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Hyena as a predator of small mammals? Taphonomic analysis from the site of Bois Roche, France

Published online by Cambridge University Press:  30 May 2018

Jim Williams ,
Peter Andrews ,
Sara García-Morato ,
Paola Villa  and
Yolanda Fernández-Jalvo
Jim Williams
Affiliation:
Historic England, Windsor House, Cliftonville, Northampton NN1 5BE, United Kingdom. E-mail: [email protected]
Peter Andrews
Affiliation:
Department of Palaeontology, Natural History Museum, Cromwell Road, London 5BD-7SW, United Kingdom. E-mail: [email protected]
Sara García-Morato
Affiliation:
Universidad Complutense de Madrid, Department of Palaeontology, Jose Antonio Novais 12, 28040 Madrid, Spain; and Museo Nacional de Ciencias Naturales, José Gutiérrez Abascal 2, 28006 Madrid, Spain. E-mail: [email protected]
Paola Villa
Affiliation:
University of Colorado Museum, Boulder, UCB 265, Bruce Curtis Building, Boulder, Colorado 80309-0265, U.S.A.; and UMR 5199-PACEA, Institut de Préhistoire et Géologie du Quaternaire, Université Bordeaux 1, Avenue des Facultés, 33405 Talence, France. E-mail: [email protected]
Yolanda Fernández-Jalvo
Affiliation:
Museo Nacional de Ciencias Naturales, José Gutiérrez Abascal 2, 28006 Madrid, Spain. E-mail: [email protected]
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Abstract

Feeding behaviors may differ between past and current predators due to differences in the environments inhabited by these species at different times. We provide an example of this behavioral variability in spotted hyena (Crocuta crocuta), for which our analysis of a late Pleistocene micromammal assemblage indicates that hyenas preyed upon small rodents, a feeding habit that is rarely observed today among hyenas.

The Bois Roche cave site is situated at the edge of a low bluff overlooking the floodplain of a small stream in Cherves-Richemont (Charente, France). The deposits are dated by electron spin resonance (ESR) to about 69.7 ± 4.1 Ka. Excavations at the site recovered fossil bones and teeth of large and small mammals, together with hyena coprolites. Water screening of the sediments produced large accumulations of rodent remains with low taxonomic diversity. Small mammal bones were recovered from hyena coprolites as well. Descriptions of small mammal bone modification, both from the sediments and coprolites, are reported here. The analysis yielded a distinct taphonomic pattern representative of large carnivores (over 30 kg), which differs from any other modern or fossil predator-accumulated microfaunal assemblage taphonomically analyzed to date. To our knowledge, previous studies of hyena diet have not recorded high concentrations of a single-rodent prey species. We conclude that the low species diversity of this small mammal assemblage most likely relates to a local abundance of the prey species due to an outbreak in the rodent population, rather than from specialist predator behavior and hunting technique.

Type
Articles
Information
Paleobiology , Volume 44 , Issue 3 , August 2018 , pp. 511 - 529
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© 2018 The Paleontological Society. All rights reserved. 

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References

Literature Cited

Andrews, P. 1983. Small mammal diversity at Olduvai Gorge. Pp. 77–85 in J. C. Brook and C. Grigson, eds. Animals and archaeology, Vol. 1. Hunters and their prey. British Archaeological Reports, International Series, Oxford.Google Scholar
Andrews, P. 1990. Owls, caves and fossils. Chicago University Press, Chicago.Google Scholar
Avery, D. M. 1992. The environment of early modern humans at Border Cave, South Africa: micromammalian evidence. Palaeogeography, Palaeoclimatology, Palaeoecology 91:71–87.Google Scholar
