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Estuaries and Coasts

, Volume 41, Issue 5, pp 1223–1233 | Cite as

Marine Macrophyte Detritus and Degradation: the Role of Intraspecific Genetic Variation

  • Susan L. Williams
  • Jessica M. Abbott
  • Laura K. Reynolds
  • John J. Stachowicz
Article

Abstract

Intraspecific genetic diversity influences the primary production and biomass of coastal marine foundation plants. The majority of their primary production ends up as detritus, yet the relationship between their intraspecific genetic diversity and detritus-based functions has rarely been considered. We addressed the relationship between these functions (detritus standing stock, degradation, sediment ammonium production) and genotypic diversity (richness, evenness, relatedness) in eelgrass (Zostera marina L.), a widely distributed coastal foundation plant, grown in the field at different levels of genotypic richness and relatedness. The functions were largely insensitive to the genotypic diversity, density, and biomass of the living plants in a plot, which suggests that changes in eelgrass genotypic diversity have minimal effects on these important functions and their consequences ranging from trophic support to carbon sequestration. Instead, detritus-based functions are perhaps more related to the sediment environment, the genotypic composition of the detritus itself, and macro- and microscopic detritus consumers.

Keywords

Ammonification Detritus Decomposition Eelgrass Genotypes Marine macrophyte 

Notes

Acknowledgments

Genotyping was carried out in the laboratory of R.K. Grosberg. We thank the following for field and laboratory assistance: J. Blaze, B. Cameron, K. Chan, J. Chow, K. DuBois, N. Kollars, K. Griffith, E. Huynh, M. Luerig, N. Nichols, J. Toy, and A. R. Hughes. We thank N. Marbà, R. Howarth, A.R. Hughes, and anonymous reviewers for helpful comments.

Funding Information

This research was supported by NSF grant OCE-12-34345 to J.J.S., R.K. Grosberg, and S.L.W. and an IGERT Reach fellowship (DGE #0801430) to J.M.A.

Supplementary material

12237_2017_360_MOESM1_ESM.docx (96 kb)
ESM 1 (DOCX 96 kb)

