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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Veröffentlicht in:Ecology and evolution 2017-05, Vol.7 (10), p.3532-3541
Hauptverfasser: Steffan, Shawn A., Chikaraishi, Yoshito, Dharampal, Prarthana S., Pauli, Jonathan N., Guédot, Christelle, Ohkouchi, Naohiko
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container_end_page 3541
container_issue 10
container_start_page 3532
container_title Ecology and evolution
container_volume 7
creator Steffan, Shawn A.
Chikaraishi, Yoshito
Dharampal, Prarthana S.
Pauli, Jonathan N.
Guédot, Christelle
Ohkouchi, Naohiko
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
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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. 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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 &amp; 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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