Advertisement

Estuaries and Coasts

, Volume 41, Issue 1, pp 177–192 | Cite as

Large-Scale Differences in Community Structure and Ecosystem Services of Eelgrass (Zostera marina) Beds Across Three Regions in Eastern Canada

  • Mizuho Namba
  • Heike K. Lotze
  • Allison L. Schmidt
Article

Abstract

Eelgrass (Zostera marina) forms extensive beds in temperate coastal and estuarine environments worldwide and provides important ecosystem services, including habitat for a wide range of species as well as nutrient cycling and carbon storage. However, little is known about how eelgrass ecosystem structure and services differ naturally among regions. Using large-scale field surveys, we examined differences in eelgrass bed structure, carbon and nitrogen storage, community composition, and habitat services across three distinct regions in Eastern Canada. We focused on eelgrass beds with low anthropogenic impacts to compare natural differences. In addition, we analyzed the relationships of eelgrass bed structure with environmental conditions, and species composition with bed structure and environmental conditions, to elucidate potential drivers of observed differences. Our results indicate that regional differences in eelgrass bed structure were weakly correlated with water column properties, whereas differences in carbon and nitrogen storage were mainly driven by differences in eelgrass biomass. There were distinct regional differences in species composition and diversity, which were particularly linked to temperature, as well as eelgrass bed structure indicating differences in habitat provision. Our results highlight natural regional differences in ecosystem structure and services which could inform spatial management and conservation strategies for eelgrass beds.

Keywords

Eelgrass beds Ecosystem services Species composition Nutrient storage Coastal ecosystem 

Notes

Acknowledgements

We thank M. Coll, J. Wysmyk, A. Battersby, K. Varsava, J. Lindley, and AquaPrime Mussel Ranch for field support, M. Kienast for CN analysis, and D. Ibarra for support with water samples. Our thanks go to Kouchibouguac National Park, Taylor Head Provincial Park, Spry Bay Campground, all those who hosted us or granted us access to our study sites in Nova Scotia, New Brunswick, and Prince Edward Island, and the anonymous reviewers who have improved this manuscript. This work was funded by a National Science and Engineering Research Council (NSERC) Discovery grant to HKL, a NSERC Post Graduate Scholarship—Doctoral and Killam Trust Predoctoral Scholarship to ALS, and the Sarah Lawson Research Scholarship and the Gary Hicks Memorial Award to MN.

Supplementary material

12237_2017_271_MOESM1_ESM.pdf (276 kb)
ESM 1 (PDF 275 kb)

