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Abstract Food web ecology has revolutionized our understanding of ecological processes, but the drivers of food web properties like trophic position (TP) and food chain length are notoriously enigmatic. In terrestrial ecosystems, above‐ and belowground systems were historically compartmentalized into “green” and “brown” food webs, but the coupling of these systems by animal consumers is increasingly recognized, with potential consequences for trophic structure. We used stable isotope analysis (δ¹³C, δ¹⁵N) of individual amino acids to trace the flow of essential biomolecules and jointly measure multichannel feeding, food web coupling, and TP in a guild of small mammals. We then tested the hypothesis that brown energy fluxes to aboveground consumers increase terrestrial food chain length via cryptic trophic transfers during microbial decomposition. We found that the average small mammal consumer acquired nearly 70% of their essential amino acids (69.0% ± 7.6%) from brown food webs, leading to significant increases in TP across species and functional groups. Fungi were the primary conduit of brown energy to aboveground consumers, providing nearly half the amino acid budget for small mammals on average (44.3% ± 12.0%). These findings illustrate the tightly coupled nature of green and brown food webs and show that microbially mediated energy flow ultimately regulates food web structure in aboveground consumers. Consequently, we propose that the integration of green and brown energy channels is a cryptic driver of food chain length in terrestrial ecosystems. 

Abstract Animals often consume resources from multiple energy channels, thereby connecting food webs and driving trophic structure. Such ‘multichannel feeding’ can dictate ecosystem function and stability, but tools to quantify this process are lacking. Stable isotope ‘fingerprints’ are unique patterns in essential amino acid (EAA) δ¹³C values that vary consistently between energy channels like primary production and detritus, and they have emerged as a tool to trace energy flow in wild systems. Because animals cannot synthesize EAAs de novo and must acquire them from dietary proteins, ecologists often assume δ¹³C fingerprints travel through food webs unaltered. Numerous studies have used this approach to quantify energy flow and multichannel feeding in animals, but δ¹³C fingerprinting has never been experimentally tested in a vertebrate consumer.We tested the efficacy of δ¹³C fingerprinting using captive deer micePeromyscus maniculatusraised on diets containing bacterial, fungal and plant protein, as well as a combination of all three sources. We measured the transfer of δ¹³C fingerprints from diet to consumer liver, muscle and bone collagen, and we used linear discriminant analysis (LDA) and isotopic mixing models to estimate dietary proportions compared to known contributions. Lastly, we tested the use of published δ¹³C source fingerprints previously used to estimate energy flow and multichannel feeding by consumers.We found that EAA δ¹³C values exhibit significant isotopic (i.e. trophic) fractionation between consumer tissues and diets. Nevertheless, LDA revealed that δ¹³C fingerprints are consistently routed and assimilated into consumer tissues, regardless of isotopic incorporation rate. Isotopic mixing models accurately estimated the proportional diets of consumers, but all models overestimated plant‐based protein contributions, likely due to the digestive efficiencies of protein sources. Lastly, we found that δ¹³C source fingerprints from published literature can lead to erroneous diet reconstruction.We show that δ¹³C fingerprints accurately measure energy flow to vertebrate consumers across tissues with different isotopic incorporation rates, thereby enabling the estimation of multichannel feeding at various temporal scales. Our findings illustrate the power of δ¹³C fingerprinting for quantifying food web dynamics, but also reveal that careful selection of dietary source data is critical to the accuracy of this emerging technique.