal, A. Lillebø, S. Ferreira, D. Raffaelli, and J. Marques. 2004. Dynamic changes in seagrass assemblages under eutrophication and implications for recovery. Journal of Experimental Marine Biology and Ecology 302: 233–248.

    Article  Google Scholar 

  • Cardoso, P.G., D. Raffaelli, and M.A. Pardal. 2007. Seagrass beds and intertidal invertebrates: an experimental test of the role of habitat structure. Hydrobiologia 575: 221–230.

    Article  Google Scholar 

  • Cebrian, J., D. Corcoran, and J. Lartigue. 2014. Eutrophication-driven shifts in primary producers in shallow coastal systems: implications for system functional change. Estuaries and Coasts 37: 180–197.

    Article  Google Scholar 

  • Cebrian, J., J.P. Stutes, and B. Christiaen. 2013. Effects of grazing and fertilization on epiphyte growth dynamics under moderately eutrophic conditions: implications for grazing rate estimates. Marine Ecology Progress Series 474: 121–133.

    Article  Google Scholar 

  • Christie, H., K.M. Norderhaug, and S. Fredriksen. 2009. Macrophytes as habitat for fauna. Marine Ecology Progress Series 396: 221–233.

    Article  Google Scholar 

  • Clarke, K., and R. Gorley. 2006. Primer v6. 1.6: user manual/tutorial. Plymouth: PRIMER-E Ltd..

    Google Scholar 

  • Clarke, K.R., and R.M. Warwick. 2001. Change in marine communities: an approach to statistical analysis and interpretation. Plymouth: PRIMER-E Ltd..

    Google Scholar 

  • Coll, M., A. Schmidt, T. Romanuk, and H.K. Lotze. 2011. Food-web structure of seagrass communities across different spatial scales and human impacts. PloS One 6: e22591.

    Article  CAS  Google Scholar 

  • Deegan, L.A., A. Wright, S.G. Ayvazian, J.T. Finn, H. Golden, R.R. Merson, and J. Harrison. 2002. Nitrogen loading alters seagrass ecosystem structure and support of higher trophic levels. Aquatic Conservation: Marine and Freshwater Ecosystems 12: 193–212.

    Article  Google Scholar 

  • Diaz, R.J., and R. Rosenberg. 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanography and Marine Biology Annual Review 33: 245–303.

    Google Scholar 

  • Dolbeth, M., M. Pardal, A. Lillebø, U. Azeiteiro, and J. Marques. 2003. Short-and long-term effects of eutrophication on the secondary production of an intertidal macrobenthic community. Marine Biology 143: 1229–1238.

    Article  Google Scholar 

  • Duarte, C.M. 2002. The future of seagrass meadows. Environmental Conservation 29: 192–206.

    Article  Google Scholar 

  • Fisheries and Oceans Canada. 2000. Inshore Gulf of Main rock crab (Cancer irroratus). Fisheries and Oceans Canada (DFO) Stock Status Report C3-67(2000).

  • Fisheries and Oceans Canada. 2009. Does eelgrass (Zostera marina) meet the criteria as an ecologically significant species? Fisheries and Oceans Canada (DFO) Canadian Science Advisory Secretariat Science Advisory Report. 2009/018. Moncton.

  • Fisheries and Oceans Canada. 2012. Definitions of harmful alteration, disruption or destruction (HADD) of habitat provided by eelgrass (Zostera marina). Fisheries and Oceans Canada (DFO) Canadian Science Advisory Secretariat Science Advisory Report. 2011/058. Moncton.

  • Fishman, J.R., R.J. Orth, S. Marion, and J. Bieri. 2004. A comparative test of mechanized and manual transplanting of relgrass, Zostera marina in Chesapeake Bay. Restoration Ecology 12: 214–219.

    Article  Google Scholar 

  • Fox, S.E., M. Teichberg, Y.S. Olsen, L. Heffner, and I. Valiela. 2009. Restructuring of benthic communities in eutrophic estuaries: lower abundance of prey leads to trophic shifts from omnivory to grazing. Marine Ecology Progress Series 380: 43–57.