References

  1. Akoumianaki, I., and A. Nicolaidou. 2007. Spatial variability and dynamics of macrobenthos in a Mediterranean delta front area: The role of physical processes. Journal of Sea Research 57: 47–64. doi: 10.1016/j.seares.2006.07.003.CrossRefGoogle Scholar
  2. Anderson, M.J., R.N. Gorley, and K.R. Clarke. 2008. PERMANOVA+ for PRIMER: Guide to software and statistical methods. PRIMER-E Ltd.Google Scholar
  3. Arkema, K.K., G.M. Verutes, S.A. Wood, C. Clarke-Samuels, S. Rosado, M. Canto, A. Rosenthal, et al. 2015. Embedding ecosystem services in coastal planning leads to better outcomes for people and nature. Proceedings of the National Academy of Sciences of the United States of America 112: 7390–7395. doi: 10.1073/pnas.1406483112.CrossRefGoogle Scholar
  4. Barbier, E.B., S.D. Hacker, C. Kennedy, E.W. Koch, A.C. Stier, and B.R. Silliman. 2010. The value of estuarine and coastal ecosystem services. Ecological Monographs 81: 169–193. doi: 10.1890/10-1510.1.CrossRefGoogle Scholar
  5. Barrell, J., and J. Grant. 2013. Detecting hot and cold spots in a seagrass landscape using local indicators of spatial association. Landscape Ecology 28: 2005–2018. doi: 10.1007/s10980-013-9937-2.CrossRefGoogle Scholar
  6. Benson, J.L., D. Schlezinger, and B.L. Howes. 2013. Relationship between nitrogen concentration, light, and Zostera marina habitat quality and survival in southeastern Massachusetts estuaries. Journal of Environmental Management 131: 129–137. doi: 10.1016/j.jenvman.2013.09.033.CrossRefGoogle Scholar
  7. Bologna, P.A.X., and K.L. Heck. 2000. Impacts of seagrass habitat architecture on bivalve settlement. Estuaries 23: 449–457.CrossRefGoogle Scholar
  8. Borowitzka, M., P.S. Lavery, and M. van Keulen. 2006. Epiphytes of seagrasses. In Seagrasses: Biology, Ecology, and Conservation, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 441–461. Dordrecht, The Netherlands: Springer.Google Scholar
  9. Boström, C., and E. Bonsdorff. 1997. Community structure and spatial variation of benthic invertebrates associated with Zostera marina(L.) beds in the northern Baltic Sea. Journal of Sea Research 37: 153–166.CrossRefGoogle Scholar
  10. Brickman, D. 2014. Could ocean currents be responsible for the west to east spread of aquatic invasive species in Maritime Canadian waters? Marine Pollution Bulletin 85: 235–243. doi: 10.1016/j.marpolbul.2014.05.034.CrossRefGoogle Scholar
  11. Buck, C.M., F.P. Wilkerson, A.E. Parker, and R.C. Dugdale. 2014. The influence of coastal nutrients on phytoplankton productivity in a shallow low inflow estuary, Drakes Estero, California (USA). Estuaries and Coasts 37: 847–863. doi: 10.1007/s12237-013-9737-6.CrossRefGoogle Scholar
  12. Chavanich, S., and L.G. Harris. 2002. The influence of macroalgae on seasonal abundance and feeding preference of a subtidal snail, Lacuna vincta (Montagu) (Littorinidae) in the Gulf of Maine. Journal of Molluscan Studies 68: 73–78. doi: 10.1093/mollus/68.1.73.CrossRefGoogle Scholar
  13. Clarke, K.R., and M. Ainsworth. 1993. A method of linking multivariate community structure to environmental variables. Marine Ecology Progress Series 92: 205–219.CrossRefGoogle Scholar
  14. Clarke, K.R., and R.N. Gorley. 2006. Primer v6. 1. 6: user manual/tutorial. PRIMER-E Ltd.Google Scholar
  15. Clarke, K.R., and R.M. Warwick. 2001. Change in marine communities: An approach to statistical analysis and interpretation, 2nd ed. PRIMER-E Ltd.Google Scholar
  16. Costanza, R., R. D’Arge, R. de Groot, S. Farber, M. Grasso, B. Hannon, K. Limburg, et al. 1997. The value of the world’s ecosystem services and natural capital. Nature 387: 253–260. doi: 10.1038/387253a0.
