Biodiversity increases multitrophic energy use efficiency, flow and storage in grasslands.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
21
09
2019
accepted:
15
01
2020
pubmed:
26
2
2020
medline:
1
4
2020
entrez:
26
2
2020
Statut:
ppublish
Résumé
The continuing loss of global biodiversity has raised questions about the risk that species extinctions pose for the functioning of natural ecosystems and the services that they provide for human wellbeing. There is consensus that, on single trophic levels, biodiversity sustains functions; however, to understand the full range of biodiversity effects, a holistic and multitrophic perspective is needed. Here, we apply methods from ecosystem ecology that quantify the structure and dynamics of the trophic network using ecosystem energetics to data from a large grassland biodiversity experiment. We show that higher plant diversity leads to more energy stored, greater energy flow and higher community-energy-use efficiency across the entire trophic network. These effects of biodiversity on energy dynamics were not restricted to only plants but were also expressed by other trophic groups and, to a similar degree, in aboveground and belowground parts of the ecosystem, even though plants are by far the dominating group in the system. The positive effects of biodiversity on one trophic level were not counteracted by the negative effects on adjacent levels. Trophic levels jointly increased the performance of the community, indicating ecosystem-wide multitrophic complementarity, which is potentially an important prerequisite for the provisioning of ecosystem services.
Identifiants
pubmed: 32094542
doi: 10.1038/s41559-020-1123-8
pii: 10.1038/s41559-020-1123-8
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
393-405Références
Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).
pubmed: 22678280
doi: 10.1038/nature11148
Hautier, Y. et al. Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 348, 336–340 (2015).
pubmed: 25883357
doi: 10.1126/science.aaa1788
pmcid: 25883357
Balvanera, P. et al. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol. Lett. 9, 1146–1156 (2006).
pubmed: 16972878
doi: 10.1111/j.1461-0248.2006.00963.x
pmcid: 16972878
Hector, A. et al. Plant diversity and productivity experiments in european grasslands. Science 286, 1123–1127 (1999).
pubmed: 10550043
pmcid: 10550043
doi: 10.1126/science.286.5442.1123
Tilman, D. et al. Diversity and productivity in a long-term grassland experiment. Science 294, 843–845 (2001).
pubmed: 11679667
doi: 10.1126/science.1060391
Hector, A., Beale, A., Minns, A., Otway, S. & Lawton, J. Consequences of the reduction of plant diversity for litter decomposition: effects through litter quality and microenvironment. Oikos 90, 357–371 (2000).
doi: 10.1034/j.1600-0706.2000.900217.x
Milcu, A., Partsch, S., Scherber, C., Weisser, W. W. & Scheu, S. Earthworms and legumes control litter decomposition in a plant diversity gradient. Ecology 89, 1872–1882 (2008).
pubmed: 18705374
doi: 10.1890/07-1377.1
Ebeling, A. et al. Plant diversity impacts decomposition and herbivory via changes in aboveground arthropods. PLoS ONE 9, e106529 (2014).
pubmed: 25226237
pmcid: 4165753
doi: 10.1371/journal.pone.0106529
Barnes, A. D. et al. Energy flux: the link between multitrophic biodiversity and ecosystem functioning. Trends Ecol. Evol. 33, 186–197 (2018).
Duffy, J. E. et al. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol. Lett. 10, 522–538 (2007).
pubmed: 17498151
doi: 10.1111/j.1461-0248.2007.01037.x
pmcid: 17498151
Lindeman, R. L. The trophic-dynamic aspect of ecology. Ecology 23, 399–417 (1942).
doi: 10.2307/1930126
Juday, C. The annual energy budget of an inland lake. Ecology 21, 438–450 (1940).
doi: 10.2307/1930283
Getz, W. M. Biomass transformation webs provide a unified approach to consumer-resource modelling. Ecol. Lett. 14, 113–124 (2011).
pubmed: 21199247
doi: 10.1111/j.1461-0248.2010.01566.x
pmcid: 21199247
Barnes, A. D. et al. Consequences of tropical land use for multitrophic biodiversity and ecosystem functioning. Nat. Commun. 5, 5351 (2014).
pubmed: 25350947
pmcid: 4220457
doi: 10.1038/ncomms6351
Ghedini, G., Loreau, M., White, C. R. & Marshall, D. J. Testing MacArthur’s minimisation principle: do communities minimise energy wastage during succession? Ecol. Lett. 21, 1182–1190 (2018).
