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Ancient ecology of 15-million-year-old browsing mammals within C3 plant communities from Panama

Oecologia volume 140, pages 169–182 (2004)Cite this article

Abstract

Middle Miocene mammals are known from ~15 million-year-old sediments exposed along the Panama Canal of Central America, a region that otherwise has an exceedingly poor terrestrial fossil record. These land mammals, which represent a part of the ancient terrestrial herbivore community, include an oreodont Merycochoerus matthewi, small camel-like protoceratid artiodactyl Paratoceras wardi, two horses Anchitherium clarencei and Archaeohippus sp., and two rhinos Menoceras barbouri and Floridaceras whitei. Bulk and serial carbon and oxygen isotope analyses of the tooth enamel carbonate allow reconstruction of the ancient climate and ecology of these fossil mammals. Ancient Panama had an equable climate with seasonal temperature and rainfall fluctuations less than those seen today. The middle Miocene terrestrial community consisted predominantly, or exclusively, of C3 plants, i.e., there is no evidence for C4 grasses. Statistically different mean carbon isotope values for the mammalian herbivores indicate niche partitioning of the C3 plant food resources. The range of individual carbon isotope analyses, i.e., δ13C from −15.9 to −10.1‰, indicates herbivores feeding on diverse plants from different habitats with extrapolated δ13C values of −29.9 to −24.2‰, possibly ranging from dense forest to more open country woodland. The ecological niches of individual mammalian herbivore species were differentiated either by diet or body size.

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References

  • Ambrose SH, Norr L (1993) Isotopic composition of dietary protein and energy versus bone collagen and apatite: purified diet growth experiments. In: Lambert JB, Grupe G (eds) Molecular archaeology of prehistoric human bone. Springer, Berlin Heidelberg New York, pp 1–37

  • Balasse M (2003) Potential biases in sampling design and interpretation of intra-tooth isotope analysis. Int J Osteoarchaeol 13:3–10

    Article  Google Scholar 

  • Bard E, Delaygue G, Rostek F, Antonioli F, Silenzi S, Schrag DP (2002) Hydrological conditions over the western Mediterranean basin during the deposition of the cold Sapropel 6 (ca. 175 kyr BP). Earth Planet Sci Lett 202:481–494

    Article  CAS  Google Scholar 

  • Berggren WA, Kent DV, Swisher CC III, Aubry M-P (1995) A revised Cenozoic geochronology and chronostratigraphy. In: Berggren WA, Kent DV, Aubry M-P, Hardenbol J (eds) Geochronology, time scales and global stratigraphic correlation. Special Publication 54. SEPM, Tulsa, pp 129–212

  • Boutton TW (1991) Stable carbon isotopic ratios of natural materials. II. Atmospheric, terrestrial, marine, and freshwater environments. In: Coleman DC, Fry B (eds) Carbon isotope techniques. Academic, San Diego, pp 173–195

  • Bryant JD (1991) New early Barstovian (middle Miocene) vertebrates from the Upper Torreya Formation, eastern Florida panhandle. J Vertebr Paleontol 11:472–489

    Google Scholar 

  • Bryant JD, Froelich PN (1995) A model of oxygen isotope fractionation in body water of large mammals. Geochim Cosmochim Acta 59:4523–4537

    Article  CAS  Google Scholar 

  • Bryant JD, Froelich PN, Showers WJ, Genna BJ (1996) Biologic and climatic signals in the oxygen isotopic composition of Eocene–Oligocene equid enamel phosphate. Palaeogeogr Palaeoclimatol Palaeoecol 126:75–89

    Article  Google Scholar 

  • Cerling TE, Harris JM (1999) Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120:347–363

    Article  Google Scholar 

  • Cerling TE, Wang Y, Quade J (1993) Global ecological change in the late Miocene: expansion of C4 ecosystems. Nature 361:344–345

    Article  Google Scholar 

  • Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158

    Article  CAS  Google Scholar 

  • Cerling TE, Harris JM, MacFadden BJ (1998) Carbon isotopes, diets of North American equids, and the evolution of North American grasslands. In: Griffiths H, Robinson D, Van Gardingen P (eds) Stable isotopes and the integration of biological, ecological, and geochemical processes. BIOS, Oxford, pp 363–379

  • Cerling TE, Hart JA, Hart TB (2004) Stable isotope ecology in the Ituri Forest. Oecologia 138:5–12

    Article  PubMed  Google Scholar 

  • Coates AG, Obando JA (1996) The geologic evolution of the Central American Isthmus. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and environment in tropical America. University of Chicago Press, Chicago, pp 21–56

