Host and parasite diversity jointly control disease risk in complex communities
Host–parasite interactions are embedded within complex communities composed of multiple host species and a cryptic assemblage of other parasites. To date, however, surprisingly few studies have explored the joint effects of host and parasite richness on disease risk, despite growing interest in the...
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description | Host–parasite interactions are embedded within complex communities composed of multiple host species and a cryptic assemblage of other parasites. To date, however, surprisingly few studies have explored the joint effects of host and parasite richness on disease risk, despite growing interest in the diversity–disease relationship. Here, we combined field surveys and mechanistic experiments to test how transmission of the virulent trematode Ribeiroia ondatrae was affected by the diversity of both amphibian hosts and coinfecting parasites. Within natural wetlands, host and parasite species richness correlated positively, consistent with theoretical predictions. Among sites that supported Ribeiroia , however, host and parasite richness interacted to negatively affect Ribeiroia transmission between its snail and amphibian hosts, particularly in species-poor assemblages. In laboratory and outdoor experiments designed to decouple the relative contributions of host and parasite diversity, increases in host richness decreased Ribeiroia infection by 11–65%. Host richness also tended to decrease total infections by other parasite species (four of six instances), such that more diverse host assemblages exhibited ∼40% fewer infections overall. Importantly, parasite richness further reduced both per capita and total Ribeiroia infection by 15–20%, possibly owing to intrahost competition among coinfecting species. These findings provide evidence that parasitic and free-living diversity jointly regulate disease risk, help to resolve apparent contradictions in the diversity–disease relationship, and emphasize the challenges of integrating research on coinfection and host heterogeneity to develop a community ecology-based approach to infectious diseases. |
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J. ; Preston, Daniel L. ; Hoverman, Jason T. ; LaFonte, Bryan E.</creator><creatorcontrib>Johnson, Pieter T. J. ; Preston, Daniel L. ; Hoverman, Jason T. ; LaFonte, Bryan E.</creatorcontrib><description>Host–parasite interactions are embedded within complex communities composed of multiple host species and a cryptic assemblage of other parasites. To date, however, surprisingly few studies have explored the joint effects of host and parasite richness on disease risk, despite growing interest in the diversity–disease relationship. Here, we combined field surveys and mechanistic experiments to test how transmission of the virulent trematode Ribeiroia ondatrae was affected by the diversity of both amphibian hosts and coinfecting parasites. Within natural wetlands, host and parasite species richness correlated positively, consistent with theoretical predictions. Among sites that supported Ribeiroia , however, host and parasite richness interacted to negatively affect Ribeiroia transmission between its snail and amphibian hosts, particularly in species-poor assemblages. In laboratory and outdoor experiments designed to decouple the relative contributions of host and parasite diversity, increases in host richness decreased Ribeiroia infection by 11–65%. Host richness also tended to decrease total infections by other parasite species (four of six instances), such that more diverse host assemblages exhibited ∼40% fewer infections overall. Importantly, parasite richness further reduced both per capita and total Ribeiroia infection by 15–20%, possibly owing to intrahost competition among coinfecting species. These findings provide evidence that parasitic and free-living diversity jointly regulate disease risk, help to resolve apparent contradictions in the diversity–disease relationship, and emphasize the challenges of integrating research on coinfection and host heterogeneity to develop a community ecology-based approach to infectious diseases.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1310557110</identifier><identifier>PMID: 24082092</identifier><identifier>CODEN: PNASA6</identifier><language>eng</language><publisher>Washington, DC: National Academy of Sciences</publisher><subject>Amphibians ; Amphibians - parasitology ; Animal and plant ecology ; Animal, plant and microbial ecology ; Animals ; Applied ecology ; Biodiversity ; Biological and medical sciences ; Biological Sciences ; Conservation, protection and management of environment and wildlife ; correlation ; disease control ; Disease risk ; Disease transmission ; Fundamental and applied biological sciences. Psychology ; Host-Parasite Interactions - physiology ; host-parasite relationships ; hosts ; Infections ; Infectious diseases ; mixed infection ; Models, Biological ; Parasite hosts ; Parasites ; Parks, reserves, wildlife conservation. Endangered species: population survey and restocking ; prediction ; Reptiles & amphibians ; Ribeiroia ; Ribeiroia ondatrae ; risk ; Risk assessment ; Snails ; Snails - parasitology ; Species diversity ; surveys ; Synecology ; Terrestrial ecosystems ; Trematoda - pathogenicity ; Trematoda - physiology ; Trematode Infections ; virulence ; Wetlands</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2013-10, Vol.110 (42), p.16916-16921</ispartof><rights>copyright © 1993–2008 National Academy of Sciences of the United States of America</rights><rights>2015 INIST-CNRS</rights><rights>Copyright National Academy of Sciences Oct 15, 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c654t-ab63dd6829a6bd555112773f57f011df424e5ab07f52de0eac9085202e0765593</citedby><cites>FETCH-LOGICAL-c654t-ab63dd6829a6bd555112773f57f011df424e5ab07f52de0eac9085202e0765593</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/110/42.