Skip to main content

Feeding ecology and habitat preferences of top predators from two Miocene carnivore-rich assemblages

  • M. Soledad Domingo (a1), Laura Domingo (a2) (a3) (a4), Juan Abella (a5) (a6), Alberto Valenciano (a2) (a3), Catherine Badgley (a7) and Jorge Morales (a8)...

Carnivore-rich fossil sites are uncommon in the fossil record and, accordingly, provide valuable opportunities to study predators from vantages that are rarely applied to ancient faunas. Through stable isotopes of carbon and a Bayesian mixing model, we analyze time-successive (nearly contemporaneous), late Miocene carnivoran populations from two fossil sites (Batallones-1 and Batallones-3) from central Spain. Stable isotopes of carbon in tooth enamel provide a reliable and direct methodology to track ancient diets. These two carnivoran-dominated fossil sites display differences in the composition and abundance of the carnivoran species, with some species present at both sites and some present only at one site. This disparity has been interpreted as the consequence of habitat differences between Batallones-1, the older site, and Batallones-3, the younger site. However, carbon isotope values of carnivore and herbivore tooth enamel suggest a common habitat of C3 woodland originally present at both sites. The differences in the carnivoran faunas rather may be the consequence of the dynamics of species entrance and exit from the Madrid Basin during the time elapsed between Batallones-1 and Batallones-3 and changes in population densities due to biotic factors. We infer higher levels of interspecific competition in Batallones-3 than in Batallones-1 because of the larger number of similar-sized, sympatric predators; the clear overlap in their δ13C values (except for the amphicyonid Magericyon anceps); and similarity of their preferred prey: the hipparionine horses. Finally, carbon stable isotopic composition of Indarctos arctoides teeth implies that this ursid was a carnivorous omnivore rather than a herbivorous omnivore. This work demonstrates the insights that stable isotopes can provide in characterizing the feeding ecology and trophic interactions of ancient carnivoran taxa.