References

  1. Abbott, J.M., and J.J. Stachowicz. 2016. The relative importance of trait vs. genetic differentiation for the outcome of interactions among plant genotypes. Ecology 97 (1): 84–94.  https://doi.org/10.1890/15-0148.1.CrossRefGoogle Scholar
  2. Abbott, J.M., R.K. Grosberg, S.L. Williams, and J.J. Stachowicz. 2017. Multiple dimensions of intraspecific diversity affect biomass of eelgrass and its associated community. Ecology 98 (12): 3152–3164.  https://doi.org/10.1002/ecy.2037.CrossRefGoogle Scholar
  3. Bailey, J.K., J.A. Schweitzer, F. Úbeda, J. Koricheva, C.J. LeRoy, M.D. Madritch, B.J. Rehill, R.K. Bangert, D.G. Fishcher, G.J. Allan, and T.G. Whitham. 2009. From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization. Philosophical Transactions of the Royal Society B 364 (1523): 1607–1616.  https://doi.org/10.1098/rstb.2008.0336.CrossRefGoogle Scholar
  4. Banta, G.T., M.F. Pedersen, and S.L. Nielsen. 2004. Decomposition of marine primary producers: consequences for nutrient recycling and retention in coastal ecosystems. In Estuarine nutrient cycling: the influence of primary producers, ed. S.L. Laurentius Nielsen, G.T. Banta, and M.F. Pedersen, 187–216. Sunderland: Kluwer Academic Publishers.Google Scholar
  5. Blum, L.K., and A.L. Mills. 1991. Microbial growth and activity during the initial stages of seagrass decomposition. Marine Ecology Progress Series 70: 73–82.  https://doi.org/10.3354/meps070073.CrossRefGoogle Scholar
  6. Caffrey, J.M. 1995. Spatial and seasonal patterns in sediment nitrogen remineralization and ammonium concentrations in San Francisco Bay, California. Estuaries 18 (1): 219–233.  https://doi.org/10.2307/1352632.CrossRefGoogle Scholar
  7. Caffrey, J.M., and W.M. Kemp. 1990. Nitrogen cycling in sediments with estuarine populations of Potamogeton perfoliatus and Zostera marina. Marine Ecology Progress Series 66: 147–160.  https://doi.org/10.3354/meps066147.CrossRefGoogle Scholar
  8. Canuel, E.A., A.C. Spivak, E.J. Waterson, and J.E. Duffy. 2007. Biodiversity and food web structure influences short-term accumulation of sediment organic matter in an experimental seagrass system. Limnology and Oceanography 52 (2): 590–602.  https://doi.org/10.4319/lo.2007.52.2.0590.CrossRefGoogle Scholar
  9. Cebrián, J. 2004. Role of first-order consumers in ecosystem carbon flow. Ecology Letters 7 (3): 232–240.  https://doi.org/10.1111/j.1461-0248.2004.00574.x.CrossRefGoogle Scholar
  10. Cebrián, J., and J. Lartique. 2004. Patterns of herbivory and decomposition in aquatic and terrestrial ecosystems. Ecological Monographs 74 (2): 237–259.  https://doi.org/10.1890/03-4019.CrossRefGoogle Scholar
  11. Crutsinger, G.M., S.M. Rudman, M.A. Rodriquez-Cabal, A.D. McKown, T. Sato, A.M. MacDonald, J. Heavyside, A. Geraldes, E.M. Hart, C.J. LeRoy, and R.W. El-Sabaawi. 2014. Testing a ‘genes-to ecosystems’ approach to understanding aquatic-terrestrial linkages. Molecular Ecology 23 (23): 5888–5903.  https://doi.org/10.1111/mec.12931.CrossRefGoogle Scholar
  12. Cúcio, C., A.H. Engelen, R. Costa, and G. Muyzer. 2016. Rhizosphere microbiomass of European seagrasses are selected by the plant, but are not species specific. Frontiers in Microbiology 7.  https://doi.org/10.3389/fmicb.2016.00440.
  13. Danovaro, E. 1996. Detritus-bacteria-meiofauna interactions in a seagrass bed (Posidonia oceanica) of the NW Medterranean. Marine Biology 127 (1): 1–13.  https://doi.org/10.1007/BF00993638.CrossRefGoogle Scholar
