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Cited by 706Ecology and Vegetation Dynamics StudiesLand Use and Ecosystem ServicesSoil Carbon and Nitrogen Dynamics

Land-use intensification causes multitrophic homogenization of grassland communities

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Gossner, Martin M., Lewinsohn, Thomas M., Kahl, Tiemo, Grassein, Fabrice, Boch, Steffen, Prati, Daniel, Birkhofer, Klaus, Renner, Swen C. +37 more·2016·Nature
DOI 10.1038/nature20575
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Abstract

Land-use intensification is a major driver of biodiversity loss. Alongside reductions in local species diversity, biotic homogenization at larger spatial scales is of great concern for conservation. Biotic homogenization means a decrease in β-diversity (the compositional dissimilarity between sites). Most studies have investigated losses in local (α)-diversity and neglected biodiversity loss at larger spatial scales. Studies addressing β-diversity have focused on single or a few organism groups (for example, ref. 4), and it is thus unknown whether land-use intensification homogenizes communities at different trophic levels, above- and belowground. Here we show that even moderate increases in local land-use intensity (LUI) cause biotic homogenization across microbial, plant and animal groups, both above- and belowground, and that this is largely independent of changes in α-diversity. We analysed a unique grassland biodiversity dataset, with abundances of more than 4,000 species belonging to 12 trophic groups. LUI, and, in particular, high mowing intensity, had consistent effects on β-diversity across groups, causing a homogenization of soil microbial, fungal pathogen, plant and arthropod communities. These effects were nonlinear and the strongest declines in β-diversity occurred in the transition from extensively managed to intermediate intensity grassland. LUI tended to reduce local α-diversity in aboveground groups, whereas the α-diversity increased in belowground groups. Correlations between the β-diversity of different groups, particularly between plants and their consumers, became weaker at high LUI. This suggests a loss of specialist species and is further evidence for biotic homogenization. The consistently negative effects of LUI on landscape-scale biodiversity underscore the high value of extensively managed grasslands for conserving multitrophic biodiversity and ecosystem service provision. Indeed, biotic homogenization rather than local diversity loss could prove to be the most substantial consequence of land-use intensification.

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  • Intensively used grasslands are relatively species-poor.

    “Intensively used grasslands are relatively species-poor (34)”

    From Restoring Degraded Lands (2021) · cites this paper as [34]

    The Results text (page not available in our copy) says land-use intensification reduced species richness for most aboveground groups. But it reports neutral or positive effects on belowground organisms, so the unqualified claim that intensively used grasslands are relatively species-poor overgeneralizes the finding. (LLM, conf=0.88)

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Research works printed but not linked: 47

