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Phylogeny determines the role of helminth parasites in intertidal food webs
Parasites affect interactions among species in food webs and should be considered in any analysis of the structure, dynamics or resilience of trophic networks. However, the roles of individual parasite species, such as their importance as connectors within the network, and what factors determine the...
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Published in: | The Journal of animal ecology 2013-11, Vol.82 (6), p.1265-1275 |
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description | Parasites affect interactions among species in food webs and should be considered in any analysis of the structure, dynamics or resilience of trophic networks. However, the roles of individual parasite species, such as their importance as connectors within the network, and what factors determine these roles, are yet to be investigated. Here, we test the hypotheses that the species roles of trematode, cestode and nematode parasites in aquatic food webs are influenced by the type of definitive host they use, and also determined by their phylogenetic affiliations. We quantified the network role of 189 helminth species from six highly resolved intertidal food webs. We focused on four measures of centrality (node degree, closeness centrality, betweenness centrality and eigenvalue centrality), which characterize each parasite's position within the web, and on relative connectedness of a parasite species to taxa in its own module vs. other modules of the web (within‐module degree and participation coefficient). All six food webs displayed a significant modular structure, that is, they consisted of subsets of species interacting mostly with each other and less with species from other subsets. We demonstrated that the parasites themselves are not generating this modularity, though they contribute to intermodule connectivity. Mixed‐effects models revealed only a modest influence of the type of definitive host used (bird or fish) and of the web of origin on the different measures of parasite species roles. In contrast, the taxonomic affiliations of the parasites, included in the models as nested random factors, accounted for 37–93% of the total variance, depending on the measure of species role. Our findings indicate that parasites are important intermodule connectors and thus contribute to web cohesion. We also uncover a very strong phylogenetic signal in parasite species roles, suggesting that the role of any parasite species in a food web, including new invasive species, is to some extent predictable based solely on its taxonomic affiliations. |
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However, the roles of individual parasite species, such as their importance as connectors within the network, and what factors determine these roles, are yet to be investigated. Here, we test the hypotheses that the species roles of trematode, cestode and nematode parasites in aquatic food webs are influenced by the type of definitive host they use, and also determined by their phylogenetic affiliations. We quantified the network role of 189 helminth species from six highly resolved intertidal food webs. We focused on four measures of centrality (node degree, closeness centrality, betweenness centrality and eigenvalue centrality), which characterize each parasite's position within the web, and on relative connectedness of a parasite species to taxa in its own module vs. other modules of the web (within‐module degree and participation coefficient). All six food webs displayed a significant modular structure, that is, they consisted of subsets of species interacting mostly with each other and less with species from other subsets. We demonstrated that the parasites themselves are not generating this modularity, though they contribute to intermodule connectivity. Mixed‐effects models revealed only a modest influence of the type of definitive host used (bird or fish) and of the web of origin on the different measures of parasite species roles. In contrast, the taxonomic affiliations of the parasites, included in the models as nested random factors, accounted for 37–93% of the total variance, depending on the measure of species role. Our findings indicate that parasites are important intermodule connectors and thus contribute to web cohesion. We also uncover a very strong phylogenetic signal in parasite species roles, suggesting that the role of any parasite species in a food web, including new invasive species, is to some extent predictable based solely on its taxonomic affiliations.