  14. Danovaro, R., and C. Gambi. 2002. Biodiversity and trophic structure of nematode assemblages in seagrass systems: evidence for a coupling with changes in food availability. Marine Biology 141: 667–677.CrossRefGoogle Scholar
  15. Danovaro, R., M. Fabiano, and M. Boyer. 1994. Seasonal changes of benthic bacteria in a seagrass bed (Posidonia oceanica) of the Ligurian Sea in relation to origin, composition and fate of the sediment organic matter. Marine Biology 119 (4): 489–500.  https://doi.org/10.1007/BF00354310.CrossRefGoogle Scholar
  16. Dennison, W.C., R.C. Aller, and R.S. Alberte. 1987. Sediment ammonium availability and eelgrass (Zostera marina) growth. Marine Biology 94 (3): 469–477.  https://doi.org/10.1007/BF00428254.CrossRefGoogle Scholar
  17. Duarte, C.M., and J. Cebrián. 1986. The fate of marine autotrophic production. Limnology and Oceanography 41: 1758–1766.CrossRefGoogle Scholar
  18. Duarte, C.M., and D. Krause-Jensen. 2017. Export from seagrass meadows contributes to marine carbon sequestration. Frontiers in Marine Science 17.  https://doi.org/10.3389/fmars.2017.00013.
  19. Duarte, C.M., H. Kennedy, N. Marbà, and I. Hendriks. 2013. The capacity of seagrass meadows for carbon burial: current limitations and future strategies. Ocean and Coastal Management 83: 32–38.  https://doi.org/10.1016/j.ocecoaman.2011.09.001.CrossRefGoogle Scholar
  20. Duffy, J.E., J.P. Richardson, and E.A. Canuel. 2003. Grazer diversity effects on ecosystem functioning in seagrass beds. Ecology Letters 6 (7): 637–645.  https://doi.org/10.1046/j.1461-0248.2003.00474.x.CrossRefGoogle Scholar
  21. Duffy, J.E., J.P. Richardson, and K.E. France. 2005. Ecosystem consequences of diversity depend on food chain length in estuarine vegetation. Ecology Letters 8 (3): 301–309.  https://doi.org/10.1111/j.1461-0248.2005.00725.x.CrossRefGoogle Scholar
  22. Duffy, J.E., B.J. Cardinale, K.E. France, P.B. McIntyre, E. Thebault, and M. Loreau. 2007. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecology Letters 10 (6): 522–538.  https://doi.org/10.1111/j.1461-0248.2007.01037.x.CrossRefGoogle Scholar
  23. Duffy, J.E., A.R. Hughes, and P.-O. Moksnes. 2014. Ecology of seagrass communities. In Marine community ecology and conservation, ed. M.D. Bertness, J.F. Bruno, B.R. Silliman, and J.J. Stachowicz, 271–298. Sunderland: Sinauer Associates, Incorporated.Google Scholar
  24. Duffy, E.J., P.L. Reynolds, C. Boström, J.A. Coyer, M. Cusson, S. Donadi, J.G. Douglass, J.S. Eklöf, A.H. Engelen, B.K. Eriksson, S. Fredriksen, L. Gamfeldt, C. Gustafsoon, G. Hoarau, M. Hori, K. Hovel, K. Iken, J.S. Lefcheck, P.-O. Moksnes, M. Nakaoka, M.I. O'connor, J.L. Olsen, J.P. Richardson, J.L. Ruesink, E.E. Sotka, J. Thormar, M.A. Whalen, and J.J. Stachowicz. 2015. Biodiversity mediates top-down control in eelgrass ecosystems: a global comparative-experimental approach. Ecology Letters 18 (7): 696–705.  https://doi.org/10.1111/ele.12448.CrossRefGoogle Scholar
  25. Enriquez, S., C.M. Duarte, and K. Sand-Jensen. 1993. Patterns in decomposition rates among photosynthetic organisms. Oecologia 94 (4): 457–471.  https://doi.org/10.1007/BF00566960.CrossRefGoogle Scholar
  26. Ettinger, C.L., S.E. Voerman, J.M. Lang, J.J. Stachowicz, and J.A. Eisen. 2017a. Microbial communities in sediment from Zostera marina patches, but not the Z. marina leaf or root microbiomes, vary in relation to distance from patch edge. PeerJ 5: e3246.  https://doi.org/10.7717/peerj.3246.CrossRefGoogle Scholar