Hide All
Abella J. 2011. Indarctos arctoides Depéret, 1895 (Carnivora, Mammalia) del yacimiento vallesiense de Batallones 3 (Cuenca de Madrid). Ph.D. thesis. Universidad Autónoma de Madrid, Madrid, Spain.
Abella J., Domingo M. S., Valenciano A., Montoya P., and Morales J.. 2011. La asociación de carnívoros de Batallones 3, Mioceno Superior del Cerro de los Batallones, Cuenca de Madrid. Paleontologia i Evolució, Memòria Especial 5:2124.
Abella J., Valenciano A., Pérez-Ramos A., Montoya P., and Morales J.. 2013. On the socio–sexual behaviour of the extinct ursid Indarctos arctoides: an approach based on its baculum size and morphology. PLoS ONE 8:e73711.
Abella J., Montoya P., and Morales J.. 2014. Paleodiversity of the Superfamily Ursoidea (Carnivora, Mammalia) in the Spanish Neogene, related to environmental changes. Journal of Iberian Geology 40:1118.
Abella J., Pérez-Marcos A., Valenciano A., Alba D. M., Ercoli M. D., Hontecillas D., Montoya P., and Morales J.. 2015. Tracing the origin of the panda’s thumb. Science of Nature 102:35.
Bump J. K., Fox-Dobbs K., Bada J. L., Koch P. L., Peterson R. O., and Vucetich J. A.. 2007. Stable isotopes, ecological integration and environmental change: wolves record atmospheric carbon isotope trend better than tree rings. Proceedings of the Royal Society B 274:24712480.
Calvo J. P., Alonso Zarza A. M., and García del Cura M. A.. 1989. Models of Miocene marginal lacustrine sedimentation in response to varied depositional regimes and source areas in the Madrid Basin (Central Spain). Palaeogeography, Palaeoclimatology, Palaeoecology 70:199214.
Calvo J. P., Pozo M., Silva P. G., and Morales J.. 2013. Pattern of sedimentary infilling of fossil mammal traps formed in pseudokarst at Cerro de los Batallones, Madrid Basin, central Spain. Sedimentology 60:16811708.
Clementz M. T. 2012. New insight from old bones: stable isotope analysis of fossil mammals. Journal of Mammalogy 93:368380.
Clementz M. T., Fox-Dobbs K., Wheatley P. V., Koch P. L., and Doak D. F.. 2009. Revisiting old bones: coupled carbon isotope analysis of bioapatite and collagen as an ecological and palaeoecological tool. Geological Journal 44:605620.
Domingo L., Koch P. L., Grimes S. T., Morales J., and López-Martínez N.. 2012. Isotopic paleoecology of mammals and the Middle Miocene Cooling event in the Madrid Basin (Spain). Palaeogeography, Palaeoclimatology, Palaeoecology 339–341:98113.
Domingo L., Koch P., Hernández Fernández M., Fox D. L., Domingo M. S., and Alberdi M. T.. 2013. Late Neogene and Early Quaternary paleoenvironmental and paleoclimatic conditions in Southwestern Europe: isotopic analyses on mammalian taxa. PLoS ONE 8:e63739.
Domingo M. S., Alberdi M. T., and Azanza B.. 2007. A new quantitative biochronological ordination for the Upper Neogene mammalian localities of Spain. Palaeogeography, Palaeoclimatology, Palaeoecology 255:361376.
Domingo M. S., Alberdi M. T., Azanza B., Silva P. G., and Morales J.. 2013a. Origin of an assemblage massively dominated by carnivorans from the Miocene of Spain. PLoS ONE 8:e63046.
Domingo M. S., Domingo L., Badgley C., Sanisidro O., and Morales J.. 2013b. Resource partitioning among top predators in a Miocene food web. Proceedings of the Royal Society B 280:20122138.
Domingo M. S., Badgley C., Azanza B., DeMiguel D., and Alberdi M. T.. 2014. Diversification of mammals from the Miocene of Spain. Paleobiology 40:196200.
Donohue S. L., DeSantis L. R. G., Schubert B. W., and Ungar P. S.. 2013. Was the giant short-faced bear a hyper-scavenger? A new approach to the dietary study of ursids using dental microwear textures. PLoS ONE 8:e77531.
Farlow J. O. 1993. On the rareness of big, fierce animals: speculations about the body sizes, population densities, and geographic ranges of predatory mammals and large carnivorous dinosaurs. American Journal of Science 293:167199.
Feranec R. S. 2003. Stable isotopes, hypsodonty, and the paleodiet of Hemiauchenia (Mammalia: Camelidae): a morphological specialization creating ecological generalization. Paleobiology 29:230242.
Feranec R. S. 2004. Isotopic evidence of saber-tooth development, growth rate, and diet from the adult canine of Smilodon fatalis from Rancho La Brea. Palaeogeography, Palaeoclimatology, Palaeoecology 206:303310.
Feranec R. S., and DeSantis L. R. G.. 2014. Understanding specifics in generalist diets of carnivorans by analyzing stable carbon isotope values in Pleistocene mammals of Florida. Paleobiology 40:477493.
Feranec R. S., García N., Díez J. C., and Arsuaga J. L.. 2010. Understanding the ecology of mammalian carnivorans and herbivores from Valdegova cave (Burgos, northern Spain) through stable isotope analysis. Palaeogeography, Palaeoclimatology, Palaeoecology 297:263272.
Friedli H., Lotscher H., Oeschger H., Siegenthaler U., and Stauver B.. 1986. Ice core record of the 13C/12C ratio of atmospheric CO2 in the past two centuries. Nature 324:237238.