</description><identifier>ISSN: 0021-8790</identifier><identifier>EISSN: 1365-2656</identifier><identifier>DOI: 10.1111/1365-2656.12101</identifier><identifier>PMID: 23800281</identifier><identifier>CODEN: JAECAP</identifier><language>eng</language><publisher>Oxford: Blackwell Publishing</publisher><subject>Animal and plant ecology ; Animal ecology ; Animal, plant and microbial ecology ; Animals ; aquatic food webs ; Biological and medical sciences ; Biological taxonomies ; birds ; Birds - parasitology ; Cestoda ; Cestoda - physiology ; cohesion ; connectedness ; fish ; Fishes - parasitology ; Food Chain ; Food chains ; Food webs ; Fundamental and applied biological sciences. Psychology ; General aspects ; helminths ; Helminths - physiology ; Host-Parasite Interactions ; invasive species ; Invertebrates ; Marine ; Marine ecology ; Models, Biological ; Modularity ; Nemathelminthia. Plathelmintha ; Nematoda ; Nematoda - physiology ; network centrality ; Parasite and disease ecology ; Parasite hosts ; Parasites ; phylogenetic signal ; Phylogenetics ; Phylogeny ; Species ; Taxa ; Trematoda ; Trematoda - physiology ; trematodes ; variance</subject><ispartof>The Journal of animal ecology, 2013-11, Vol.82 (6), p.1265-1275</ispartof><rights>2013 British Ecological Society</rights><rights>2013 The Authors. Journal of Animal Ecology © 2013 British Ecological Society</rights><rights>2014 INIST-CNRS</rights><rights>2013 The Authors. Journal of Animal Ecology © 2013 British Ecological Society.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5881-99b9c2248abcf1197f4f10ecad346f07629cb7cdbaca3c4933c2f85cf285ac203</citedby><cites>FETCH-LOGICAL-c5881-99b9c2248abcf1197f4f10ecad346f07629cb7cdbaca3c4933c2f85cf285ac203</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/24034919$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/24034919$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27888131$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23800281$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Montgomery, Ian</contributor><creatorcontrib>Poulin, Robert</creatorcontrib><creatorcontrib>Krasnov, Boris R</creatorcontrib><creatorcontrib>Pilosof, Shai</creatorcontrib><creatorcontrib>Thieltges, David W</creatorcontrib><creatorcontrib>Montgomery, Ian</creatorcontrib><title>Phylogeny determines the role of helminth parasites in intertidal food webs</title><title>The Journal of animal ecology</title><addtitle>J Anim Ecol</addtitle><description>Parasites affect interactions among species in food webs and should be considered in any analysis of the structure, dynamics or resilience of trophic networks. However, the roles of individual parasite species, such as their importance as connectors within the network, and what factors determine these roles, are yet to be investigated. Here, we test the hypotheses that the species roles of trematode, cestode and nematode parasites in aquatic food webs are influenced by the type of definitive host they use, and also determined by their phylogenetic affiliations. We quantified the network role of 189 helminth species from six highly resolved intertidal food webs. We focused on four measures of centrality (node degree, closeness centrality, betweenness centrality and eigenvalue centrality), which characterize each parasite's position within the web, and on relative connectedness of a parasite species to taxa in its own module vs. other modules of the web (within‐module degree and participation coefficient). All six food webs displayed a significant modular structure, that is, they consisted of subsets of species interacting mostly with each other and less with species from other subsets. We demonstrated that the parasites themselves are not generating this modularity, though they contribute to intermodule connectivity. Mixed‐effects models revealed only a modest influence of the type of definitive host used (bird or fish) and of the web of origin on the different measures of parasite species roles. In contrast, the taxonomic affiliations of the parasites, included in the models as nested random factors, accounted for 37–93% of the total variance, depending on the measure of species role. Our findings indicate that parasites are important intermodule connectors and thus contribute to web cohesion. We also uncover a very strong phylogenetic signal in parasite species roles, suggesting that the role of any parasite species in a food web, including new invasive species, is to some extent predictable based solely on its taxonomic affiliations.