Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative‐experimental approach

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom–up and top–down forcing remain unres...

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Published in:Ecology letters Vol. 18; no. 7; pp. 696 - 705
Main Authors: Duffy, J. Emmett, Reynolds, Pamela L, Boström, Christoffer, Coyer, James A, Cusson, Mathieu, Donadi, Serena, Douglass, James G, Eklöf, Johan S, Engelen, Aschwin H, Eriksson, Britas Klemens, Fredriksen, Stein, Gamfeldt, Lars, Gustafsson, Camilla, Hoarau, Galice, Hori, Masakazu, Hovel, Kevin, Iken, Katrin, Lefcheck, Jonathan S, Moksnes, Per‐Olav, Nakaoka, Masahiro, O'Connor, Mary I, Olsen, Jeanine L, Richardson, J. Paul, Ruesink, Jennifer L, Sotka, Erik E, Thormar, Jonas, Whalen, Matthew A, Stachowicz, John J, Worm, Boris
Format: Journal Article
Language:English
Published: England Blackwell Science 01.07.2015
Blackwell Publishing Ltd
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ISSN:1461-023X, 1461-0248, 1461-0248
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Abstract Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom–up and top–down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top–down and bottom–up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top–down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross‐site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large‐scale patterns corresponded strikingly with prior small‐scale experiments. Our results link global and local evidence that biodiversity and top–down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.
AbstractList Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom–up and top–down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass ( Zostera marina ) to quantify how top–down and bottom–up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top–down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross‐site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large‐scale patterns corresponded strikingly with prior small‐scale experiments. Our results link global and local evidence that biodiversity and top–down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.
Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.
Author Engelen, Aschwin H
Duffy, J. Emmett
Reynolds, Pamela L
Hoarau, Galice
Thormar, Jonas
Richardson, J. Paul
Lefcheck, Jonathan S
Nakaoka, Masahiro
Douglass, James G
Fredriksen, Stein
Coyer, James A
O'Connor, Mary I
Gamfeldt, Lars
Iken, Katrin
Cusson, Mathieu
Hori, Masakazu
Hovel, Kevin
Ruesink, Jennifer L
Sotka, Erik E
Whalen, Matthew A
Worm, Boris
Moksnes, Per‐Olav
Boström, Christoffer
Eriksson, Britas Klemens
Eklöf, Johan S
Olsen, Jeanine L
Donadi, Serena
Gustafsson, Camilla
Stachowicz, John J
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/25983129$$D View this record in MEDLINE/PubMed
https://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-119137$$DView record from Swedish Publication Index (Stockholms universitet)
https://gup.ub.gu.se/publication/219675$$DView record from Swedish Publication Index (Göteborgs universitet)
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Issue 7
Keywords coordinated experiments
structural equation modelling
top-down control
food webs
Biodiversity-ecosystem functioning
metabolic ecology
bottom-up control
Language English
License 2015 John Wiley & Sons Ltd/CNRS.
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References Paquette, A. & Messier, C. (2010). The effect of biodiversity on tree productivity: from temperate to boreal forests. Global Ecol. Biogeogr., 20, 170-180.
Baden, S., Boström, C., Tobiasson, S., Arponen, H. & Moksnes, P.-O. (2010). Relative importance of trophic interactions and nutrient enrichment in seagrass ecosystems: a broad-scale field experiment in the Baltic-Skagerrak area. Limnol. Oceanogr., 55, 1435.
Duffy, J.E., Richardson, J.P. & Canuel, E.A. (2003). Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol. Lett., 6, 637-645.
Arnaud-Haond, S. & Khalid, B. (2007). GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol. Ecol. Notes, 7, 15-17.
Grace, J.B. (2006). Structural Equation Modeling and Natural Systems. Cambridge University Press, 1-378.
Tomas, F., Abbott, J.M., Balk, M., Steinberg, C., Williams, S.L. & Stachowicz, J.J. (2011). Plant genotype and nitrogen loading influence seagrass productivity, biochemistry, and plant-herbivore interactions. Ecology, 92, 1807-1817.
Cardinale, B.J., Matulich, K.L., Hooper, D.U., Byrnes, J.E., Duffy, E., Gamfeldt, L. et al. (2011). The functional role of producer diversity in ecosystems. Am. J. Bot., 98, 572-592.
Reusch, T.B.H., Ehlers, A., Hämmerli, A. & Worm, B. (2005). Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl. Acad. Sci. USA, 102, 2826-2831.
Chao, A. & Jost, L. (2012). Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology, 93, 2533-2547.
