Changes in belowground biodiversity during ecosystem development
Open accessAbstract
Belowground organisms play critical roles in maintaining multiple ecosystem processes, including plant productivity, decomposition, and nutrient cycling. Despite their importance, however, we have a limited understanding of how and why belowground biodiversity (bacteria, fungi, protists, and invertebrates) may change as soils develop over centuries to millennia (pedogenesis). Moreover, it is unclear whether belowground biodiversity changes during pedogenesis are similar to the patterns observed for aboveground plant diversity. Here we evaluated the roles of resource availability, nutrient stoichiometry, and soil abiotic factors in driving belowground biodiversity across 16 soil chronosequences (from centuries to millennia) spanning a wide range of globally distributed ecosystem types. Changes in belowground biodiversity during pedogenesis followed two main patterns. In lower-productivity ecosystems (i.e., drier and colder), increases in belowground biodiversity tracked increases in plant cover. In more productive ecosystems (i.e., wetter and warmer), increased acidification during pedogenesis was associated with declines in belowground biodiversity. Changes in the diversity of bacteria, fungi, protists, and invertebrates with pedogenesis were strongly and positively correlated worldwide, highlighting that belowground biodiversity shares similar ecological drivers as soils and ecosystems develop. In general, temporal changes in aboveground plant diversity and belowground biodiversity were not correlated, challenging the common perception that belowground biodiversity should follow similar patterns to those of plant diversity during ecosystem development. Taken together, our findings provide evidence that ecological patterns in belowground biodiversity are predictable across major globally distributed ecosystem types and suggest that shifts in plant cover and soil acidification during ecosystem development are associated with changes in belowground biodiversity over centuries to millennia.
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Soil development such as organic matter accumulation and aggregate formation are slow processes, often occurring over decades or centuries.
“Soil development such as organic matter accumulation and aggregate formation are slow processes, often occurring over decades or centuries [66].”
From From the Ground Up: Prairies on Reclaimed Mine Land—Impacts on Soil and Vegetation (2020) · cites this paper as [66]
The Significance section says soils develop over centuries to millennia, supporting the claim that soil development is slow. It does not establish that organic matter accumulation or aggregate formation specifically takes decades or centuries. (LLM, conf=0.84)
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Cites
Belowground biodiversity and ecosystem functioning
Bardgett, R. D., & van der Putten, W. H. (2014) · Nature · doi:10.1038/nature13855 · Cited by 4,045 · see citing works
Self-citationGlobal diversity and geography of soil fungi
Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Yorou, N. S., Wijesundera, R., Villarreal‐Ruiz, L., Vasco‐Palacios, A. M., Thu, P. Q., Suija, A., et al. (2014) · Science · doi:10.1126/science.1256688 · Cited by 3,739 · see citing works
Embracing the unknown: disentangling the complexities of the soil microbiome
Fierer, N. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.87 · Cited by 3,528 · see citing works
Self-citationSoil biodiversity and soil community composition determine ecosystem multifunctionality
Wagg, C., Bender, S. F., Widmer, F., & van der Heijden, M. G. A. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320054111 · Cited by 2,550 · see citing works
The fate of phosphorus during pedogenesis
Walker, T. W., & Syers, J. K. (1976) · Geoderma · doi:10.1016/0016-7061(76)90066-5 · Cited by 2,402 · see citing works
(2012) · Springer eBooks · doi:10.1007/springerreference_76825 · Cited by 2,071 · see citing works
Factors of Soil Formation: A System of Quantitative Pedology
Pendleton, R. L., & Jenny, H. (1945) · Geographical Review · doi:10.2307/211491 · Cited by 1,760 · see citing works
Factors of Soil Formation, a System of Quantitative Pedology
C., R. C. (1941) · Agronomy Journal · doi:10.2134/agronj1941.00021962003300090016x · Cited by 1,374 · see citing works
The use of chronosequences in studies of ecological succession and soil development