Bartram, L., and Villa, P.. 1998. The archaeological excavation of prehistoric hyena dens: why bother? Pp. 15–29 in J. P. Brugal, L. Meignen, and M. Patou-Mathis, eds. Economie préhistorique: les comportements de subsistance au Paléolithique. Actes des XVIII Rencontres Internationales d’Archéologie et d’Histoire d’Antibes. Editions APDCA, Sophia-Antipolis, France.Google Scholar
Bennett, E. A., Gorgé, O., Grange, T., Fernández-Jalvo, Y., and Geigl, E.-M.. 2016. Coprolites, paleogenomics and bone content analysis. Pp. 271–286 in Y. Fernández-Jalvo, T. King, L. Yepiskoposyan, and P. Andrews, eds. Azokh Cave and the Transcaucasian Corridor. Springer, Dordrecht, Netherlands.Google Scholar
Binford, L. R. 1981. Bones: ancient men and modern myths. Academic, New York.Google Scholar
Blain, H. A., and Villa, P.. 2006. Amphibians and squamate reptiles from the early Upper Pleistocene of Bois Roche Cave (Charente, southwestern France). Acta Zoologica Cracoviensia 49A:1–32.Google Scholar
Blumenschine, R. J., Cavallo, J. A., and Capaldo, S. D.. 1994. Competition for carcasses and early hominid behavioral ecology: a case study and conceptual framework. Journal of Human Evolution 27:197–213.Google Scholar
Bon, C., Berthonaud, V., Maksud, F., Labadie, K., Poulain, J., Artiguenave, F., Wincker, P., Aury, J. M., and Elalouf, J. M.. 2012. Coprolites as a source of information on the genome and diet of the cave hyena. Proceedings of the Royal Society of London B 279:2825–2830.Google Scholar
Bramwell, D., Yalden, D. W., and Yalden, P. E.. 1990. Ossum’s Eyrie Cave: an archaeological contribution to the recent history of vertebrates in Britain. Zoological Journal of the Linnean Society 98:1–25.Google Scholar
Brain, C. K. 1969. The contribution of Namib desert Hottentots to an understanding of australopithecine bone accumulations. Scientific Papers of the Namib Desert Research Station 39:13–22.Google Scholar
Brain, C. K. 1981. The hunters or the hunted? An introduction to African cave taphonomy. University of Chicago Press, Chicago.Google Scholar
Brantingham, P. J. 1998. Hominid–carnivore coevolution and invasion of the predatory guild. Journal of Anthropological Archaeology 17:237–353.Google Scholar
Buckland, P. C. 1976. The environmental evidence from the Church Street Roman sewer system. The archaeology of York 14/1. Council for British Archaeology, London.Google Scholar
Bunn, H. T., Harris, J. W. K., Isaac, G., Kaufulu, Z., Kroll, E., Schick, K., Toth, N., and Behrensmeyer, A. K.. 1980. FxJj50: an early Pleistocene site in northern Kenya. World Archaeology 12:109–136.Google Scholar
Demirel, A., Andrews, P., Yalçinkaya, I., and Ersoy, A.. 2011. The taphonomy and palaeoenvironmental implications of the small mammals from Karain Cave, Turkey. Journal of Archaeological Science 38:3048–3059.Google Scholar
Denys, C. 1986. Le gisement Pliocene de Laetoli (Tanzanie, Afrique de l’Est): analyse taphonomique des assemblages de microvertebres. Paleontographica 194:69–98.Google Scholar
d’Errico, F., and Villa, P.. 1997. Holes and grooves. The contribution of microscopy and taphonomy to the problem of art origins. Journal of Human Evolution 33:1–31.Google Scholar
Diamond, J. 2002. Evolution, consequences and future of plant and animal domestication. Nature 418:700–707.Google Scholar
Dobney, K., Jaques, D., Carrott, J., Hail, A., Issitt, M., and Large, F.. 1996. Biological remains from excavations at Carr Naze, Filey, N. Yorkshire: Technical Report. Reports from the Environmental Archaeology Unit, York 96/26. York Archaeological Trust, York, U.K.Google Scholar
Dodson, P., and Wexlar, D.. 1979. Taphonomic investigations of owl pellets. Paleobiology 5:275–284.Google Scholar
Fernández-Jalvo, Y. 1995. Small mammal taphonomy at La Trinchera de Atapuerca (Burgos, Spain). A remarkable example of taphonomic criteria used for stratigraphic correlations and palaeoenvironmental interpretations. Palaeogeography, Palaeoclimatology, Palaeoecology 114:167–195.Google Scholar
Fernández-Jalvo, Y., and Andrews, P.. 1992. Small mammal taphonomy of Gran Dolina, Atapuerca (Burgos), Spain. Journal of Archaeological Science 19:407–428.Google Scholar