Cloern, J. (2001). Our evolving conceptual model of the coastal eutrophication problem. Mar. Ecol. Prog. Ser., 210, 223-253.
Moksnes, P.O., Gullström, M., Tryman, K. & Baden, S. (2008). Trophic cascades in a temperate seagrass community. Oikos, 117, 763-777.
Shipley, B. (2009). Confirmatory path analysis in a generalized multilevel context. Ecology, 90, 363-368.
Best, R.J., Caulk, N.C. & Stachowicz, J.J. (2013). Trait vs. phylogenetic diversity as predictors of competition and community composition in herbivorous marine amphipods. Ecol. Lett., 16, 72-80.
Gamfeldt, L., Snäll, T., Bagchi, R., Jonsson, M., Gustafsson, L., Kjellander, P. et al. (2013). Higher levels of multiple ecosystem services are found in forests with more tree species. Nat. Commun., 4, 1340.
Reusch, T.B. (2000). Five microsatellite loci in eelgrass Zostera marina and a test of cross-species amplification in Z. noltii and Z. japonica. Mol. Ecol., 9, 371-373.
Hughes, B.B., Eby, R., Van Dyke, E., Tinker, M.T., Marks, C.I., Johnson, K.S. et al. (2013). Recovery of a top predator mediates negative eutrophic effects on seagrass. Proc. Natl. Acad. Sci. USA, 110, 15313-15318.
Olsen, J.L., Coyer, J.A., Stam, W.T., Moy, F.E., Christie, H. & Jørgensen, N.M. (2013). Eelgrass Zostera marina populations in northern Norwegian fjords are genetically isolated and diverse. Mar. Ecol. Prog. Ser., 486, 121-132.
Hooper, D.U., Adair, E.C., Cardinale, B.J., Byrnes, J.E.K., Hungate, B.A., Matulich, K.L. et al. (2012). A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature, 486, 105-108.
Cardinale, B.J., Duffy, J.E., Gonzalez, A., Hooper, D.U., Perrings, C., Venail, P. et al. (2012). Biodiversity loss and its impact on humanity. Nature, 486, 59-67.
Eriksson, B.K., Ljunggren, L.M., Sandstrom, A., Johansson, G. & Mattila, J. Rubach, et al. (2009). Declines in predatory fish promote bloom-forming macroalgae. Ecol. Appl., 19, 1975-1988.
Shipley, B. (2013). The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology, 94, 560-564.
Hughes, A.R. & Stachowicz, J.J. (2004). Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc. Natl. Acad. Sci. USA, 101, 8998-9002.
Mattson, W.J., Jr. (1980). Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst., 11, 119-161.
Reusch, T.B., Stam, W.T. & Olsen, J.L. (1999). Microsatellite loci in eelgrass Zostera marina reveal marked polymorphism within and among populations. Mol. Ecol., 8, 317-321.
Whalen, M.A., Duffy, J.E. & Grace, J.B. (2013). Temporal shifts in top-down versus bottom-up control of epiphytic algae in a seagrass ecosystem. Ecology, 94, 510-520.
Borer, E.T., Seabloom, E.W., Gruner, D.S., Harpole, W.S., Hillebrand, H., Lind, E.M. et al. (2014). Herbivores and nutrients control grassland plant diversity via light limitation. Nature, 508, 517-520.
Frank, K., Petrie, B. & Shackell, N. (2007). The ups and downs of trophic control in continental shelf ecosystems. Trends Ecol. Evol., 22, 236-242.
Polis, G. & Strong, D. (1996). Food Web Complexity and Community Dynamics. Am. Nat., 147, 813-846.
Reynolds, P.L., Paul Richardson, J. & Emmett Duffy, J. (2014). Field experimental evidence that grazers mediate transition between microalgal and seagrass dominance. Limnol. Oceanogr., 59, 1053-1064.
Poore, A.G.B., Campbell, A.H. & Steinberg, P.D. (2009). Natural densities of mesograzers fail to limit growth of macroalgae or their epiphytes in a temperate algal bed. J. Ecol., 97, 164-175.
Heck, K.L. & Valentine, J.F. (2007). The primacy of top-down effects in shallow benthic ecosystems. Estuaries and Coasts, 30, 371-381.
Maestre, F.T., Quero, J.L., Gotelli, N.J., Escudero, A., Ochoa, V., Delgado-Baquerizo, M. et al. (2012). Plant Species Richness and Ecosystem Multifunctionality in Global Drylands. Science, 335, 214-218.