pubmed: 29781121
doi: 10.1111/ele.13087
pmcid: 29781121
Gamfeldt, L. et al. Marine biodiversity and ecosystem functioning: what’s known and what’s next? Oikos 124, 252–265 (2015).
doi: 10.1111/oik.01549
Unsicker, S. B. et al. Invertebrate herbivory along a gradient of plant species diversity in extensively managed grasslands. Oecologia 150, 233–246 (2006).
pubmed: 16917778
doi: 10.1007/s00442-006-0511-3
pmcid: 16917778
Hertzog, L. R., Ebeling, A., Weisser, W. W. & Meyer, S. T. Plant diversity increases predation by ground-dwelling invertebrate predators. Ecosphere 8, e01990 (2017).
doi: 10.1002/ecs2.1990
Odum, E. P. Trends expected in stressed ecosystems. BioScience 35, 419–422 (1985).
doi: 10.2307/1310021
Margalef, R. On certain unifying principles in ecology. Am. Nat. 97, 357–374 (1963).
doi: 10.1086/282286
Weisser, W. W. et al. Biodiversity effects on ecosystem functioning in a 15-year grassland experiment: patterns, mechanisms, and open questions. Basic Appl. Ecol. 23, 1–73 (2017).
doi: 10.1016/j.baae.2017.06.002
Eisenhauer, N., Reich, P. B. & Scheu, S. Increasing plant diversity effects on productivity with time due to delayed soil biota effects on plants. Basic Appl. Ecol. 13, 571–578 (2012).
doi: 10.1016/j.baae.2012.09.002
Ludovisi, A., Pandolfi, P. & Taticchi, M. I. The strategy of ecosystem development: specific dissipation as an indicator of ecosystem maturity. J. Theor. Biol. 235, 33–43 (2005).
pubmed: 15833311
doi: 10.1016/j.jtbi.2004.12.017
Poisot, T., Mouquet, N. & Gravel, D. Trophic complementarity drives the biodiversity–ecosystem functioning relationship in food webs. Ecol. Lett. 16, 853–861 (2013).
pubmed: 23692591
doi: 10.1111/ele.12118
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).
doi: 10.1890/03-9000
Reich, P. B. et al. Impacts of biodiversity loss escalate through time as redundancy fades. Science 336, 589–592 (2012).
pubmed: 22556253
doi: 10.1126/science.1217909
pmcid: 22556253
Meyer, S. T. et al. Effects of biodiversity strengthen over time as ecosystem functioning declines at low and increases at high biodiversity. Ecosphere 7, e01619 (2016).
Fagan, W. F. et al. Nitrogen in insects: implications for trophic complexity and species diversification. Am. Nat. 160, 784–802 (2002).
pubmed: 18707465
doi: 10.1086/343879
pmcid: 18707465
Scherber, C. et al. Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468, 553–556 (2010).
pubmed: 20981010
doi: 10.1038/nature09492
pmcid: 20981010
Bessler, H. et al. Aboveground overyielding in grassland mixtures is associated with reduced biomass partitioning to belowground organs. Ecology 90, 1520–1530 (2009).
pubmed: 19569367
doi: 10.1890/08-0867.1
pmcid: 19569367
Lange, M. et al. Plant diversity increases soil microbial activity and soil carbon storage. Nat. Commun. 6, 6707 (2015).
pubmed: 25848862
doi: 10.1038/ncomms7707
pmcid: 25848862
Berlow, E. Strong effects of weak interactions in ecological communities. Nature 398, 330–334 (1999).
doi: 10.1038/18672
Moore, J. C., de Ruiter, P. C. & Hunt, H. W. Influence of productivity on the stability of real and model ecosystems. Science 261, 906–908 (1993).
pubmed: 17783740
doi: 10.1126/science.261.5123.906
pmcid: 17783740
Pfisterer, A. B. & Schmid, B. Diversity-dependent production can decrease the stability of ecosystem functioning. Nature 416, 84–86 (2002).
pubmed: 11882897
doi: 10.1038/416084a
pmcid: 11882897
Pilette, R. Evaluating direct and indirect effects in ecosystems. Am. Nat. 133, 303–307 (1989).