Fernández-Jalvo, Y., and Andrews, P.. 2016. Atlas of taphonomy. Springer, New York.Google Scholar
Fernández-Jalvo, Y., Denys, C., Andrews, P., Williams, T., Dauphin, Y., and Humphrey, L.. 1998. Taphonomy and palaeoecology of Olduvai Bed-1 (Pleistocene, Tanzania). Journal of Human Evolution 34:137–172.Google Scholar
Fernández-Jalvo, Y., Andrews, P., Sevilla, P., and Requejo, V.. 2014. Digestion versus abrasion features in rodent bones. Lethaia 47:323–336.Google Scholar
Fernández-Jalvo, Y., Andrews, P., Denys, C., Sesé, C., Stoetzel, E., Marin-Monfort, D., and Pesquero, M. D.. 2016. Taphonomy for taxonomists: implications of predation in small mammal studies. Quaternary Science Reviews 139:138–157.Google Scholar
Gómez, G. N. 2003. Análisis Tafonómico y Paleoecológico de micro y mesomamíferos del sitio arqueológico de Arroyo Seco (Partido de Tres Arroyos, Buenos Aires, Argentina). Ph.D. thesis. University Complutense, Madrid.Google Scholar
Goldberg, P. 2001. Some micromorphological aspects of prehistoric cave deposits. Cahiers d’Archèologie du CELAT, Quebec 10:161–175.Google Scholar
Harrison, T. 2011. Coprolites: taphonomic and paleoecological implications. Pp. 279–292 in T. Harrison, ed. Paleontology and geology of Laetoli: human evolution in context, Vol. 1. Geology, geochronology, paleoecology and paleoenvironment. Springer, Dordrecht, Netherlands.Google Scholar
Haynes, G. 1983. A guide for differentiating mammalian carnivore taxa responsible for gnaw damage in herbivore limb bones. Paleobiology 9:164–172.Google Scholar
Hill, A. 1984. Hyaenas and hominids: taphonomy and hypothesis testing. Pp. 111–128 in R. Foley, ed. Hominid evolution and community ecology. Academic, London.Google Scholar
Hofer, H. 1998. Spotted hyaena Crocuta crocuta (Erxleben, 1777). Pp. 29–38 in M. G. L. Mills, and H. Hofer, eds. Hyaenas: status survey and conservation action plan. IUCN, Gland, Switzerland.Google Scholar
Holekamp, K. E. 2007. Questioning the social intelligence hypothesis. Trends in Cognitive Sciences 11:65–69.Google Scholar
Holekamp, K. E., and Smale, L.. 1990. Provisioning and food sharing by lactating spotted hyenas, Crocuta crocuta (Mammalia, Hyaenidae). Ethology 86:191–202.Google Scholar
Horwitz, L. K., and Goldberg, P.. 1989. A study of Pleistocene and Holocene hyaena coprolites. Journal of Archaeological Science 16:71–94.Google Scholar
Jenks, S. M., and Werdelin, L.. 1998. Taxonomy and systematics of living hyaenas (Family Hayenidae). Pp. 8–17 in M. G. L. Mills, and H. Hofer, eds. Hyaenas: status survey and conservation action plan. IUCN, Gland, Switzerland.Google Scholar
Korb, J. 2000. Methods to study elusive spotted hyenas in the Comoé National Park, Côte d’Ivoire. Hyaena Specialist Group Newsletter IUCN 7:3–12.Google Scholar
Korth, W. W. 1979. Taphonomy of microvertebrate fossil assemblages. Annals of Carnegie Museum 48:235–285.Google Scholar
Kruuk, H. 1972. The spotted hyaena. A study of predation and social behavior. University of Chicago Press, Chicago.Google Scholar
Kuhn, B. 2011. Hyaenids: taphonomy and implications for the palaeoenvironment. Cambridge Scholars Publishing, Newcastle upon Tyne, U.K.Google Scholar
Kurten, B. 1968. Pleistocene mammals of Europe. Weidenfeld and Nicholson, London.Google Scholar
Larkin, N. R., Alexander, J., and Lewis, M. D.. 2000. Using experimental studies of recent faecal material to examine hyaena coprolites from the West Runton Freshwater Bed, Norfolk, U.K. Journal of Archaeological Science 27:19–31.Google Scholar
Lewis, M. 2011. Pleistocene hyaena coprolite palynology in Britain: implications for the environments of early humans. Pp. 263–278 in N. M. Ashton, S. G. Lewis, and C. B. Stringer, eds. The ancient human occupation of Britain. Elsevier, Amsterdam.Google Scholar
