Using proxies of microbial community‐weighted means traits to explain the cascading effect of management intensity, soil and plant traits on ecosystem resilience in mountain grasslands
Trait‐based approaches provide a framework to understand the role of functional biodiversity on ecosystem functioning under global change. While plant traits have been reported as potential drivers of soil microbial community composition and resilience, studies directly assessing microbial traits ar...
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Veröffentlicht in: | The Journal of ecology 2020-05, Vol.108 (3), p.876-893 |
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creator | Piton, Gabin Legay, Nicolas Arnoldi, Cindy Lavorel, Sandra Clément, Jean-Christophe Foulquier, Arnaud Lamb, Eric |
description | Trait‐based approaches provide a framework to understand the role of functional biodiversity on ecosystem functioning under global change. While plant traits have been reported as potential drivers of soil microbial community composition and resilience, studies directly assessing microbial traits are scarce, limiting our mechanistic understanding of ecosystem functioning.
We used microbial biomass and enzyme stoichiometry, and mass‐specific enzymes activity as proxies of microbial community‐weighted mean (CWM) traits, to infer trade‐offs in microbial strategies of resource use with cascading effects on ecosystem resilience. We simulated a drought event on intact plant–soil mesocosms extracted from mountain grasslands along a management intensity gradient. Ecosystem processes and properties related to nitrogen cycling were quantified before, during and after drought to characterize ecosystem resilience.
Soil microbial CWM traits and ecosystem resilience to drought were strongly influenced by grassland type. Structural equation modelling revealed a cascading effect from management to ecosystem resilience through modifications in soil nutrients, and plant and microbial CWM traits. Overall, our results depict a shift from high investment in extracellular enzymes in nutrient‐poor soils (oligotrophic strategy), to a copiotrophic strategy with low microbial biomass N:P and low investment in extracellular enzymes associated with exploitative plant traits in nutrient‐rich soils.
Microbial CWM traits responses to management intensity were highly related to ecosystem resilience. Microbial communities with a copiotrophic strategy had lower resistance but higher recovery to drought, while microbial communities with an oligotrophic strategy showed the opposite responses. The unexpected trade‐off between plant and microbial resistance suggested that the lower resistance of copiotrophic microbial communities enabled plant resistance to drought.
Synthesis. Grassland management has cascading effects on ecosystem resilience through its combined effects on soil nutrients and plant traits propagating to microbial traits and resilience. We suggest that intensification of permanent grassland management and associated increases in soil nutrient availability decreased plant–microbe competition for N under drought through the selection of drought‐sensitive microbial communities with a copiotrophic strategy that promoted plant resistance. Including proxies of microbial CWM traits in |
doi_str_mv | 10.1111/1365-2745.13327 |
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We used microbial biomass and enzyme stoichiometry, and mass‐specific enzymes activity as proxies of microbial community‐weighted mean (CWM) traits, to infer trade‐offs in microbial strategies of resource use with cascading effects on ecosystem resilience. We simulated a drought event on intact plant–soil mesocosms extracted from mountain grasslands along a management intensity gradient. Ecosystem processes and properties related to nitrogen cycling were quantified before, during and after drought to characterize ecosystem resilience.
Soil microbial CWM traits and ecosystem resilience to drought were strongly influenced by grassland type. Structural equation modelling revealed a cascading effect from management to ecosystem resilience through modifications in soil nutrients, and plant and microbial CWM traits. Overall, our results depict a shift from high investment in extracellular enzymes in nutrient‐poor soils (oligotrophic strategy), to a copiotrophic strategy with low microbial biomass N:P and low investment in extracellular enzymes associated with exploitative plant traits in nutrient‐rich soils.
Microbial CWM traits responses to management intensity were highly related to ecosystem resilience. Microbial communities with a copiotrophic strategy had lower resistance but higher recovery to drought, while microbial communities with an oligotrophic strategy showed the opposite responses. The unexpected trade‐off between plant and microbial resistance suggested that the lower resistance of copiotrophic microbial communities enabled plant resistance to drought.