  • Colinvaux PA, DeOliveira PE, Bush ME (2000) Amazonian and Neotropical plant communities on glacial time-scales: the failure of the aridity and refuge hypothesis. Quat Sci Rev 19:141–169

    Article  Google Scholar 

  • Coplen TB (1994) Reporting of stable hydrogen, carbon, and oxygen isotopic abundances. Pure Appl Chem 66:273–276

    CAS  Google Scholar 

  • Crepet WL, Feldman GD (1991) The earliest remains of grasses in the fossil record. Am J Bot 78:1010–1014

    Google Scholar 

  • Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16:436–468

    Google Scholar 

  • Dienes P (1980) The isotopic composition of reduced organic carbon. In: Fritz P, Fontes JC (eds) Handbook of environmental isotopic chemistry. 1. The terrestrial environment. Elsevier, Amsterdam, pp 329–406

  • Downs T (1956) The Mascall Fauna from the Miocene of Oregon. Univ Calif Publ Geol Sci 31:199–354

    Google Scholar 

  • Eisenberg JF (1981) The mammalian radiations: an analysis of trends in evolution, adaptation, and behavior. University of Chicago Press, Chicago

    Google Scholar 

  • Farquahar GD, Ehleringer JR, Hubick KT (1989) Carbon isotopic discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537

    CAS  Google Scholar 

  • Feranec RS (2003) Determination of resource partitioning in a predominantly C3 environment by the analysis of stable isotope values from herbivores in Yellowstone National Park. J Vert Paleo Abstracts 23:49A

    Google Scholar 

  • Feranec RS, MacFadden BJ (2000) Evolution of the grazing niche in Pleistocene mammals from Florida: evidence from stable isotopes. Palaeogeogr Palaeoclimatol Palaeoecol 162:155–169

    Article  Google Scholar 

  • Ferrusquía-Villafranca I (1978) Distribution of Cenozoic vertebrate faunas in middle America and problems of migration between North and South America. Conexiones terrestres entre Norte y Sudamerica. Inst Geol Univ Nac Auton México 101:193–329

  • Fox DL, Koch PL (2003) Tertiary history of C4 biomass in the Great Plains, USA. Geology 31:809–812

    Article  CAS  Google Scholar 

  • Fricke HC, O’Neil JR (1996) Inter- and intra-tooth variation in the oxygen isotope composition of mammalian tooth enamel phosphate: implications for palaeoclimatological and palaeobiological research. Palaeogeogr Palaeoclimatol Palaeoecol 126:91–99

    Article  Google Scholar 

  • Gadbury C, Todd L, Jahren AH, Amundson R (2000) Spatial and temporal variations in the isotopic composition of bison tooth enamel from the Early Holocene Hudson−Meng Bone bed, Nebraska. Palaeogeogr Palaeoclimatol Palaeoecol 157:79–93

    Article  Google Scholar 

  • Goddard J (1970) Age criteria and vital statistics of a black rhinoceros population. E Afr Wildl J 8:105–121

    Google Scholar 

  • Graham A (1988) Studies in neotropical paleobotany. VI. The lower Miocene communities of Panama—the Cucaracha formation. Ann Missouri Bot Gard 75:1467–1479

    Google Scholar 

  • Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–137

    Google Scholar 

  • Higgins P, MacFadden BJ (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. Palaeogeogr Palaeoclimatol Palaeoecol (in press)

  • Hoefs J (1997) Stable isotope geochemistry. Springer, Berlin Heidelberg New York

  • Hoppe KA, Stover SM, Pascoe JR, Amundson R (2004) Tooth enamel biomineralization in extant horses: implications for isotopic microsampling. Palaeogeogr Palaeoclimatol. Palaeoecol (in press)

    Google Scholar 

  • IAEA/WMO (2001) Global network of isotopes in precipitation. The GNIP database. http://isohis.iaea.org. Cited 27 July 2003

  • Jacobs BF, Kingston JD, Jacobs LL (1999) The origin of grass-dominated ecosystems. Ann Missouri Bot Gard 86:590–643

    Google Scholar 

  • Janis CM (1982) Evolution of horns in ungulates: ecology and paleoecology. Biol Rev 57:261–318

    Google Scholar 

  • Janis CM (1988) An estimation of tooth volume and hypsodonty indices in ungulate mammals, and the correlation of these factors with dietary preference. In: Russell DE, Santoro JP, Sigogneau-Russell D (eds) Teeth revisited: proceedings of the VIIth international symposium on dental morphology, Paris 1986. Mém Mus Hist Nat Paris (sér C) 53:367–387

  • Janis CM, Damuth J, Theodor JM (2000) Miocene ungulates and terrestrial primary productivity: Where have all the browsers gone? Proc Natl Acad Sci USA 97:7899–7904