López, J. M., Rossi, M. I., Tabeni, S., Bender, B., and Chiavazza, H.. 2017. Taphonomic analysis of small mammal bone remains preyed upon by wildcats (Carnivora: Felidae) from the central Monte Desert (Mendoza, Argentina). Boreas 47:282–293.Google Scholar
Lupo, K. D., and Schmitt, D. N.. 2005. Small prey hunting technology and zooarchaeological measures of taxonomic diversity and abundance: ethnoarchaeological evidence from Central African forest foragers. Journal of Anthropological Archaeology 24:335–353.Google Scholar
Maas, M. C. 1985. Taphonomy of a Late Eocene microvertebrate locality, Wind River Basin, Wyoming (U.S.A.). Palaeogeography, Palaeoclimatology, Palaeoecology 52:123–142.Google Scholar
Marra, C., Villa, P., Beuval, C., Bonfiglio, L., and Goldberg, P.. 2004. Same predator, variable prey: taphonomy of two Upper Pleistocene hyena dens in Sicily and SW France. In J. P. Brugal, and P. Fosse, eds. Humans and carnivores. Revue de Paléobiologie, Special Issue 23: 787–801.Google Scholar
Mayhew, D. F. 1977. Avian predators as accumulators of fossil mammal material. Boreas 6:25–31.Google Scholar
Medina, M. E., Teta, P., and Rivero, D.. 2012. Burning damage and small mammal human consumption in Quebrada del Real 1 (Cordoba, Argentina): an experimental approach. Journal of Archaeological Science 39:737–743.Google Scholar
Mills, G., and Hofer, H.. 1998. Hyaenas: status survey and conservation action plan. World Conservation Union, Devon, U.K.Google Scholar
Mills, M. G. L. 1990. Kalahari hyaenas: comparative behavioral ecology of two species. Unwin Hyman, London.Google Scholar
Mondini, M. 2000. Tafonomía de abrigos rocosos de la Puna. Formación de conjuntos escatológicos por zorros y sus implicancias arqueológicas. Archaeofauna 9:151–164.Google Scholar
Montalvo, C. I., Pessino, M. E. M., and González, V. H.. 2007. Taphonomic analysis of remains of mammals eaten by pumas (Puma concolor Carnivora, Felidae) in central Argentina. Journal of Archaeological Science 34:2151–2160.Google Scholar
Montalvo, C. I., Bisceglia, S., Kin, M. S., and Sosa, R. A.. 2012. Taphonomic analysis of rodent bone accumulations produced by Geoffrey’s cat (Leopardus geoffroyi, Carnivora, Felidae) in Central Argentina. Jouirnal of Archaeological Science 39:1933–1941.Google Scholar
Murphey, P. C., Torick, L. L., Bray, E. S., Chandler, R., and Evanoff, E.. 2001. Taphonomy, fauna and depositional environment of the Omomys Quarry, an unusual accumulation from the Bridger Formation (Middle Eocene) of Southwestern Wyoming (USA). Pp. 361–402 in G. F. Gunnell, ed. Eocene biodiversity: unusual occurrences and rarely sampled habitats. Kluwer Academic/Plenum, New York.Google Scholar
Pesquero, M. D., Salesa, M. J., Espílez, E., Mampel, L., Siliceo, G., and Alcalá, L.. 2011. An exceptionally rich hyaena coprolites concentration in the Late Miocene mammal fossil site of La Roma 2 (Teruel, Spain): taphonomical and palaeoenvironmental inferences. Palaeogeography, Palaeoclimatology, Palaeoecology 311:30–37.Google Scholar
Pokines, J. T., and Kerbis Peterhans, J. C.. 2007. Spotted hyena (Crocuta crocuta) den use and taphonomy in the Masai Mara National Reserve, Kenya. Journal of Archaeological Science 34:1914–1931.Google Scholar
Potts, R. 1989. Olorgesailie: new excavations and findings in Early and Middle Pleistocene contexts, southern Kenya rift valley. Journal of Human Evolution 18:477–484.Google Scholar
Prendergast, M. E., and Dominguez-Rodrigo, M.. 2008. Taphonomic analyses of a hyena den and a natural-death assemblage near Lake Eyasi (Tanzania). Journal of Taphonomy 6:301–335.Google Scholar
R Core Team 2017. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org.Google Scholar
Rodríguez-Hidalgo, A. J., Saladié, P., and Canals, A.. 2011. Following the white rabbit: a case of small game procurement site in the Upper Palaeolithic (Sala de las Chimeneas, Maltravieso Cave, Spain). International Journal of Osteoarchaeology 23:34–54.Google Scholar