  17. Cullain, N. 2014. Seasonality of Eelgrass (Zostera marina) and Associated Community in Nova Scotia, Canada. B.Sc.Hon. Thesis, Dalhousie University, Halifax, NS, unpublished.Google Scholar
  18. de Groot, R.S., M.A. Wilson, and R.M.J. Boumans. 2002. A typology for the classification, description and valuation of ecosystem functions, goods and services. Ecological Economics 41: 393–408. doi: 10.1016/S0921-8009(02)00089-7.CrossRefGoogle Scholar
  19. Duarte, C.M. 2002. The future of seagrass meadows. Environmental Conservation 29: 192–206. doi: 10.1017/S0376892902000127.CrossRefGoogle Scholar
  20. Duffy, J.E. 2006. Biodiversity and the functioning of seagrass ecosystems. Marine Ecology Progress Series 311: 233–250. doi: 10.3354/meps311233.CrossRefGoogle Scholar
  21. Filbee-Dexter, K., C.J. Feehan, and R.E. Scheibling. 2016. Large-scale degradation of a kelp ecosystem in an ocean warming hotspot. Marine Ecology Progress Series 543: 141–152. doi: 10.3354/meps11554.CrossRefGoogle Scholar
  22. Fisheries and Oceans Canada. 2009a. Does eelgrass (Zostera marina) meet the criteria as an ecologically significant species? Department of Fisheries and Oceans Canadian Science Advisory Secretariat Science Advisory Report 2009/018. Fisheries and Oceans Canada. 2009. The Role of the Provincial and Territorial Governments in the Oceanic Sector. Ottawa, ON.Google Scholar
  23. Fisheries and Oceans Canada. 2009b. The Role of the Provincial and Territorial Governments in the Oceanic Sector. Oceans Directorate, Fisheries and Oceans Canada, Ottawa, ON.Google Scholar
  24. Fourqurean, J.W., C.M. Duarte, H. Kennedy, N. Marbà, M. Holmer, M.A. Mateo, E.T. Apostolaki, et al. 2012. Seagrass ecosystems as a globally significant carbon stock. Nature Geoscience 5: 505–509. doi: 10.1038/ngeo1477.CrossRefGoogle Scholar
  25. Galbraith, P.S., D. Gilbert, R.G. Pettipas, and J. Chassé. 2008. Physical oceanographic conditions in the Gulf of St. Lawrence in 2007. Fisheries and Oceans Canada Canadian Science Advisory Secretariat Research Document 2008/001. Fisheries and Oceans Canada, Ottawa, ON.Google Scholar
  26. Garbary, D.J., A.G. Miller, J. Williams, and N.R. Seymour. 2014. Drastic decline of an extensive eelgrass bed in Nova Scotia due to the activity of the invasive green crab (Carcinus maenas). Marine Biology 161: 3–15. doi: 10.1007/s00227-013-2323-4.CrossRefGoogle Scholar
  27. Garbary, D.J., and J. Munro. 2004. Eelgrass decline: reality and causation. In Status and conservation of eelgrass (Zostera marina) in eastern Canada, ed. A.R. Hanson, 2004. Canadian Wildlife Service Technical Report. Sackville, New Brunswick, Canada.Google Scholar
  28. Greening, H., and A. Janicki. 2006. Toward reversal of eutrophic conditions in a subtropical estuary: Water quality and seagrass response to nitrogen loading reductions in Tampa Bay, Florida, USA. Environmental Management 38: 163–178. doi: 10.1007/s00267-005-0079-4.CrossRefGoogle Scholar
  29. Gregory, D., M. Petrie, F. Jordan, and P. Langille. 1993. Oceanographic, geographic and hydrological parameters of Scotia-Fundy and southern Gulf of St. Lawrence inlets. Canadian Technical Report of Hydrography and Ocean Sciences. Dartmouth, Nova Scotia.Google Scholar
  30. Greiner, J.T., K.J. McGlathery, J. Gunnell, and B.A. McKee. 2013. Seagrass restoration enhances “Blue Carbon” sequestration in coastal waters. PloS One 8: 1–1. doi: 10.1371/journal.pone.0072469.Google Scholar
  31. Grizard, P. 2013. Modeling Nitrate Loading from Watersheds to Coastal Waters of the Northumberland Strait. M.Sc.Eng. Thesis, University of New Brunswick, Fredericton, NB, unpublished.Google Scholar