    Article  CAS  Google Scholar 

  • Galbraith, P., J. Chassé, P. Nicot, C. Caverhill, D. Gilbert, B. Pettigrew, D. Lefaivre, D. Brickman, L. Devine, and C. Lafleur. 2015. Physical Oceanographic Conditions in the Gulf of St. Lawrence in 2014. In: Fisheries and Oceans Canada (DFO) Canadian Science Advisory Secretariat Science Advisory Research Document. 2015/032, 82.

  • Galbraith, P., D. Gilbert, C. Lafleur, P. Larouche, B. Pettigrew, J. Chassé, R. Pettipas, and W. Petrie. 2007. Physical oceanographic conditions in the Gulf of St. Lawrence in 2006. In: Fisheries and Oceans Canada (DFO) Canadian Science Advisory Secretariat Science Advisory Research Document. 2007/024, 56.

  • Gillanders, B. 2006. Seagrasses, fish, and fisheries. In Seagrasses: biology, ecology and conservation, ed. A.W.D. Larkum, R. Orth, and C.M. Duarte, 503–536. Dordrecht: Springer.

    Google Scholar 

  • Gilmurray, M., and G. Daborn. 1981. Feeding relations of the Atlantic silverside Menidia menidia in the Minas Basin, Bay of Fundy. Marine Ecology Progress Series 6: 231–235.

    Article  Google Scholar 

  • Goodman, J.L., K.A. Moore, and W.C. Dennison. 1995. Photosynthetic responses of eelgrass (Zostera marina L.) to light and sediment sulfide in a shallow barrier island lagoon. Aquatic Botany 50: 37–47.

    Article  Google Scholar 

  • Gotceitas, V., S. Fraser, and J.A. Brown. 1997. Use of eelgrass beds (Zostera marina) by juvenile Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 54: 1306–1319.

    Article  Google Scholar 

  • Gray, J.S., R.S. Wu, and Y.Y. Or. 2002. Effects of hypoxia and organic enrichment on the coastal marine environment. Marine Ecology Progress Series 238: 249–279.

    Article  Google Scholar 

  • Grizard, P. 2013. Modeling nitrate loading from watershed to coastal waters of the northumberland strait. MSc, University of Prince Edward Island.

  • Hauxwell, J., J. Cebrián, C. Furlong, and I. Valiela. 2001. Macroalgal canopies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems. Ecology 82: 1007–1022.

    Article  Google Scholar 

  • Hauxwell, J., J. Cebrian, and I. Valiela. 2003. Eelgrass Zostera marina loss in temperate estuaries: relationship to land-derived nitrogen loads and effect of light limitation imposed by algae. Marine Ecology Progress Series 247: 59–73.

    Article  CAS  Google Scholar 

  • Hazlett, B.A. 1981. The behavioral ecology of hermit crabs. Annual Review of Ecology and Systematics 12: 1–22.

    Article  Google Scholar 

  • Heck, K.L., G. Hays, and R.J. Orth. 2003. Critical evaluation of the nursery role hypothesis for seagrass meadows. Marine Ecology Progress Series 253: 123–136.

    Article  Google Scholar 

  • Heck, K.L., and R.J. Orth. 2006. Predation in seagrass beds. In Seagrasses: biology, ecology and conservation, ed. A.W.D. Larkum, R. Orth, and C.M. Duarte, 537–550. Dordrecht: Springer.

    Chapter  Google Scholar 

  • Hessing-Lewis, M.L., and S.D. Hacker. 2013. Upwelling-influence, macroalgal blooms, and seagrass production; temporal trends from latitudinal and local scales in Northeast Pacific estuaries. Limnology and Oceanography 58: 1103–1112.

    Article  Google Scholar 

  • Hodder, J. 1986. Production biology of an estuarine population of the green algae, Ulva spp. in Coos Bay, Oregon. PhD dissertation, University of Oregon, Washington.

