Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on the common milkweed Asclepias syriaca
Dietary specialization in insect herbivores has long been hypothesized to predict tolerance of plant defences, with more specialized herbivores being highly tolerant of and sometimes sequestering plant secondary compounds. Plant variation in secondary compounds should thus play an important and pred...
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Veröffentlicht in: | Functional ecology 2016-04, Vol.30 (4), p.547-556 |
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description | Dietary specialization in insect herbivores has long been hypothesized to predict tolerance of plant defences, with more specialized herbivores being highly tolerant of and sometimes sequestering plant secondary compounds. Plant variation in secondary compounds should thus play an important and predictable role in shaping the performance and distribution of insect communities. We compared the performance of four naturally co‐occurring aphid species on twenty genotypes of the common milkweed Asclepias syriaca. Genotypes of milkweed consistently differed in functional traits, including concentrations of toxic cardenolides, while the diet breadths of the four aphids ranged from broadly generalized to monophagous. The two more generalized species had the highest population growth rate overall, while growth rates decreased with increasing specialization. In contrast, honeydew exudation as a measure of phloem consumption increased with specialization; thus, resource‐use efficiency was lower in specialist aphids. The two more generalized aphids grew best on genotypes with the highest plant growth rate (as an approximation for resource availability), while specialist aphids were not affected by plant growth. All four species contained apolar cardenolides in their bodies and excreted polar cardenolides, but only the most specialized aphid Myzocallis asclepiadis was negatively affected by increasing cardenolide concentrations of the host plant. Sequestration of cardenolides increased with diet specialization, with M. asclepiadis accumulating twice as much as any other species, perhaps explaining its susceptibility to plant cardenolides. Heritable plant traits differentially impacted co‐occurring insect herbivores within the same guild. Generalist aphids were susceptible to variation in plant vigour but not defensive compounds. Increased host specialization resulted in lower resource‐use efficiency, increased phloem throughput and ultimately higher cardenolide sequestration. Variation in these traits is thus likely to determine the relative distribution of generalist and specialist herbivores on plants in natural communities. |
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Plant variation in secondary compounds should thus play an important and predictable role in shaping the performance and distribution of insect communities. We compared the performance of four naturally co‐occurring aphid species on twenty genotypes of the common milkweed Asclepias syriaca. Genotypes of milkweed consistently differed in functional traits, including concentrations of toxic cardenolides, while the diet breadths of the four aphids ranged from broadly generalized to monophagous. The two more generalized species had the highest population growth rate overall, while growth rates decreased with increasing specialization. In contrast, honeydew exudation as a measure of phloem consumption increased with specialization; thus, resource‐use efficiency was lower in specialist aphids. The two more generalized aphids grew best on genotypes with the highest plant growth rate (as an approximation for resource availability), while specialist aphids were not affected by plant growth. All four species contained apolar cardenolides in their bodies and excreted polar cardenolides, but only the most specialized aphid Myzocallis asclepiadis was negatively affected by increasing cardenolide concentrations of the host plant. Sequestration of cardenolides increased with diet specialization, with M. asclepiadis accumulating twice as much as any other species, perhaps explaining its susceptibility to plant cardenolides. Heritable plant traits differentially impacted co‐occurring insect herbivores within the same guild. Generalist aphids were susceptible to variation in plant vigour but not defensive compounds. Increased host specialization resulted in lower resource‐use efficiency, increased phloem throughput and ultimately higher cardenolide sequestration. Variation in these traits is thus likely to determine the relative distribution of generalist and specialist herbivores on plants in natural communities.