The fate of small-mammal carrion is affected by carcass size and visual conspicuousness in a Neotropical rainforest
Keywords:
Canis latrans, Coprophanaeus, Didelphis marsupialis, Eira barbara, food web, leaf litter, Nasua narica, Philander opossum, rainforest, scarabaeidae.Abstract
Scavenging of carrion is essential to terrestrial ecosystems and can shape food webs and behavior. The prevalence and importance of scavenging has often been underestimated and overlooked in food web studies. Small-mammal carrion is even less studied and difficult to estimate, especially in the Neotropics. This project explored small-mammal carcass scavenging in a Neotropical, mid-elevation rainforest, and specifically studied the rate of carcass removal by scavengers, how the conspicuousness and weight of carcasses affect scavenging, and what vertebrate scavengers utilize this carrion resource. I deployed 194 mouse carcasses of various weights, above and below the leaf litter, and surveyed them daily until disappearance. I paired each carcass with a trail camera to help identify vertebrate scavengers. A general linear model analysis showed that most mouse carcasses disappeared within 1 to 2 days. Carcasses above the leaf litter were removed quicker and larger mice generally lasted longer. Only 6.25 % of the carcasses were removed by vertebrates. Most carcasses were removed by something too small to trigger the trail cameras, likely scarab beetles. The results of this study show that small-mammal carcasses are a sought-after resource in Neotropical forests, and that invertebrates are able to quickly hoard and secure small carrion more efficiently than vertebrate scavengers. A better understanding of scavenging ecology in Neotropical forests will help in developing a broader framework of the trophic interactions within and across ecosystems.References
AKOPYAN, M. M. 1953. The fate of suslik corpses on the steppe. Zoologicheskii Zhurnal 32:1014–1019.
ALLEN M. L., L. M. ELBROCH, C. C. WILMERS, AND H. U. WITTMER. 2015. The comparative effects of large carnivores on the acquisition of carrion by scavengers. The American Naturalist 185:822–833.
ARROYA-ARCE, S., I. THOMAS, AND K. CUTLER. 2016. King Culture (Sarcoramphus papa) scavenging of green turtle (Chelonia mydas) carcasses in Tortuguero National Park, Costa Rica. Vulture News 70:30–36.
BARTON, P. S., S. A. CUNNINGHAM, D. B. LINDEMAYER, AND A. D. MANNING. 2013. The role of carrion in maintaining biodiversity and ecological processes in terrestrial ecosystems. Oecologia 171:761–772.
BARTON, P. S., M. J. EVANS, C. N. FOSTER, J. L. PECHAL, J. K. BUMP, M. M. QUAGGIOTTO, AND M. E. BENBOW. 2019. Towards quantifying carrion biomass in ecosystems. Trends in Ecology & Evolution 34:950–961.
BEASLEY, J. C., Z. H. OLSON, AND T. L. DEVAULT. 2015. Ecological role of vertebrate scavengers. Pp. 107–127 in Carrion ecology, evolution and their applications (Benbow, M. E., J. K. Tomberlin, and A. M. Tarone, eds.). USDA National Wildlife Research Center - Staff Publications. Boca Raton, U.S.A.
BEASLEY, J. C., Z. H. OLSON, N. SELVA, AND T. L. DEVAULT. 2019. Ecological functions of vertebrate scavenging. Pp. 126–157 in Carrion ecology and management (Olea, P. P., P. Mateo-Tomás, and J. A. Sánchez-Zapata, eds.). Springer. Cham, Switzerland.
BRAACK, L. 1987. Community dynamics of carrion-attendant arthropods in tropical african woodland. Oecologia 72:402–409.
BUECHLEY, E. R., AND Ç. H. ŞEKERCIOĞLU. 2016. The avian scavenger crisis: Looming extinctions, trophic cascades, and loss of critical ecosystem functions. Biological Conservation 198:220–228.
Bump, J. K., C. R. Webster, J. A. Vucetich, R. O. Peterson, J. M. Shields, and M. D. Powers. 2009. Ungulate carcasses perforate ecological filters and create biogeochemical hotspots in forest herbaceous layers allowing trees a competitive advantage. Ecosystems 12:996–1007.
COOPER, S. M. 1991. Optimal hunting group-size: the need for lions to defend their kills against loss to spotted hyaenas. African Journal of Ecology 29:130–136.