Synthesis. Grassland management has cascading effects on ecosystem resilience through its combined effects on soil nutrients and plant traits propagating to microbial traits and resilience. We suggest that intensification of permanent grassland management and associated increases in soil nutrient availability decreased plant–microbe competition for N under drought through the selection of drought‐sensitive microbial communities with a copiotrophic strategy that promoted plant resistance. Including proxies of microbial CWM traits into the functional trait framework will strengthen our understanding of soil ecosystem functioning under global change.
Using community‐level proxies of microbial traits, we identify important trade‐offs in microbial strategies along inter‐related gradients of management, soil properties and plant community traits. These underpin the cascading effects of grassland management on ecosystem resilience. Intensification of permanent grassland management with increased soil nutrient availability selects for drought‐sensitive microbial communities with growth‐oriented traits (copiotrophic strategy), promoting plant resistance.</description><identifier>ISSN: 0022-0477</identifier><identifier>EISSN: 1365-2745</identifier><identifier>DOI: 10.1111/1365-2745.13327</identifier><language>eng</language><publisher>Oxford: Blackwell Publishing Ltd</publisher><subject>Biodiversity ; Biodiversity and Ecology ; Biomass ; Cascading ; Community composition ; Computer simulation ; Drought ; Ecosystem assessment ; Ecosystem management ; Ecosystem resilience ; Ecosystems ; Environmental changes ; Environmental Sciences ; Enzymes ; Extracellular ; Extracellular enzymes ; functional traits ; Grassland management ; Grasslands ; Investment ; Management ; Mathematical models ; Mesocosms ; Microbial activity ; Microbiomes ; Microorganisms ; Mineral nutrients ; mountain grassland ; Mountains ; Multivariate statistical analysis ; Nitrogen ; Nitrogen cycle ; nitrogen cycling ; Nutrient availability ; Nutrients ; Plant communities ; Plant extracts ; Plant resistance ; Resilience ; resistance ; Soil ; Soil management ; soil microbial community ; Soil microorganisms ; Soil nutrients ; Soils ; Stoichiometry ; Strategy</subject><ispartof>The Journal of ecology, 2020-05, Vol.108 (3), p.876-893</ispartof><rights>2019 British Ecological Society</rights><rights>Journal of Ecology © 2020 British Ecological Society</rights><rights>Attribution</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3907-b0875c6a088da267946a4e36d9b80e83eed220a08d7caa46271d467a20b2a9c93</citedby><cites>FETCH-LOGICAL-c3907-b0875c6a088da267946a4e36d9b80e83eed220a08d7caa46271d467a20b2a9c93</cites><orcidid>0000-0002-2490-2602 ; 0000-0002-0841-7199 ; 0000-0002-7300-2811 ; 0000-0002-8308-5841 ; 0000-0002-6036-5787</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1365-2745.13327$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1365-2745.13327$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,777,781,882,1412,1428,27905,27906,45555,45556,46390,46814</link.rule.ids><backlink>$$Uhttps://hal.science/hal-02408942$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Lamb, Eric</contributor><creatorcontrib>Piton, Gabin</creatorcontrib><creatorcontrib>Legay, Nicolas</creatorcontrib><creatorcontrib>Arnoldi, Cindy</creatorcontrib><creatorcontrib>Lavorel, Sandra</creatorcontrib><creatorcontrib>Clément, Jean-Christophe</creatorcontrib><creatorcontrib>Foulquier, Arnaud</creatorcontrib><creatorcontrib>Lamb, Eric</creatorcontrib><title>Using proxies of microbial community‐weighted means traits to explain the cascading effect of management intensity, soil and plant traits on ecosystem resilience in mountain grasslands</title><title>The Journal of ecology</title><description>Trait‐based approaches provide a framework to understand the role of functional biodiversity on ecosystem functioning under global change. While plant traits have been reported as potential drivers of soil microbial community composition and resilience, studies directly assessing microbial traits are scarce, limiting our mechanistic understanding of ecosystem functioning.
We used microbial biomass and enzyme stoichiometry, and mass‐specific enzymes activity as proxies of microbial community‐weighted mean (CWM) traits, to infer trade‐offs in microbial strategies of resource use with cascading effects on ecosystem resilience. We simulated a drought event on intact plant–soil mesocosms extracted from mountain grasslands along a management intensity gradient. Ecosystem processes and properties related to nitrogen cycling were quantified before, during and after drought to characterize ecosystem resilience.