Rohland, N., Pollack, J. L., Nagel, D., Beauval, C., Airvaux, J., Pääbo, S., and Hofreiter, M.. 2005. The population history of extant and extinct hyenas. Molecular Biology and Evolution 22:2435–2443.Google Scholar
Sealy, J. 2006. Diet, mobility and settlement patterns among Holocene hunter-gatherers in southernmost Africa. Current Anthropology 47:569–595.Google Scholar
Sesé, C., and Villa, P.. 2008. Micromammals (rodents and insectivores) from the early Upper Pleistocene cave site of Bois Roche (Charente, France): systematics and paleoclimatology. Geobios 41:399–414.Google Scholar
Shipman, P., and Walker, A.. 1989. The costs of becoming a predator. Journal of Human Evolution 18:373–392.Google Scholar
Skinner, J. D., Haupt, M. A., Hoffmann, M., and Dott, H. M.. 1998. Bone collection by brown hyaenas Hyaena brunnea in the Namib Desert: rate of accumulation. Journal of Archeological Science 25:69–71.Google Scholar
Stiner, M. C. 1991. Food procurement and transport by human and non-human predators. Journal of Archaeological Science 18:455–482.Google Scholar
Stiner, M. C. 1994. Honor among thieves. A zooarchaeological study of Neandertal ecology. Princeton University Press, Princeton, N.J.Google Scholar
Stiner, M. C. 2004. Comparative ecology and taphonomy of spotted hyenas, humans and wolves in Pleistocene Italy. Revue de Paléobiologie 23:771–785.Google Scholar
Stiner, M. C., Munro, N. D., and Surovell, T. A.. 2000. The tortoise and the hare: small game use, the broad spectrum revolution, and Paleolithic demography. Current Anthropology 41:39–79.Google Scholar
Sutcliffe, A. J. 1970. Spotted hyena: crusher, gnawer, digestor and collector of bones. Nature 227:1110–1113.Google Scholar
Turner, A. 1990. The evolution of the guild of larger terrestrial carnivores during the Plio-Pleistocene in Africa. Geobios 23:349–368.Google Scholar
Turner, A., and Anton, M.. 1996. The giant hyaena, Pachycrocuta brevirostris (Mammalia, Carnivora, Hyaenidae). Geobios 29:455–468.Google Scholar
Villa, P., and Bartram, L.. 1996. Flaked bone from a hyena den. Paléo 8:1–22.Google Scholar
Villa, P., and d’Errico, F.. 2001. Bone and ivory points in the Lower and Middle Paleolithic of Europe. Journal of Human Evolution 41:69–112.Google Scholar
Villa, P., and Soressi, M.. 2000. Stone tools in carnivore sites: the case of Bois Roche. Journal of Anthropological Research 56:187–215.Google Scholar
Villa, P., Castel, J. C., Bourdillat, V., Beauval, C., and Goldberg, P.. 2004. Human and carnivore sites in the European Middle and Upper Paleolithic: similarities and differences in bone modification and fragmentation. In J. P. Brugal, and P. Fosse, eds. Humans and carnivores. Revue de Palébiologie, Special Issue 23: 705–730.Google Scholar
Villa, P., Sánchez-Goñi, M.F., Cuenca Bescós, G., Grün, R., Ajas, A., García Pimienta, J.C., and Lees, W.. 2010. The archaeology and paleoenvironment of an Upper Pleistocene hyena den: an integrated approach. Journal of Archaeological Science 37:919–935.Google Scholar
Werdelin, L., and Solounias, N.. 1991. The Hyaenidae: taxonomy, systematics and evolution. Fossils and Strata 30:1–104.Google Scholar
Wesselman, H. B. 1984. The Omo micromammals. Contributions to vertebrate evolution 7. Karger, London.Google Scholar
Wiesel, I. 2006. Predatory and foraging behaviour of brown hyenas (Parahyaena brunnea (Thunberg, 1820) at Cape fur seal (Arctocephalus pusillus pusillus Schreber, 1776) colonies. University of Hamburg, Hamburg, Germany.Google Scholar
Williams, J. 2003. Bones of comprehension: the analysis of small mammal predator–prey relationships. Pp. 341–358 in P. Kelley, ed. Predator–prey interactions in the fossil record. Kluwer, New York.Google Scholar
Williams, J. P. 1997. What is the contribution of small mammals to our understanding of palaeoecology, how is it relevant to archaeology, and how can taphonomic studies aid in that interpretation. Undergraduate dissertation. Department of Archaeology and Prehistory, University of Sheffield, Sheffield, U.K.Google Scholar