  32. Halpern, B.S., S.E. Lester, and K.L. Mcleod. 2010. Placing marine protected areas onto the ecosystem- based management seascape. Proceedings of the National Academy of Sciences of the United States of America 107: 18312–18317. doi: 10.1073/pnas.0908503107.CrossRefGoogle Scholar
  33. Hemminga, M.A., N. Marba, and J. Stapel. 1999. Leaf nutrient resorption, leaf lifespan and the retention of nutrients in seagrass systems. Aquatic Botany 65: 141–158.CrossRefGoogle Scholar
  34. 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. doi: 10.4319/lo.2013.58.3.1103.CrossRefGoogle Scholar
  35. Huete-Ortega, M., T. Rodríguez-Ramos, D.C. López-Sandoval, P. Cermeño, J.M. Blanco, R.L. Palomino, J. Rodríguez, and E. Marañón. 2014. Distinct patterns in the size-scaling of abundance and metabolism in coastal and open-ocean phytoplankton communities. Marine Ecology Progress Series 515: 61–71. doi: 10.3354/meps11007.CrossRefGoogle Scholar
  36. Johnson, C.R., and K.H. Mann. 1986. The importance of plant defence abilities to the structure of subtidal seaweed comunities: The kelp Laminaria longicruris de la Pylaie survives grazing by the snail Lacuna vincta (Montagu) at high population densities. Journal of Experimental Marine Biology and Ecology 97: 231–267. doi: 10.1016/0022-0981(86)90244-3.CrossRefGoogle Scholar
  37. Joseph, V., A. Locke, and J.-G.J. Godin. 2006. Spatial distribution of fishes and decapods in eelgrass (Zostera marina L.) and sandy habitats of a New Brunswick estuary, eastern Canada. Aquatic Ecology 40: 111–123.CrossRefGoogle Scholar
  38. Kemp, W.M., R. Batleson, P. Bergstrom, V. Carter, C.L. Gallegos, W. Hunley, L. Karrh, et al. 2004. Habitat requirements for submerged aquatic vegetation in Chesapeake Bay: Water quality, light regime, and physical-chemical factors. Estuaries 27: 363–377. doi: 10.1007/BF02803529.CrossRefGoogle Scholar
  39. Krumhansl, K.A., and R.E. Scheibling. 2011. Spatial and temporal variation in grazing damage by the gastropod Lacuna vincta in Nova Scotian kelp beds. Aquatic Biology 13: 163–173. doi: 10.3354/ab00366.CrossRefGoogle Scholar
  40. Kuk-Dzul, J.G., G. Gold-Bouchot, and P.-L. Ardisson. 2012. Benthic infauna variability in relation to environmental factors and organic pollutants in tropical coastal lagoons from the northern Yucatan Peninsula. Marine Pollution Bulletin 64: 2725–2733. doi: 10.1016/j.marpolbul.2012.09.022.CrossRefGoogle Scholar
  41. Larkum, A.W.D., E.A. Drew, and P.J. Ralph. 2006. Photosynthesis and metabolism in seagrasses at the cellular level. In Seagrasses: Biology, Ecology, and Conservation, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 323–345. Dordrecht, The Netherlands: Springer.Google Scholar
  42. Le Bris, A., A. Fréchet, P.S. Galbraith, and J.S. Wroblewski. 2013. Evidence for alternative migratory behaviours in the northern Gulf of St Lawrence population of Atlantic cod (Gadus morhua L.). ICES Journal of Marine Science: Journal du Conseil 70: 793–804. doi: 10.1093/icesjms/fst068.CrossRefGoogle Scholar
  43. Lee, K.S., and K.H. Dunton. 1996. Production and carbon reserve dynamics of the seagrass Thalassia testudinum in Corpus Christi Bay, Texas, USA. Marine Ecology Progress Series 143: 201–210. doi: 10.3354/meps143201.CrossRefGoogle Scholar
  44. Lee, K.S., F.T. Short, and D.M. Burdick. 2004. Development of a nutrient pollution indicator using the seagrass, Zostera marina, along nutrient gradients in three New England estuaries. Aquatic Botany 78: 197–216. doi: 10.1016/j.aquabot.2003.09.010.CrossRefGoogle Scholar
  45. Lemmens, J.W.T.J., G. Clapin, P. Lavery, and J. Cary. 1996. Filtering capacity of seagrass meadows and other habitats of Cockburn Sound, Western Australia. Marine Ecology Progress Series 143: 187–200. doi: 10.3354/meps143187.CrossRefGoogle Scholar