Hunter, M.D. & Price, P.W. (1992). Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology, 73, 723-732.
Srivastava, D.S. & Vellend, M. (2005). Biodiversity-ecosystem function research: is it relevant to conservation? Annu. Rev. Ecol. Evol. Syst., 36, 267-294.
Hughes, A.R., Bando, K.J., Rodriguez, L.F. & Williams, S.L. (2004). Relative effects of grazers and nutrients on seagrasses: a meta-analysis approach. Mar. Ecol. Prog. Ser., 282, 87-99.
Nakagawa, S. & Schielzeth, H. (2013). A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol., 4, 133-142.
Lefcheck, J.S. & Duffy, J.E. (2015). Multitrophic functional diversity predicts ecosystem functioning in experimental assemblages of estuarine consumers. PeerJ. PrePrints 3:e1137.
Spivak, A.C., Canuel, E.A., Duffy, J.E. & Richardson, J.P. (2009). Nutrient enrichment and food web composition affect ecosystem metabolism in an experimental seagrass habitat. PLoS ONE, 4, e7473.
Mora, C., Aburto-Oropeza, O., Bocos, A.A., Ayotte, P.M., Banks, S., Bauman, A.G. et al. (2011). Global human footprint on the linkage between biodiversity and ecosystem functioning in reef fishes. PLoS Biol., 9, e1000606.
O'Connor, M.I. (2009). Warming strengthens an herbivore-plant interaction. Ecology, 90, 388-398.
Strong, D.R. (1992). Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology, 73, 747-754.
Edgar, G.J. (1990). The use of the size structure of benthic macrofaunal communities to estimate faunal biomass and secondary production. J. Exp. Mar. Biol. Ecol., 137, 195-214.
Gruner, D.S., Smith, J.E., Seabloom, E.W., Sandin, S.A., Ngai, J.T., Hillebrand, H. et al. (2008). A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol. Lett., 11, 740-755.
Oksanen, L. & Oksanen, T. (2000). The logic and realism of the hypothesis of exploitation ecosystems. Am. Nat., 155, 703-723.
Burkholder, J., Tomasko, D. & Touchette, B. (2007). Seagrasses and eutrophication. J. Exp. Mar. Biol. Ecol., 350, 46-72.
Duffy, J.E., Cardinale, B.J., France, K.E., McIntyre, P.B., Thébault, E. & Loreau, M. (2007). The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol. Lett., 10, 522-538.
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References_xml – reference: Chao, A. & Jost, L. (2012). Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology, 93, 2533-2547.
– reference: Duffy, J.E., Richardson, J.P. & Canuel, E.A. (2003). Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol. Lett., 6, 637-645.
– reference: Burkholder, J., Tomasko, D. & Touchette, B. (2007). Seagrasses and eutrophication. J. Exp. Mar. Biol. Ecol., 350, 46-72.
– reference: Polis, G. & Strong, D. (1996). Food Web Complexity and Community Dynamics. Am. Nat., 147, 813-846.
– reference: O'Connor, M.I. (2009). Warming strengthens an herbivore-plant interaction. Ecology, 90, 388-398.
– reference: Maestre, F.T., Quero, J.L., Gotelli, N.J., Escudero, A., Ochoa, V., Delgado-Baquerizo, M. et al. (2012). Plant Species Richness and Ecosystem Multifunctionality in Global Drylands. Science, 335, 214-218.
– reference: Spivak, A.C., Canuel, E.A., Duffy, J.E. & Richardson, J.P. (2009). Nutrient enrichment and food web composition affect ecosystem metabolism in an experimental seagrass habitat. PLoS ONE, 4, e7473.
– reference: Reusch, T.B.H., Ehlers, A., Hämmerli, A. & Worm, B. (2005). Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl. Acad. Sci. USA, 102, 2826-2831.
– reference: Hughes, A.R. & Stachowicz, J.J. (2004). Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc. Natl. Acad. Sci. USA, 101, 8998-9002.
– reference: Tomas, F., Abbott, J.M., Balk, M., Steinberg, C., Williams, S.L. & Stachowicz, J.J. (2011). Plant genotype and nitrogen loading influence seagrass productivity, biochemistry, and plant-herbivore interactions. Ecology, 92, 1807-1817.
– reference: Srivastava, D.S. & Vellend, M. (2005). Biodiversity-ecosystem function research: is it relevant to conservation? Annu. Rev. Ecol. Evol. Syst., 36, 267-294.