Soil microbial CWM traits and ecosystem resilience to drought were strongly influenced by grassland type. Structural equation modelling revealed a cascading effect from management to ecosystem resilience through modifications in soil nutrients, and plant and microbial CWM traits. Overall, our results depict a shift from high investment in extracellular enzymes in nutrient‐poor soils (oligotrophic strategy), to a copiotrophic strategy with low microbial biomass N:P and low investment in extracellular enzymes associated with exploitative plant traits in nutrient‐rich soils.
Microbial CWM traits responses to management intensity were highly related to ecosystem resilience. Microbial communities with a copiotrophic strategy had lower resistance but higher recovery to drought, while microbial communities with an oligotrophic strategy showed the opposite responses. The unexpected trade‐off between plant and microbial resistance suggested that the lower resistance of copiotrophic microbial communities enabled plant resistance to drought.
Synthesis. Grassland management has cascading effects on ecosystem resilience through its combined effects on soil nutrients and plant traits propagating to microbial traits and resilience. We suggest that intensification of permanent grassland management and associated increases in soil nutrient availability decreased plant–microbe competition for N under drought through the selection of drought‐sensitive microbial communities with a copiotrophic strategy that promoted plant resistance. Including proxies of microbial CWM traits into the functional trait framework will strengthen our understanding of soil ecosystem functioning under global change.
Using community‐level proxies of microbial traits, we identify important trade‐offs in microbial strategies along inter‐related gradients of management, soil properties and plant community traits. These underpin the cascading effects of grassland management on ecosystem resilience. Intensification of permanent grassland management with increased soil nutrient availability selects for drought‐sensitive microbial communities with growth‐oriented traits (copiotrophic strategy), promoting plant resistance.</description><subject>Biodiversity</subject><subject>Biodiversity and Ecology</subject><subject>Biomass</subject><subject>Cascading</subject><subject>Community composition</subject><subject>Computer simulation</subject><subject>Drought</subject><subject>Ecosystem assessment</subject><subject>Ecosystem management</subject><subject>Ecosystem resilience</subject><subject>Ecosystems</subject><subject>Environmental changes</subject><subject>Environmental Sciences</subject><subject>Enzymes</subject><subject>Extracellular</subject><subject>Extracellular enzymes</subject><subject>functional traits</subject><subject>Grassland management</subject><subject>Grasslands</subject><subject>Investment</subject><subject>Management</subject><subject>Mathematical models</subject><subject>Mesocosms</subject><subject>Microbial activity</subject><subject>Microbiomes</subject><subject>Microorganisms</subject><subject>Mineral nutrients</subject><subject>mountain grassland</subject><subject>Mountains</subject><subject>Multivariate statistical analysis</subject><subject>Nitrogen</subject><subject>Nitrogen cycle</subject><subject>nitrogen cycling</subject><subject>Nutrient availability</subject><subject>Nutrients</subject><subject>Plant communities</subject><subject>Plant extracts</subject><subject>Plant resistance</subject><subject>Resilience</subject><subject>resistance</subject><subject>Soil</subject><subject>Soil management</subject><subject>soil microbial community</subject><subject>Soil microorganisms</subject><subject>Soil nutrients</subject><subject>Soils</subject><subject>Stoichiometry</subject><subject>Strategy</subject><issn>0022-0477</issn><issn>1365-2745</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNqFkc9u1DAQxi0EEkvhzNUSJyTS-l_i5FitWgpaiQs9W7P2ZNdVYi-xl3ZvPALPw-PwJDhN1Su-jDTzfb-x5iPkPWfnvLwLLpu6ElrV51xKoV-Q1XPnJVkxJkTFlNavyZuU7hhjja7Zivy5TT7s6GGKDx4TjT0dvZ3i1sNAbRzHY_D59PfX73v0u31GR0eEkGiewOdSIsWHwwA-0LxHaiFZcDMP-x5tfsRBgB2OGDL1IWNIhfeJpugHCsHRYi6TJ1wMFG1Mp5RxpBMmP3gMFouRjvEY8rxnN0FKxeTSW_KqhyHhu6d6Rm6vr76vb6rNt89f1pebysqO6WrLWl3bBljbOhCN7lQDCmXjum3LsJWITghWxk5bANUIzZ1qNAi2FdDZTp6Rjwt3D4M5TH6E6WQieHNzuTFzjwnF2k6Jn7xoPyzactAfR0zZ3MXjFMr3jJAdb5XmciZeLKpy6ZQm7J-xnJk5TDNHZ-bozGOYxVEvjns_4Ol_cvP1ar34_gHVJqWr</recordid><startdate>202005</startdate><enddate>202005</enddate><creator>Piton, Gabin</creator><creator>Legay, Nicolas</creator><creator>Arnoldi, Cindy</creator><creator>Lavorel, Sandra</creator><creator>Clément, Jean-Christophe</creator><creator>Foulquier, Arnaud</creator><creator>Lamb, Eric</creator><general>Blackwell