</description><identifier>ISSN: 0269-8463</identifier><identifier>EISSN: 1365-2435</identifier><identifier>DOI: 10.1111/1365-2435.12523</identifier><identifier>CODEN: FECOE5</identifier><language>eng</language><publisher>London: British Ecological Society</publisher><subject>Aphididae ; Approximation ; Asclepias syriaca ; cardenolides ; Consumption ; Diet ; Efficiency ; Exudation ; Functional anatomy ; genotype ; Genotypes ; Growth rate ; Herbivores ; honeydew ; Host plants ; insect communities ; Insects ; Mathematical analysis ; Myzocallis ; Myzocallis asclepiadis ; phloem ; phytotoxins ; plant genotype × insect species interactions ; Plant growth ; Plant-animal interactions ; Population growth ; Resource availability ; Sequestering ; sequestration ; Specialization ; toxicity ; Toxins ; trait variation ; vigor</subject><ispartof>Functional ecology, 2016-04, Vol.30 (4), p.547-556</ispartof><rights>2015 The Authors. © 2015 British Ecological Society</rights><rights>2015 The Authors. Functional Ecology © 2015 British Ecological Society</rights><rights>Functional Ecology © 2016 British Ecological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4633-692acb79b3e5b852d9f1895d4a859e6fd2b5ef3167a4143a7dd63e558e8cfaef3</citedby><cites>FETCH-LOGICAL-c4633-692acb79b3e5b852d9f1895d4a859e6fd2b5ef3167a4143a7dd63e558e8cfaef3</cites><orcidid>0000-0001-7142-8731</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/48582430$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/48582430$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,776,780,799,1411,1427,27901,27902,45550,45551,46384,46808,57992,58225</link.rule.ids></links><search><contributor>Lee, Kwang Pum</contributor><creatorcontrib>Züst, Tobias</creatorcontrib><creatorcontrib>Agrawal, Anurag A</creatorcontrib><creatorcontrib>Lee, Kwang Pum</creatorcontrib><title>Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on the common milkweed Asclepias syriaca</title><title>Functional ecology</title><description>Dietary specialization in insect herbivores has long been hypothesized to predict tolerance of plant defences, with more specialized herbivores being highly tolerant of and sometimes sequestering plant secondary compounds. Plant variation in secondary compounds should thus play an important and predictable role in shaping the performance and distribution of insect communities. We compared the performance of four naturally co‐occurring aphid species on twenty genotypes of the common milkweed Asclepias syriaca. Genotypes of milkweed consistently differed in functional traits, including concentrations of toxic cardenolides, while the diet breadths of the four aphids ranged from broadly generalized to monophagous. The two more generalized species had the highest population growth rate overall, while growth rates decreased with increasing specialization. In contrast, honeydew exudation as a measure of phloem consumption increased with specialization; thus, resource‐use efficiency was lower in specialist aphids. The two more generalized aphids grew best on genotypes with the highest plant growth rate (as an approximation for resource availability), while specialist aphids were not affected by plant growth. All four species contained apolar cardenolides in their bodies and excreted polar cardenolides, but only the most specialized aphid Myzocallis asclepiadis was negatively affected by increasing cardenolide concentrations of the host plant. Sequestration of cardenolides increased with diet specialization, with M. asclepiadis accumulating twice as much as any other species, perhaps explaining its susceptibility to plant cardenolides. Heritable plant traits differentially impacted co‐occurring insect herbivores within the same guild. Generalist aphids were susceptible to variation in plant vigour but not defensive compounds. Increased host specialization resulted in lower resource‐use efficiency, increased phloem throughput and ultimately higher cardenolide sequestration. Variation in these traits is thus likely to determine the relative distribution of generalist and specialist herbivores on plants in natural communities.</description><subject>Aphididae</subject><subject>Approximation</subject><subject>Asclepias syriaca</subject><subject>cardenolides</subject><subject>Consumption</subject><subject>Diet</subject><subject>Efficiency</subject><subject>Exudation</subject><subject>Functional anatomy</subject><subject>genotype</subject><subject>Genotypes</subject><subject>Growth rate</subject><subject>Herbivores</subject><subject>honeydew</subject><subject>Host plants</subject><subject>insect communities</subject><subject>Insects</subject><subject>Mathematical analysis</subject><subject>Myzocallis</subject><subject>Myzocallis asclepiadis</subject><subject>phloem</subject><subject>phytotoxins</subject><subject>plant genotype × insect species interactions</subject><subject>Plant growth</subject><subject>Plant-animal interactions</subject><subject>Population growth</subject><subject>Resource availability</subject><subject>Sequestering</subject><subject>sequestration</subject><subject>Specialization</subject><subject>toxicity</subject><subject>Toxins</subject><subject>trait variation</subject><subject>vigor</subject><issn>0269-8463</issn><issn>1365-2435</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><recordid>eNqFkU9v1DAQxSMEEkvhzAlhiQuXtP4TO_axWrUFqRKV2p6tWdvZ9eLEwc5qWb4H37feBnrgUHyxNe_3RvM8VfWe4FNSzhlhgte0YfyUUE7Zi2rxVHlZLTAVqpaNYK-rNzlvMcaKU7qoft_EcRdg8nFA6xT30wbBYFF2P3YuT2kWYofGAMOEpvjTDxlBiMMaQTGA9a7UC5BHZzwE_2u2-AF1cZcQjBtvZ9FlVIRp45CJfV-evQ_f985ZdJ5NcKOHjPIheTDwtnrVQcju3Z_7pLq_vLhbfqmvv119XZ5f16YkYbVQFMyqVSvm-EpyalVHpOK2AcmVE52lK-46RkQLDWkYtNaKgnLppOmgKCfV57nvmOJjYN37bFwoYV3cZU1aiTltsRIF_fQPui35hjKdJgoLLKRqyLNU27aKcCZxoc5myqSYc3KdHpPvIR00wfq4TH1cnT6uTj8uszj47Nj74A7_w_XlxfKv78Ps2-YppidfI7ks-HGSj7PeQdSwTj7r-1uKicC4NFDllx8Aipa1hA</recordid><startdate>201604</startdate><enddate>201604</enddate><creator>Züst, Tobias</creator><creator>Agrawal, Anurag