  27. Ettinger, C.L., S.L. Williams, J.A. Abbott, J.J. Stachowicz, and J.A. Eisen. 2017b. Microbiome succession during ammonification in eelgrass bed sediments. PeerJ 5: e3674.  https://doi.org/10.7717/peerj.3674.CrossRefGoogle Scholar
  28. Evans, S.M., E.A. Sinclair, A.G.B. Poore, P.D. Steinberg, G.A. Kendrick, and A. Vergés. 2014. Genetic diversity in threatend Posidonia australis seagrass meadows. Conservation Genetics 15: 517–728.CrossRefGoogle Scholar
  29. Fahimipour, A.K., M.R. Kardish, J.M. Long, J.L. Green, J.A. Eisen, and J.J. Stachowicz. 2017. Global-scale structure of the eelgrass microbiome. Applied and Environmental Microbiology 83: e03391–e03316.CrossRefGoogle Scholar
  30. Fischer, D.G., G.M. Wimp, E. Hersch-Green, R.K. Bangert, C.J. LeRoy, J.K. Bailey, J.A. Schweitzer, C. Dirks, S.C. Hart, G.J. Allan, and T.G. Whitham. 2017. Tree genetics strongly affect forest productivity, but intraspecific diversity–productivity relationships do not. Functional Ecology 31 (2): 520–529.  https://doi.org/10.1111/1365-2435.12733.CrossRefGoogle Scholar
  31. Fonseca, M.S., and M.A.R. Koehl. 2006. Flow in seagrass canopies: the influence of patch width. Estuarine, Coastal and Shelf Science 67 (1-2): 1–9.  https://doi.org/10.1016/j.ecss.2005.09.018.CrossRefGoogle Scholar
  32. Fourqurean, J.W., C.M. Duarte, H. Kennedy, N. Marbà, M. Holmer, M.A. Mateo, E.T. Apostolaki, G.A. Kendrick, D. Krause-Jensen, K.J. McGlathery, and O. Serrano. 2012. Seagrass ecosystem as a globally significant carbon stock. Nature Geoscience 5 (7): 505–509.  https://doi.org/10.1038/NGEO1477.CrossRefGoogle Scholar
  33. Fraser, T.R. 2008. STORM: software for testing hypotheses of relatedness and mating patterns. Molecular Ecology Resources 8 (6): 1263–1266.  https://doi.org/10.1111/j.1755-0998.2008.02358.x.CrossRefGoogle Scholar
  34. Gamfeldt, L., J.S. Lefcheck, J.E.K. Byrnes, B.J. Cardinale, J.E. Duffy, and J.N. Griffin. 2015. Marine biodiversity and ecosystem functioning: what’s known and what’s next? Oikos 124 (3): 252–265.  https://doi.org/10.1111/oik.01549.CrossRefGoogle Scholar
  35. Gessner, M.O., C.M. Swan, C.K. Dang, B.G. McKie, R.D. Bardgett, D.H. Wall, and S. Hättenschwiler. 2010. Diversity meets decomposition. Trends in Ecology & Evolution 25 (6): 372–380.  https://doi.org/10.1016/j.tree.2010.01.010.CrossRefGoogle Scholar
  36. Godshalk, G.L., and R.G. Wetzel. 1978. Decomposition of aquatic angiosperms. III. Zostera marina L. and a conceptual model of decomposition. Aquatic Botany 5: 329–354.  https://doi.org/10.1016/0304-3770(78)90075-X.CrossRefGoogle Scholar
  37. Hättenschwiler, A., A.V. Tiunov, and S. Scheu. 2005. Biodiversity and litter decomposition in terrestrial ecosystems. Annual Review of Ecology, Evolution, and Systematics 36 (1): 191–218.  https://doi.org/10.1146/annurev.ecolsys.36.112904.151932.CrossRefGoogle Scholar
  38. Heck, K.L., Jr., T.J.B. Carruthers, C.M. Duarte, A.R. Hughes, G. Kendrick, R.J. Orth, and S. Williams. 2008. Trophic transfers from seagrass meadows subsidize diverse marine and terrestrial consumers. Ecosystems 11 (7): 1198–1210.  https://doi.org/10.1007/s10021-008-9155-y.CrossRefGoogle Scholar
  39. Hemminga, M.A., B.P. Koutstall, J. van Soelen, and A.G.A. Merks. 1994. The nitrogen supply to intertidal eelgrass (Zostera marina). Marine Biology 118 (2): 223–227.  https://doi.org/10.1007/BF00349788.CrossRefGoogle Scholar