  1. Allan, E. et al. Interannual variation in land-use intensity enhances grassland multidiversity. Proc. Natl. Acad. Sci. 111, 308-313, doi:10.1073/pnas.1312213111 (2014). · DOI
  2. Anderson, M. J. et al. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol. Lett. 14, 19-28, doi:10.1111/j.1461-0248.2010.01552.x (2011). · DOI
  3. Gámez-Virués, S. et al. Landscape simplification filters species traits and drives biotic homogenization Nat. Commun. 6, 8568 (2015).
  4. Karp, D. S. et al. Intensive agriculture erodes β-diversity at large scales. Ecol. Lett. 15, 963-970, doi:10.1111/j.1461-0248.2012.01815.x (2012). · DOI
  5. McKinney, M. L. & Lockwood, J. L. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol. Evol. 14, 450-453, doi:http://dx.doi.org/10.1016/S0169-5347(99)01679-1 (1999). · DOI
  6. Smart, S. M. et al. Biotic homogenization and changes in species diversity across human-modified ecosystems. Proc. R. Soc. B-Biol. Sci. 273, 2659-2665, doi:10.1098/rspb.2006.3630 (2006). · DOI
  7. van der Plas, F. et al. Biotic homogenization can decrease landscape-scale forest multifunctionality. Proc. Natl. Acad. Sci. 113, 3557-3562, doi:10.1073/pnas.1517903113 (2016). · DOI
  8. Dornelas, M. et al. Assemblage time series reveal biodiversity change but not systematic loss. Science 344, 296-299, doi:10.1126/science.1248484 (2014). · DOI · Paper page
  9. Solar, R. R. d. C. et al. How pervasive is biotic homogenization in human-modified tropical forest landscapes? Ecol. Lett. 18, 1108-1118, doi:10.1111/ele.12494 (2015). · DOI
  10. Kleijn, D. et al. On the relationship between farmland biodiversity and land-use intensity in Europe. Proc. R. Soc. B-Biol. Sci. 276, 903-909, doi:10.1098/rspb.2008.1509 (2009). · DOI · Paper page
  11. Ferrier, S., Manion, G., Elith, J. & Richardson, K. Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Divers. Distrib. 13, 252-264, doi:10.1111/j.1472-4642.2007.00341.x (2007). · DOI
  12. Fitzpatrick, M. C. et al. Environmental and historical imprints on beta diversity: insights from variation in rates of species turnover along gradients. Proc. R. Soc. B- Biol. Sci. 280, doi:10.1098/rspb.2013.1201 (2013). · DOI
  13. Carvalho, J. C., Cardoso, P., Borges, P. A. V., Schmera, D. & Podani, J. Measuring fractions of beta diversity and their relationships to nestedness: a theoretical and empirical comparison of novel approaches. Oikos 122, 825-834, doi:10.1111/j.1600- 0706.2012.20980.x (2013). · DOI
  14. Baselga, A. & Leprieur, F. Comparing methods to separate components of beta diversity. Methods Ecol. Evol. 6, 1069-1079, doi:10.1111/2041-210x.12388 (2015). · DOI
  15. Rodrigues, J. L. M. et al. Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc. Natl. Acad. Sci. 110, 988- 993, doi:10.1073/pnas.1220608110 (2013). · DOI
  16. Pellissier, L. et al. Turnover of plant lineages shapes herbivore phylogenetic beta diversity along ecological gradients. Ecol. Lett. 16, 600-608, doi:10.1111/ele.12083 (2013). · DOI
  17. De Deyn, G. B. & Van der Putten, W. H. Linking aboveground and belowground diversity. Trends Ecol. Evol. 20, 625-633, doi:http://dx.doi.org/10.1016/j.tree.2005.08.009 (2005). · DOI
  18. Haimi, J., Fritze, H. & Moilanen, P. Responses of soil decomposer animals to wood- ash fertilisation and burning in a coniferous forest stand. For. Ecol. Manag. 129, 53- 61, doi:http://dx.doi.org/10.1016/S0378-1127(99)00158-9 (2000). · DOI
  19. Bardgett, R., Hobbs, P. & Frostegård, Å. Changes in soil fungal:bacterial biomass ratios following reductions in the intensity of management of an upland grassland. Biol. Fertil. Soils 22, 261-264, doi:10.1007/bf00382522 (1996). · DOI
  20. Fenchel, T. & Finlay, B. J. The ubiquity of small species: patterns of local and global diversity. Bioscience 54, 777-784, doi:10.1641/0006-3568 (2004). · DOI
  21. Finlay, B. J. Global dispersal of free-living microbial eukaryote species. Science 296, 1061-1063, doi:10.1126/science.1070710 (2002). · DOI
  22. Hanski, I. Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38, 210-221, doi:10.2307/3544021 (1982). · DOI
  23. Bommarco, R. et al. Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proc. R. Soc. B-Biol. Sci., doi:10.1098/rspb.2009.2221 (2010). · DOI
  24. Öckinger, E. et al. Life-history traits predict species responses to habitat area and isolation: a cross-continental synthesis. Ecol. Lett. 13, 969-979, doi:10.1111/j.1461- 0248.2010.01487.x (2010). · DOI · Paper page
  25. Manning, P. et al. Grassland management intensification weakens the associations among the diversities of multiple plant and animal taxa. Ecology 96, 1492-1501, doi:10.1890/14-1307.1 (2014). · DOI