A</creator><creator>Lee, Kwang Pum</creator><general>British Ecological Society</general><general>Wiley</general><general>Wiley Subscription Services, Inc</general><scope>FBQ</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><orcidid>https://orcid.org/0000-0001-7142-8731</orcidid></search><sort><creationdate>201604</creationdate><title>Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on the common milkweed Asclepias syriaca</title><author>Züst, Tobias ; Agrawal, Anurag A ; Lee, Kwang Pum</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4633-692acb79b3e5b852d9f1895d4a859e6fd2b5ef3167a4143a7dd63e558e8cfaef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Aphididae</topic><topic>Approximation</topic><topic>Asclepias syriaca</topic><topic>cardenolides</topic><topic>Consumption</topic><topic>Diet</topic><topic>Efficiency</topic><topic>Exudation</topic><topic>Functional anatomy</topic><topic>genotype</topic><topic>Genotypes</topic><topic>Growth rate</topic><topic>Herbivores</topic><topic>honeydew</topic><topic>Host plants</topic><topic>insect communities</topic><topic>Insects</topic><topic>Mathematical analysis</topic><topic>Myzocallis</topic><topic>Myzocallis asclepiadis</topic><topic>phloem</topic><topic>phytotoxins</topic><topic>plant genotype × insect species interactions</topic><topic>Plant growth</topic><topic>Plant-animal interactions</topic><topic>Population growth</topic><topic>Resource availability</topic><topic>Sequestering</topic><topic>sequestration</topic><topic>Specialization</topic><topic>toxicity</topic><topic>Toxins</topic><topic>trait variation</topic><topic>vigor</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Züst, Tobias</creatorcontrib><creatorcontrib>Agrawal, Anurag A</creatorcontrib><creatorcontrib>Lee, Kwang Pum</creatorcontrib><collection>AGRIS</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><jtitle>Functional ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Züst, Tobias</au><au>Agrawal, Anurag A</au><au>Lee, Kwang Pum</au><au>Lee, Kwang Pum</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on the common milkweed Asclepias syriaca</atitle><jtitle>Functional ecology</jtitle><date>2016-04</date><risdate>2016</risdate><volume>30</volume><issue>4</issue><spage>547</spage><epage>556</epage><pages>547-556</pages><issn>0269-8463</issn><eissn>1365-2435</eissn><coden>FECOE5</coden><abstract>Dietary specialization in insect herbivores has long been hypothesized to predict tolerance of plant defences, with more specialized herbivores being highly tolerant of and sometimes sequestering plant secondary compounds. Plant variation in secondary compounds should thus play an important and predictable role in shaping the performance and distribution of insect communities. We compared the performance of four naturally co‐occurring aphid species on twenty genotypes of the common milkweed Asclepias syriaca. Genotypes of milkweed consistently differed in functional traits, including concentrations of toxic cardenolides, while the diet breadths of the four aphids ranged from broadly generalized to monophagous. The two more generalized species had the highest population growth rate overall, while growth rates decreased with increasing specialization. In contrast, honeydew exudation as a measure of phloem consumption increased with specialization; thus, resource‐use efficiency was lower in specialist aphids. The two more generalized aphids grew best on genotypes with the highest plant growth rate (as an approximation for resource availability), while specialist aphids were not affected by plant growth. All four species contained apolar cardenolides in their bodies and excreted polar cardenolides, but only the most specialized aphid Myzocallis asclepiadis was negatively affected by increasing cardenolide concentrations of the host plant. Sequestration of cardenolides increased with diet specialization, with M. asclepiadis accumulating twice as much as any other species, perhaps explaining its susceptibility to plant cardenolides. Heritable plant traits differentially impacted co‐occurring insect herbivores within the same guild. Generalist aphids were susceptible to variation in plant vigour but not defensive compounds. Increased host specialization resulted in lower resource‐use efficiency, increased phloem throughput and ultimately higher cardenolide sequestration. Variation in these traits is thus likely to determine the relative distribution of generalist and specialist herbivores on plants in natural communities.</abstract><cop>London</cop><pub>British Ecological Society</pub><doi>10.1111/1365-2435.12523</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-7142-8731</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Aphididae Approximation Asclepias syriaca cardenolides Consumption Diet Efficiency Exudation Functional anatomy genotype Genotypes Growth rate Herbivores honeydew Host plants insect communities Insects Mathematical analysis Myzocallis Myzocallis asclepiadis phloem phytotoxins plant genotype × insect species interactions Plant growth Plant-animal interactions Population growth Resource availability Sequestering sequestration Specialization toxicity Toxins trait variation vigor |
title | Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on the common milkweed Asclepias syriaca |
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