  40. Hensel, M.J.S., and B.R. Silliman. 2013. Consumer diversity across kingdoms supports multiple functions in a coastal ecosystem. Proceedings of the National Academy of Sciences 110 (51): 20621–20626.  https://doi.org/10.1073/pnas.1312317110.CrossRefGoogle Scholar
  41. Hughes, A.R. 2014. Genetic diversity and trait variance interact to affect plant performance. Journal of Ecology 102 (3): 651–658.  https://doi.org/10.1111/1365-2745.12244.CrossRefGoogle Scholar
  42. Hughes, A.R., and J.J. Stachowicz. 2004. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proceedings of the National Academy of Sciences of the United States of America 101 (24): 8998–9002.  https://doi.org/10.1073/pnas.0402642101.CrossRefGoogle Scholar
  43. Hughes, A.R., and J.J. Stachowicz. 2009. Ecological impacts of genotypic diversity in the clonal seagrass Zostera marina. Ecology 90 (5): 1412–1419.  https://doi.org/10.1890/07-2030.1.CrossRefGoogle Scholar
  44. Hughes, A.R., and J.J. Stachowicz. 2011. Seagrass genotypic diversity increases disturbance response via complementarity and dominance. Journal of Ecology 99: 445–453.Google Scholar
  45. Hughes, A.R., B.D. Inouye, M.T.J. Johnson, N. Underwood, and M. Vellend. 2008. Ecological consequences of genetic diversity. Ecology Letters 11 (6): 609–623.  https://doi.org/10.1111/j.1461-0248.2008.01179.x.CrossRefGoogle Scholar
  46. Hughes, A.R., J.J. Stachowicz, and S.L. Williams. 2009. Morphological and physiological variation among seagrass (Zostera marina) genotypes. Oecologia 159 (4): 725–733.  https://doi.org/10.1007/s00442-008-1251-3.CrossRefGoogle Scholar
  47. Hughes, A.R., R.J. Best, and J.J. Stachowicz. 2010. Genotypic diversity and grazer identity interactively influence seagrass and grazer biomass. Marine Ecology Progress Series 403: 43–51.  https://doi.org/10.3354/meps08506.CrossRefGoogle Scholar
  48. Hyndes, G.A., I. Nagelkerken, R.J. McLeod, R.M. Connolly, P.S. Lavery, and M.A. Vanderklift. 2014. Mechanisms and ecological role of carbon transfer within coastal seascapes. Biological Reviews 89 (1): 232–254.  https://doi.org/10.1111/brv.12055.CrossRefGoogle Scholar
  49. Iizumi, H., A. Hattori, and C.P. McRoy. 1980. Nitrate and nitrite in the interstitial waters of eelgrass beds, in relation to the rhizosphere. Journal of Experimental Marine Biology and Ecology 47 (2): 191–201.  https://doi.org/10.1016/0022-0981(80)90112-4.CrossRefGoogle Scholar
  50. Josselyn, M.N., and A.C. Mathieson. 1980. Seasonal influx and decomposition of autochthonous macrophyte litter in a north temperate estuary. Hydrobiologia 71: 197–208.Google Scholar
  51. Kamel, S., A.R. Hughes, R. Grosberg, and J.J. Stachowicz. 2012. Fine-scale genetic structure and relatedness in the eelgrass Zostera marina. Marine Ecology Progress Series 447: 127–137.  https://doi.org/10.3354/meps09447.CrossRefGoogle Scholar
  52. Koch, E.W., J.D. Ackerman, J. Verduin, and M. van Keulen. 2006. Fluid dynamics in seagrass ecology—from molecules to ecosystems. In Seagrasses: biology, ecology and conservation, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 193–225. The Netherlands: Springer.Google Scholar
  53. Kominoski, J.S., T.J. Hoellein, C.J. LeRoy, C.M. Pringle, and C.M. Swan. 2010. Beyond species richness: expanding biodiversity-ecosystem functioning theory in detritus-based streams. River Research and Applications 26 (1): 67–75.  https://doi.org/10.1002/rra.1285.CrossRefGoogle Scholar
  54. Koroleff, F. 1976. Determination of NH4 +-N. In Methods of seawater analysis, ed. K. Grasshoff, 127–133. Weinheim: Verlag Chemie.Google Scholar