CORNABY, B. W. 1974. Carrion reduction by animals in contrasting tropical habitats. Biotropica 6:51–63.
Cowles, R. B., and R. L. Phelan. 1958. Olfaction in Rattlesnakes. Copeia 1958:77–83.
DEVAULT, T. L., I. L. BRISBIN, JR., AND O. E. RHODES, JR. 2004. Factors influencing the acquisition of rodent carrion by vertebrate scavengers and decomposers. Canadian Journal of Zoology 82:502–509.
DEVAULT, T. L., Z. H. OLSON, J. C. BEASLEY, AND O. E. RHODES, JR. 2011. Mesopredators dominate competition for carrion in an agricultural landscape. Basic and Applied Ecology 12:268-274.
DEVAULT, T. L., AND O. E. RHODES. 2002. Identification of vertebrate scavengers of small mammal carcasses in a forested landscape. Acta Theriologica 47:185–192.
DEVAULT, T. L., O. E. RHODES, AND J. A. SHIVIK. 2003. Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102:225–234.
DOS SANTOS, W. E., L. T. CARNIERO, A. C. F. ALVES, A. J. CREÃO-DUARTE, AND C. F. MARTINS. 2014. Stingless bees (Hymenoptera: Apidae: Meliphonini) attracted to animal carcasses in the Brazilian dry forest and implications for forensic entomology. Sociobiology 61:490–493.
EDMONDS, W. 2010. A taxonomic review of the neotropical genus Coprophanaeus Olsoufief, 1924 (Coleoptera: Scarabaeidae, Scarabaeinae). Insecta Mundi 129:1–111.
GOMEZ, L. G., D. C. HOUSTON, P. COTTON, AND A. TYE. 1994. The role of Greater Yellow-headed Vultures Cathartes melambrotus as scavengers in neotropical forest. Ibis 136:193–196.
GUTIÉRREZ-CÁNOVAS, C., M. MOLEÓN, P. MATEO-TOMÁS, P. P. OLEA, E. SEBASTIÁN-GONZÁLEZ, AND J. A. SÁNCHEZ-ZAPATA. 2020. Large home range scavengers support higher rates of carcass removal. Functional Ecology doi:10.1111/1365-2435.13619.
HOCKING M. D., AND J. D. REYNOLDS. 2011. Impacts of salmon on riparian plant diversity. Science 331:1609–1612.
HOUSTON, D. C. 1979. The adaptations of scavengers. Pp. 263–286 in Serengeti, dynamics of an ecosystem (Sinclair, A. R. E., and M. N. Griffiths, eds.). University of Chicago Press, Chicago, Illinois.
HOUSTON, D. C. 1985. Evolutionary ecology of Afrotropical and Neotropical vultures in forests. Ornithological Monographs 36:856–864.
HOUSTON, D. C. 1986. Scavenging efficiency of turkey vultures in tropical forest. The Condor 88:318–323.
Houston, D. C. 1988. Competition for food between Neotropical vultures in forest. Ibis 130:402–417.
JĘDRZEJEWSKI, W., K. SCHMIDT, L. MILKOWSKI, B. JĘDRZEJEWSKA, AND H. OKARMA. 1993. Foraging by lynx and its role in ungulate mortality: the local (Bialowieza Forest) and the Palaearctic viewpoints. Acta Theriologica 38:385–403.
KLEIN, B. C. 1989. Effects of forest fragmentation on dung and carrion beetle communities in central Amazonia. Ecology 70:1715–1725.
KROFEL, M., I. KOS, AND K. JERINA. 2012. The noble cats and the big bad scavengers: effects of dominant scavengers on solitary predators. Behavioral Ecology and Sociobiology 66:1297–1304.
LAS BRISAS NATURE RESERVE ABOUT US. 2020. Retrieved from https://www.lasbrisasreserve.com/aboutus Accessed on January 17, 2020.
LEMON, W. C. 1991. Foraging behavior of a guild of Neotropical vultures. The Wilson Bulletin 103:698–702.
MALLON, J. M., K. SWING, AND D. MOSQUERA. 2013. Neotropical vulture scavenging succession at a capybara carcass in eastern Ecuador. Ornitología Neotropical 24:475–480.