  26. Birkhofer, K. et al. General relationships between abiotic soil properties and soil biota across spatial scales and different land-use types. PLoS ONE 7, e43292, doi:10.1371/journal.pone.0043292 (2012). · DOI
  27. Socher, S. A. et al. Interacting effects of fertilization, mowing and grazing on plant species diversity of 1500 grasslands in Germany differ between regions. Basic Appl. Ecol. 14, 126-136, doi:http://dx.doi.org/10.1016/j.baae.2012.12.003 (2013). · DOI
  28. Socher, S. A. et al. Direct and productivity-mediated indirect effects of fertilization, mowing and grazing on grassland species richness. J. Ecol. 100, 1391-1399, doi:10.1111/j.1365-2745.2012.02020.x (2012). · DOI
  29. Boch, S., Prati, D., Schöning, I. & Fischer, M. Lichen species richness is highest in non-intensively used grasslands promoting suitable microhabitats and low vascular plant competition. Biodivers. Conserv. 25, 225-238, doi:10.1007/s10531-015-1037-y (2016). · DOI
  30. Müller, J. et al. Impact of land-use intensity and productivity on bryophyte diversity in agricultural grasslands. PLoS ONE 7, e51520, doi:10.1371/journal.pone.0051520 (2012). · DOI
  31. Simons, N. K. et al. Resource-Mediated Indirect Effects of Grassland Management on Arthropod Diversity. PLoS ONE 9, e107033, doi:10.1371/journal.pone.0107033 (2014). · DOI
  32. Simons, N. K. et al. Effects of land-use intensity on arthropod species abundance distributions in grasslands. J. Anim. Ecol. 84, 143-154, doi:10.1111/1365-2656.12278 (2015). · DOI
  33. Weiner, C. N., Werner, M., Linsenmair, K. E. & Blüthgen, N. Land-use impacts on plant-pollinator networks: interaction strength and specialization predict pollinator declines. Ecology 95, 466-474, doi:10.1890/13-0436.1 (2013). · DOI
  34. Börschig, C. Effects of land-use intensity in grasslands on diversity, life-history traits and multitrophic interactions Dr. rer. nat. thesis, Georg-August-Universität (2012).
  35. Renner, S. C. et al. Temporal changes in randomness of bird communities across Central Europe. PLoS One 9, e112347, doi:10.1371/journal.pone.0112347 (2014). · DOI
  36. Rydell, J., Entwistle, A. & Racey, P. A. Timing of foraging flights of three species of bats in relation to insect activity and predation risk. Oikos 76, 243-252, doi:10.2307/3546196 (1996). · DOI
  37. Estrada-Villegas, S., Meyer, C. F. J. & Kalko, E. K. V. Effects of tropical forest fragmentation on aerial insectivorous bats in a land-bridge island system. Biol. Conserv. 143, 597-608, doi:http://dx.doi.org/10.1016/j.biocon.2009.11.009 (2010). · DOI
  38. Jung, K., Kaiser, S., Böhm, S., Nieschulze, J. & Kalko, E. K. V. Moving in three dimensions: effects of structural complexity on occurrence and activity of insectivorous bats in managed forest stands. J. Appl. Ecol. 49, 523-531, doi:10.1111/j.1365-2664.2012.02116.x (2012). · DOI
  39. Denzinger, A., Siemers, B., Schaub, A. & Schnitzler, H.-U. Echolocation by the barbastelle bat, Barbastella barbastellus. J. Comp. Physiol. A 187, 521-528, doi:10.1007/s003590100223 (2001). · DOI
  40. Russo, D. & Jones, G. Identification of twenty-two bat species (Mammalia: Chiroptera) from Italy by analysis of time-expanded recordings of echolocation calls. J. Zool. 258, 91-103, doi:10.1017/s0952836902001231 (2002). · DOI
  41. Obrist, M., K., Boesch, R. & Flückiger, P., F. Variability in echolocation call design of 26 Swiss bat species: consequences, limits and options for automated field identification with a synergetic pattern recognition approach. Mammalia 68, 307-322, doi:10.1515/mamm.2004.030 (2004). · DOI
  42. Aronesty, E. Comparison of sequencing utility programs. The Open Bioinformatics Journal 7, 1-8 (2013).
  43. Cole, J. R. et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37, D141-D145, doi:10.1093/nar/gkn879 (2009). · DOI
  44. Domonell, A., Brabender, M., Nitsche, F., Bonkowski, M. & Arndt, H. Community structure of cultivable protists in different grassland and forest soils of Thuringia. Pedobiologia 56, 1-7, doi:http://dx.doi.org/10.1016/j.pedobi.2012.07.001 (2013). · DOI
  45. Morris, E. K. et al. Land use and host neighbor identity effects on arbuscular mycorrhizal fungal community composition in focal plant rhizosphere. Biodivers. Conserv. 22, 2193-2205, doi:10.1007/s10531-013-0527-z (2013). · DOI
  46. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541, doi:10.1128/aem.01541-09 (2009). · DOI
  47. Öpik, M. et al. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol. 188, 223-241, doi:10.1111/j.1469-8137.2010.03334.x (2010). · DOI