  55. Kristensen, E., and K. Hansen. 1995. Decay of plant detritus in organic-poor marine sediments: production rates and stoichiometry of dissolved C and N compounds. Journal of Marine Research 53 (4): 675–701.  https://doi.org/10.1357/0022240953213115.CrossRefGoogle Scholar
  56. Kristensen, E., F.Ø. Andersen, N. Holmboe, M. Holmer, and N. Thongtham. 2000. Carbon and nitrogen mineralization in sediments of the Bangrong mangrove area, Phuket, Thailand. Aquatic Microbial Ecology 22: 199–213.  https://doi.org/10.3354/ame022199.CrossRefGoogle Scholar
  57. Mackin, J.E., and R.C. Aller. 1984. Ammonium adsorption in marine sediments. Limnology and Oceanography 29 (2): 250–257.  https://doi.org/10.4319/lo.1984.29.2.0250.CrossRefGoogle Scholar
  58. Mann, K.H. 1988. Production and use of detritus in various freshwater, estuarine, and coastal marine ecosystems. Limnology and Oceanography 33: 910–930.Google Scholar
  59. Marbà, N., M. Holmer, E. Gacia, and C. Barrón. 2006. Seagrass beds and coastal biogeochemistry. In Seagrasses: biology, ecology and conservation, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 135–157. The Netherlands: Springer.Google Scholar
  60. Mcleod, E., G.L. Chuma, S. Bouillon, R. Salm, M. Björk, C.M. Duarte, C.E. Lovelock, W.H. Schlesinger, and B.R. Silliman. 2011. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Frontiers in Ecology and the Environment 9 (10): 552–560.  https://doi.org/10.1890/110004.CrossRefGoogle Scholar
  61. Moore, T.N., and P.G. Fairweather. 2006. Decay of multiple species of seagrass detritus is dominated by species identity, with an important influence of mixing litters. Oikos 114 (2): 329–227.  https://doi.org/10.1111/j.2006.0030-1299.14576.x.CrossRefGoogle Scholar
  62. Moore, K.A., and F.T. Short. 2006. Zostera: biology, ecology, and management. In Seagrasses: biology, ecology and conservation, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 361–386. The Netherlands: Springer.Google Scholar
  63. Moore, J.C., E.L. Berlow, D.C. Coleman, P.C. de Ruiter, Q. Dong, A. Hastings, N.C. Johnson, K.S. McCann, K. Melville, P.J. Morin, K. Nadelhoffer, A.D. Rosemond, D.M. Post, J.L. Sabo, K.M. Scow, M.J. Vanni, and D.H. Wall. 2004. Detritus, trophic dynamics, and biodiversity. Ecology Letters 7 (7): 584–600.  https://doi.org/10.1111/j.1461-0248.2004.00606.x.CrossRefGoogle Scholar
  64. Nicastro, A., Y. Onoda, and M.J. Bishop. 2012. Direct and indirect effects of tidal elevation on eelgrass decomposition. Marine Ecology Progress Series 456: 53–62.  https://doi.org/10.3354/meps09635.CrossRefGoogle Scholar
  65. Olyarnik, S.V., and J.J. Stachowicz. 2012. Multi-year study of the effects of Ulva sp. blooms on eelgrass Zostera marina. Marine Ecology Progress Series 468: 107–117.  https://doi.org/10.3354/meps09973.CrossRefGoogle Scholar
  66. Pedersen, M.F., and J. Borum. 1992. Nitrogen dynamics of eelgrass Zostera marina during a late summer period of high growth and low nutrient availability. Marine Ecology Progress Series 80: 65–72.  https://doi.org/10.3354/meps080065.CrossRefGoogle Scholar
  67. Pielou, E.C. 1975. Ecological diversity. New York: Wiley.Google Scholar
  68. Reusch, T.B.H., and A.R. Hughes. 2006. The emerging role of genetic diversity for ecosystem functioning: estuarine macrophytes as models. Estuaries and Coasts 29: 195–164.CrossRefGoogle Scholar
