Biodiversity loss disrupts seasonal carbon dynamics in a species-rich temperate grassland

. 2025 May ; 106 (5) : e70091.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40342156

Grantová podpora
23-07087S Grantová Agentura České Republiky
RVO 67985939 Czech Academy of Sciences

Biodiversity loss poses a significant threat to ecosystem functioning. However, much of the empirical evidence for these effects is based on artificial experiments that often fail to simulate the structure of natural communities. Hence, it is still unclear whether natural diversity losses would significantly affect the functioning of "real-world" ecosystems. As subordinate and rare species constitute most of the diversity in natural communities and are often more vulnerable to local extinction, we evaluated their contribution to ecosystem functioning in a naturally species-rich grassland. We focused on two mechanisms by which they can support ecosystem functions: redundancy and complementarity. We conducted two long-term field experiments (>6 years) simulating contrasting biodiversity loss scenarios through the manual removal of plant species and measured the consequences of species loss on various ecosystem functions related to carbon dynamics. The latter were examined seasonally to explore diversity effects outside the typical peak of vegetation. We found that dominant removal led to substantial reductions in aboveground phytomass and litter production and altered the annual carbon fixation capacity of the vegetation, highlighting the pivotal role of dominant species in driving ecosystem functioning. Despite high species diversity, other species could not fully compensate for the loss of a single dominant even after more than 25 years, challenging assumptions about redundancy. Complementarity effects were not detected at the peak of vegetation but were evident in early spring and autumn when subordinate and rare species enhanced ecosystem functions. Surprisingly, belowground phytomass, soil organic carbon content, and litter decomposition were unaffected by species removal, suggesting complex interactions in belowground processes. These findings underscore the importance of dominant species in maintaining ecosystem functioning and emphasize the need for nuanced approaches to studying biodiversity loss in real-world communities. Comprehensive seasonal measurements are essential for accurately discerning the effects of biodiversity on ecosystem dynamics and informing effective conservation strategies that maintain ecosystem functioning.

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Avolio, M. L. , Forrestel E. J., Chang C. C., La Pierre K. J., Burghardt K. T., and Smith M. D.. 2019. “Demystifying Dominant Species.” New Phytologist 223: 1106–1126. PubMed

Bai, Y. , and Cotrufo M. F.. 2022. “Grassland Soil Carbon Sequestration: Current Understanding, Challenges, and Solutions.” Science 377: 603–608. PubMed

Barry, K. E. , Mommer L., van Ruijven J., Wirth C., Wright A. J., Bai Y., Connolly J., et al. 2019. “The Future of Complementarity: Disentangling Causes from Consequences.” Trends in Ecology & Evolution 34: 167–180. PubMed

Bates, D. , Mächler M., Bolker B., and Walker S.. 2015. “Fitting Linear Mixed‐Effects Models Using lme4.” Journal of Statistical Software 67: 1–48.

Cardinale, B. J. , Duffy J. E., Gonzalez A., Hooper D. U., Perrings C., Venail P., Narwani A., et al. 2012. “Biodiversity Loss and its Impact on Humanity.” Nature 486: 59–67. PubMed

Cardinale, B. J. , Wright J. P., Cadotte M. W., Carroll I. T., Hector A., Srivastava D. S., Loreau M., and Weis J. J.. 2007. “Impacts of Plant Diversity on Biomass Production Increase through Time because of Species Complementarity.” Proceedings of the National Academy of Sciences of the United States of America 104: 18123–18128. PubMed PMC

Catovsky, S. , Bradford M. A., and Hector A.. 2002. “Biodiversity and Ecosystem Productivity: Implications for Carbon Storage.” Oikos 97: 443–448.

Chen, C. , Chen H. Y. H., Chen X., and Huang Z.. 2019. “Meta‐Analysis Shows Positive Effects of Plant Diversity on Microbial Biomass and Respiration.” Nature Communications 10: 1332. PubMed PMC

Chen, S. , Wang W., Xu W., Wang Y., Wan H., Chen D., Tang Z., et al. 2018. “Plant Diversity Enhances Productivity and Soil Carbon Storage.” Proceedings of the National Academy of Sciences of the United States of America 115: 4027–4032. PubMed PMC

Chen, X. , Chen H. Y. H., Chen C., Ma Z., Searle E. B., Yu Z., and Huang Z.. 2020. “Effects of Plant Diversity on Soil Carbon in Diverse Ecosystems: A Global Meta‐Analysis.” Biological Reviews 95: 167–183. PubMed

De Deyn, G. B. , Shiel R. S., Ostle N. J., McNamara N. P., Oakley S., Young I., Freeman C., Fenner N., Quirk H., and Bardgett R. D.. 2011. “Additional Carbon Sequestration Benefits of Grassland Diversity Restoration.” Journal of Applied Ecology 48: 600–608.