</description><subject>Animal and plant ecology</subject><subject>Animal ecology</subject><subject>Animal, plant and microbial ecology</subject><subject>Animals</subject><subject>aquatic food webs</subject><subject>Biological and medical sciences</subject><subject>Biological taxonomies</subject><subject>birds</subject><subject>Birds - parasitology</subject><subject>Cestoda</subject><subject>Cestoda - physiology</subject><subject>cohesion</subject><subject>connectedness</subject><subject>fish</subject><subject>Fishes - parasitology</subject><subject>Food Chain</subject><subject>Food chains</subject><subject>Food webs</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>General aspects</subject><subject>helminths</subject><subject>Helminths - physiology</subject><subject>Host-Parasite Interactions</subject><subject>invasive species</subject><subject>Invertebrates</subject><subject>Marine</subject><subject>Marine ecology</subject><subject>Models, Biological</subject><subject>Modularity</subject><subject>Nemathelminthia. Plathelmintha</subject><subject>Nematoda</subject><subject>Nematoda - physiology</subject><subject>network centrality</subject><subject>Parasite and disease ecology</subject><subject>Parasite hosts</subject><subject>Parasites</subject><subject>phylogenetic signal</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Species</subject><subject>Taxa</subject><subject>Trematoda</subject><subject>Trematoda - physiology</subject><subject>trematodes</subject><subject>variance</subject><issn>0021-8790</issn><issn>1365-2656</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNqNkl1LHDEUhoO06Gq99qrtgBR6M5qTj5nkUsR-qFSh9TpkMok7S3ayJrPI_vtmnFWhNzUEAuc85z05eYPQEeATyOsUaMVLUvHqBAhg2EGzl8g7NMOYQClqiffQfkoLjHFNMN1Fe4SKnBMwQ1e3840P97bfFK0dbFx2vU3FMLdFDN4WwRVz63NwmBcrHXXqhpzu-rwzPHSt9oULoS0ebZM-oPdO-2QPt-cBuvt28ef8R3l98_3n-dl1abgQUErZSEMIE7oxDkDWjjnA1uiWssrhuiLSNLVpG200NUxSaogT3DgiuDZ5gAP0ddJdxfCwtmlQyy4Z673ubVgnBUxKIJjQt6AV48BqxjN6_A-6COvY50EyxRivqOQyU6cTZWJIKVqnVrFb6rhRgNVoiRoNUKMB6smSXPFpq7tulrZ94Z89yMCXLaCT0d5F3ZsuvXK1yK9GR66auMfO283_-qrLs18Xzzf4OBUu0hDiqzDDlEkYZ_o85Z0OSt_H3PzuN8HA8ocRHFNJ_wJTdLPe</recordid><startdate>201311</startdate><enddate>201311</enddate><creator>Poulin, Robert</creator><creator>Krasnov, Boris R</creator><creator>Pilosof, Shai</creator><creator>Thieltges, David W</creator><creator>Montgomery, Ian</creator><general>Blackwell Publishing</general><general>Blackwell</general><general>Blackwell Publishing Ltd</general><scope>FBQ</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>7X8</scope></search><sort><creationdate>201311</creationdate><title>Phylogeny determines the role of helminth parasites in intertidal food webs</title><author>Poulin, Robert ; Krasnov, Boris R ; Pilosof, Shai ; Thieltges, David W ; Montgomery, Ian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5881-99b9c2248abcf1197f4f10ecad346f07629cb7cdbaca3c4933c2f85cf285ac203</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animal and plant ecology</topic><topic>Animal ecology</topic><topic>Animal, plant and microbial ecology</topic><topic>Animals</topic><topic>aquatic food webs</topic><topic>Biological and medical sciences</topic><topic>Biological taxonomies</topic><topic>birds</topic><topic>Birds - parasitology</topic><topic>Cestoda</topic><topic>Cestoda - physiology</topic><topic>cohesion</topic><topic>connectedness</topic><topic>fish</topic><topic>Fishes - parasitology</topic><topic>Food Chain</topic><topic>Food chains</topic><topic>Food webs</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>General aspects</topic><topic>helminths</topic><topic>Helminths - physiology</topic><topic>Host-Parasite Interactions</topic><topic>invasive species</topic><topic>Invertebrates</topic><topic>Marine</topic><topic>Marine ecology</topic><topic>Models, Biological</topic><topic>Modularity</topic><topic>Nemathelminthia. Plathelmintha</topic><topic>Nematoda</topic><topic>Nematoda - physiology</topic><topic>network centrality</topic><topic>Parasite and disease