– reference: Cardinale, B.J., Duffy, J.E., Gonzalez, A., Hooper, D.U., Perrings, C., Venail, P. et al. (2012). Biodiversity loss and its impact on humanity. Nature, 486, 59-67.
– reference: Hooper, D.U., Adair, E.C., Cardinale, B.J., Byrnes, J.E.K., Hungate, B.A., Matulich, K.L. et al. (2012). A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature, 486, 105-108.
– reference: Hughes, A.R., Bando, K.J., Rodriguez, L.F. & Williams, S.L. (2004). Relative effects of grazers and nutrients on seagrasses: a meta-analysis approach. Mar. Ecol. Prog. Ser., 282, 87-99.
– reference: Moksnes, P.O., Gullström, M., Tryman, K. & Baden, S. (2008). Trophic cascades in a temperate seagrass community. Oikos, 117, 763-777.
– reference: Shipley, B. (2009). Confirmatory path analysis in a generalized multilevel context. Ecology, 90, 363-368.
– reference: Reusch, T.B. (2000). Five microsatellite loci in eelgrass Zostera marina and a test of cross-species amplification in Z. noltii and Z. japonica. Mol. Ecol., 9, 371-373.
– reference: Duffy, J.E., Cardinale, B.J., France, K.E., McIntyre, P.B., Thébault, E. & Loreau, M. (2007). The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol. Lett., 10, 522-538.
– reference: Lefcheck, J.S. & Duffy, J.E. (2015). Multitrophic functional diversity predicts ecosystem functioning in experimental assemblages of estuarine consumers. PeerJ. PrePrints 3:e1137.
– reference: Cloern, J. (2001). Our evolving conceptual model of the coastal eutrophication problem. Mar. Ecol. Prog. Ser., 210, 223-253.
– reference: Nakagawa, S. & Schielzeth, H. (2013). A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol., 4, 133-142.
– reference: Mora, C., Aburto-Oropeza, O., Bocos, A.A., Ayotte, P.M., Banks, S., Bauman, A.G. et al. (2011). Global human footprint on the linkage between biodiversity and ecosystem functioning in reef fishes. PLoS Biol., 9, e1000606.
– reference: Grace, J.B. (2006). Structural Equation Modeling and Natural Systems. Cambridge University Press, 1-378.
– reference: Reusch, T.B., Stam, W.T. & Olsen, J.L. (1999). Microsatellite loci in eelgrass Zostera marina reveal marked polymorphism within and among populations. Mol. Ecol., 8, 317-321.
– reference: Frank, K., Petrie, B. & Shackell, N. (2007). The ups and downs of trophic control in continental shelf ecosystems. Trends Ecol. Evol., 22, 236-242.
– reference: Hunter, M.D. & Price, P.W. (1992). Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology, 73, 723-732.
– reference: Strong, D.R. (1992). Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology, 73, 747-754.
– reference: Heck, K.L. & Valentine, J.F. (2007). The primacy of top-down effects in shallow benthic ecosystems. Estuaries and Coasts, 30, 371-381.
– reference: Poore, A.G.B., Campbell, A.H. & Steinberg, P.D. (2009). Natural densities of mesograzers fail to limit growth of macroalgae or their epiphytes in a temperate algal bed. J. Ecol., 97, 164-175.
– reference: Eriksson, B.K., Ljunggren, L.M., Sandstrom, A., Johansson, G. & Mattila, J. Rubach, et al. (2009). Declines in predatory fish promote bloom-forming macroalgae. Ecol. Appl., 19, 1975-1988.
– reference: Shipley, B. (2013). The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology, 94, 560-564.
– reference: Gruner, D.S., Smith, J.E., Seabloom, E.W., Sandin, S.A., Ngai, J.T., Hillebrand, H. et al. (2008). A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol. Lett., 11, 740-755.
– reference: Best, R.J., Caulk, N.C. & Stachowicz, J.J. (2013). Trait vs. phylogenetic diversity as predictors of competition and community composition in herbivorous marine amphipods. Ecol. Lett., 16, 72-80.
– reference: Borer, E.T., Seabloom, E.W., Gruner, D.S., Harpole, W.S., Hillebrand, H., Lind, E.M. et al. (2014). Herbivores and nutrients control grassland plant diversity via light limitation. Nature, 508, 517-520.
– reference: Olsen, J.L., Coyer, J.A., Stam, W.T., Moy, F.E., Christie, H. & Jørgensen, N.M. (2013). Eelgrass Zostera marina populations in northern Norwegian fjords are genetically isolated and diverse. Mar. Ecol. Prog. Ser., 486, 121-132.