Walker, L. R., Wardle, D. A., Bardgett, R. D., & Clarkson, B. D. (2010) · Journal of Ecology · doi:10.1111/j.1365-2745.2010.01664.x · Cited by 1,267 · see citing works
Self-citationComparative aspects of cycling of organic C, N, S and P through soil organic matter
McGill, W. B., & Cole, C. V. (1981) · Geoderma · doi:10.1016/0016-7061(81)90024-0 · Cited by 1,123 · see citing works
Ecosystem Properties and Forest Decline in Contrasting Long-Term Chronosequences
Wardle, D. A., Walker, L. R., & Bardgett, R. D. (2004) · Science · doi:10.1126/science.1098778 · Cited by 1,114 · see citing works
Self-citationSoil pH mediates the balance between stochastic and deterministic assembly of bacteria
Tripathi, B. M., Stegen, J., Kim, M., Dong, K., Adams, J. M., & Lee, Y. K. (2018) · The ISME Journal · doi:10.1038/s41396-018-0082-4 · Cited by 1,049 · see citing works
Changes in Soil Phosphorus Fractions and Ecosystem Dynamics across a Long Chronosequence in Hawaii
Crews, T. E., Kitayama, K., Fownes, J. H., Riley, R. H., Herbert, D. A., Mueller‐Dombois, D., & Vitousek, P. M. (1995) · Ecology · doi:10.2307/1938144 · Cited by 945 · see citing works
Self-citationNutrient Cycling and Limitation
Vitousek, P. M. (2004) · Princeton University Press eBooks · doi:10.1515/9780691190341 · Cited by 657 · see citing works
Self-citationLarge contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils
Rillig, M. C., Wright, S. F., Nichols, K. A., et al. (2001) · Plant and Soil · doi:10.1023/a:1010364221169 · Cited by 652 · see citing works
Delgado‐Baquerizo, M., Eldridge, D. J., Ochoa, V., Gozalo, B., Singh, B. K., & Maestre, F. T. (2017) · Ecology Letters · doi:10.1111/ele.12826 · Cited by 507 · see citing works
Self-citationLinking aboveground and belowground diversity
Deyn, G. B. D., & van der Putten, W. H. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.08.009 · Cited by 471 · see citing works
Understanding ecosystem retrogression
Peltzer, D. A., Wardle, D. A., Allison, V. J., Baisden, W. T., Bardgett, R. D., Chadwick, O. A., Condron, L. M., Parfitt, R. L., Porder, S., Richardson, S. J., et al. (2010) · Ecological Monographs · doi:10.1890/09-1552.1 · Cited by 441 · see citing works
Self-citationNutrient cycling and limitation: Hawai'i as a model system
(2005) · Choice Reviews Online · doi:10.5860/choice.42-2800 · Cited by 409 · see citing works
Environmental filtering explains variation in plant diversity along resource gradients
Laliberté, É., Zemunik, G., & Turner, B. L. (2014) · Science · doi:10.1126/science.1256330 · Cited by 319 · see citing works
Molecular study of worldwide distribution and diversity of soil animals
Wu, T., Ayres, E., Bardgett, R. D., Wall, D. H., & Garey, J. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103824108 · Cited by 244 · see citing works
Self-citationHow does pedogenesis drive plant diversity?
Laliberté, É., Grace, J. B., Huston, M. A., Lambers, H., Teste, F. P., Turner, B. L., & Wardle, D. A. (2013) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2013.02.008 · Cited by 209 · see citing works
Self-citationOrtiz‐Álvarez, R., Fierer, N., Rı́os, A. D. L., Casamayor, E. O., & Barberán, A. (2018) · The ISME Journal · doi:10.1038/s41396-018-0076-2 · Cited by 155 · see citing works
Self-citationWardle, D. A., Bardgett, R. D., Walker, L. R., Peltzer, D. A., & Lagerström, A. (2007) · Oikos · doi:10.1111/j.2007.0030-1299.16130.x · Cited by 103 · see citing works
Self-citationTarlera, S., Jangid, K., Ivester, A. H., Whitman, W. B., & Williams, M. A. (2008) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2008.00444.x · Cited by 96 · see citing works
Self-citationWardle, D. A., Bardgett, R. D., Walker, L. R., & Bonner, K. I. (2008) · Functional Ecology · doi:10.1111/j.1365-2435.2008.01513.x · Cited by 84 · see citing works
Self-citationAlfaro, F. D., Manzano, M., Marquet, P. A., et al. (2017) · Journal of Ecology · doi:10.1111/1365-2745.12766 · Cited by 80 · see citing works
Self-citationCarlson, M. L., Flagstad, L. A., Gillet, F., & Mitchell, E. A. D. (2010) · Journal of Ecology · doi:10.1111/j.1365-2745.2010.01699.x · Cited by 74 · see citing works
Roy‐Bolduc, A., Laliberté, É., & Hijri, M. (2015) · Ecology and Evolution · doi:10.1002/ece3.1881 · Cited by 32 · see citing works
Jangid, K., Whitman, W. B., Condron, L. M., et al. (2013) · Plant and Soil · doi:10.1007/s11104-013-1720-2 · Cited by 24 · see citing works
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“Soil development such as organic matter accumulation and aggregate formation are slow processes, often occurring over decades or centuries [66].”