Dee, L. E. , Cowles J., Isbell F., Pau S., Gaines S. D., and Reich P. B.. 2019. “When Do Ecosystem Services Depend on Rare Species?” Trends in Ecology & Evolution 34: 746–758. PubMed

Díaz, S. , Symstad A. J., Chapin F. S., Wardle D. A., and Huenneke L. F.. 2003. “Functional Diversity Revealed by Removal Experiments.” Trends in Ecology & Evolution 18: 140–146.

Dietrich, P. , Ebeling A., Meyer S. T., Asato A. E. B., Bröcher M., Gleixner G., Huang Y., et al. 2024. “Plant Diversity and Community Age Stabilize Ecosystem Multifunctionality.” Global Change Biology 30: e17225. PubMed

Doležal, J. , Lanta V., Mudrák O., and Lepš J.. 2019. “Seasonality Promotes Grassland Diversity: Interactions with Mowing, Fertilization and Removal of Dominant Species.” Journal of Ecology 107: 203–215.

Dooley, Á. , Isbell F., Kirwan L., Connolly J., Finn J. A., and Brophy C.. 2015. “Testing the Effects of Diversity on Ecosystem Multifunctionality Using a Multivariate Model.” Ecology Letters 18: 1242–1251.

Duffy, J. E. 2009. “Why Biodiversity Is Important to the Functioning of Real‐World Ecosystems.” Frontiers in Ecology and the Environment 7: 437–444.

Fitter, A. H. 1986. “Spatial and Temporal Patterns of Root Activity in a Species‐Rich Alluvial Grassland.” Oecologia 69: 594–599. PubMed

Fornara, D. A. , and Tilman D.. 2008. “Plant Functional Composition Influences Rates of Soil Carbon and Nitrogen Accumulation.” Journal of Ecology 96: 314–322.

Fox, J. , and Weisberg S.. 2018. An R Companion to Applied Regression. Thousand Oaks CA: SAGE Publications.

Freitag, M. , Hölzel N., Neuenkamp L., van der Plas F., Manning P., Abrahão A., Bergmann J., et al. 2023. “Increasing Plant Species Richness by Seeding Has Marginal Effects on Ecosystem Functioning in Agricultural Grasslands.” Journal of Ecology 111: 1968–1984.

Genung, M. A. , Fox J., and Winfree R.. 2020. “Species Loss Drives Ecosystem Function in Experiments, but in Nature the Importance of Species Loss Depends on Dominance.” Global Ecology and Biogeography 29: 1531–1541.

Gracia, C. , Lisner A., Applová M., Chondol T., Dolejšek V., Janíková E., Karpate Y., et al. 2025. “Plant Diversity Loss Has Limited Effects on Below‐Ground Biomass and Traits but Alters Community Short‐Term Root Production in a Species‐Rich Grassland.” Journal of Ecology 113: 662–671.

Grime, J. P. 1998. “Benefits of Plant Diversity to Ecosystems: Immediate, Filter and Founder Effects.” Journal of Ecology 86: 902–910.

Guo, C. , Cornelissen J. H. C., Tuo B., Ci H., and Yan E.‐R.. 2020. “Non‐Negligible Contribution of Subordinates in Community‐Level Litter Decomposition: Deciduous Trees in an Evergreen World.” Journal of Ecology 108: 1713–1724.

Habel, J. C. , Dengler J., Janišová M., Török P., Wellstein C., and Wiezik M.. 2013. “European Grassland Ecosystems: Threatened Hotspots of Biodiversity.” Biodiversity and Conservation 22: 2131–2138.