  69. Reusch, T.B.H., A. Ehlers, and B. Worm. 2005. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences of the United States of America 102 (8): 2826–2831.  https://doi.org/10.1073/pnas.0500008102.CrossRefGoogle Scholar
  70. Reynolds, L.K., K.J. McGlathery, and M. Waycott. 2012. Genetic diversity enhances restoration success by augmenting ecosystem services. PLoS One 7 (6): e38397.  https://doi.org/10.1371/journal.pone.0038397.CrossRefGoogle Scholar
  71. Reynolds, L.K., K. DuBois, J.M. Abbott, S.L. Williams, and J.J. Stachowicz. 2016. Response of a habitat-forming marine plant to a simulated warming event is delayed, genotypic specific, and varies with phenology. PLoS One 11 (6): e0154532.  https://doi.org/10.1371/journal.pone.0154532.CrossRefGoogle Scholar
  72. Reynolds, L.K., K.M. Chan, E. Huynh, S.L. Williams, and J.J. Stachowicz. 2017. Plant genotype identity and diversity interact with mesograzer species diversity to influence detrital consumption in eelgrass meadows. Oikos.  https://doi.org/10.1111/oik.04471.
  73. Rice, D.L. 1982. The detritus nitrogen problem: new observations and perspectives from organic geochemistry. Marine Ecology Progress Series 9: 153–162.  https://doi.org/10.3354/meps009153.CrossRefGoogle Scholar
  74. Romero, J., K.-S. Lee, M. Pérez, M.A. Mateo, and T. Alcoverro. 2006. Nutrient dynamics in seagrass ecosystems. In Seagrasses: biology, ecology and conservation, ed. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 227–254. The Netherlands: Springer.Google Scholar
  75. Rudman, S.M., M.A. Rodriguez-Cabal, A. Stier, T. Sato, J. Heavyside, R.W. El-Sabaawi, and G.M. Crutsinger. 2015. Adaptive genetic variation mediates bottom-up and top-down control in an aquatic ecosystem. Proceedings of the Royal Society B 282 (1812): 20151234.  https://doi.org/10.1098/rspb.2015.1234.CrossRefGoogle Scholar
  76. Short, F.T., and C.P. McRoy. 1984. Nitrogen uptake by leaves and roots of the seagrass Zostera marina L. Botanica Marina 27: 547–555.CrossRefGoogle Scholar
  77. Spiegelhalter, D.G., N.G. Best, C.P. Bradley, and A. van der Linde. 2002. Bayesian measures of model complexity and fit. Journal of the Royal Statistical Society. Series B, Methodological 64 (4): 583–639.  https://doi.org/10.1111/1467-9868.00353.CrossRefGoogle Scholar
  78. Spivak, A.C., E.A. Canuel, J.E. Duffy, and J.P. Richardson. 2007. Top-down and bottom-up controls on sediment organic matter in an experimental seagrass ecosystem. Limnology and Oceanography 52 (6): 2595–2607.  https://doi.org/10.4319/lo.2007.52.6.2595.CrossRefGoogle Scholar
  79. Stachowicz, J.J., J.F. Bruno, and J.E. Duffy. 2007. Understanding the effects of marine biodiversity on communities and ecosystems. Annual Review of Ecology, Evolution, and Systematics 38 (1): 739–766.  https://doi.org/10.1146/annurev.ecolsys.38.091206.095659.CrossRefGoogle Scholar
  80. Stachowicz, J.J., S.T. Kamel, A.R. Hughes, and R.K. Grosberg. 2013. Genetic relatedness influences plant biomass accumulation in eelgrass (Zostera marina L.). The American Naturalist 181 (5): 715–724.  https://doi.org/10.1086/669969.CrossRefGoogle Scholar
  81. Suchanek, T.H., S.L. Williams, J.C. Ogden, D.K. Hubbard, and I.P. Gill. 1984. Utilization of shallow-water seagrass detritus by Caribbean deep sea macrofauna: del C-13 evidence. Deep Sea Research 29: 853–967.Google Scholar
