Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles
The immune system is a necessary, but potentially costly, defense against infectious diseases. When nutrition is limited, immune activity may consume a significant amount of an organism's energy budget. Levels of dietary protein affect immune system function; high levels can enhance disease res...
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Veröffentlicht in: | Oecologia 2012-05, Vol.169 (1), p.23-31 |
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description | The immune system is a necessary, but potentially costly, defense against infectious diseases. When nutrition is limited, immune activity may consume a significant amount of an organism's energy budget. Levels of dietary protein affect immune system function; high levels can enhance disease resistance. We exposed southern leopard frog [Lithobates sphenocephalus (= Rana sphenocephala)] tadpoles to high and low protein diets crossed with the presence or absence of the pathogenic amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) and quantified: (1) tadpole resistance to Bd; (2) tadpole skin-swelling in response to phytohaemagglutinin (PHA) injection (a measure of the T cell-mediated response of the immune system); (3) bacterial killing ability (BKA) of tadpole blood (a measure of the complement-mediated cytotoxicity of the innate immune system); and (4) tadpole growth and development. Tadpoles raised on a low-protein diet were smaller and less developed than tadpoles on a high-protein diet. When controlled for developmental stage, tadpoles raised on a low-protein diet had reduced PHA and BKA responses relative to tadpoles on a highprotein diet, but these immune responses were independent of Bd exposure. High dietary protein significantly increased resistance to Bd. Our results support the general hypothesis that host condition can strongly affect disease resistance; in particular, fluctuations in dietary protein availability may change how diseases affect populations in the field. |
doi_str_mv | 10.1007/s00442-011-2171-1 |
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When nutrition is limited, immune activity may consume a significant amount of an organism's energy budget. Levels of dietary protein affect immune system function; high levels can enhance disease resistance. We exposed southern leopard frog [Lithobates sphenocephalus (= Rana sphenocephala)] tadpoles to high and low protein diets crossed with the presence or absence of the pathogenic amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) and quantified: (1) tadpole resistance to Bd; (2) tadpole skin-swelling in response to phytohaemagglutinin (PHA) injection (a measure of the T cell-mediated response of the immune system); (3) bacterial killing ability (BKA) of tadpole blood (a measure of the complement-mediated cytotoxicity of the innate immune system); and (4) tadpole growth and development. Tadpoles raised on a low-protein diet were smaller and less developed than tadpoles on a high-protein diet. When controlled for developmental stage, tadpoles raised on a low-protein diet had reduced PHA and BKA responses relative to tadpoles on a highprotein diet, but these immune responses were independent of Bd exposure. High dietary protein significantly increased resistance to Bd. Our results support the general hypothesis that host condition can strongly affect disease resistance; in particular, fluctuations in dietary protein availability may change how diseases affect populations in the field.</description><identifier>ISSN: 0029-8549</identifier><identifier>EISSN: 1432-1939</identifier><identifier>DOI: 10.1007/s00442-011-2171-1</identifier><identifier>PMID: 22038058</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer</publisher><subject>Amphibians ; Animal Diseases - immunology ; Animals ; Anura ; Batrachochytrium dendrobatidis ; Biomedical and Life Sciences ; Blood ; Chytridiomycota ; Cytotoxicity ; Developmental stages ; Diet ; Dietary protein ; Dietary Proteins - pharmacology ; Dietary restrictions ; Disease resistance ; Disease Resistance - drug effects ; Disease susceptibility ; Ecology ; Frogs ; Growth ; Hydrology/Water Resources ; Immune system ; Immunity, Innate - drug effects ; Infections ; Infectious diseases ; Larva - growth & development ; Larva - immunology ; Larva - microbiology ; Life Sciences ; Low protein diets ; Mycoses - immunology ; Parasite hosts ; PHYSIOLOGICAL ECOLOGY ; Physiological ecology - Original Paper ; Plant Sciences ; Ranidae - growth & development ; Ranidae - immunology ; Ranidae - microbiology ; Skin ; T cells ; Tadpoles</subject><ispartof>Oecologia, 2012-05, Vol.169 (1), p.23-31</ispartof><rights>Springer-Verlag Berlin Heidelberg 2012</rights><rights>Springer-Verlag 2011</rights><rights>COPYRIGHT 2012 Springer</rights><rights>Springer-Verlag 2012</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c594t-e70237a255d2f266080574de8ef54bd79c6ed7620d8e59732c56bf138494fbe03</citedby><cites>FETCH-LOGICAL-c594t-e70237a255d2f266080574de8ef54bd79c6ed7620d8e59732c56bf138494fbe03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41487928$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41487928$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>315,782,786,805,27931,27932,41495,42564,51326,58024,58257</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22038058$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Venesky, Matthew D.