Hagan, J. G. , Vanschoenwinkel B., and Gamfeldt L.. 2021. “We Should Not Necessarily Expect Positive Relationships between Biodiversity and Ecosystem Functioning in Observational Field Data.” Ecology Letters 24: 2537–2548. PubMed

Hector, A. , and Bagchi R.. 2007. “Biodiversity and Ecosystem Multifunctionality.” Nature 448: 188–190. PubMed

Hector, A. , Hautier Y., Saner P., Wacker L., Bagchi R., Joshi J., Scherer‐Lorenzen M., et al. 2010. “General Stabilizing Effects of Plant Diversity on Grassland Productivity through Population Asynchrony and Overyielding.” Ecology 91: 2213–2220. PubMed

Hector, A. , Schmid B., Beierkuhnlein C., Caldeira M. C., Diemer M., Dimitrakopoulos P. G., Finn J. A., et al. 1999. “Plant Diversity and Productivity Experiments in European Grasslands.” Science 286: 1123–1127. PubMed

Hernández, D. L. , Antia A., and McKone M. J.. 2022. “The Ecosystem Impacts of Dominant Species Exclusion in a Prairie Restoration.” Ecological Applications 32: e2592. PubMed

Hooper, D. U. , and Vitousek P. M.. 1998. “Effects of Plant Composition and Diversity on Nutrient Cycling.” Ecological Monographs 68: 121–149.

Hothorn, T. , Bretz F., and Westfall P.. 2008. “Simultaneous Inference in General Parametric Models.” Biometrical Journal 50: 346–363. PubMed

Isbell, F. , Calcagno V., Hector A., Connolly J., Harpole W. S., Reich P. B., Scherer‐Lorenzen M., et al. 2011. “High Plant Diversity Is Needed to Maintain Ecosystem Services.” Nature 477: 199–202. PubMed

Jochum, M. , Fischer M., Isbell F., Roscher C., van der Plas F., Boch S., Boenisch G., et al. 2020. “The Results of Biodiversity–Ecosystem Functioning Experiments Are Realistic.” Nature Ecology & Evolution 4: 1–10. PubMed

Kazakou, E. , Bumb I., and Garnier E.. 2022. “Species Dominance Rather than Complementarity Drives Community Digestibility and Litter Decomposition in Species‐Rich Mediterranean Rangelands.” Applied Vegetation Science 25: e12685.

Keuskamp, J. A. , Dingemans B. J. J., Lehtinen T., Sarneel J. M., and Hefting M. M.. 2013. “Tea Bag Index: A Novel Approach to Collect Uniform Decomposition Data across Ecosystems.” Methods in Ecology and Evolution 4: 1070–1075.

Klopf, R. P. , Baer S. G., Bach E. M., and Six J.. 2017. “Restoration and Management for Plant Diversity Enhances the Rate of Belowground Ecosystem Recovery.” Ecological Applications 27: 355–362. PubMed

Kotas, P. , Choma M., Šantrůčková H., Lepš J., Tříska J., and Kaštovská E.. 2017. “Linking above‐ and Belowground Responses to 16 Years of Fertilization, Mowing, and Removal of the Dominant Species in a Temperate Grassland.” Ecosystems 20: 354–367.

Lange, M. , Eisenhauer N., Chen H., and Gleixner G.. 2023. “Increased Soil Carbon Storage through Plant Diversity Strengthens with Time and Extends into the Subsoil.” Global Change Biology 29: 2627–2639. PubMed

Lange, M. , Eisenhauer N., Sierra C. A., Bessler H., Engels C., Griffiths R. I., Mellado‐Vázquez P. G., et al. 2015. “Plant Diversity Increases Soil Microbial Activity and Soil Carbon Storage.” Nature Communications 6: 1–8. PubMed

Leitão, R. P. , Zuanon J., Villéger S., Williams S. E., Baraloto C., Fortunel C., Mendonça F. P., and Mouillot D.. 2016. “Rare Species Contribute Disproportionately to the Functional Structure of Species Assemblages.” Proceedings of the Royal Society B: Biological Sciences 283: 20160084. PubMed PMC

Lepš, J. 2004. “What Do the Biodiversity Experiments Tell us about Consequences of Plant Species Loss in the Real World?” Basic and Applied Ecology 5: 529–534.

Lepš, J. , Májeková M., Vítová A., Doležal J., and De Bello F.. 2018. “Stabilizing Effects in Temporal Fluctuations: Management, Traits, and Species Richness in High‐Diversity Communities.” Ecology 99: 360–371. PubMed

Lisner, A. , Konečná M., Blažek P., and Lepš J.. 2023. “Community Biomass Is Driven by Dominants and Their Characteristics – The Insight from a Field Biodiversity Experiment with Realistic Species Loss Scenario.” Journal of Ecology 111: 240–250.