  82. Sun, F., X. Zhang, Q. Zhang, F. Liu, J. Zhang, and J. Gong. 2015. Seagrass (Zostera marina) colonization promotes the accumulation of diazotrophic bacteria and alters the relative abundances of specific bacterial lineages involved in benthic carbon and sulfur cycling. Applied and Environmental Microbiology 81 (19): 6901–6914.  https://doi.org/10.1128/AEM.01382-15.CrossRefGoogle Scholar
  83. Tenore, K.R. 1988. Nitrogen in benthic food chains. In Nitrogen cycling in coastal marine environments, ed. T.H. Blackburn and J. Sorensen, 191–206. New York: Wiley.Google Scholar
  84. Thresher, R.E., P.D. Nichols, J.S. Gunn, B.D. Bruce, and D.M. Furlani. 1992. Seagrass detritus as the basis of a coastal planktonic food chain. Limnology and Oceanography 37 (8): 1754–1758.  https://doi.org/10.4319/lo.1992.37.8.1754.CrossRefGoogle Scholar
  85. Tomas, F., J.M. Abbott, C. Steinberg, M. Balk, S.L. Williams, and J.J. Stachowicz. 2011. Plant genotype and nitrogen loading influence seagrass productivity, biochemistry, and plant-herbivore interactions. Ecology 92 (9): 1807–1817.  https://doi.org/10.1890/10-2095.1.CrossRefGoogle Scholar
  86. Wardle, D.A., K.I. Bonner, and K.S. Nicholson. 1997. Biodiversity and plant litter: Experimental evidence which does not support the view that enhanced species richness improves ecosystem function. Oikos 79 (2): 247–258.  https://doi.org/10.2307/3546010.CrossRefGoogle Scholar
  87. 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 Jr., A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, F.T. Short, and S.L. Williams. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America 106 (30): 12377–12381.  https://doi.org/10.1073/pnas.0905620106.CrossRefGoogle Scholar
  88. Williams, S.L. 1990. Experimental studies of Caribbean seagrass bed development. Ecological Monographs 60 (4): 449–469.  https://doi.org/10.2307/1943015.CrossRefGoogle Scholar
  89. Williams, S.L. 2001. Reduced genetic diversity in eelgrass transplantations affects both population growth and individual fitness. Ecological Applications 11 (5): 1472–1488.  https://doi.org/10.1890/1051-0761(2001)011[1472:RGDIET]2.0.CO;2.CrossRefGoogle Scholar
  90. Williams, S.L. 2016. From sea to sea. Nature 530 (7590): 290–291.  https://doi.org/10.1038/nature16869.CrossRefGoogle Scholar
  91. Williams, S.L., and C.A. Davis. 1996. Population genetic analyses of transplanted eelgrass (Zostera marina) reveal reduced genetic diversity in southern California. Restoration Ecology 4 (2): 163–180.  https://doi.org/10.1111/j.1526-100X.1996.tb00117.x.CrossRefGoogle Scholar
  92. Williams, S.L., and K.L. Heck Jr. 2001. Seagrass community ecology. In Marine community ecology, ed. M.D. Bertness, S.D. Gaines, and M.E. Hay, 317–337. Sunderland: Sinauer Associates, Incorporated.Google Scholar
  93. Worm, B., E.B. Barbier, N. Beaumont, J.E. Duffy, C. Folke, B.S. Halpern, J.B.C. Jackson, H.K. Lotze, F. Micheli, S.R. Palumbi, E. Sala, K.A. Selkoe, J.J. Stachowicz, and R. Watson. 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314 (5800): 787–790.  https://doi.org/10.1126/science.1132294.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  • Susan L. Williams
    • 1
    • 2
  • Jessica M. Abbott
    • 1
    • 3
  • Laura K. Reynolds
    • 2
    • 4
  • John J. Stachowicz
    • 2
  1. 1.Bodega Marine LaboratoryUniversity of California—DavisBodega BayUSA
  2. 2.Department of Evolution and EcologyUniversity of California—DavisDavisUSA
  3. 3.Institute for Wildlife StudiesArcataUSA
  4. 4.Soil and Water Sciences DepartmentUniversity of FloridaGainsvilleUSA

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