Carcasses are more than just meat to obligate scavengers

Gonzalo Barceló, Paula L. Perrig, William Karasov and Jonathan N. Pauli, Department of Forest & Wildlife Ecology, University of Wisconsin-Madison, Madison, WI, Paula L. Perrig, Grupo de Investigaciones en Biología de la Conservación, INIBIOMA, Bariloche, Argentina, Prarthana Dharampal and Shawn A. Steffan, Dept. of Entomology, University of Wisconsin-Madison, Madison, WI, Emiliano Donadio, Rewildling Argentina, Buenos Aires, Argentina, Shawn A. Steffan, USDA-ARS, WI

Background/Question/Methods
Many food webs models do not 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 macro- and microbiome, effectively uniting autotrophs, consumers, predators and microbiota. Obligate scavengers, then, should feed from multiple trophic groups. We quantified the trophic positions (TP) for a simple and well-studied community of camelids (Vicugna vicugna and Lama guanicoe), camelid carrion, pumas (Puma concolor), and Andean condors (Vultur gryphus) in the High Andes via compound-specific stable isotopes analysis of amino-acids. We hypothesized that microbe presence in puma-killed camelids would inflate TP values in the carrion and that condors, by consuming across TPs found within a carcass, would exhibit variable TP values when compared to other community members. We further assessed condor foraging across TPs by analyzing regurgitated pellets and bulk isotopes.
Results/Conclusions
Isotope analysis of amino-acids revealed that condors had highly variable and non-integer TPs (mean ± s.d.; 2.9±0.3; n=15) especially compared to pumas (3.0±0.0, Barlett’s K2=7.70, p=0.006; n=4) – monophagous predators of living camelids – and camelids (2.0±0.1, K2=11.05, p<0.001; n=6). This high variability found among condors is likely because of “trophic omnivory,” wherein condors consume plant digesta (TP=1.0±0.1; n=4) and microbe-colonized meat (TP=2.3±0.1; n=4) all found within carrion. Female condors exhibited a TP (2.8±0.2; n=8) lower than strict carnivory (t7=-2.85, p =0.025), suggesting that they are consuming more plant biomass in a carcass, while males (3.1±0.3; n=7) consumed more of the microbe-rich animal tissue. Our analysis of condor pellets (n=177) and bulk isotopes (n=47) also revealed that condors primarily consumed camelid carrion but also exhibited non-trivial consumption of plants, close to 10% of their diet. Our study highlights that carcasses represent a trophically heterogeneous resource, and that obligate scavengers feed preferentially on certain trophic groups within the carcass, from autotrophs to secondary consumers, and from both the macro- and microbiome. The integration of microbes into food webs, even those featuring large-bodied vertebrates, can help identify and resolve the functional roles and resource partitioning of organisms in ecological communities.