  46. 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 26: 595–605. doi: 10.1016/j.tree.2011.07.008.CrossRefGoogle Scholar
  47. Macreadie, P.I., M.E. Baird, S.M. Trevathan-Tackett, A.W.D. Larkum, and P.J. Ralph. 2014. Quantifying and modelling the carbon sequestration capacity of seagrass meadows—a critical assessment. Marine Pollution Bulletin 83: 430–439.CrossRefGoogle Scholar
  48. Malyshev, A., and P.A. Quijón. 2011. Disruption of essential habitat by a coastal invader: new evidence of the effects of green crabs on eelgrass beds. ICES Journal of Marine Science / Journal du Conseil 68: 1852–1856.CrossRefGoogle Scholar
  49. Mapstone, B.D., and A.M. Ayling. 1998. An investigation of optimum methods and unit sizes for the visual estimation of abundances of some coral reef organisms. Great Barrier Reef Marine Park Authority. Research Publication 47, Townsville, Queensland.Google Scholar
  50. Mcdonald, A.M., P. Prado, K.L. Heck, J.W. Fourqurean, T.A. Frankovich, K.H. Dunton, and J. Cebrian. 2016. Seagrass growth, reproductive, and morphological plasticity across environmental gradients over a large spatial scale. Aquatic Botany 134: 87–96. doi: 10.1016/j.aquabot.2016.07.007.CrossRefGoogle Scholar
  51. McIver, R., I. Milewsky, 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.CrossRefGoogle Scholar
  52. McMahon, R.F., and W.D. Russell-Hunter. 1977. Temperature relations of aerial and aquatic respiration in six littoral snails in relation to their vertical zonation. The Biological Bulletin 152: 182–198. doi: 10.2307/1540558.CrossRefGoogle Scholar
  53. Mills, V.S., and K. Berkenbusch. 2009. Seagrass (Zostera muelleri) patch size and spatial location influence infaunal macroinvertebrate assemblages. Estuarine, Coastal and Shelf Science 81: 123–129. doi: 10.1016/j.ecss.2008.10.005.CrossRefGoogle Scholar
  54. Mitchell, S. 2000. St. Georges Bay Ecosystem Project (GBEP): Research Report Ill: A Review of Benthic Fauna/Community Studies in Atlantic Canada and Northeastem American Shallow Waters. Antigonish; NS.Google Scholar
  55. Nagelkerken, I., M. Dorenbosch, W.C.E.P. Verberk, E. Cocheret de la Morinire, and G. van der Velde. 2000. Day-night shifts of fishes between shallow-water biotopes of a Caribbean bay, with emphasis on the nocturnal feeding of Haemulidae and Lutjanidae. Marine Ecology Progress Series 194: 55–64. doi: 10.3354/meps194055.CrossRefGoogle Scholar
  56. Nordlund, L.M., E.W. Koch, E.B. Barbier, and J.C. Creed. 2017. Correction: Seagrass ecosystem services and their variability across genera and geographical regions. PloS One 12: e0169942. doi: 10.1371/journal.pone.0169942.CrossRefGoogle Scholar
  57. O’Neill, J.D., M. Costa, and T. Sharma. 2011. Remote sensing of shallow coastal benthic substrates: In situ spectra and mapping of eelgrass (Zostera marina) in the Gulf Islands National Park Reserve of Canada. Remote Sensing 3: 975–1005. doi: 10.3390/rs3050975.CrossRefGoogle Scholar
  58. Olesen, B. 1996. Regulation of light attenuation and eelgrass Zostera marina depth distribution in a Danish embayment. Marine Ecology Progress Series 134: 187–194. doi: 10.3354/meps134187.CrossRefGoogle Scholar
  59. Ondiviela, B., I.J. Losada, J.L. Lara, M. Maza, C. Galván, T.J. Bouma, and J. van Belzen. 2014. The role of seagrasses in coastal protection in a changing climate. Coastal Engineering 87: 158–168.CrossRefGoogle Scholar
  60. Orth, R.J., T.J.B. Carruthers, W.C. Dennison, C.M. Duarte, J.W. Fourqurean, K.L. Heck Jr., A.R. Hughes, et al. 2006. A global crisis for seagrass ecosystems. Bioscience 56: 987–996.CrossRefGoogle Scholar
