Spatial heterogeneity in soil microbes alters outcomes of plant competition.
Identifieur interne : 001469 ( Main/Corpus ); précédent : 001468; suivant : 001470Spatial heterogeneity in soil microbes alters outcomes of plant competition.
Auteurs : Karen C. Abbott ; Justine Karst ; Lori A. Biederman ; Stuart R. Borrett ; Alan Hastings ; Vonda Walsh ; James D. BeverSource :
- PloS one [ 1932-6203 ] ; 2015.
English descriptors
- KwdEn :
- MESH :
- chemical , chemistry : Soil.
- microbiology : Plants.
- physiology : Seed Dispersal, Symbiosis.
- Ecosystem, Models, Theoretical, Mycorrhizae, Plant Development, Soil Microbiology.
Abstract
Plant species vary greatly in their responsiveness to nutritional soil mutualists, such as mycorrhizal fungi and rhizobia, and this responsiveness is associated with a trade-off in allocation to root structures for resource uptake. As a result, the outcome of plant competition can change with the density of mutualists, with microbe-responsive plant species having high competitive ability when mutualists are abundant and non-responsive plants having high competitive ability with low densities of mutualists. When responsive plant species also allow mutualists to grow to greater densities, changes in mutualist density can generate a positive feedback, reinforcing an initial advantage to either plant type. We study a model of mutualist-mediated competition to understand outcomes of plant-plant interactions within a patchy environment. We find that a microbe-responsive plant can exclude a non-responsive plant from some initial conditions, but it must do so across the landscape including in the microbe-free areas where it is a poorer competitor. Otherwise, the non-responsive plant will persist in both mutualist-free and mutualist-rich regions. We apply our general findings to two different biological scenarios: invasion of a non-responsive plant into an established microbe-responsive native population, and successional replacement of non-responders by microbe-responsive species. We find that resistance to invasion is greatest when seed dispersal by the native plant is modest and dispersal by the invader is greater. Nonetheless, a native plant that relies on microbial mutualists for competitive dominance may be particularly vulnerable to invasion because any disturbance that temporarily reduces its density or that of the mutualist creates a window for a non-responsive invader to establish dominance. We further find that the positive feedbacks from associations with beneficial soil microbes create resistance to successional turnover. Our theoretical results constitute an important first step toward developing a general understanding of the interplay between mutualism and competition in patchy landscapes, and generate qualitative predictions that may be tested in future empirical studies.
DOI: 10.1371/journal.pone.0125788
PubMed: 25946068
PubMed Central: PMC4422530
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pubmed:25946068Le document en format XML
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Biederman</name><affiliation><nlm:affiliation>Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Borrett, Stuart R" sort="Borrett, Stuart R" uniqKey="Borrett S" first="Stuart R" last="Borrett">Stuart R. Borrett</name><affiliation><nlm:affiliation>Department of Biology and Marine Biology, University of North Carolina-Wilmington, Wilmington, NC, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Hastings, Alan" sort="Hastings, Alan" uniqKey="Hastings A" first="Alan" last="Hastings">Alan Hastings</name><affiliation><nlm:affiliation>Department of Environmental Science and Policy, University of California Davis, Davis, CA, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Walsh, Vonda" sort="Walsh, Vonda" uniqKey="Walsh V" first="Vonda" last="Walsh">Vonda Walsh</name><affiliation><nlm:affiliation>Department of Applied Mathematics, Virginia Military Institute, Lexington, VA, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Bever, James D" sort="Bever, James D" uniqKey="Bever J" first="James D" last="Bever">James D. 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Abbott</name><affiliation><nlm:affiliation>Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA, United States of America; Department of Biology, Case Western Reserve University, Cleveland, OH, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Karst, Justine" sort="Karst, Justine" uniqKey="Karst J" first="Justine" last="Karst">Justine Karst</name><affiliation><nlm:affiliation>Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada.</nlm:affiliation></affiliation></author><author><name sortKey="Biederman, Lori A" sort="Biederman, Lori A" uniqKey="Biederman L" first="Lori A" last="Biederman">Lori A. Biederman</name><affiliation><nlm:affiliation>Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Borrett, Stuart R" sort="Borrett, Stuart R" uniqKey="Borrett S" first="Stuart R" last="Borrett">Stuart R. Borrett</name><affiliation><nlm:affiliation>Department of Biology and Marine Biology, University of North Carolina-Wilmington, Wilmington, NC, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Hastings, Alan" sort="Hastings, Alan" uniqKey="Hastings A" first="Alan" last="Hastings">Alan Hastings</name><affiliation><nlm:affiliation>Department of Environmental Science and Policy, University of California Davis, Davis, CA, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Walsh, Vonda" sort="Walsh, Vonda" uniqKey="Walsh V" first="Vonda" last="Walsh">Vonda Walsh</name><affiliation><nlm:affiliation>Department of Applied Mathematics, Virginia Military Institute, Lexington, VA, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Bever, James D" sort="Bever, James D" uniqKey="Bever J" first="James D" last="Bever">James D. Bever</name><affiliation><nlm:affiliation>Department of Biology, Indiana University, Bloomington, IN, United States of America.