Publishing Ltd</general><general>Wiley</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-2490-2602</orcidid><orcidid>https://orcid.org/0000-0002-0841-7199</orcidid><orcidid>https://orcid.org/0000-0002-7300-2811</orcidid><orcidid>https://orcid.org/0000-0002-8308-5841</orcidid><orcidid>https://orcid.org/0000-0002-6036-5787</orcidid></search><sort><creationdate>202005</creationdate><title>Using proxies of microbial community‐weighted means traits to explain the cascading effect of management intensity, soil and plant traits on ecosystem resilience in mountain grasslands</title><author>Piton, Gabin ; Legay, Nicolas ; Arnoldi, Cindy ; Lavorel, Sandra ; Clément, Jean-Christophe ; Foulquier, Arnaud ; Lamb, Eric</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3907-b0875c6a088da267946a4e36d9b80e83eed220a08d7caa46271d467a20b2a9c93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Biodiversity</topic><topic>Biodiversity and Ecology</topic><topic>Biomass</topic><topic>Cascading</topic><topic>Community composition</topic><topic>Computer simulation</topic><topic>Drought</topic><topic>Ecosystem assessment</topic><topic>Ecosystem management</topic><topic>Ecosystem resilience</topic><topic>Ecosystems</topic><topic>Environmental changes</topic><topic>Environmental Sciences</topic><topic>Enzymes</topic><topic>Extracellular</topic><topic>Extracellular enzymes</topic><topic>functional traits</topic><topic>Grassland management</topic><topic>Grasslands</topic><topic>Investment</topic><topic>Management</topic><topic>Mathematical models</topic><topic>Mesocosms</topic><topic>Microbial activity</topic><topic>Microbiomes</topic><topic>Microorganisms</topic><topic>Mineral nutrients</topic><topic>mountain grassland</topic><topic>Mountains</topic><topic>Multivariate statistical analysis</topic><topic>Nitrogen</topic><topic>Nitrogen cycle</topic><topic>nitrogen cycling</topic><topic>Nutrient availability</topic><topic>Nutrients</topic><topic>Plant communities</topic><topic>Plant extracts</topic><topic>Plant resistance</topic><topic>Resilience</topic><topic>resistance</topic><topic>Soil</topic><topic>Soil management</topic><topic>soil microbial community</topic><topic>Soil microorganisms</topic><topic>Soil nutrients</topic><topic>Soils</topic><topic>Stoichiometry</topic><topic>Strategy</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Piton, Gabin</creatorcontrib><creatorcontrib>Legay, Nicolas</creatorcontrib><creatorcontrib>Arnoldi, Cindy</creatorcontrib><creatorcontrib>Lavorel, Sandra</creatorcontrib><creatorcontrib>Clément, Jean-Christophe</creatorcontrib><creatorcontrib>Foulquier, Arnaud</creatorcontrib><creatorcontrib>Lamb, Eric</creatorcontrib><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>The Journal of ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Piton, Gabin</au><au>Legay, Nicolas</au><au>Arnoldi, Cindy</au><au>Lavorel, Sandra</au><au>Clément, Jean-Christophe</au><au>Foulquier, Arnaud</au><au>Lamb, Eric</au><au>Lamb, Eric</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Using proxies of microbial community‐weighted means traits to explain the cascading effect of management intensity, soil and plant traits on ecosystem resilience in mountain grasslands</atitle><jtitle>The Journal of ecology</jtitle><date>2020-05</date><risdate>2020</risdate><volume>108</volume><issue>3</issue><spage>876</spage><epage>893</epage><pages>876-893</pages><issn>0022-0477</issn><eissn>1365-2745</eissn><abstract>Trait‐based approaches provide a framework to understand the role of functional biodiversity on ecosystem functioning under global change. While plant traits have been reported as potential drivers of soil microbial community composition and resilience, studies directly assessing microbial traits are scarce, limiting our mechanistic understanding of ecosystem functioning.