  61. Petrie, B., R.G. Pettipas, W.M. Petrie, and V.V. Soukhovtsev. 2008. Scientific Council Meeting June 2008. Serial No. N5505. Northwest Atlantic Fisheries Organization, Department of Fisheries and Oceans, Dartmouth, NS.Google Scholar
  62. R Core Team 2014. R: A language and environment for statistical computing. Vienna.Q.Google Scholar
  63. Richaud, B., Y.-O. Kwon, T.M. Joyce, P.S. Fratantoni, and S.J. Lentz. 2016. Surface and bottom temperature and salinity climatology along the continental shelf off the Canadian and U.S. East Coasts. Continental Shelf Research 124: 165–181. doi: 10.1016/j.csr.2016.06.005.CrossRefGoogle Scholar
  64. Righton, D., K.H. Andersen, F. Neat, V. Thorsteinsson, P. Steingrund, H. Svedäng, K. Michalsen, et al. 2010. Thermal niche of Atlantic cod Gadus morhua: limits, tolerance and optima. Marine Ecology Progress Series 420: 1–13.CrossRefGoogle Scholar
  65. Saunders, M., and A. Metaxas. 2007. Temperature explains settlement patterns of the introduced bryozoan Membranipora membranacea in Nova Scotia, Canada. Marine Ecology Progress Series 344: 95–106. doi: 10.3354/meps06924.CrossRefGoogle Scholar
  66. Saunders, M.I., J. Leon, S.R. Phinn, D.P. Callaghan, K.R. O’Brien, C.M. Roelfsema, C.E. Lovelock, M.B. Lyons, and P.J. Mumby. 2013. Coastal retreat and improved water quality mitigate losses of seagrass from sea level rise. Global Change Biology 19: 2569–2583.CrossRefGoogle Scholar
  67. Saunders, M.I., E. Bayraktarov, C.M. Roelfsema, J.X. Leon, J. Samper-Villarreal, S.R. Phinn, C.E. Lovelock, and P.J. Mumby. 2015. Spatial and temporal variability of seagrass at Lizard Island, Great Barrier Reef. Botanica Marina 58: 35–49. doi: 10.1515/bot-2014-0060.CrossRefGoogle Scholar
  68. Schmidt, A.L., M. Coll, and H.K. Lotze. 2017. Regional-scale differences in eutrophication effects on eelgrass-associated (Zostera marina) macrofauna. Estuaries and Coasts: 1–17. doi:DOI  10.1007/s12237-016-0204-z.
  69. 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. doi: 10.3354/meps09276.CrossRefGoogle Scholar
  70. Schmidt, A.L., and R.E. Scheibling. 2007. Effects of native and invasive macroalgal canopies on composition and abundance of mobile benthic macrofauna and turf-forming algae. Journal of Experimental Marine Biology and Ecology 341: 110–130. doi: 10.1016/j.jembe.2006.10.003.CrossRefGoogle Scholar
  71. 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 57: 1389.CrossRefGoogle Scholar
  72. Schückel, U., M. Beck, and I. Kröncke. 2013. Spatial variability in structural and functional aspects of macrofauna communities and their environmental parameters in the Jade Bay (Wadden Sea Lower Saxony, southern North Sea). Helgoland Marine Research 67: 121–136. doi: 10.1007/s10152-012-0309-0.CrossRefGoogle Scholar
  73. Scrosati, R., and C. Heaven. 2007. Spatial trends in community richness, diversity, and evenness across rocky intertidal environmental stress gradients in eastern Canada. Marine Ecology Progress Series 342: 1–14.CrossRefGoogle Scholar
  74. Seitz, R.D., H. Wennhage, U. Bergström, R.N. Lipcius, and T. Ysebaert. 2014. Ecological value of coastal habitats for commercially and ecologically important species. ICES Journal of Marine Science: Journal du Conseil 71: 648–665. doi: 10.1093/icesjms/fst152.CrossRefGoogle Scholar
  75. Short, F.T., D.M. Burdick, and J.E.K. Kaldy III. 1995. Mesocosme experiments quantify the effects of eutrophication on eelgrass, Zostera marina. Limnology and Oceanography 40: 740–749.CrossRefGoogle Scholar
  76. Short, F.T., and H.A. Neckles. 1999. The effects of global climate change on seagrasses. Aquatic Botany 63: 169–196. doi: 10.1016/S0304-3770(98)00117-X.CrossRefGoogle Scholar