Fox-Dobbs K., Wheatley P. V., and Koch P. L.. 2006. Carnivore specific bone bioapatite and collagen carbon isotope fractionations: case studies of modern and fossil grey wolf populations. American Geophysical Union, Fall Meeting 2006, Abstracts, no. B53C-0366.
García García N., Feranec R. S., Arsuaga J. L., Bermúdez de Castro J. M., and Carbonell E.. 2009. Isotopic analysis of the ecology of herbivores and carnivores from the Middle Pleistocene deposits of the Sierra de Atapuerca, northern Spain. Journal of Archaeological Science 36:11421151.
Gómez Cano A. R., Hernández Fernández M., and Álvarez-Sierra M. A.. 2011. Biogeographic provincialism in rodent faunas from the Iberoccitanian Region (southwestern Europe) generates severe diachrony within the Mammalian Neogene (MN) biochronologic scale during the Late Miocene. Palaeogeography, Palaeoclimatology, Palaeoecology 307:193204.
Higgins P., and MacFadden B. J.. 2004. “Amount effect” recorded in oxygen isotopes of Late Glacial horse (Equus) and bison (Bison) teeth from the Sonoran and Chihuahuan deserts, southwestern United States. Palaeogeography, Palaeoclimatology, Palaeoecology 206:337353.
Karanth K. U., and Sunquist M. E.. 2000. Behavioural correlates of predation by tiger (Panthera tigris), leopard (Panthera pardus) and dhole (Cuon alpinus) in Nagarahole, India. Journal of Zoology 250:255265.
Koch P. 2007. Isotopic study of the biology of modern and fossil vertebrates. Pp. 99154 in R. Michener, and K. Lajtha, eds. Stable isotopes in ecology and environmental science. Blackwell, Boston.
Koch P. L., Tuross N., and Fogel M. L.. 1997. The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. Journal of Archaeological Science 24:417429.
Kohn M. J., and Cerling T. E.. 2002. Stable isotope compositions of biological apatite. Reviews in Mineralogy and Geochemistry 48:455488.
Kohn M. J., and McKay M. P.. 2012. Paleoecology of late Pleistocene–Holocene faunas of Eastern and Central Wyoming, USA, with implications for LGM climate models. Palaeogeography, Palaeoclimatology, Palaeoecology 326–328:4253.
Kohn M. J., McKay M. P., and Knight J. L.. 2005. Dining in the Pleistocene—who’s on the menu? Geology 33:649652.
Lee-Thorp J. A., Sponheimer M., and Luyt J.. 2007. Tracking changing environments using stable carbon isotopes in fossil tooth enamel: an example from the South African hominin sites. Journal of Human Evolution 53:595601.
Liu L. 2003. Chinese fossil Suoidea. Systematics, evolution and paleoecology. Ph.D. thesis. Univeristy of Helsinki, Helsinki, Finland.
López-Antoñanzas R., Peláez-Campomanes P., Álvarez-Sierra M. A., and García-Paredes I.. 2010. New species of Hispanomys (Rodentina, Cricetodontinae) from the Upper Miocene of Batallones (Madrid, Spain). Zoological Journal of the Linnean Society 160:725747.
MacFadden B. J., and Cerling T. E.. 1996. Mammalian herbivore communities, ancient feeding ecology, and carbon isotopes: a 10 million-year sequence from the Neogene of Florida. Journal of Vertebrate Paleontology 16:103115.
Marino B. D., and McElroy M. B.. 1991. Isotopic composition of atmospheric CO2 inferred from carbon in C4 plant cellulose. Nature 349:127131.
Matson S. D., Rook L., Oms O., and Fox D. L.. 2012. Carbon isotopic record of terrestrial ecosystems spanning the Late Miocene extinction of Oreopithecus bambolii, Baccinello Basin (Tuscany, Italy). Journal of Human Evolution 63:127139.
Monescillo M. F. G., Salesa M. J., Antón M., Siliceo G., and Morales J.. 2014. Machairodus aphanistus (Felidae, Machairodontinae, Homotherini) from the Late Miocene (Vallesian, MN10) site of Batallones-3 (Torrejón de Velasco, Madrid, Spain). Journal of Vertebrate Paleontology 34:699709.
Moore J. W., and Semmens B. X.. 2008. Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11:470480.
Morales J., Pozo M., Silva P. G., Domingo M. S., López-Antoñanzas R., Sierra M. A. Álvarez, Antón M., Escorza C. Martín, Quiralte V., Salesa M. J., Sánchez I. M., Azanza B., Calvo J. P., Carrasco P., García-Paredes I., Knoll F., Fernández M. Hernández, Ostende L. van den Hoek, Merino L., van der Meulen A. J., Montoya P., Peigné S., Peláez-Campomanes P., Sánchez-Marco A., Turner A., Abella J., Alcalde G. M., Andrés M., DeMiguel D., Cantalapiedra J. L., Fraile S., Yelo B. A. García, Cano A. R. Gómez, Guerrero P. López, Pérez A. Oliver, and Siliceo G.. 2008. El sistema de yacimientos de mamíferos miocenos del Cerro de los Batallones, Cuenca de Madrid: estado actual y perspectivas. Paleontologica Nova SEPAZ 8:41117.
Moyà-Solà S. 1983. Los Boselaphini (Bovidae, Mammalia) del Neógeno de la Península Ibérica. Ph.D. thesis. Universitat Autònoma de Barcelona, Barcelona, Spain.
Owen-Smith N., and Mills M. G. L.. 2008. Predator–prey size relationships in an African large-mammal food web. Journal of Animal Ecology 77:173183.
Parnell A. C., Inger R., Bearhop S., and Jackson A. L.. 2010. Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672.
Peigné S., Salesa M. J., Antón M., and Morales J.. 2008. A new Amphicyonine (Carnivora: Amphicyonidae) from the Upper Miocene of Batallones-1, Madrid, Spain. Palaeontology 51:943965.