– reference: Paquette, A. & Messier, C. (2010). The effect of biodiversity on tree productivity: from temperate to boreal forests. Global Ecol. Biogeogr., 20, 170-180.
– reference: Gamfeldt, L., Snäll, T., Bagchi, R., Jonsson, M., Gustafsson, L., Kjellander, P. et al. (2013). Higher levels of multiple ecosystem services are found in forests with more tree species. Nat. Commun., 4, 1340.
– reference: Mattson, W.J., Jr. (1980). Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst., 11, 119-161.
– reference: Cardinale, B.J., Matulich, K.L., Hooper, D.U., Byrnes, J.E., Duffy, E., Gamfeldt, L. et al. (2011). The functional role of producer diversity in ecosystems. Am. J. Bot., 98, 572-592.
– reference: Arnaud-Haond, S. & Khalid, B. (2007). GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol. Ecol. Notes, 7, 15-17.
– reference: Whalen, M.A., Duffy, J.E. & Grace, J.B. (2013). Temporal shifts in top-down versus bottom-up control of epiphytic algae in a seagrass ecosystem. Ecology, 94, 510-520.
– reference: Oksanen, L. & Oksanen, T. (2000). The logic and realism of the hypothesis of exploitation ecosystems. Am. Nat., 155, 703-723.
– reference: Baden, S., Boström, C., Tobiasson, S., Arponen, H. & Moksnes, P.-O. (2010). Relative importance of trophic interactions and nutrient enrichment in seagrass ecosystems: a broad-scale field experiment in the Baltic-Skagerrak area. Limnol. Oceanogr., 55, 1435.
– reference: Edgar, G.J. (1990). The use of the size structure of benthic macrofaunal communities to estimate faunal biomass and secondary production. J. Exp. Mar. Biol. Ecol., 137, 195-214.
– reference: Hughes, B.B., Eby, R., Van Dyke, E., Tinker, M.T., Marks, C.I., Johnson, K.S. et al. (2013). Recovery of a top predator mediates negative eutrophic effects on seagrass. Proc. Natl. Acad. Sci. USA, 110, 15313-15318.
– reference: Reynolds, P.L., Paul Richardson, J. & Emmett Duffy, J. (2014). Field experimental evidence that grazers mediate transition between microalgal and seagrass dominance. Limnol. Oceanogr., 59, 1053-1064.
– volume: 137
  start-page: 195
  year: 1990
  end-page: 214
  article-title: The use of the size structure of benthic macrofaunal communities to estimate faunal biomass and secondary production
  publication-title: J. Exp. Mar. Biol. Ecol.
– volume: 9
  start-page: e1000606
  year: 2011
  article-title: Global human footprint on the linkage between biodiversity and ecosystem functioning in reef fishes
  publication-title: PLoS Biol.
– volume: 20
  start-page: 170
  year: 2010
  end-page: 180
  article-title: The effect of biodiversity on tree productivity: from temperate to boreal forests
  publication-title: Global Ecol. Biogeogr.
– volume: 210
  start-page: 223
  year: 2001
  end-page: 253
  article-title: Our evolving conceptual model of the coastal eutrophication problem
  publication-title: Mar. Ecol. Prog. Ser.
– volume: 11
  start-page: 119
  year: 1980
  end-page: 161
  article-title: Herbivory in relation to plant nitrogen content
  publication-title: Annu. Rev. Ecol. Syst.
– volume: 350
  start-page: 46
  year: 2007
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Snippet Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural...
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StartPage 696
SubjectTerms Algae
algae control
Algal blooms
Animals
Biodiversity
Biodiversity-ecosystem functioning
Biomass
bottom-up control
COMMUNITY
coordinated experiments
Crustacea
DIVERSITY
Ecosystems
Environmental factors
Environmental gradient
Environmental Sciences
EUTROPHICATION
Experiments
Food Chain
food webs
FUNCTIONAL-ROLE
Gastropoda
Genotype
global change
Grazing
Herbivory
metabolic ecology
Microalgae
MICROSATELLITE LOCI
Miljövetenskap
Models, Biological
NUTRIENT ENRICHMENT
Nutrient pollution
Nutrients
pollution
Pollution control
Population Dynamics
POPULATIONS
SEAGRASS ECOSYSTEM
seagrasses
structural equation modelling
top-down control
TROPHIC INTERACTIONS
ZOSTERA-MARINA
Zosteraceae - genetics
Zosteraceae - physiology
Title Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative‐experimental approach
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Volume 18
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