  77. Skinner, M.A., S.C. Courtenay, and C.W. McKindsey. 2013. Reductions in distribution, photosynthesis, and productivity of eelgrass Zostera marina associated with oyster Crassostrea virginica aquaculture. Marine Ecology Progress Series 486: 105–119. doi: 10.3354/meps10345.CrossRefGoogle Scholar
  78. Sogard, S.M., and K.W. Able. 1994. Diel variation in immigration of fishes and decapod crustaceans to artificial seagrass habitat. Estuaries 17: 622–630.CrossRefGoogle Scholar
  79. Sokolova, M., and O. Pörtner. 2001. Temperature effects on key metabolic enzymes in Littorina saxatilis and L. obtusata from different latitudes and shore levels. Marine Biology 139: 113–126. doi: 10.1007/s002270100557.CrossRefGoogle Scholar
  80. Somero, G.N. 2002. Thermal physiology and vertical zonation of intertidal animals : Optima, limits, and costs of living. Integrative and Comparative Biology 42: 780–789. doi: 10.1093/icb/42.4.780.CrossRefGoogle Scholar
  81. Spalding, M.D., H.E. Fox, G.R. Allen, N. Davidson, Z.A. Ferdaña, M. Finlayson, B.S. Halpern, et al. 2007. Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. Bioscience 57: 573–583. doi: 10.1641/B570707.CrossRefGoogle Scholar
  82. Strickland, J.D.H., and T.R. Parsons. 1972. A Practical Handbook of Seawater Analysis. Fisheries Research Board of Canada, Ottawa. Second Edi. Ottawa, ON.Google Scholar
  83. Thom, R.M., A.B. Borde, S. Rumrill, D.L. Woodruff, G.D. Williams, J.A. Southard, and S.L. Sargeant. 2003. Factors influencing spatial and annual variability in eelgrass (Zostera marina L.) meadows in Willapa Bay, Washington, and Coos Bay, Oregon. Estuaries 26: 1117–1129. doi: 10.1007/BF02803368.CrossRefGoogle Scholar
  84. Urra, J., Á. Mateo Ramírez, P. Marina, C. Salas, S. Gofas, and J.L. Rueda. 2013. Highly diverse molluscan assemblages of Posidonia oceanica meadows in northwestern Alboran Sea (W Mediterranean): Seasonal dynamics and environmental drivers. Estuarine, Coastal and Shelf Science 117: 136–147. doi: 10.1016/j.ecss.2012.11.005.CrossRefGoogle Scholar
  85. Ushakova, O.O. 2003. Combined effect of salinity and temperature on Spirorbis spirorbis L. and Circeus spirillum L. larvae from the White Sea. Journal of Experimental Marine Biology and Ecology 296: 23–33. doi: 10.1016/S0022-0981(03)00301-0.CrossRefGoogle Scholar
  86. Vadrucci, M.R., F. Vignes, A. Fiocca, A. Basset, I. Santarpia, G.C. Carrada, M. Cabrini, and S.F. Umani. 2003. Space–time patterns of co-variation of biodiversity and primary production in phytoplankton guilds of coastal marine environments. Aquatic Conservation: Marine and Freshwater Ecosystems 13: 489–506. doi: 10.1002/aqc.590.CrossRefGoogle Scholar
  87. Waycott, M., C.M. Duarte, T.J.B. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnik, A. Calladine, et al. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences 106: 12377–12381. doi: 10.1073/pnas.0905620106.CrossRefGoogle Scholar
  88. Webster, P.J., A.A. Rowden, and M.J. Attrill. 1998. Effect of shoot density on the infaunal macro-invertebrate community within a Zostera marina seagrass bed. Estuarine, Coastal and Shelf Science 47: 351–357.CrossRefGoogle Scholar
  89. Welschmeyer, N.A. 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnology and Oceanography 39: 1985–1992.CrossRefGoogle Scholar
  90. Worm, B., E.B. Barbier, N. Beaumont, J.E. Duffy, C. Folke, B.S. Halpern, J.B.C. Jackson, et al. 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314: 787–790. doi: 10.1126/science.1132294.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  1. 1.Department of BiologyDalhousie UniversityHalifaxCanada
  2. 2.Akkeshi Marine Station, Field Science Center for Northern BiosphereHokkaido UniversityAkkeshiJapan

Personalised recommendations