  • Hootsmans, M., and J. Vermaat. 1985. The effect of periphyton-grazing by three epifaunal species on the growth of Zostera marina L. under experimental conditions. Aquatic Botany 22: 83–88.

    Article  Google Scholar 

  • Hughes, A.R., S.L. Williams, C.M. Duarte, K.L. Heck Jr., and M. Waycott. 2009. Associations of concern: declining seagrasses and threatened dependent species. Frontiers in Ecology and the Environment 7: 242–246.

    Article  Google Scholar 

  • Hughes, B.B., R. Eby, E. Van Dyke, M.T. Tinker, C.I. Marks, K.S. Johnson, and K. Wasson. 2013. Recovery of a top predator mediates negative eutrophic effects on seagrass. Proceedings of the National Academy of Sciences 110: 15313–15318.

    Article  CAS  Google Scholar 

  • Hughes, J.E., L.A. Deegan, J.C. Wyda, M.J. Weaver, and A. Wright. 2002. The effects of eelgrass habitat loss on estuarine fish communities of southern New England. Estuaries 25: 235–249.

    Article  Google Scholar 

  • Hutchings, J.A., and J.D. Reynolds. 2004. Marine fish population collapses: consequences for recovery and extinction risk. Bioscience 54: 297–309.

    Article  Google Scholar 

  • Isaksson, I., L. Pihl, and J. van Montfrans. 1994. Eutrophication-related changes in macrovegetation and foraging of young cod (Gadus morhua L.): a mesocosm experiment. Journal of Experimental Marine Biology and Ecology 177: 203–217.

    Article  Google Scholar 

  • Jackson, J.B.C., M.X. Kirby, W.H. Berger, K.A. Bjorndal, L.W. Botsford, B.J. Bourque, R.H. Bradbury, R. Cooke, J. Erlandson, and J.A. Estes. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293: 629–638.

    Article  CAS  Google Scholar 

  • Jiang, Y., P. Nishimura, M.R. van den Heuvel, K.T. MacQuarrie, C.S. Crane, Z. Xing, B.G. Raymond, and B.L. Thompson. 2015. Modeling land-based nitrogen loads from groundwater-dominated agricultural watersheds to estuaries to inform nutrient reduction planning. Journal of Hydrology 529: 213–230.

    Article  CAS  Google Scholar 

  • Jiang, Y., B. Zebarth, and J. Love. 2011. Long-term simulations of nitrate leaching from potato production systems in Prince Edward Island, Canada. Nutrient Cycling in Agroecosystems 91: 307–325.

    Article  CAS  Google Scholar 

  • Lotze, H.K., M. Coll, A.M. Magera, C. Ward-Paige, and L. Airoldi. 2011. Recovery of marine animal populations and ecosystems. Trends in Ecology & Evolution 29: 595–605.

    Article  Google Scholar 

  • Lotze, H.K., H.S. Lenihan, B.J. Bourque, R.H. Bradbury, R.G. Cooke, M.C. Kay, S.M. Kidwell, M.X. Kirby, C.H. Peterson, and J.B.C. Jackson. 2006. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312: 1806–1809.

    Article  CAS  Google Scholar 

  • Lotze, H.K., I. Milewski, B. Worm, and Z. Koller. 2003. Nutrient pollution: a eutrophication survey of eelgrass beds in estuaries and coastal bays in northern and eastern New Brunswick. Fredricton: Conservation Council of New Brunswick.

    Google Scholar 

  • Lotze, H.K., and B. Worm. 2002. Complex interactions of climatic and ecological controls on macroalgal recruitment. Limnology and Oceanography 47: 1734–1741.

    Article  Google Scholar 

  • Lubbers, L., W. Boynton, and W. Kemp. 1990. Variations in structure of estuarine fish communities in relation to abundance of submersed vascular plants. Marine Ecology Progress Series 65: 1–14.

