Marine Macrophyte Detritus and Degradation: the Role of Intraspecific Genetic Variation
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.
KeywordsAmmonification Detritus Decomposition Eelgrass Genotypes Marine macrophyte
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.
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.
- 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
- 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
- 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
- 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
- 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.
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Koroleff, F. 1976. Determination of NH4 +-N. In Methods of seawater analysis, ed. K. Grasshoff, 127–133. Weinheim: Verlag Chemie.Google Scholar
- 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
- 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
- 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
- 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
- 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
- Pielou, E.C. 1975. Ecological diversity. New York: Wiley.Google Scholar
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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