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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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Autores principales: Steffan, Shawn A., Chikaraishi, Yoshito, Dharampal, Prarthana S., Pauli, Jonathan N., Guédot, Christelle, Ohkouchi, Naohiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5433990/
https://www.ncbi.nlm.nih.gov/pubmed/28515888
http://dx.doi.org/10.1002/ece3.2951
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author Steffan, Shawn A.
Chikaraishi, Yoshito
Dharampal, Prarthana S.
Pauli, Jonathan N.
Guédot, Christelle
Ohkouchi, Naohiko
author_facet Steffan, Shawn A.
Chikaraishi, Yoshito
Dharampal, Prarthana S.
Pauli, Jonathan N.
Guédot, Christelle
Ohkouchi, Naohiko
author_sort Steffan, Shawn A.
collection PubMed
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 ((15)N) 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.
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spelling pubmed-54339902017-05-17 Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory Steffan, Shawn A. Chikaraishi, Yoshito Dharampal, Prarthana S. Pauli, Jonathan N. Guédot, Christelle Ohkouchi, Naohiko Ecol Evol Original Research 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 ((15)N) 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. John Wiley and Sons Inc. 2017-04-09 /pmc/articles/PMC5433990/ /pubmed/28515888 http://dx.doi.org/10.1002/ece3.2951 Text en © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Steffan, Shawn A.
Chikaraishi, Yoshito
Dharampal, Prarthana S.
Pauli, Jonathan N.
Guédot, Christelle
Ohkouchi, Naohiko
Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory
title Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory
title_full Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory
title_fullStr Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory
title_full_unstemmed Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory
title_short Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory
title_sort unpacking brown food‐webs: animal trophic identity reflects rampant microbivory
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5433990/
https://www.ncbi.nlm.nih.gov/pubmed/28515888
http://dx.doi.org/10.1002/ece3.2951
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