</nlm:affiliation></affiliation></author></analytic><series><title level="j">PloS one</title><idno type="eISSN">1932-6203</idno><imprint><date when="2015" type="published">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Ecosystem (MeSH)</term><term>Models, Theoretical (MeSH)</term><term>Mycorrhizae (MeSH)</term><term>Plant Development (MeSH)</term><term>Plants (microbiology)</term><term>Seed Dispersal (physiology)</term><term>Soil (chemistry)</term><term>Soil Microbiology (MeSH)</term><term>Symbiosis (physiology)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Soil</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plants</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Seed Dispersal</term><term>Symbiosis</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Ecosystem</term><term>Models, Theoretical</term><term>Mycorrhizae</term><term>Plant Development</term><term>Soil Microbiology</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plant species vary greatly in their responsiveness to nutritional soil mutualists, such as mycorrhizal fungi and rhizobia, and this responsiveness is associated with a trade-off in allocation to root structures for resource uptake. As a result, the outcome of plant competition can change with the density of mutualists, with microbe-responsive plant species having high competitive ability when mutualists are abundant and non-responsive plants having high competitive ability with low densities of mutualists. When responsive plant species also allow mutualists to grow to greater densities, changes in mutualist density can generate a positive feedback, reinforcing an initial advantage to either plant type. We study a model of mutualist-mediated competition to understand outcomes of plant-plant interactions within a patchy environment. We find that a microbe-responsive plant can exclude a non-responsive plant from some initial conditions, but it must do so across the landscape including in the microbe-free areas where it is a poorer competitor. Otherwise, the non-responsive plant will persist in both mutualist-free and mutualist-rich regions. We apply our general findings to two different biological scenarios: invasion of a non-responsive plant into an established microbe-responsive native population, and successional replacement of non-responders by microbe-responsive species. We find that resistance to invasion is greatest when seed dispersal by the native plant is modest and dispersal by the invader is greater. Nonetheless, a native plant that relies on microbial mutualists for competitive dominance may be particularly vulnerable to invasion because any disturbance that temporarily reduces its density or that of the mutualist creates a window for a non-responsive invader to establish dominance. We further find that the positive feedbacks from associations with beneficial soil microbes create resistance to successional turnover. Our theoretical results constitute an important first step toward developing a general understanding of the interplay between mutualism and competition in patchy landscapes, and generate qualitative predictions that may be tested in future empirical studies. </div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">25946068</PMID><DateCompleted><Year>2016</Year><Month>04</Month><Day>25</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1932-6203</ISSN><JournalIssue CitedMedium="Internet"><Volume>10</Volume><Issue>5</Issue><PubDate><Year>2015</Year></PubDate></JournalIssue><Title>PloS one</Title><ISOAbbreviation>PLoS One</ISOAbbreviation></Journal><ArticleTitle>Spatial heterogeneity in soil microbes alters outcomes of plant competition.</ArticleTitle><Pagination><MedlinePgn>e0125788</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pone.0125788</ELocationID><Abstract><AbstractText>Plant species vary greatly in their responsiveness to nutritional soil mutualists, such as mycorrhizal fungi and rhizobia, and this responsiveness is associated with a trade-off in allocation to root structures for resource uptake. As a result, the outcome of plant competition can change with the density of mutualists, with microbe-responsive plant species having high competitive ability when mutualists are abundant and non-responsive plants having high competitive ability with low densities of mutualists. When responsive plant species also allow mutualists to grow to greater densities, changes in mutualist density can generate a positive feedback, reinforcing an initial advantage to either plant type. We study a model of mutualist-mediated competition to understand outcomes of plant-plant interactions within a patchy environment. We find that a microbe-responsive plant can exclude a non-responsive plant from some initial conditions, but it must do so across the landscape including in the microbe-free areas where it is a poorer competitor. Otherwise, the non-responsive plant will persist in both mutualist-free and mutualist-rich regions. We apply our general findings to two different biological scenarios: invasion of a non-responsive plant into an established microbe-responsive native population, and successional replacement of non-responders by microbe-responsive species. We find that resistance to invasion is greatest when seed dispersal by the native plant is modest and dispersal by the invader is greater. Nonetheless, a native plant that relies on microbial mutualists for competitive dominance may be particularly vulnerable to invasion because any disturbance that temporarily reduces its density or that of the mutualist creates a window for a non-responsive invader to establish dominance. We further find that the positive feedbacks from associations with beneficial soil microbes create resistance to successional turnover. Our theoretical results constitute an important first step toward developing a general understanding of the interplay between mutualism and competition in patchy landscapes, and generate qualitative predictions that may be tested in future empirical studies. </AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Abbott</LastName><ForeName>Karen C</ForeName><Initials>KC</Initials><AffiliationInfo><Affiliation>Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA, United States of America; Department of Biology, Case Western Reserve University, Cleveland, OH, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Karst</LastName><ForeName>Justine</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Biederman</LastName><ForeName>Lori A</ForeName><Initials>LA</Initials><AffiliationInfo><Affiliation>Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Borrett</LastName><ForeName>Stuart R</ForeName><Initials>SR</Initials><AffiliationInfo><Affiliation>Department of Biology and Marine Biology, University of North Carolina-Wilmington, Wilmington, NC, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hastings</LastName><ForeName>Alan</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Environmental Science and Policy, University of California Davis, Davis, CA, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Walsh</LastName><ForeName>Vonda</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>Department of Applied Mathematics, Virginia Military Institute, Lexington, VA, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bever</LastName><ForeName>James D</ForeName><Initials>JD</Initials><AffiliationInfo><Affiliation>Department of Biology, Indiana University, Bloomington, IN, United States of America.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2015</Year><Month>05</Month><Day>06</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>PLoS 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