    Article  Google Scholar 

  • Mapstone, B.D., and T. Ayling. 1998. An investigation of optimum methods and unit sizes for the visual estimation of abundances of some coral reef organisms. Townsville: Great Barrier Reef Marine Park Authority.

  • McCain, J.S.P., D.J. Cull, D.C. Schneider, and H.K. Lotze. 2015. Long-term shift in coastal fish communities before and after the collapse of Atlantic cod (Gadus morhua). ICES Journal of Marine Science: Journal du Conseil: fsv216.

  • McGlathery, K.J. 2001. Macroalgal blooms contribute to the decline of seagrass in nutrient enriched coastal waters. Journal of Phycology 37: 453–456.

    Article  Google Scholar 

  • McIver, R. 2015. Quantifying nitrogen loading and corresponding eutrophication symptoms in 7 bays in eastern New Brunswick, Canada. Canada: MSc, Dalhousie University Halifax, Nova Scotia.

    Google Scholar 

  • McIver, R., I. Milewski, and H.K. Lotze. 2015. Land use and nitrogen loading in seven estuaries along the southern Gulf of St. Lawrence, Canada. Estuarine, Coastal and Shelf Science 165: 137–148.

    Article  CAS  Google Scholar 

  • McSkimming, C., J.E. Tanner, B.D. Russell, and S.D. Connell. 2015. Compensation of nutrient pollution by herbivores in seagrass meadows. Journal of Experimental Marine Biology and Ecology 471: 112–118.

    Article  Google Scholar 

  • Millennium Ecosystem Assessment. 2005. Ecosystems and human well-being: general synthesis. Washington, DC: Island Press.

  • Moksnes, P.O., M. Gullstrom, K. Tryman, and S. Baden. 2008. Trophic cascades in a temperate seagrass community. Oikos 117: 763–777.

    Article  Google Scholar 

  • Norkko, J., E. Bonsdorff, and A. Norkko. 2000. Drifting algal mats as an alternative habitat for benthic invertebrates: species specific responses to a transient resource. Journal of Experimental Marine Biology and Ecology 248: 79–104.

    Article  CAS  Google Scholar 

  • Orav-Kotta, H., and J. Kotta. 2004. Food and habitat choice of the isopod Idotea baltica in the northeastern Baltic Sea. Hydrobiologia 514: 79–85.

    Article  Google Scholar 

  • Paerl, H.W. 2006. Assessing and managing nutrient-enhanced eutrophication in estuarine and coastal waters: interactive effects of human and climatic perturbations. Ecological Engineering 26: 40–54.

    Article  Google Scholar 

  • Pearson, T.H., and R. Rosenberg. 1978. Macrobenthic succession in relationto organic enrichment and pollution of the marine environment. Oceanography and Marine Biology: an Annual Review 16: 229–311.

    Google Scholar 

  • Pihl, L., S. Baden, and R. Diaz. 1991. Effects of periodic hypoxia on distribution of demersal fish and crustaceans. Marine Biology 108: 349–360.

    Article  Google Scholar 

  • Pihl, L., S. Baden, N. Kautsky, P. Rönnbäck, T. Söderqvist, Max Troell, and H. Wennhage. 2006. Shift in fish assemblage structure due to loss of seagrass Zostera marina habitats in Sweden. Estuarine, Coastal and Shelf Science 67: 123–132.

    Article  Google Scholar 

  • Pregnall, A.M., R.D. Smith, T.A. Kursar, and R.S. Alberte. 1984. Metabolic adaptation of Zostera marina (eelgrass) to diurnal periods of root anoxia. Marine Biology 83: 141–147.

    Article  CAS  Google Scholar 

  • Price, L.H., and J. Hylleberg. 1982. Algal-faunal interactions in a mat of Ulva fenestrata in False Bay, Washington. Ophelia 21: 75–88.

    Article  Google Scholar 

  • Raffaelli, D., J. Raven, and L. Poole. 1998. Ecological impact of green macroalgal blooms. Oceanography and Marine Biology: an Annual Review 36.