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Authors
Gossner, M. M., Lewinsohn, T. M., Kahl, T., Grassein, F., Boch, S., Prati, D., Birkhofer, K., Renner, S. C., Sikorski, J., Wubet, T., Arndt, H., Baumgartner, V., Blaser, S., Blüthgen, N., Börschig, C., Buscot, F., Diekötter, T., Jorge, L. R., Jung, K., Keyel, A. C., Klein, A.-M., Klemmer, S., Krauss, J., Lange, M., Müller, J., Overmann, J., Pašalić, E., Penone, C., Perović, D. J., Purschke, O., Schall, P., Socher, S. A., Sonnemann, I., Tschapka, M., Tscharntke, T., Türke, M., Venter, P. C., Weiner, C. N., Werner, M., Wolters, V., Wurst, S., Westphal, C., Fischer, M., Weisser, W. W., & Allan, E.
Affiliations
  • Swiss Federal Institute for Forest, Snow and Landscape Research (CH)
  • Universidade Estadual de Campinas (UNICAMP) (BR)
  • University of Freiburg (DE)
  • University of Bern (CH)
  • Black Forest Biosphere Reserve (DE)
  • Lund University (SE)
  • Universität Ulm (DE)
  • Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures (DE)
  • Helmholtz Centre for Environmental Research (DE)
  • University of Cologne (DE)
  • Technische Universität Darmstadt (DE)
  • University of Würzburg (DE)
  • Justus-Liebig-Universität Gießen (DE)
  • University of Göttingen (DE)
  • Max Planck Institute for Biogeochemistry (DE)
  • University of Potsdam (DE)
  • Technical University of Munich (DE)
  • Fujian Agriculture and Forestry University (CN)
  • German Centre for Integrative Biodiversity Research (DE)
  • University of Salzburg (AT)
  • Freie Universität Berlin (DE)
Corresponding author
Gossner, Martin M.
ORCID
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2016-11-30
Volume
540
Issue
7632
Pages
266-269
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/nature20575
OpenAlex
W2558519551
Cited by
706
References
7
Citations by year
2026: 89 · 2025: 121 · 2024: 89 · 2023: 78 · 2022: 78 · 2021: 61 · 2020: 48 · 2019: 79 · 2018: 38 · 2017: 22 · 2016: 2 · 2014: 1
FWCI
40.57
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
  • TUbilio (Technical University of Darmstadt) (acceptedVersion)
  • DORA WSL (Swiss Federal Institute for Forest, Snow and Landscape Research) (submittedVersion, other-oa)
  • HAL (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • BORIS (University Library Bern) (submittedVersion)
  • Max Planck Digital Library (submittedVersion)
  • publish.UP (University of Potsdam) (submittedVersion)
  • GRO (submittedVersion, cc-by)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
  • RUNE (Research UNE) (submittedVersion)
Funders
Deutsche Forschungsgemeinschaft
Topics
  • Physical Sciences › Environmental Science › Nature and Landscape Conservation › Ecology and Vegetation Dynamics Studies
  • Physical Sciences › Environmental Science › Global and Planetary Change › Land Use and Ecosystem Services
  • Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
Keywords
biotic homogenization, grassland biodiversity, beta diversity, trophic guilds, mowing intensity, soil microbial communities, fungal pathogens, arthropods, plant diversity, soil biodiversity, multitrophic interactions, extensive grassland management, biodiversity loss
MeSH terms
Agriculture, Animals, Arthropods, Birds, Chiroptera, Conservation of Natural Resources, Fungi, Germany, Human Activities, Lichens, Plants, Soil Microbiology, Species Specificity, Bryopsida, Food Chain, Biodiversity, Grassland, Datasets as Topic

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