doi: 10.1086/284920
Eisenhauer, N. et al. Plant diversity effects on soil food webs are stronger than those of elevated CO
pubmed: 23576722
doi: 10.1073/pnas.1217382110
pmcid: 23576722
Hines, J. et al. Towards an integration of biodiversity–ecosystem functioning and food web theory to evaluate relationships between multiple ecosystem services. Adv. Ecol. Res. 53, 161–199 (2015).
doi: 10.1016/bs.aecr.2015.09.001
Hines, J. et al. A meta food web for invertebrate species collected in a European grassland. Ecology 100, e02679 (2019).
pubmed: 30838635
doi: 10.1002/ecy.2679
pmcid: 30838635
Giling, D. P. et al. Plant diversity alters the representation of motifs in food webs. Nat. Commun. 10, 1226 (2019).
pubmed: 30874561
pmcid: 6420570
doi: 10.1038/s41467-019-08856-0
Huang, Y. et al. Impacts of species richness on productivity in a large-scale subtropical forest experiment. Science 362, 80–83 (2018).
pubmed: 30287660
doi: 10.1126/science.aat6405
pmcid: 30287660
Roscher, C. et al. The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community. Basic Appl. Ecol. 5, 107–121 (2004).
doi: 10.1078/1439-1791-00216
Peters, R. H. The Ecological Implications of Body Size (Cambridge Univ. Press, 1986).
Eisenhauer, N. et al. Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term. PLoS ONE 6, e16055 (2011).
pubmed: 21249208
pmcid: 3017561
doi: 10.1371/journal.pone.0016055
Ravenek, J. M. et al. Long-term study of root biomass in a biodiversity experiment reveals shifts in diversity effects over time. Oikos 123, 1528–1536 (2014).
doi: 10.1111/oik.01502
Swift, M. J., Heal, O. W. & Anderson, J. M. Decomposition in Terrestrial Ecosystems (Univ. California Press, 1979).
Kempson, D., Lloyd, M. & Ghelardi, R. A new extractor for woodland litter. Pedobiologia 3, 1–21 (1963).
Sechi, V., Brussaard, L., De Goede, R. G. M., Rutgers, M. & Mulder, C. Choice of resolution by functional trait or taxonomy affects allometric scaling in soil food webs. Am. Nat. 185, 142–149 (2015).
pubmed: 25560559
doi: 10.1086/678962
pmcid: 25560559
Cortois, R. et al. Possible mechanisms underlying abundance and diversity responses of nematode communities to plant diversity. Ecosphere 8, e01719 (2017).
doi: 10.1002/ecs2.1719
Andrássy, I. Die rauminhalst and gewichtsbestimmung der fadenwürmer (Nematoden). Acta Zool. Acad. Sci. 2, 1–15 (1956).
Yeates, G. W., Bongers, T., De Goede, R. G., Freckman, D. W. & Georgieva, S. S. Feeding habits in soil nematode families and genera—an outline for soil ecologists. J. Nematol. 25, 315–331 (1993).
pubmed: 19279775
pmcid: 2619405
Ferris, H. NEMAPLEX The Nematode-Plant Information System. A Virtual Encyclopedia on Soil and Plant Nematodes (Univ. California, 1999); http://nemaplex.ucdavis.edu/
Sieriebriennikov, B., Ferris, H. & de Goede, R. G. M. NINJA: an automated calculation system for nematode-based biological monitoring. Eur. J. Soil Biol. 61, 90–93 (2014).
doi: 10.1016/j.ejsobi.2014.02.004
Scheu, S. Automated measurement of the respiratory response of soil microcompartments: active microbial biomass in earthworm faeces. Soil Biol. Biochem. 24, 1113–1118 (1992).
doi: 10.1016/0038-0717(92)90061-2
Strecker, T. et al. Effects of plant diversity, functional group composition, and fertilization on soil microbial properties in experimental grassland. PLoS ONE 10, e0125678 (2015).
pubmed: 25938580
pmcid: 4418810
doi: 10.1371/journal.pone.0125678
Beck, T. et al. An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biol. Biochem. 29, 1023–1032 (1997).
doi: 10.1016/S0038-0717(97)00030-8
Eisenhauer, N. et al. Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91, 485–496 (2010).
pubmed: 20392013
doi: 10.1890/08-2338.1
pmcid: 20392013
Steinbeiss, S. et al. Plant diversity positively affects short-term soil carbon storage in experimental grasslands. Glob. Change Biol. 14, 2937–2949 (2008).
