Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory
Detritivory is the dominant trophic paradigm in most terrestrial, aquatic, and marine ecosystems, yet accurate measurement of consumer trophic position within detrital (=“brown”) food webs has remained unresolved. Measurement of detritivore trophic position is complicated by the fact that detritus i...
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description | Detritivory is the dominant trophic paradigm in most terrestrial, aquatic, and marine ecosystems, yet accurate measurement of consumer trophic position within detrital (=“brown”) food webs has remained unresolved. Measurement of detritivore trophic position is complicated by the fact that detritus is suffused with microbes, creating a detrital complex of living and nonliving biomass. Given that microbes and metazoans are trophic analogues of each other, animals feeding on detrital complexes are ingesting other detritivores (microbes), which should elevate metazoan trophic position and should be rampant within brown food webs. We tested these hypotheses using isotopic (15N) analyses of amino acids extracted from wild and laboratory‐cultured consumers. Vertebrate (fish) and invertebrate detritivores (beetles and moths) were reared on detritus, with and without microbial colonization. In the field, detritivorous animal specimens were collected and analyzed to compare trophic identities among laboratory‐reared and free‐roaming detritivores. When colonized by bacteria or fungi, the trophic positions of detrital complexes increased significantly over time. The magnitude of trophic inflation was mediated by the extent of microbial consumption of detrital substrates. When detrital complexes were fed to vertebrate and invertebrate animals, the consumers registered similar degrees of trophic inflation, albeit one trophic level higher than their diets. The wild‐collected detritivore fauna in our study exhibited significantly elevated trophic positions. Our findings suggest that the trophic positions of detrital complexes rise predictably as microbes convert nonliving organic matter into living microbial biomass. Animals consuming such detrital complexes exhibit similar trophic inflation, directly attributable to the assimilation of microbe‐derived amino acids. Our data demonstrate that detritivorous microbes elevate metazoan trophic position, suggesting that detritivory among animals is, functionally, omnivory. By quantifying the impacts of microbivory on the trophic positions of detritivorous animals and then tracking how these effects propagate “up” food chains, we reveal the degree to which microbes influence consumer groups within trophic hierarchies. The trophic inflation observed among our field‐collected fauna further suggests that microbial proteins represent an immense contribution to metazoan biomass. Collectively, these findings provide an empirical basis |
doi_str_mv | 10.1002/ece3.2951 |
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While the primacy of microbes within the empire of heterotrophy has been well‐documented, the nature and degree to which microbes may reconfigure the trophic identities of carnivore and omnivore groups has remained unresolved. This means that the trophic positions of the single most abundant, massive, and ubiquitous trophic group (detritivorous microbes) have not been measured with known, high accuracy. In our study, we show that the presence of detritivorous bacteria and fungi in brown food chains elevates significantly the trophic positions of detritivorous fauna, including the detrital complex, itself.</description><identifier>ISSN: 2045-7758</identifier><identifier>EISSN: 2045-7758</identifier><identifier>DOI: 10.1002/ece3.2951</identifier><identifier>PMID: 28515888</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Amino acids ; Animals ; Aquatic ecosystems ; Bacteria ; bacterivores ; Beetles ; Biomass ; Butterflies & moths ; Coleoptera ; Colonization ; Consumer groups ; Consumers ; Detritivores ; detritivory ; Detritus ; diet ; Empirical analysis ; Fauna ; fish ; food chain ; Food chains ; Food webs ; freshwater ecosystems ; Fungi ; Hierarchies ; invertebrates ; Laboratories ; Marine ecosystems ; microbe ; microbial biomass ; microbial colonization ; microbial proteins ; microbiome ; Microorganisms ; moths ; nitrogen ; omnivore ; omnivores ; Organic matter ; Original Research ; Position measurement ; Proteins ; rearing ; stable isotopes ; Substrates ; terrestrial ecosystems ; Terrestrial environments ; Tracking ; Trophic levels</subject><ispartof>Ecology and evolution, 2017-05, Vol.7 (10), p.3532-3541</ispartof><rights>2017 The Authors. published by John Wiley & Sons Ltd.</rights><rights>2017. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5421-29c5bcf035e0deff448abcd132b82fb3a9fa0724fcab968d8af82435bef9e28f3</citedby><cites>FETCH-LOGICAL-c5421-29c5bcf035e0deff448abcd132b82fb3a9fa0724fcab968d8af82435bef9e28f3</cites><orcidid>0000-0002-2219-6409</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5433990/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5433990/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1411,11541,27901,27902,45550,45551,46027,46451,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28515888$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Steffan, Shawn A.