</creatorcontrib><creatorcontrib>Wilcoxen, Travis E.</creatorcontrib><creatorcontrib>Rensel, Michelle A.</creatorcontrib><creatorcontrib>Rollins-Smith, Louise</creatorcontrib><creatorcontrib>Kerby, Jacob L.</creatorcontrib><creatorcontrib>Parris, Matthew J.</creatorcontrib><title>Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles</title><title>Oecologia</title><addtitle>Oecologia</addtitle><addtitle>Oecologia</addtitle><description>The immune system is a necessary, but potentially costly, defense against infectious diseases. When nutrition is limited, immune activity may consume a significant amount of an organism's energy budget. Levels of dietary protein affect immune system function; high levels can enhance disease resistance. We exposed southern leopard frog [Lithobates sphenocephalus (= Rana sphenocephala)] tadpoles to high and low protein diets crossed with the presence or absence of the pathogenic amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) and quantified: (1) tadpole resistance to Bd; (2) tadpole skin-swelling in response to phytohaemagglutinin (PHA) injection (a measure of the T cell-mediated response of the immune system); (3) bacterial killing ability (BKA) of tadpole blood (a measure of the complement-mediated cytotoxicity of the innate immune system); and (4) tadpole growth and development. Tadpoles raised on a low-protein diet were smaller and less developed than tadpoles on a high-protein diet. When controlled for developmental stage, tadpoles raised on a low-protein diet had reduced PHA and BKA responses relative to tadpoles on a highprotein diet, but these immune responses were independent of Bd exposure. High dietary protein significantly increased resistance to Bd. Our results support the general hypothesis that host condition can strongly affect disease resistance; in particular, fluctuations in dietary protein availability may change how diseases affect populations in the field.</description><subject>Amphibians</subject><subject>Animal Diseases - immunology</subject><subject>Animals</subject><subject>Anura</subject><subject>Batrachochytrium dendrobatidis</subject><subject>Biomedical and Life Sciences</subject><subject>Blood</subject><subject>Chytridiomycota</subject><subject>Cytotoxicity</subject><subject>Developmental stages</subject><subject>Diet</subject><subject>Dietary protein</subject><subject>Dietary Proteins - pharmacology</subject><subject>Dietary restrictions</subject><subject>Disease resistance</subject><subject>Disease Resistance - drug effects</subject><subject>Disease susceptibility</subject><subject>Ecology</subject><subject>Frogs</subject><subject>Growth</subject><subject>Hydrology/Water Resources</subject><subject>Immune system</subject><subject>Immunity, Innate - drug effects</subject><subject>Infections</subject><subject>Infectious diseases</subject><subject>Larva - growth & development</subject><subject>Larva - immunology</subject><subject>Larva - microbiology</subject><subject>Life Sciences</subject><subject>Low protein diets</subject><subject>Mycoses - immunology</subject><subject>Parasite hosts</subject><subject>PHYSIOLOGICAL ECOLOGY</subject><subject>Physiological ecology - Original Paper</subject><subject>Plant Sciences</subject><subject>Ranidae - growth & development</subject><subject>Ranidae - immunology</subject><subject>Ranidae - microbiology</subject><subject>Skin</subject><subject>T cells</subject><subject>Tadpoles</subject><issn>0029-8549</issn><issn>1432-1939</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkluL1TAUhYsoznH0B_igBHxRmI65Ns3jMN4GBgQvzyGn2e3k0CbHJEXn35vS8eARBclDSPKtxV47u6qeEnxOMJavE8ac0xoTUlMiSU3uVRvCGa2JYup-tcGYqroVXJ1Uj1LaYUw4EeJhdUIpZi0W7abybxxkE2_RPoYMzqMIKUfXZRc8ctPeuJjQEMP3fHNWztPsXb49Q8ZbZF0Ck2BRuJSN7wAVfQpzvoHo0Qhhb6JFfQwDysbuwwjpcfWgN2OCJ3f7afX13dsvlx_q64_vry4vrutOKJ5rkJgyaagQlva0aXApVnILLfSCb61UXQNWNhTbFoSSjHai2faEtVzxfguYnVYvV98S69tcIunJpQ7G0XgIc9IEE6lawlvxHyhWglEpWUFf_IHuwhx9CbIYUtkoWjp_oAYzgna-DzmabjHVF0w0nAtFaaHO_0KVZWFyXfDQu3J_JHh1JChMhh95MHNK-urzp2OWrGwXQ0oRer2PbirfXOpcAkm9jo4uo6OX0dGkaJ7fhZu3E9iD4tesFICuQCpPfoD4e_p_uz5bRbuUQzyY8tJ6qWjLfgJ4r9VM</recordid><startdate>20120501</startdate><enddate>20120501</enddate><creator>Venesky, Matthew D.</creator><creator>Wilcoxen, Travis E.</creator><creator>Rensel, Michelle A.</creator><creator>Rollins-Smith, Louise</creator><creator>Kerby, Jacob L.</creator><creator>Parris, Matthew J.