We used microbial biomass and enzyme stoichiometry, and mass‐specific enzymes activity as proxies of microbial community‐weighted mean (CWM) traits, to infer trade‐offs in microbial strategies of resource use with cascading effects on ecosystem resilience. We simulated a drought event on intact plant–soil mesocosms extracted from mountain grasslands along a management intensity gradient. Ecosystem processes and properties related to nitrogen cycling were quantified before, during and after drought to characterize ecosystem resilience.
Soil microbial CWM traits and ecosystem resilience to drought were strongly influenced by grassland type. Structural equation modelling revealed a cascading effect from management to ecosystem resilience through modifications in soil nutrients, and plant and microbial CWM traits. Overall, our results depict a shift from high investment in extracellular enzymes in nutrient‐poor soils (oligotrophic strategy), to a copiotrophic strategy with low microbial biomass N:P and low investment in extracellular enzymes associated with exploitative plant traits in nutrient‐rich soils.
Microbial CWM traits responses to management intensity were highly related to ecosystem resilience. Microbial communities with a copiotrophic strategy had lower resistance but higher recovery to drought, while microbial communities with an oligotrophic strategy showed the opposite responses. The unexpected trade‐off between plant and microbial resistance suggested that the lower resistance of copiotrophic microbial communities enabled plant resistance to drought.
Synthesis. Grassland management has cascading effects on ecosystem resilience through its combined effects on soil nutrients and plant traits propagating to microbial traits and resilience. We suggest that intensification of permanent grassland management and associated increases in soil nutrient availability decreased plant–microbe competition for N under drought through the selection of drought‐sensitive microbial communities with a copiotrophic strategy that promoted plant resistance. Including proxies of microbial CWM traits into the functional trait framework will strengthen our understanding of soil ecosystem functioning under global change.
Using community‐level proxies of microbial traits, we identify important trade‐offs in microbial strategies along inter‐related gradients of management, soil properties and plant community traits. These underpin the cascading effects of grassland management on ecosystem resilience. Intensification of permanent grassland management with increased soil nutrient availability selects for drought‐sensitive microbial communities with growth‐oriented traits (copiotrophic strategy), promoting plant resistance.</abstract><cop>Oxford</cop><pub>Blackwell Publishing Ltd</pub><doi>10.1111/1365-2745.13327</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-2490-2602</orcidid><orcidid>https://orcid.org/0000-0002-0841-7199</orcidid><orcidid>https://orcid.org/0000-0002-7300-2811</orcidid><orcidid>https://orcid.org/0000-0002-8308-5841</orcidid><orcidid>https://orcid.org/0000-0002-6036-5787</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Biodiversity Biodiversity and Ecology Biomass Cascading Community composition Computer simulation Drought Ecosystem assessment Ecosystem management Ecosystem resilience Ecosystems Environmental changes Environmental Sciences Enzymes Extracellular Extracellular enzymes functional traits Grassland management Grasslands Investment Management Mathematical models Mesocosms Microbial activity Microbiomes Microorganisms Mineral nutrients mountain grassland Mountains Multivariate statistical analysis Nitrogen Nitrogen cycle nitrogen cycling Nutrient availability Nutrients Plant communities Plant extracts Plant resistance Resilience resistance Soil Soil management soil microbial community Soil microorganisms Soil nutrients Soils Stoichiometry Strategy |
title | Using proxies of microbial community‐weighted means traits to explain the cascading effect of management intensity, soil and plant traits on ecosystem resilience in mountain grasslands |
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