</creatorcontrib><creatorcontrib>Chikaraishi, Yoshito</creatorcontrib><creatorcontrib>Dharampal, Prarthana S.</creatorcontrib><creatorcontrib>Pauli, Jonathan N.</creatorcontrib><creatorcontrib>Guédot, Christelle</creatorcontrib><creatorcontrib>Ohkouchi, Naohiko</creatorcontrib><title>Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory</title><title>Ecology and evolution</title><addtitle>Ecol Evol</addtitle><description>Detritivory is the dominant trophic paradigm in most terrestrial, aquatic, and marine ecosystems, yet accurate measurement of consumer trophic position within detrital (=“brown”) food webs has remained unresolved. Measurement of detritivore trophic position is complicated by the fact that detritus is suffused with microbes, creating a detrital complex of living and nonliving biomass. Given that microbes and metazoans are trophic analogues of each other, animals feeding on detrital complexes are ingesting other detritivores (microbes), which should elevate metazoan trophic position and should be rampant within brown food webs. We tested these hypotheses using isotopic (15N) analyses of amino acids extracted from wild and laboratory‐cultured consumers. Vertebrate (fish) and invertebrate detritivores (beetles and moths) were reared on detritus, with and without microbial colonization. In the field, detritivorous animal specimens were collected and analyzed to compare trophic identities among laboratory‐reared and free‐roaming detritivores. When colonized by bacteria or fungi, the trophic positions of detrital complexes increased significantly over time. The magnitude of trophic inflation was mediated by the extent of microbial consumption of detrital substrates. When detrital complexes were fed to vertebrate and invertebrate animals, the consumers registered similar degrees of trophic inflation, albeit one trophic level higher than their diets. The wild‐collected detritivore fauna in our study exhibited significantly elevated trophic positions. Our findings suggest that the trophic positions of detrital complexes rise predictably as microbes convert nonliving organic matter into living microbial biomass. Animals consuming such detrital complexes exhibit similar trophic inflation, directly attributable to the assimilation of microbe‐derived amino acids. Our data demonstrate that detritivorous microbes elevate metazoan trophic position, suggesting that detritivory among animals is, functionally, omnivory. By quantifying the impacts of microbivory on the trophic positions of detritivorous animals and then tracking how these effects propagate “up” food chains, we reveal the degree to which microbes influence consumer groups within trophic hierarchies. The trophic inflation observed among our field‐collected fauna further suggests that microbial proteins represent an immense contribution to metazoan biomass. Collectively, these findings provide an empirical basis to interpret detritivore trophic identity, and further illuminate the magnitude of microbial contributions to food webs.
While the primacy of microbes within the empire of heterotrophy has been well‐documented, the nature and degree to which microbes may reconfigure the trophic identities of carnivore and omnivore groups has remained unresolved. This means that the trophic positions of the single most abundant, massive, and ubiquitous trophic group (detritivorous microbes) have not been measured with known, high accuracy. In our study, we show that the presence of detritivorous bacteria and fungi in brown food chains elevates significantly the trophic positions of detritivorous fauna, including the detrital complex, itself.</description><subject>Amino acids</subject><subject>Animals</subject><subject>Aquatic ecosystems</subject><subject>Bacteria</subject><subject>bacterivores</subject><subject>Beetles</subject><subject>Biomass</subject><subject>Butterflies & moths</subject><subject>Coleoptera</subject><subject>Colonization</subject><subject>Consumer groups</subject><subject>Consumers</subject><subject>Detritivores</subject><subject>detritivory</subject><subject>Detritus</subject><subject>diet</subject><subject>Empirical analysis</subject><subject>Fauna</subject><subject>fish</subject><subject>food chain</subject><subject>Food chains</subject><subject>Food webs</subject><subject>freshwater ecosystems</subject><subject>Fungi</subject><subject>Hierarchies</subject><subject>invertebrates</subject><subject>Laboratories</subject><subject>Marine ecosystems</subject><subject>microbe</subject><subject>microbial biomass</subject><subject>microbial colonization</subject><subject>microbial proteins</subject><subject>microbiome</subject><subject>Microorganisms</subject><subject>moths</subject><subject>nitrogen</subject><subject>omnivore</subject><subject>omnivores</subject><subject>Organic matter</subject><subject>Original Research</subject><subject>Position measurement</subject><subject>Proteins</subject><subject>rearing</subject><subject>stable isotopes</subject><subject>Substrates</subject><subject>terrestrial ecosystems</subject><subject>Terrestrial environments</subject><subject>Tracking</subject><subject>Trophic 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microbivory</title><author>Steffan, Shawn