Unpacking brown food-webs: Animal trophic identity reflects rampant microbivory

Authors: Steffan, Shawn; CHIKARAISHI, YOSHITO - Japan Agency For Marine-Earth Science And Technology (JAMSTEC); DHARAMPAL, PRARTHANA - University Of Wisconsin; PAULI, JONATHON - University Of Wisconsin; GUEDOT, CHRISTELLE - University Of Wisconsin; OHKOUCHI, NAOHIKO - Japan Agency For Marine-Earth Science And Technology (JAMSTEC)

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/6/2017
Publication Date: 4/9/2017
Publication URL: https://handle.nal.usda.gov/10113/5695479
Citation: Steffan, S.A., Chikaraishi, Y., Dharampal, P.S., Pauli, J.N., Guedot, C., Ohkouchi, N. 2017. Unpacking brown food-webs: Animal trophic identity reflects rampant microbivory. Ecology and Evolution. 7(10):3532-3541. doi: 10.1002/ece3.2951.

Interpretive Summary: The nature and degree to which microbes may reconfigure the trophic identities of carnivore and omnivore groups has remained surprisingly 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. Impact: Altogether, these findings will re-frame how ecologists interpret the trophic identities of the dominant global consumer group—detritivores. Our data reveal animal trophic identities in which microbial contributions have been fully integrated. In effect, we have united the macro- and microbiome in trophic ecology, facilitating comprehensive interpretations of trophic identity among omnivorous and carnivorous animals.

Technical 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 impenetrable. Measurement of detritivore trophic position is complicated by the fact that detritus is suffused with microbes. Given that microbes and metazoans are trophic analogues of each other, animals feeding on microbe-colonised detritus ingest multiple trophic groups. This phenomenon should elevate consumer trophic position, and should be common in brown food-webs. We tested this expectation using compound-specific isotopic (15N) analysis of amino acids extracted from both wild and laboratory-cultured consumers. Vertebrate (fish) and invertebrate detritivores (beetles and moths) were reared on detritus, with and without microbial colonisation. In the field, specimens of diverse animal taxa were collected to measure the trophic identities of fauna known to be detritivorous. We show that after being colonised by bacteria or fungi, the trophic positions of detrital complexes increased significantly over time. The ‘inflation’ of detrital trophic position was mediated by the extent to which microbes consumed the detritus. In turn, animals consuming microbe-colonised detritus registered distinctly non-integer trophic positions, which were approximately one trophic level higher than their diets. All wild-collected invertebrate detritivores in our study exhibited non-integer trophic positions. Our data indicate that the trophic position of detritus rises as microbes convert non-living resources into microbial biomass. A detrital complex, therefore, will tend to have a dynamic trophic identity. Animals consuming such microbe-colonised detritus exhibit trophic inflation as a predictable function of the degree to which the animal has consumed microbial prey. For meso- or macrofauna, detritivory is omnivory. By incorporating microbes into trophic hierarchies, we quantify the microbe effect within food-chains, and provide a basis to better interpret trophic position among detritivores. Collectively, these findings help to unite the macro- and microbiome in food-web studies, refining the questions that may be posed regarding trophic structure and function.