  • Reynolds, P.L., J.P. Richardson, and J.E. Duffy. 2014. Field experimental evidence that grazers mediate transition between microalgal and seagrass dominance. Limnology and Oceanography 59: 1053–1064.

    Article  Google Scholar 

  • Rosenberg, R., H.C. Nilsson, and R.J. Diaz. 2001. Response of benthic fauna and changing sediment redox profiles over a hypoxic gradient. Estuarine, Coastal and Shelf Science 53: 343–350.

    Article  CAS  Google Scholar 

  • Sagasti, A., L.C. Schaffner, and J.E. Duffy. 2001. Effects of periodic hypoxia on mortality, feeding and predation in an estuarine epifaunal community. Journal of Experimental Marine Biology and Ecology 258: 257–283.

    Article  CAS  Google Scholar 

  • Salovius, S., M. Nyqvist, and E. Bonsdorff. 2005. Life in the fast lane: macrobenthos use temporary drifting algal habitats. Journal of Sea Research 53: 169–180.

    Article  Google Scholar 

  • Schein, A. 2009. The estuarine fish community and food web structure in areas of sea lettuce (Ulva lactuca) and eelgrass (Zostera marina) within the Stanley River Estuary, Prince Edward Island. MSc dissertation, University of Prince Edward Island Charlottetown.

  • Schein, A., S.C. Courtenay, C.S. Crane, K.L. Teather, and M.R. van den Heuvel. 2012. The role of submerged aquatic vegetation in structuring the nearshore fish community within an estuary of the southern Gulf of St. Lawrence. Estuaries and Coasts, Online First.

  • Schmidt, A.L., M. Coll, T.N. Romanuk, and H.K. Lotze. 2011. Ecosystem structure and services in eelgrass Zostera marina and rockweed Ascophyllum nodosum habitats. Marine Ecology Progress Series 437: 51–68.

    Article  Google Scholar 

  • Schmidt, A.L., J.K.C. Wysmyk, S.E. Craig, and H.K. Lotze. 2012. Regional-scale effects of eutrophication on ecosystem structure and services of seagrass beds. Limnology and Oceanography.

  • Schneider, F., and K. Mann. 1991. Rapid recovery of fauna following simulated ice rafting in a Nova Scotian seagrass bed. Marine Ecology Progress Series 78.

  • Scott, W.B. and M.G. Scott. 1988. Atlanic fishes of Canada. Canadian Bulletin of Fisheries and Aquatic Science 219: 731.

  • Seymour, N.R., A.G. Miller, and D.J. Garbary. 2002. Decline of Canada geese (Branta canadensis) and common goldeneye (Bucephala clangula) associated with a collapse of eelgrass (Zostera marina) in a Nova Scotia estuary. Helgoland Marine Research 56: 198–202.

    Article  Google Scholar 

  • Sogard, S.M., and K.W. Able. 1991. A comparison of eelgrass, sea lettuce macroalgae, and marsh creeks as habitats for epibenthic fishes and decapods. Estuarine, Coastal and Shelf Science 33: 501–519.

    Article  Google Scholar 

  • Steel, J.B., and J.B. Wilson. 2003. Which is the phyte in epiphyte? Folia Geobotanica 38: 97–99.

    Article  Google Scholar 

  • Stehlik, L.L. 1993. Diets of the brachyuran crabs Cancer irroratus, C. borealis, and Ovalipes ocellatus in the New York Bight. Journal of Crustacean Biology 13: 723–735.

    Article  Google Scholar 

  • Swartz, R. 1978. Reproductive and molt cycles in the xanthid crab, Neopanope sayi (Smith, 1869). Crustaceana 34: 15–32.

  • Thormar, J., H. Hasler-Sheetal, S. Baden, C. Boström, K.K. Clausen, D. Krause-Jensen, B. Olesen, J.R. Rasmussen, C.J. Svensson, and M. Holmer. 2016. Eelgrass (Zostera marina) food web structure in different environmental settings. PloS One 11.