Lisner, A. , Segrestin J., Konečná M., Blažek P., Janíková E., Applová M., Švancárová T., and Lepš J.. 2024. “Why Are Plant Communities Stable? Disentangling the Role of Dominance, Asynchrony and Averaging Effect Following Realistic Species Loss Scenario.” Journal of Ecology 112: 1832–1841.

Loreau, M. , Naeem S., Inchausti P., Bengtsson J., Grime J. P., Hector A., Hooper D. U., et al. 2001. “Biodiversity and Ecosystem Functioning: Current Knowledge and Future Challenges.” Science 294: 804–808. PubMed

Lyons, K. G. , Brigham C. A., Traut B. H., and Schwartz M. W.. 2005. “Rare Species and Ecosystem Functioning.” Conservation Biology 19(4): 1019–1024. 10.1111/j.1523-1739.2005.00106.x. DOI

Lyons, K. G. , and Schwartz M. W.. 2001. “Rare Species Loss Alters Ecosystem Function – Invasion Resistance.” Ecology Letters 4: 358–365.

Maestre, F. T. , Quero J. L., Gotelli N. J., Escudero A., Ochoa V., Delgado‐Baquerizo M., García‐Gómez M., et al. 2012. “Plant Species Richness and Ecosystem Multifunctionality in Global Drylands.” Science 335: 214–218. PubMed PMC

Mariotte, P. 2014. “Do Subordinate Species Punch above Their Weight? Evidence from Above‐ and Below‐Ground.” The New Phytologist 203: 16–21. PubMed

Mariotte, P. , Vandenberghe C., Meugnier C., Rossi P., Bardgett R. D., and Buttler A.. 2013. “Subordinate Plant Species Impact on Soil Microbial Communities and Ecosystem Functioning in Grasslands: Findings from a Removal Experiment.” Perspectives in Plant Ecology, Evolution and Systematics 15: 77–85.

Mouillot, D. , Bellwood D. R., Baraloto C., Chave J., Galzin R., Harmelin‐Vivien M., Kulbicki M., et al. 2013. “Rare Species Support Vulnerable Functions in High‐Diversity Ecosystems.” PLoS Biology 11: e1001569. PubMed PMC

Munson, S. M. , and Lauenroth W. K.. 2009. “Plant Population and Community Responses to Removal of Dominant Species in the Shortgrass Steppe.” Journal of Vegetation Science 20: 224–232.

Pan, Q. , Tian D., Naeem S., Auerswald K., Elser J. J., Bai Y., Huang J., et al. 2016. “Effects of Functional Diversity Loss on Ecosystem Functions Are Influenced by Compensation.” Ecology 97: 2293–2302. PubMed

Pinder, J. E., III . 1975. “Effects of Species Removal on an Old‐Field Plant Community.” Ecology 56: 747–751.

Pornon, A. , Escaravage N., and Lamaze T.. 2007. “Complementarity in Mineral Nitrogen Use among Dominant Plant Species in a Subalpine Community.” American Journal of Botany 94: 1778–1785. PubMed

Prommer, J. , Walker T. W. N., Wanek W., Braun J., Zezula D., Hu Y., Hofhansl F., and Richter A.. 2020. “Increased Microbial Growth, Biomass, and Turnover Drive Soil Organic Carbon Accumulation at Higher Plant Diversity.” Global Change Biology 26: 669–681. PubMed PMC

R Core Team . 2020. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

Ravenek, J. M. , Bessler H., Engels C., Scherer‐Lorenzen M., Gessler A., Gockele A., De Luca E., et al. 2014. “Long‐Term Study of Root Biomass in a Biodiversity Experiment Reveals Shifts in Diversity Effects over Time.” Oikos 123: 1528–1536.