</creator><general>Springer</general><general>Springer-Verlag</general><general>Springer Nature B.V</general><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>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>F1W</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>H95</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>L.G</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PCBAR</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope><scope>7T5</scope></search><sort><creationdate>20120501</creationdate><title>Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles</title><author>Venesky, Matthew D. ; Wilcoxen, Travis E. ; Rensel, Michelle A. ; Rollins-Smith, Louise ; Kerby, Jacob L. ; Parris, Matthew J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c594t-e70237a255d2f266080574de8ef54bd79c6ed7620d8e59732c56bf138494fbe03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Amphibians</topic><topic>Animal Diseases - immunology</topic><topic>Animals</topic><topic>Anura</topic><topic>Batrachochytrium dendrobatidis</topic><topic>Biomedical and Life Sciences</topic><topic>Blood</topic><topic>Chytridiomycota</topic><topic>Cytotoxicity</topic><topic>Developmental stages</topic><topic>Diet</topic><topic>Dietary protein</topic><topic>Dietary Proteins - pharmacology</topic><topic>Dietary restrictions</topic><topic>Disease resistance</topic><topic>Disease Resistance - drug effects</topic><topic>Disease susceptibility</topic><topic>Ecology</topic><topic>Frogs</topic><topic>Growth</topic><topic>Hydrology/Water Resources</topic><topic>Immune system</topic><topic>Immunity, Innate - drug effects</topic><topic>Infections</topic><topic>Infectious diseases</topic><topic>Larva - growth & development</topic><topic>Larva - immunology</topic><topic>Larva - microbiology</topic><topic>Life Sciences</topic><topic>Low protein diets</topic><topic>Mycoses - immunology</topic><topic>Parasite hosts</topic><topic>PHYSIOLOGICAL ECOLOGY</topic><topic>Physiological ecology - Original Paper</topic><topic>Plant Sciences</topic><topic>Ranidae - growth & development</topic><topic>Ranidae - immunology</topic><topic>Ranidae - microbiology</topic><topic>Skin</topic><topic>T cells</topic><topic>Tadpoles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Venesky, Matthew D.</creatorcontrib><creatorcontrib>Wilcoxen, Travis E.</creatorcontrib><creatorcontrib>Rensel, Michelle A.</creatorcontrib><creatorcontrib>Rollins-Smith, Louise</creatorcontrib><creatorcontrib>Kerby, Jacob L.</creatorcontrib><creatorcontrib>Parris, Matthew J.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Earth, Atmospheric & Aquatic Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Immunology Abstracts</collection><jtitle>Oecologia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Venesky, Matthew D.</au><au>Wilcoxen, Travis E.</au><au>Rensel, Michelle A.</au><au>Rollins-Smith, Louise</au><au>Kerby, Jacob L.</au><au>Parris, Matthew J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles</atitle><jtitle>Oecologia</jtitle><stitle>Oecologia</stitle><addtitle>Oecologia</addtitle><date>2012-05-01</date><risdate>2012</risdate><volume>169</volume><issue>1</issue><spage>23</spage><epage>31</epage><pages>23-31</pages><issn>0029-8549</issn><eissn>1432-1939</eissn><abstract>The immune system is a necessary, but potentially costly, defense against infectious diseases. When nutrition is limited, immune activity may consume a significant amount of an organism's energy budget. Levels of dietary protein affect immune system function; high levels can enhance disease resistance. We exposed southern leopard frog [Lithobates sphenocephalus (= Rana sphenocephala)] tadpoles to high and low protein diets crossed with the presence or absence of the pathogenic amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) and quantified: (1) tadpole resistance to Bd; (2) tadpole skin-swelling in response to phytohaemagglutinin (PHA) injection (a measure of the T cell-mediated response of the immune system); (3) bacterial killing ability (BKA) of tadpole blood (a measure of the complement-mediated cytotoxicity of the innate immune system); and (4) tadpole growth and development. Tadpoles raised on a low-protein diet were smaller and less developed than tadpoles on a high-protein diet. When controlled for developmental stage, tadpoles raised on a low-protein diet had reduced PHA and BKA responses relative to tadpoles on a highprotein diet, but these immune responses were independent of Bd exposure. High dietary protein significantly increased resistance to Bd. Our results support the general hypothesis that host condition can strongly affect disease resistance; in particular, fluctuations in dietary protein availability may change how diseases affect populations in the field.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer</pub><pmid>22038058</pmid><doi>10.1007/s00442-011-2171-1</doi><tpages>9</tpages></addata></record> |
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subjects | Amphibians Animal Diseases - immunology Animals Anura Batrachochytrium dendrobatidis Biomedical and Life Sciences Blood Chytridiomycota Cytotoxicity Developmental stages Diet Dietary protein Dietary Proteins - pharmacology Dietary restrictions Disease resistance Disease Resistance - drug effects Disease susceptibility Ecology Frogs Growth Hydrology/Water Resources Immune system Immunity, Innate - drug effects Infections Infectious diseases Larva - growth & development Larva - immunology Larva - microbiology Life Sciences Low protein diets Mycoses - immunology Parasite hosts PHYSIOLOGICAL ECOLOGY Physiological ecology - Original Paper Plant Sciences Ranidae - growth & development Ranidae - immunology Ranidae - microbiology Skin T cells Tadpoles |
title | Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles |
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