  • Tober, J.D., M.P.A. Griffin, and I. Valiela. 2000. Growth and abundance of Fundulus heteroclitus and Menidia menidia in estuaries of Waquoit Bay, Massachusetts exposed to different rates of nitrogen loading. Aquatic Ecology 34: 299–306.

    Article  CAS  Google Scholar 

  • Tupper, M., and R. Boutilier. 1995. Effects of habitat on settlement, growth, and postsettlement survival of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 52: 1834–1841.

    Article  Google Scholar 

  • Valiela, I., K. Foreman, M. LaMontagne, D. Hersh, J. Costa, P. Peckol, B. DeMeo-Andreson, C. D’Avanzo, M. Babione, and C.H. Sham. 1992. Couplings of watersheds and coastal waters: sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts. Estuaries and Coasts 15: 443–457.

    Article  CAS  Google Scholar 

  • Walker, D.I., G.A. Kendrick, and A.J. McComb. 2006. Decline and recovery of seagrass ecosystems—the dynamics of change. In Seagrasses: biology, ecology and conservation, ed. A.W.D. Larkum, R. Orth, and C.M. Duarte, 551–565. Dordrecht: Springer.

    Google Scholar 

  • Watson, D.C., and T.A. Norton. 1985. Dietary preferences of the common periwinkle, Littorina littorea (L.). Journal of Experimental Marine Biology and Ecology 88: 193–211.

    Article  Google Scholar 

  • Waycott, M., C.M. Duarte, T.J.B. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnik, A. Calladine, J.W. Fourqurean, K.L. Heck, and A.R. Hughes. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences 106: 12377–12381.

    Article  CAS  Google Scholar 

  • Wilcox, J.R., and H.P. Jeffries. 1974. Feeding habits of the sand shrimp Crangon septemspinosa. Biological Bulletin 146: 424–434.

    Article  Google Scholar 

  • Williams, G.A. 1996. Seasonal variation in a low shore Fucus serratus (Fucales, Phaeophyta) population and its epiphytic fauna. Hydrobiologia 326: 191–197.

    Article  Google Scholar 

  • Worm, B., and H.K. Lotze. 2006. Effects of eutrophication, grazing, and algal blooms on rocky shores. Limnology and Oceanography 51: 569–579.

    Article  Google Scholar 

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Acknowledgements

We thank A. Battersby, K. Varsava and Kouchibouguac National Park for field support, R. Scheibling for a critical review of the manuscript and D. Ibarra for intellectual and artistic input on Fig. 6. Our sincerest thanks to all those who hosted us or granted us access to our study sites in NB and PEI. This work was funded by a National Science and Engineering Research Council (NSERC) Discovery grant to HKL, a NSERC Post-Graduate Doctoral Scholarship and Killam Trust Predoctoral Scholarship to ALS, and postdoctoral fellowships from the Spanish Ministry of Science and Technology and the European Community Marie-Curie Program through the International Outgoing Fellowships to MC.

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  1. Department of Biology, Dalhousie University, 1355 Oxford Street, P.O. Box 15000, Halifax, NS, B3H4R2, Canada

    Allison L. Schmidt, Marta Coll & Heike K. Lotze

  2. Institut de Ciencies del Mar (ICM-CSIC), Passeig maritim de la Barceloneta, 37-49, 08003, Barcelona, Spain

    Marta Coll

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  1. Allison L. Schmidt
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Correspondence to Allison L. Schmidt.

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Communicated by Masahiro Nakaoka

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Table 5 Minimum length at maturity data for species observed in eelgrass beds in Atlantic Canada
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Schmidt, A.L., Coll, M. & Lotze, H.K. Regional-Scale Differences in Eutrophication Effects on Eelgrass-Associated (Zostera marina) Macrofauna. Estuaries and Coasts 40, 1096–1112 (2017). https://doi.org/10.1007/s12237-016-0204-z

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