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23750686$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23750686$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27843748$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24082092$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Johnson, Pieter T. J.</creatorcontrib><creatorcontrib>Preston, Daniel L.</creatorcontrib><creatorcontrib>Hoverman, Jason T.</creatorcontrib><creatorcontrib>LaFonte, Bryan E.</creatorcontrib><title>Host and parasite diversity jointly control disease risk in complex communities</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Host–parasite interactions are embedded within complex communities composed of multiple host species and a cryptic assemblage of other parasites. To date, however, surprisingly few studies have explored the joint effects of host and parasite richness on disease risk, despite growing interest in the diversity–disease relationship. Here, we combined field surveys and mechanistic experiments to test how transmission of the virulent trematode Ribeiroia ondatrae was affected by the diversity of both amphibian hosts and coinfecting parasites. Within natural wetlands, host and parasite species richness correlated positively, consistent with theoretical predictions. Among sites that supported Ribeiroia , however, host and parasite richness interacted to negatively affect Ribeiroia transmission between its snail and amphibian hosts, particularly in species-poor assemblages. In laboratory and outdoor experiments designed to decouple the relative contributions of host and parasite diversity, increases in host richness decreased Ribeiroia infection by 11–65%. Host richness also tended to decrease total infections by other parasite species (four of six instances), such that more diverse host assemblages exhibited ∼40% fewer infections overall. Importantly, parasite richness further reduced both per capita and total Ribeiroia infection by 15–20%, possibly owing to intrahost competition among coinfecting species. These findings provide evidence that parasitic and free-living diversity jointly regulate disease risk, help to resolve apparent contradictions in the diversity–disease relationship, and emphasize the challenges of integrating research on coinfection and host heterogeneity to develop a community ecology-based approach to infectious diseases.</description><subject>Amphibians</subject><subject>Amphibians - parasitology</subject><subject>Animal and plant ecology</subject><subject>Animal, plant and microbial ecology</subject><subject>Animals</subject><subject>Applied ecology</subject><subject>Biodiversity</subject><subject>Biological and medical sciences</subject><subject>Biological Sciences</subject><subject>Conservation, protection and management of environment and wildlife</subject><subject>correlation</subject><subject>disease control</subject><subject>Disease risk</subject><subject>Disease transmission</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Host-Parasite Interactions - physiology</subject><subject>host-parasite relationships</subject><subject>hosts</subject><subject>Infections</subject><subject>Infectious diseases</subject><subject>mixed infection</subject><subject>Models, Biological</subject><subject>Parasite hosts</subject><subject>Parasites</subject><subject>Parks, reserves, wildlife conservation. Endangered species: population survey and restocking</subject><subject>prediction</subject><subject>Reptiles & amphibians</subject><subject>Ribeiroia</subject><subject>Ribeiroia ondatrae</subject><subject>risk</subject><subject>Risk assessment</subject><subject>Snails</subject><subject>Snails - parasitology</subject><subject>Species diversity</subject><subject>surveys</subject><subject>Synecology</subject><subject>Terrestrial ecosystems</subject><subject>Trematoda - pathogenicity</subject><subject>Trematoda - physiology</subject><subject>Trematode Infections</subject><subject>virulence</subject><subject>Wetlands</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkk1v1DAQhi0EokvhzAmIhJC4pJ3xdy5IqAKKVKkH6NnyJk7xksTBTir23-Owyy5wgdNYnsfvvDMeQp4inCEodj4ONp0hQxBCIcI9skKosJS8gvtkBUBVqTnlJ-RRShsAqISGh-SEctAUKroi15chTYUdmmK00SY_uaLxdy7m07bYBD9M3baowzDF0OVMcja5Ivr0tfBDvu_Hzn1fYj8PfvIuPSYPWtsl92QfT8nN-3efLy7Lq-sPHy_eXpW1FHwq7VqyppGaVlauGyEEIlWKtUK1gNi02bMTdg2qFbRx4GxdgRYUqAMlhajYKXmz0x3nde-a2mWHtjNj9L2NWxOsN39mBv_F3IY7w3SeQqWywOu9QAzfZpcm0_tUu66zgwtzMqiBZVMo-b9RLrI3pel_qHLOcm-C6Yy-_AvdhDkOeWg_qSzIkWbqfEfVMaQUXXtoEcEsK2CWFTDHFcgvnv8-mQP_688z8GoP2FTbro12qH06ckpzpvhisNhzS4VD2VyXU4OyQpmRZztkk6YQjxJMCZB6yb_Y5VsbjL3Ne2NuPlFACYAcUVP2AysW1fg</recordid><startdate>20131015</startdate><enddate>20131015</enddate><creator>Johnson, Pieter T. J.</creator><creator>Preston, Daniel L.</creator><creator>Hoverman, Jason T.</creator><creator>LaFonte, Bryan E.