Sasaki, T. , Yoshihara Y., Takahashi M., Byambatsetseg L., Futahashi R., Nyambayar D., and Suyama Y.. 2017. “Differential Responses and Mechanisms of Productivity Following Experimental Species Loss Scenarios.” Oecologia 183: 785–795. PubMed

Segrestin, J. , Lisner A., and Lepš J.. 2025. “Data from: Biodiversity Loss Disrupts Seasonal Carbon Dynamics in a Species‐Rich Temperate Grassland.” Zenodo. 10.5281/zenodo.14967638. DOI

Smith, M. D. , and Knapp A. K.. 2003. “Dominant Species Maintain Ecosystem Function with Non‐Random Species Loss.” Ecology Letters 6: 509–517.

Smith, M. D. , Koerner S. E., Knapp A. K., Avolio M. L., Chaves F. A., Denton E. M., Dietrich J., et al. 2020. “Mass Ratio Effects Underlie Ecosystem Responses to Environmental Change.” Journal of Ecology 108: 855–864.

Spohn, M. , Bagchi S., Biederman L. A., Borer E. T., Bråthen K. A., Bugalho M. N., Caldeira M. C., et al. 2023. “The Positive Effect of Plant Diversity on Soil Carbon Depends on Climate.” Nature Communications 14(1): 6624. 10.1038/s41467-023-42340-0. PubMed DOI PMC

Steinbeiss, S. , Beßler H., Engels C., Temperton V. M., Buchmann N., Roscher C., Kreutziger Y., Baade J., Habekost M., and Gleixner G.. 2008. “Plant Diversity Positively Affects Short‐Term Soil Carbon Storage in Experimental Grasslands.” Global Change Biology 14: 2937–2949.

Stevens, M. H. H. , and Carson W. P.. 2001. “Phenological Complementarity, Species Diversity, and Ecosystem Function.” Oikos 92: 291–296.

Theodose, T. A. , Jaeger C. H., Bowman W. D., and Schardt J. C.. 1996. “Uptake and Allocation of 15N in Alpine Plants: Implications for the Importance of Competitive Ability in Predicting Community Structure in a Stressful Environment.” Oikos 75: 59–66.

Tilman, D. , Isbell F., and Cowles J. M.. 2014. “Biodiversity and Ecosystem Functioning.” Annual Review of Ecology, Evolution, and Systematics 45: 471–493.

Tilman, D. , Reich P. B., Knops J., Wedin D., Mielke T., and Lehman C.. 2001. “Diversity and Productivity in a Long‐Term Grassland Experiment.” Science 294: 843–845. PubMed

Valencia, E. , Maestre F. T., Le Bagousse‐Pinguet Y., Quero J. L., Tamme R., Börger L., García‐Gómez M., and Gross N.. 2015. “Functional Diversity Enhances the Resistance of Ecosystem Multifunctionality to Aridity in Mediterranean Drylands.” New Phytologist 206: 660–671. PubMed PMC

van der Plas, F. 2019. “Biodiversity and Ecosystem Functioning in Naturally Assembled Communities.” Biological Reviews 94: 1220–1245. PubMed

Wagg, C. , Bender S. F., Widmer F., and van der Heijden M. G. A.. 2014. “Soil Biodiversity and Soil Community Composition Determine Ecosystem Multifunctionality.” Proceedings of the National Academy of Sciences of the United States of America 111: 5266–5270. PubMed PMC

Walker, B. , Kinzig A., and Langridge J.. 1999. “Plant Attribute Diversity, Resilience, and Ecosystem Function: The Nature and Significance of Dominant and Minor Species.” Ecosystems 2: 95–113.

Wardle, D. A. 2016. “Do Experiments Exploring Plant Diversity–Ecosystem Functioning Relationships Inform how Biodiversity Loss Impacts Natural Ecosystems?” Journal of Vegetation Science 27: 646–653.

Weisser, W. W. , Roscher C., Meyer S. T., Ebeling A., Luo G., Allan E., Beßler H., et al. 2017. “Biodiversity Effects on Ecosystem Functioning in a 15‐Year Grassland Experiment: Patterns, Mechanisms, and Open Questions.” Basic and Applied Ecology 23: 1–73.

Yachi, S. , and Loreau M.. 1999. “Biodiversity and Ecosystem Productivity in a Fluctuating Environment: The Insurance Hypothesis.” Proceedings of the National Academy of Sciences of the United States of America 96: 1463–1468. PubMed PMC

Yang, Y. , Tilman D., Furey G., and Lehman C.. 2019. “Soil Carbon Sequestration Accelerated by Restoration of Grassland Biodiversity.” Nature Communications 10: 718. PubMed PMC

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