Quantifying niche partitioning and multichannel feeding among tree squirrels

Pauli, Jonathan N.; Manlick, Philip J.; Dharampal, Prarthana S.; Takizawa, Yasuko; Chikaraishi, Yoshito; Niccolai, Laura J.; Grauer, Jennifer A.; Black, Kristina; Restrepo, Mario Garces; Perrig, Paula L.; Wilson, Evan C.; Martin, Marie E.; Curras, Mauriel Rodriguez; Bougie, Tierney; Thompson, Kimberly L.; Smith, Matthew M.; Steffan, Shawn A.

doi:10.1016/j.fooweb.2019.e00124

Cited by 9 publications

(6 citation statements)

References 45 publications

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“…Second, omnivory can extend food chains, and we found that all small mammal species were feeding across trophic levels, with TPs ranging from 2.6 to 4.2 as a function of brown energy assimilation. Similar patterns have been reported in squirrels (Pauli et al, 2019), bees , and earthworms (Potapov et al, 2019), all exhibiting higher TPs due to omnivory, microbivory, or mycophagy. As prey for many predators, this widespread variance in TP within and among species due to omnivory can propagate through food webs leading to food chain extensions (Post & Takimoto, 2007;Sprules & Bowerman, 1988).…”

Section: Discussionsupporting

confidence: 81%

“…Indeed, detrital webs are typified by longer food chains due to omnivory (Digel et al, 2014;Moore et al, 2004;Rooney & McCann, 2012), and here we show that detrital energy is ultimately linked to aboveground consumers, leading to elevated TPs in purported green web consumers as well (Figure 1). Ecologists often segregate above-and belowground food webs into green and brown energy channels, but our results join a growing body of empirical evidence illustrating that these channels are coupled by aboveground consumers (Haraguchi et al, 2013;Hyodo et al, 2015;Pauli et al, 2019;Perkins et al, 2017). On average, we found that nearly 70% of energy assimilated by small mammals was derived from detrital channels, indicating that belowground food webs were a critical source of energy for vertebrate consumers.…”

Section: Discussionsupporting

confidence: 74%

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The coupling of green and brown food webs regulates trophic position in a montane mammal guild

Manlick

Cook

Newsome

2023

Ecology

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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, aboveand 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 (δ 13 C, δ 15 N) 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.

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Section: Discussionsupporting

confidence: 81%

Section: Discussionsupporting

confidence: 74%

The coupling of green and brown food webs regulates trophic position in a montane mammal guild

Manlick

Cook

Newsome

2023

Ecology

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“…This is one of the few studies to report trophic inflation (i.e. higher TP due to consumption of detritivores organisms) in a terrestrial vertebrate consumer (Pauli et al, 2019) and the first suggesting microbivory for a large vertebrate. These findings highlight the importance of CSIA in trophic positions and necrobiomes where regular bulk isotopes analysis have shown variable differences (Burrows et al, 2014;Keenan & DeBruyn, 2019;Payo-Payo et al, 2013;Yurkowski et al, 2017).…”

Section: Discussionmentioning

confidence: 96%

“…All these samples were analysed following Chikaraishi et al (2007Chikaraishi et al ( , 2009. Our sample sizes exceed those of previous work addressing trophic ecology with CSIA which have repeatedly demonstrated sufficient precision to identify trophic position (Blanke et al, 2017;Pauli et al, 2019;Steffan et al, 2015;Takizawa et al, 2020). This is because of the lower variance of the intra-trophic δ 15 N difference value between glutamic acid and phenylalanine and the greater magnitude of effect in glutamic acid fractionation compared to bulk isotopes.…”

Section: Materials S and Me Thodsmentioning

confidence: 96%

More than just meat: Carcass decomposition shapes trophic identities in a terrestrial vertebrate

et al. 2022

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1. Most food web models fail to account for the full complexity of interactions within a community, particularly where microbes are involved. Carcasses are microbe-rich resources and may represent a common nexus for the macrobiome and microbiome, effectively uniting autotrophs, consumers, predators and microbiota.2. We evaluated the role of carcasses as multitrophic resources and explored dietary partitioning for a sexually dimorphic obligate scavenger known for its hierarchical social system. This study was set in a well-studied community of camelids Vicugna, Lama guanicoe, pumas Puma concolor and Andean condors Vultur gryphus in the Andes. We hypothesized that condors, by feeding on trophically distinct dietary substrates within any given carcass, would have highly variable trophic position (TP) values. Furthermore, we expected that the microbial consumers within the carcass would inflate TP values in both, the carrion and the condors. Thus, we expected that the trophic heterogeneity within a carcass could facilitate sex-based dietary partitioning in condors.3. We used a multifaceted approach to assess the foraging of Andean condors, using regurgitated pellet and bulk isotopic analyses, and also quantified the TP of the entire community of graminoids, camelids, camelid carrion, pumas, and female and male condors employing compound-specific stable isotopes analysis of amino acids.4. Our analysis of condor pellets and bulk isotopes revealed non-trivial plant consumption, close to 10% of condor diet. Isotope analysis of amino acids revealed that condors had highly variable TPs (2.9 ± 0.3) compared to pumas (3.0 ± 0.0) and camelids (2.0 ± 0.1), likely representing 'trophic omnivory', wherein the condors consume plants (TP = 1.0 ± 0.1) and microbe-colonized carrion (2.3 ± 0.1). Female condors exhibited a TP (2.8 ± 0.2) lower than strict carnivory, suggesting that they consume more plant biomass in a carcass, while males (TP = 3.1 ± 0.3) are likely consuming more of the microbe-rich animal tissue.

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“…Consumers play a central role in connecting food webs by foraging on resources from both green and brown energy channels (Wolkovich et al, 2014). Such ‘multichannel feeding’ is exceedingly common and has been documented in taxa ranging from arthropods (Perkins et al, 2017) to fishes (Elliott Smith et al, 2020) to mammals (Pauli et al, 2019). Quantifying multichannel feeding by consumers is challenging, however, and ecologists have historically relied on visual observations and gut content analysis, which can be subjective or provide biased estimates of energy flow (Symondson, 2002).…”

Section: Introductionmentioning

confidence: 99%

Stable isotope fingerprinting traces essential amino acid assimilation and multichannel feeding in a vertebrate consumer

Manlick

Newsome

2022

Methods Ecol Evol

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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 mice Peromyscus maniculatus raised 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.

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Quantifying niche partitioning and multichannel feeding among tree squirrels

Cited by 9 publications

References 45 publications

The coupling of green and brown food webs regulates trophic position in a montane mammal guild

The coupling of green and brown food webs regulates trophic position in a montane mammal guild

More than just meat: Carcass decomposition shapes trophic identities in a terrestrial vertebrate

Stable isotope fingerprinting traces essential amino acid assimilation and multichannel feeding in a vertebrate consumer

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