doi: 10.1111/j.1365-2486.2008.01697.x
Loranger, H. et al. Invertebrate herbivory increases along an experimental gradient of grassland plant diversity. Oecologia 174, 183–193 (2014).
pubmed: 23907703
doi: 10.1007/s00442-013-2741-5
pmcid: 23907703
Vogel, A., Eisenhauer, N., Weigelt, A. & Scherer-Lorenzen, M. Plant diversity does not buffer drought effects on early-stage litter mass loss rates and microbial properties. Glob. Change Biol. 19, 2795–2803 (2013).
doi: 10.1111/gcb.12225
Engelmann, M. D. The role of soil arthropods in the energetics of an old field community. Ecol. Monogr. 31, 221–238 (1961).
doi: 10.2307/1948553
De Ruiter, P. C., Van Veen, J. A., Moore, J. C., Brussaard, L. & Hunt, H. W. Calculation of nitrogen mineralization in soil food webs. Plant Soil 157, 263–273 (1993).
doi: 10.1007/BF00011055
Sneath, P. H. A. Longevity of micro-organisms. Nature 195, 643–646 (1962).
pubmed: 13914562
doi: 10.1038/195643a0
Ehnes, R. B., Rall, B. C. & Brose, U. Phylogenetic grouping, curvature and metabolic scaling in terrestrial invertebrates. Ecol. Lett. 14, 993–1000 (2011).
pubmed: 21794052
doi: 10.1111/j.1461-0248.2011.01660.x
Reich, P. B., Tjoelker, M. G., Machado, J.-L. & Oleksyn, J. Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439, 457–461 (2006).
pubmed: 16437113
doi: 10.1038/nature04282
Eisenhauer, N., Milcu, A., Sabais, A. C. W. & Scheu, S. Animal ecosystem engineers modulate the diversity-invasibility relationship. PLoS ONE 3, e3489 (2008).
pubmed: 18941521
pmcid: 2565839
doi: 10.1371/journal.pone.0003489
Eisenhauer, N. Earthworms in a Plant Diversity Gradient: Direct and Indirect Effects on Plant Competition and Establishment. PhD thesis, TU Darmstadt (2008).
Kazanci, C. EcoNet: a new software for ecological modeling, simulation and network analysis. Ecol. Modell. 208, 3–8 (2007).
doi: 10.1016/j.ecolmodel.2007.04.031
MATLAB—the language of technical computing. v.8.1, 2013a (MathWorks, 2013); https://www.mathworks.com/products/matlab/
Borrett, S. R. & Lau, M. K. enaR: an R package for ecosystem network analysis. Methods Ecol. Evol. 5, 1206–1213 (2014).
doi: 10.1111/2041-210X.12282
Borrett, S. R., Whipple, S. J. & Patten, B. C. Rapid development of indirect effects in ecological networks. Oikos 119, 1136–1148 (2010).
doi: 10.1111/j.1600-0706.2009.18104.x
Borrett, S. R. & Scharler, U. M. Walk partitions of flow in ecological network analysis: review and synthesis of methods and indicators. Ecol. Indic. 106, 105451 (2019).
doi: 10.1016/j.ecolind.2019.105451
Wiegert, R. G. & Kozlowski, J. Indirect causality in ecosystems. Am. Nat. 124, 293–298 (1984).
doi: 10.1086/284272
Hines, D. E., Ray, S. & Borrett, S. R. Uncertainty analyses for ecological network analysis enable stronger inferences. Environ. Modell. Softw. 101, 117–127 (2018).
doi: 10.1016/j.envsoft.2017.12.011
Soetaert, K., Van den Meersche, K. & van Oevelen, D. limSolve: solving linear inverse models in R. R package v.1.5.1 (2009).
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017); http://www.R-project.org/
Murray, A. A Chaos of Delight. The Wonderful World of Soil Mesofauna (accessed 2 December 2019); https://www.chaosofdelight.org/
IAN/UMCES Symbol and Image Libraries (Integration and Application Network, Univ. Maryland Center for Environmental Science, accessed 2 December 2019); https://ian.umces.edu/symbols/
Smith, M. et al. NodeXL: A Free and Open Network Overview, Discovery and Exploration add-in for Excel Version NodeXL Basic (The Social Media Research Foundation, 2010); https://www.smrfoundation.org