MOLEÓN, M., J. A. SÁNCHEZ-ZAPATA, N. SELVA, J. A. DONÁZAR, AND N. OWEN-SMITH. 2014. Inter-specific interactions linking predation and scavenging in terrestrial vertebrate assemblages. Biological Reviews 89:1042–1054.
MOLEÓN, M., C. MARTÍNEZ-CARRASCO, O. C. MUELLERKLEIN, W. M. GETZ, C. MUÑOZ-LOZANO, AND J. A. SÁNCHEZ-ZAPATA. 2017. Carnivore carcasses are avoided by carnivores. Journal of Animal Ecology 86:1179–1191.
MOLEÓN, M., N. SELVA, M. M. QUAGGIOTTO, D. M. BAILEY, A. CORTÉS-AVIZANDA, AND T. L. DEVAULT. 2019. Carrion availability in space and time. Pp. 23–44 in Carrion Ecology and Management (Olea, P., P. Mateo-Tomas, and J. Sanchez-Zapata, eds.) Wildlife Research Monographs, vol. 2. Springer Nature. Cham, Switzerland.
MOLEÓN, M., N. SELVA, AND J. A. SÁNCHEZ-ZAPATA. 2020. The components and spatiotemporal dimensión of carrion biomass quantification. Trends in Ecology & Evolution 35:91–92.
MULLEN, D. A., AND F. A. PITELKA. 1972. Efficiency of winter scavengers in the Arctic. Arctic 25:169–248.
MUÑOZ-LOZANO, C., D. MARTÍN-VEGA, C. MARTÍNEZ-CARRASCO, J. A. SÁNCHEZ-ZAPATA, Z. MORALES-REYES, M. GONZÁLVEZ, AND M. MOLEÓN. 2019. Avoidance of carnivore carcasses by vertebrate scavengers enables colonization by a diverse community of carrion insect. Plos One 14:e0221890.
O’DONNELL, S. 1995. Necrophagy by neotropical swarm-founding wasps (Hymenoptera: Vespidae, Epiponini). Biotropica 27:133–136.
OKSANEN, L., M. AUNAPUU, T. OKSANEN, M. SCHNEIDER, P. EKERHOLM, P. A. LUNDBERG, T. ARMULIK, V. ARUOJA, AND L. BONDESTAD. 1997. Outlines of food webs in a low arctic tundra landscape in relation to three theories on trophic dynamics. Pp. 351–373. in Multitrophic Interaction in Terrestrial Systems. Blackwell Scientific Publications, Oxford, England.
OLSON, Z. H., J. C. BEASLEY, T. L. DEVAULT, AND O. E. RHODES, JR. 2012. Scavenger community response to the removal of a dominant scavenger. Oikos 121:77–84.
OLSON, Z. H., J. C. BEASLEY, AND O. E. RHODES, JR. 2016. Carcass type affects local scavenger guilds more than habitat connectivity. Plos One 11:e0147798.
PARDO-BARQUÍN, E., P. MATEO-TOMÁS, AND P. P. OLEA. 2019. Habitat characteristics from local landscape scales combine to shape vertebrate scavenging communities. Basic and Applied Ecology 34:126–139.
PARMENTER, R. R., AND J. A. MACMAHON. 2009. Carrion decomposition and nutrient cycling in a semiarid shrub-steppe ecosystem. Ecological Monographs 79:637–661.
POTIER, S., O. DURIEZ, A. CÉLÉRIER, J. L. LIEGEOIS, AND F. BONADONNA. 2019. Sight or smell: which senses do scavenging raptors use to find food? Animal Cognition 22:49–59.
PUTMAN, R. J. 1976. Energetics of the decomposition of animal carrion. PhD thesis, University of Oxford, Oxford, England.
PUTMAN, R. J. 1978. The role of carrion frequenting arthropods in the decay process. Ecological Entomology 3:133–139.
RAY, R. R., H. SEIBOLD, AND M. HEURICH. 2014. Invertebrates outcompete vertebrate facultative scavengers in simulated lynx kills in the Bavarian Forest National Park, Germany. Animal Biodiversity and Conservation 37:77–88.
ROMERO, A., J. MONTAÑO, A. SOTO CEDEÑO, AND G. OLIVEROS LAYOLA. 2020. First report of bullet ants (Parponera clavata) sequestering vertebrate carrion. Food Webs 24: e00151.
SAYER, E. J. 2006. Using experimental manipulation to assess the roles of leaf litter in the functioning of forest ecosystems. Biological Reviews 81:1–31.