A. ; Chikaraishi, Yoshito ; Dharampal, Prarthana S. ; Pauli, Jonathan N. ; Guédot, Christelle ; Ohkouchi, Naohiko</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5421-29c5bcf035e0deff448abcd132b82fb3a9fa0724fcab968d8af82435bef9e28f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Amino acids</topic><topic>Animals</topic><topic>Aquatic ecosystems</topic><topic>Bacteria</topic><topic>bacterivores</topic><topic>Beetles</topic><topic>Biomass</topic><topic>Butterflies & moths</topic><topic>Coleoptera</topic><topic>Colonization</topic><topic>Consumer groups</topic><topic>Consumers</topic><topic>Detritivores</topic><topic>detritivory</topic><topic>Detritus</topic><topic>diet</topic><topic>Empirical analysis</topic><topic>Fauna</topic><topic>fish</topic><topic>food chain</topic><topic>Food chains</topic><topic>Food 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Evol</addtitle><date>2017-05</date><risdate>2017</risdate><volume>7</volume><issue>10</issue><spage>3532</spage><epage>3541</epage><pages>3532-3541</pages><issn>2045-7758</issn><eissn>2045-7758</eissn><abstract>Detritivory is the dominant trophic paradigm in most terrestrial, aquatic, and marine ecosystems, yet accurate measurement of consumer trophic position within detrital (=“brown”) food webs has remained unresolved. Measurement of detritivore trophic position is complicated by the fact that detritus is suffused with microbes, creating a detrital complex of living and nonliving biomass. Given that microbes and metazoans are trophic analogues of each other, animals feeding on detrital complexes are ingesting other detritivores (microbes), which should elevate metazoan trophic position and should be rampant within brown food webs. We tested these hypotheses using isotopic (15N) analyses of amino acids extracted from wild and laboratory‐cultured consumers. Vertebrate (fish) and invertebrate detritivores (beetles and moths) were reared on detritus, with and without microbial colonization. In the field, detritivorous animal specimens were collected and analyzed to compare trophic identities among laboratory‐reared and free‐roaming detritivores. When colonized by bacteria or fungi, the trophic positions of detrital complexes increased significantly over time. The magnitude of trophic inflation was mediated by the extent of microbial consumption of detrital substrates. When detrital complexes were fed to vertebrate and invertebrate animals, the consumers registered similar degrees of trophic inflation, albeit one trophic level higher than their diets. The wild‐collected detritivore fauna in our study exhibited significantly elevated trophic positions. Our findings suggest that the trophic positions of detrital complexes rise predictably as microbes convert nonliving organic matter into living microbial biomass. Animals consuming such detrital complexes exhibit similar trophic inflation, directly attributable to the assimilation of microbe‐derived amino acids. Our data demonstrate that detritivorous microbes elevate metazoan trophic position, suggesting that detritivory among animals is, functionally, omnivory. By quantifying the impacts of microbivory on the trophic positions of detritivorous animals and then tracking how these effects propagate “up” food chains, we reveal the degree to which microbes influence consumer groups within trophic hierarchies. The trophic inflation observed among our field‐collected fauna further suggests that microbial proteins represent an immense contribution to metazoan biomass. Collectively, these findings provide an empirical basis to interpret detritivore trophic identity, and further illuminate the magnitude of microbial contributions to food webs.
While the primacy of microbes within the empire of heterotrophy has been well‐documented, the nature and degree to which microbes may reconfigure the trophic identities of carnivore and omnivore groups has remained unresolved. This means that the trophic positions of the single most abundant, massive, and ubiquitous trophic group (detritivorous microbes) have not been measured with known, high accuracy. In our study, we show that the presence of detritivorous bacteria and fungi in brown food chains elevates significantly the trophic positions of detritivorous fauna, including the detrital complex, itself.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>28515888</pmid><doi>10.1002/ece3.2951</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-2219-6409</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amino acids Animals Aquatic ecosystems Bacteria bacterivores Beetles Biomass Butterflies & moths Coleoptera Colonization Consumer groups Consumers Detritivores detritivory Detritus diet Empirical analysis Fauna fish food chain Food chains Food webs freshwater ecosystems Fungi Hierarchies invertebrates Laboratories Marine ecosystems microbe microbial biomass microbial colonization microbial proteins microbiome Microorganisms moths nitrogen omnivore omnivores Organic matter Original Research Position measurement Proteins rearing stable isotopes Substrates terrestrial ecosystems Terrestrial environments Tracking Trophic levels |
title | Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory |
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