</creator><general>National Academy of Sciences</general><general>NATIONAL ACADEMY OF SCIENCES</general><general>National Acad Sciences</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7ST</scope><scope>7U1</scope><scope>7U2</scope><scope>7U6</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20131015</creationdate><title>Host and parasite diversity jointly control disease risk in complex communities</title><author>Johnson, Pieter T. J. ; Preston, Daniel L. ; Hoverman, Jason T. ; LaFonte, Bryan E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c654t-ab63dd6829a6bd555112773f57f011df424e5ab07f52de0eac9085202e0765593</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Amphibians</topic><topic>Amphibians - parasitology</topic><topic>Animal and plant ecology</topic><topic>Animal, plant and microbial ecology</topic><topic>Animals</topic><topic>Applied ecology</topic><topic>Biodiversity</topic><topic>Biological and medical sciences</topic><topic>Biological Sciences</topic><topic>Conservation, protection and management of environment and wildlife</topic><topic>correlation</topic><topic>disease control</topic><topic>Disease risk</topic><topic>Disease transmission</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Host-Parasite Interactions - physiology</topic><topic>host-parasite relationships</topic><topic>hosts</topic><topic>Infections</topic><topic>Infectious diseases</topic><topic>mixed infection</topic><topic>Models, Biological</topic><topic>Parasite hosts</topic><topic>Parasites</topic><topic>Parks, reserves, wildlife conservation. Endangered species: population survey and restocking</topic><topic>prediction</topic><topic>Reptiles & amphibians</topic><topic>Ribeiroia</topic><topic>Ribeiroia ondatrae</topic><topic>risk</topic><topic>Risk assessment</topic><topic>Snails</topic><topic>Snails - parasitology</topic><topic>Species diversity</topic><topic>surveys</topic><topic>Synecology</topic><topic>Terrestrial ecosystems</topic><topic>Trematoda - pathogenicity</topic><topic>Trematoda - physiology</topic><topic>Trematode Infections</topic><topic>virulence</topic><topic>Wetlands</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Johnson, Pieter T. J.</creatorcontrib><creatorcontrib>Preston, Daniel L.</creatorcontrib><creatorcontrib>Hoverman, Jason T.</creatorcontrib><creatorcontrib>LaFonte, Bryan E.</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>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Environment Abstracts</collection><collection>Risk Abstracts</collection><collection>Safety Science and Risk</collection><collection>Sustainability Science 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>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Johnson, Pieter T. J.</au><au>Preston, Daniel L.</au><au>Hoverman, Jason T.</au><au>LaFonte, Bryan E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Host and parasite diversity jointly control disease risk in complex communities</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2013-10-15</date><risdate>2013</risdate><volume>110</volume><issue>42</issue><spage>16916</spage><epage>16921</epage><pages>16916-16921</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><coden>PNASA6</coden><abstract>Host–parasite interactions are embedded within complex communities composed of multiple host species and a cryptic assemblage of other parasites. To date, however, surprisingly few studies have explored the joint effects of host and parasite richness on disease risk, despite growing interest in the diversity–disease relationship. Here, we combined field surveys and mechanistic experiments to test how transmission of the virulent trematode Ribeiroia ondatrae was affected by the diversity of both amphibian hosts and coinfecting parasites. Within natural wetlands, host and parasite species richness correlated positively, consistent with theoretical predictions. Among sites that supported Ribeiroia , however, host and parasite richness interacted to negatively affect Ribeiroia transmission between its snail and amphibian hosts, particularly in species-poor assemblages. In laboratory and outdoor experiments designed to decouple the relative contributions of host and parasite diversity, increases in host richness decreased Ribeiroia infection by 11–65%. Host richness also tended to decrease total infections by other parasite species (four of six instances), such that more diverse host assemblages exhibited ∼40% fewer infections overall. Importantly, parasite richness further reduced both per capita and total Ribeiroia infection by 15–20%, possibly owing to intrahost competition among coinfecting species. These findings provide evidence that parasitic and free-living diversity jointly regulate disease risk, help to resolve apparent contradictions in the diversity–disease relationship, and emphasize the challenges of integrating research on coinfection and host heterogeneity to develop a community ecology-based approach to infectious diseases.</abstract><cop>Washington, DC</cop><pub>National Academy of Sciences</pub><pmid>24082092</pmid><doi>10.1073/pnas.1310557110</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amphibians Amphibians - parasitology Animal and plant ecology Animal, plant and microbial ecology Animals Applied ecology Biodiversity Biological and medical sciences Biological Sciences Conservation, protection and management of environment and wildlife correlation disease control Disease risk Disease transmission Fundamental and applied biological sciences. Psychology Host-Parasite Interactions - physiology host-parasite relationships hosts Infections Infectious diseases mixed infection Models, Biological Parasite hosts Parasites Parks, reserves, wildlife conservation. Endangered species: population survey and restocking prediction Reptiles & amphibians Ribeiroia Ribeiroia ondatrae risk Risk assessment Snails Snails - parasitology Species diversity surveys Synecology Terrestrial ecosystems Trematoda - pathogenicity Trematoda - physiology Trematode Infections virulence Wetlands |
title | Host and parasite diversity jointly control disease risk in complex communities |
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