SEBASTIÁN-GONZÁLEZ, E., M. MOLEÓN, J. P. GIBERT, F. BOTELLA, P. MATEO-TOMÁS, P. P. OLEA, P. R. GUIMARÃES JR, AND J. A. SÁNCHEZ-ZAPATA. 2016. Nested species-rich networks of scavenging vertebrates support high level of interspecific competition. Ecology 97:95–105.
SEBASTIÁN-GONZÁLEZ, E., J. MAGALHÃES BARBOSA, J. J. PÉREZ-GARCÍA, Z. MORALES-REYES, F. BOTELLA, P. P. OLEA, P. MATEO-TOMÁS, ET AL. 2019. Scavenging in the Anthropocene: human impact drives vertebrate scavenger species richness at a global scale. Global Change Biology 25:3005–3017.
SEBASTIÁN-GONZÁLEZ, E., Z. MORALES-REYES, F. BOTELLA, L. NAVES-ALEGRE, J. J. PÉREZ-GARCÍA, P. MATEO-TOMÁS, P. P. OLEA, ET AL. 2020. Network structure of vertebrate scavenger assemblages at the global scale: drivers and ecosystem functioning implications. Ecography 43:1143–1155.
SELVA, N., JȨDREJEWSKA, B., W. JȨDREJEWSKI, AND A. WAJRAK. 2005. Factors affecting carcass use by a guild of scavengers in European temperate woodland. Canadian Journal of Zoology 83:1590–1601.
SELVA, N., AND M. A. FORTUNA. 2007. The nested structure of a scavenger community. Proceedings of the Royal Society B - Biological Sciences 274:1101–1108.
SHEAN, B. S., L. MESSINGER, AND M PAPWORTH. 1993. Observations of differential decomposition on sun exposed v. sun shaded pig carrion in coastal Washington State. Journal of Forensic Sciences 38:938–949.
SHIVIK, J. A. 2006. Are vultures birds, and do snakes have venom, because of macro- and microscavenger conflict? BioScience 56:819–823.
STIEGLER, J., C. VON HOERMANN, J. MÃœLLER, M. E. BENBOW, AND M. HEURICH. 2020. Carcass provisioning for scavenger conservation in a temperate forest ecosystem. Ecosphere 11:e03063.
SUGIURA, S., R. TANAKA, H. TAKI, AND N. KANZAKI. 2013. Differential responses of scavenging arthropods and vertebrates to forest loss maintain ecosystem function in a heterogeneous landscape. Biological conservation 159:206–213.
SUGIURA, S., AND M. HAYASHI. 2018. Functional compensation by insular scavengers: the relative contributions of vertebrates and invertebrates vary among islands. Ecography 41:1173–1183.
TOWNE, E. G. 2000. Prairie vegetation and soil nutrient responses to ungulate carcasses. Oecologia 122:232–239.
TURNER, K. L., E. F. ABERNETHY, L. M. CONNER, O. E. RHODES JR., AND J. C. BEASLEY. 2017. Abiotic and biotic factors modulate carrion fate and vertebrate scavenging communities. Ecology 98:2413–2424.
TYLER, N. J. C., AND N. A. ØRITSLAND. 1999. Varig utstabilitet og bestandsregulering hos svalbardrein. Norsk Polarinstitutt Meddelelser 150:125–138.
UCHA, J. L., AND T. G. SANTOS. 2017. Death and life on the roadway: scavenging behavior of the green racer snake Philodryas patagoniensis (Girard, 1858)(Dipsadidae). Herpetology Notes 10:439–441.
VILLEGAS-PATRACA, R., S. MACÍAS-SÁNCHEZ, I. MACGREGOR-FORS, AND C. MUÑOZ-ROBLES. 2012. Scavenger removal: Bird and bat carcass persistence in a tropical wind farm. Act Oecologica 43:121–125.
WILSON, E. E., AND E. M. WOLKOVICH. 2011. Scavenging: how carnivores and carrion structure communities. Trends in Ecology and Evolution 26:129–135.
WOLF, J. M., AND J. P. GIBBS. 2004. Silphids in urban forests: diversity and function. Urban Ecosystems 7:371–384.
YANG, L. H. 2004. Periodical cicadas as resources pulses in North American forests. Science 306:1565–1567.
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