ecology</topic><topic>Parasite hosts</topic><topic>Parasites</topic><topic>phylogenetic signal</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Species</topic><topic>Taxa</topic><topic>Trematoda</topic><topic>Trematoda - physiology</topic><topic>trematodes</topic><topic>variance</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Poulin, Robert</creatorcontrib><creatorcontrib>Krasnov, Boris R</creatorcontrib><creatorcontrib>Pilosof, Shai</creatorcontrib><creatorcontrib>Thieltges, David W</creatorcontrib><creatorcontrib>Montgomery, Ian</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>MEDLINE - Academic</collection><jtitle>The Journal of animal ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Poulin, Robert</au><au>Krasnov, Boris R</au><au>Pilosof, Shai</au><au>Thieltges, David W</au><au>Montgomery, Ian</au><au>Montgomery, Ian</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Phylogeny determines the role of helminth parasites in intertidal food webs</atitle><jtitle>The Journal of animal ecology</jtitle><addtitle>J Anim Ecol</addtitle><date>2013-11</date><risdate>2013</risdate><volume>82</volume><issue>6</issue><spage>1265</spage><epage>1275</epage><pages>1265-1275</pages><issn>0021-8790</issn><eissn>1365-2656</eissn><coden>JAECAP</coden><abstract>Parasites affect interactions among species in food webs and should be considered in any analysis of the structure, dynamics or resilience of trophic networks. However, the roles of individual parasite species, such as their importance as connectors within the network, and what factors determine these roles, are yet to be investigated. Here, we test the hypotheses that the species roles of trematode, cestode and nematode parasites in aquatic food webs are influenced by the type of definitive host they use, and also determined by their phylogenetic affiliations. We quantified the network role of 189 helminth species from six highly resolved intertidal food webs. We focused on four measures of centrality (node degree, closeness centrality, betweenness centrality and eigenvalue centrality), which characterize each parasite's position within the web, and on relative connectedness of a parasite species to taxa in its own module vs. other modules of the web (within‐module degree and participation coefficient). All six food webs displayed a significant modular structure, that is, they consisted of subsets of species interacting mostly with each other and less with species from other subsets. We demonstrated that the parasites themselves are not generating this modularity, though they contribute to intermodule connectivity. Mixed‐effects models revealed only a modest influence of the type of definitive host used (bird or fish) and of the web of origin on the different measures of parasite species roles. In contrast, the taxonomic affiliations of the parasites, included in the models as nested random factors, accounted for 37–93% of the total variance, depending on the measure of species role. Our findings indicate that parasites are important intermodule connectors and thus contribute to web cohesion. We also uncover a very strong phylogenetic signal in parasite species roles, suggesting that the role of any parasite species in a food web, including new invasive species, is to some extent predictable based solely on its taxonomic affiliations.</abstract><cop>Oxford</cop><pub>Blackwell Publishing</pub><pmid>23800281</pmid><doi>10.1111/1365-2656.12101</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animal and plant ecology Animal ecology Animal, plant and microbial ecology Animals aquatic food webs Biological and medical sciences Biological taxonomies birds Birds - parasitology Cestoda Cestoda - physiology cohesion connectedness fish Fishes - parasitology Food Chain Food chains Food webs Fundamental and applied biological sciences. Psychology General aspects helminths Helminths - physiology Host-Parasite Interactions invasive species Invertebrates Marine Marine ecology Models, Biological Modularity Nemathelminthia. Plathelmintha Nematoda Nematoda - physiology network centrality Parasite and disease ecology Parasite hosts Parasites phylogenetic signal Phylogenetics Phylogeny Species Taxa Trematoda Trematoda - physiology trematodes variance |
title | Phylogeny determines the role of helminth parasites in intertidal food webs |
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