Phillips D. L., and Gregg J. W.. 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261269.
Phillips D. L., Newsome S. D., and Gregg J. W.. 2005. Combining sources in stable isotope mixing models: alternative methods. Oecologia 144:520527.
Phillips D. L., Inger R., Bearhop S., Jackson A. L., Moore J. W., Parnell A. C., Semmens B. X., and Ward E. J.. 2014. Best practices for use of stable mixing models in food-web studies. Canadian Journal of Zoology 92:823835.
Plummer M. 2003. JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In K. Hornik, F. Leisch, and A. Zeileis, eds. Proceedings of the Third International Workshop on Distributed Statistical Computing. Vienna, Austria.
Pozo M., Calvo J. P., Silva P. G., Morales J., Peláez-Campomanes P., and Nieto M.. 2004. Geología del sistema de yacimientos de mamíferos miocenos del Cerro de los Batallones, Cuenca de Madrid. Geogaceta 35:143146.
R Development Core Team. 2015. R: a language and environment for statistical computing.
Ripple W. J., Estes J. A., Beschta R. L., Wilmers C. C., Ritchie E. G., Hebblewhite M., Berger J., Elmhagen B., Letnic M., Nelson M. P., Schmitz O. J., Smith D. W., Wallach A. D., and Wirsing A. J.. 2014. Status and ecological effects of the world’s largest carnivores. Science 343, doi: 10.1126/science.1241484.
Salesa M. J., Antón M., Turner A., and Morales J.. 2006. Inferred behaviour and ecology of the primitive sabre-toothed cat Paramachairodus ogygia (Felidae, Machairodontinae) from the late Miocene from Spain. Journal of Zoology 268:243254.
Salesa M. J., Antón M., Morales J., and Peigné S.. 2012. Systematics and phylogeny of the small felines (Carnivora, Felidae) from the Late Miocene of Europe: a new species of Felinae from the Vallesian of Batallones (MN10, Madrid, Spain). Journal of Systematic Palaeontology 10:87102.
Siliceo G., Salesa M. J., Antón M., Monescillo M. F. G., and Morales J.. 2014. Promegantereon ogygia (Felidae, Machairodontinae, Smilodontini) from the Vallesian (Late Miocene, MN10) of Spain: morphological and functional differences in two noncontemporary populations. Journal of Vertebrate Paleontology 34:407418.
Soibelzon L. H. 2012. Los Ursidae, Carnivora Fissipedia, fósiles de la República Argentina: aspectos sistemáticos y paleoecológicos. Universidad Nacional de La Plata, La Plata, Argentina.
Soibelzon L. H., Grinspan G. A., Bocherens H., Acosta W. G., Jones W., Blanco E. R., and Prevosti F.. 2014. South American giant short-faced bear (Arctotherium angustidens) diet: evidence from pathology, morphology, stable isotopes, and biomechanics. Journal of Paleontology 88:12401250.
Spencer L. M., Van Valkenburgh B., and Harris J. M.. 2003. Taphonomic analysis of large mammals recovered from the Pleistocene Rancho La Brea tar seeps. Paleobiology 29:561575.
Stock B. C., and Semmens B. X.. 2013. MixSIAR GUI User Manual, Version 1.0. (accessed October 2014).
Terborgh J., Holt R. D., and Estes J. A.. 2010. Trophic cascades: what they are, how they work, and why they matter. Pp. 135in J. Terborgh, and J. A. Estes, eds. Trophic cascades. Island Press, Washington, D.C.
Tipple B. J., Meyers S. R., and Pagani M.. 2010. Carbon isotope ratio of Cenozoic CO2: a comparative evaluation of available geochemical proxies. Paleoceanography 25:PA3202.
Tütken T., Kaiser T. M., Venneman T., and Merceron G.. 2013. Opportunistic feeding strategy for the earlie. st Old World hypsodont equids: evidence from stable isotope and dental wear proxies. PLoS ONE 8:e74463.
Valenciano A., Abella J., Sanisidro O., Hartstone-Rose A., Álvarez-Sierra M. A., and Morales J.. 2015. Complete description of the skull and mandible of the giant mustelid Eomellivora piveteaui Ozansoy, 1965 (Mammalia, Carnivora, Mustelidae) from Batallones (MN10), Late Miocene (Madrid, Spain). Journal of Vertebrate Paleontology 35:e934570.
van Dam J. A., Alcalá L., Alonso Zarza A., Calvo J. P., Garcés M., and Krijgsman W.. 2001. The Upper Miocene mammal record from the Teruel-Alfambra region (Spain). The MN system and continental stage/age concepts discussed. Journal of Vertebrate Paleontology 21:367385.
van Dam J. A., Abdul Aziz H., Álvarez Sierra M. A., Hilgen F. J., van den Hoek Ostende L. W., Lourens L. J., Mein P., van der Meulen A. J., and Peláez-Campomanes P.. 2006. Long-period astronomical forcing of mammal turnover. Nature 443:687691.
Van Valkenburgh B. 2007. Déja vù: the evolution of feeding morphologies in the Carnivora. Integrative and Comparative Biology 47:147163.
White F. 1983. The vegetation of Africa. Vol. 20 of natural resources research. United Nations Scientific and Cultural Organization, Paris.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0094-8373
  • EISSN: 1938-5331
  • URL: /core/journals/paleobiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Altmetric attention score

Full text views

Total number of HTML views: 8
Total number of PDF views: 50 *
Loading metrics...

Abstract views

Total abstract views: 270 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 17th January 2018. This data will be updated every 24 hours.