Background
- Authors
- Delgado-Baquerizo, M., Bardgett, R. D., Vitousek, P. M., Maestre, F. T., Williams, M. A., Eldridge, D. J., Lambers, H., Neuhauser, S., Gallardo, A., García-Velázquez, L., Sala, O. E., Abades, S. R., Alfaro, F. D., Berhe, A. A., Bowker, M. A., Currier, C. M., Cutler, N. A., Hart, S. C., Hayes, P. E., Hseu, Z.-Y., Kirchmair, M., Peña-Ramírez, V. M., Pérez, C. A., Reed, S. C., Santos, F., Siebe, C., Sullivan, B. W., Weber-Grullon, L., & Fierer, N.
- Affiliations
- Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO 80309;
- University of Manchester (GB)
- Stanford University (US)
- Universidad Rey Juan Carlos (ES)
- Virginia Tech (US)
- UNSW Sydney (AU)
- The University of Western Australia (AU)
- Universität Innsbruck (AT)
- Universidad Pablo de Olavide (ES)
- Departamento de Biología y Geología, Física y Química Inorgánica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, Calle Tulipán Sin Número, 28933 Móstoles, Spain;
- Arizona State University (US)
- GEMA Center for Genomics, Ecology & Environment, Universidad Mayor, Huechuraba, Santiago 8580745, Chile;
- Universidad Mayor (CL)
- University of California, Merced (US)
- Northern Arizona University (US)
- Newcastle University (GB)
- National Taiwan University (TW)
- Institute of Microbiology, University of Innsbruck, 6020 Innsbruck, Austria;
- Instituto de Geología, Universidad Nacional Autónoma de México, Ciudad Universitaria, México DF CP 04510, México;
- Institute of Ecology and Biodiversity (CL)
- United States Geological Survey (US)
- Instituto de Geología (MX)
- University of Nevada, Reno (US)
- Global Drylands Center, Arizona State University, Tempe, AZ 85287;
- Cooperative Institute for Research in Environmental Sciences (US)
- ORCID
- Delgado-Baquerizo, Manuel
- Bardgett, Richard D.
- Vitousek, Peter M.
- Maestre, Fernando T.
- Williams, Mark A.
- Eldridge, David J.
- Lambers, Hans
- Neuhauser, Sigrid
- Gallardo, Antonio
- García-Velázquez, Laura
- Sala, Osvaldo E.
- Abades, Sebastián R.
- Alfaro, Fernando D.
- Berhe, Asmeret A.
- Bowker, Matthew A.
- Currier, Courtney M.
- Cutler, Nick A.
- Hart, Stephen C.
- Hayes, Patrick E.
- Hseu, Zeng-Yei
- Pérez, Cecilia A.
- Reed, Sasha C.
- Santos, Fernanda
- Siebe, Christina
- Sullivan, Benjamin W.
- Weber-Grullon, Luis
- Fierer, Noah
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2019-03-15
- Volume
- 116
- Issue
- 14
- Pages
- 6891-6896
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC6452688
- OpenAlex
- W2921879478
- Cited by
- 244
- References
- 30
- Citations by year
- 2026: 27 · 2025: 41 · 2024: 38 · 2023: 30 · 2022: 29 · 2021: 43 · 2020: 29 · 2019: 7
- FWCI
- 21.49
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion, other-oa)
- UWA Profiles and Research Repository (UWA) (submittedVersion, other-oa)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- NOAA Institutional Repository (submittedVersion, public-domain)
- Universidad de Chile (submittedVersion, cc-by-nc-nd)
- VTechWorks (Virginia Tech) (submittedVersion, public-domain)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- EC | FP7 | FP7 People: Marie-Curie Actions (702057)
- National Science Foundation (EAR1331828, DEB 1556090)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycorrhizal Fungi and Plant Interactions
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- soil biodiversity, soil formation, soil chronosequence, soil bacteria, soil fungi, soil protists, soil invertebrates, soil acidification, nutrient stoichiometry, resource availability, vegetation cover, ecosystem development
- MeSH terms
- Models, Biological, Biodiversity
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