    Article  CAS  PubMed  Google Scholar 

  • Kay RF, Madden RH, Cifelli RL, Flynn JJ (eds) (1997) Vertebrate paleontology in the Neotropics: the Miocene fauna of La Venta, Colombia. Smithsonian, Washington, p 592

    Google Scholar 

  • Knapp S, Mallet J (2003) Refuting refugia? Science 300:71–72

    Article  CAS  PubMed  Google Scholar 

  • Koch PL (1998) Isotopic reconstruction of past continental environments. Annu Rev Earth Planet Sci 26:573–613

    Article  CAS  Google Scholar 

  • Koch PL, Zachos JC, Gingerich PD (1992) Correlation between isotope records in marine and continental carbon reservoirs near the Palaeocene/Eocene boundary. Nature 358:319–322

    Article  CAS  Google Scholar 

  • Kohn MJ (1999) You are what you eat. Science 283:335–336

    Article  CAS  PubMed  Google Scholar 

  • Lee-Thorp JA, Sealy JC, Merwe NJ van der (1989) Stable carbon isotope ratio differences between bone collagen and bone apatite, and their relationship to diet. J Arch Sci 16:585–599

    Google Scholar 

  • MacFadden BJ (1987) Fossil horses from “Eohippus” (Hyracotherium) to Equus: Scaling, Cope’s Law, and the evolution of body size. Paleobiology 12:355–370

    Google Scholar 

  • MacFadden BJ (1988) Fossil horses from “Eohippus” (Hyracotherium) to Equus. 2. Rates of dental evolution revisited. Biol J Linn Soc 35:37–48

    Google Scholar 

  • MacFadden BJ (2000) Cenozoic mammalian faunas from the Americas: reconstructing ancient diets and terrestrial communities. Annu Rev Ecol Syst 31:33–59

    Article  Google Scholar 

  • MacFadden BJ (2001) Three-toed browsing horse Anchitherium clarencei from the early Miocene (Hemingfordian) Thomas Farm, Florida. Bull FL Mus Nat Hist 43:79–109

    Google Scholar 

  • MacFadden BJ (2004) Middle Miocene land mammals from the Cucaracha Formation (Hemingfordian-Barstovian) of Panama. Fl Mus Nat Hist Bull (in press)

  • MacFadden BJ, Hulbert RC (1988) Explosive speciation at the base of the adaptive radiation of Miocene grazing horses. Nature 336:466–468

    Article  Google Scholar 

  • MacFadden BJ, Cerling TE, Harris JM, Prado J (1999) Ancient latitudinal gradients of C3/C4 grasses interpreted from stable isotopes of New World Pleistocene horse (Equus) teeth. Global Ecol Biogeogr 8:137–149

    Google Scholar 

  • McKenna MC, Bell SK (1997) Classification of mammals above the species level. Columbia University Press, New York

  • McCrea JM (1950) On the isotopic chemistry of carbonates and a paleotemperature scale. J Chem Phys 18:849–857

    CAS  Google Scholar 

  • Merwe NJ van der, Medina E (1989) Photosynthesis and 13C/12 C ratios in Amazonian rain forests. Geochim Cosmochim Acta 53:1091–1094

    Article  Google Scholar 

  • Nowak RM (1999) Mammals of the world, 6th edn. Johns Hopkins University Press, Baltimore

  • Passey BH, Cerling TE (2002) Tooth enamel mineralization in ungulates: implications for recovering a primary isotopic time-series. Geochim Cosmochim Acta 66:3225–3234

    Article  CAS  Google Scholar 

  • Patton TH, Taylor BE (1973) The Protoceratinae (Mammalia, Tylopoda, Protoceratidae) and the systematics of the Protoceratidae. Bull Am Mus Nat Hist 150:347–414

    Google Scholar 

  • Prothero DR (1998) Protoceratidae. In: Janis CM, Scott KM, Jacobs LL (eds) Evolution of tertiary mammals in North America. Cambridge University Press, New York, pp 431–438

  • Rich PV, Rich TH (1983) The Central American dispersal route: Biotic history and paleogeography. In: Janzen DH (ed) Costa Rican natural history. University of Chicago Press, Chicago, pp 12–34

  • Rozanski K, Araguás-Araguás L, Gonfiantini R (1993) Isotopic patterns in modern global precipitation. In: Swart PK, Lohmann KC, McKenzie J, Savin S (eds) Climate change in continental isotopic records. Am Geophys Union Geophys Monogr 78:1–36

    Google Scholar 

  • Schultz CB, Falkenbach C (1940) Merycochoerinae: a new subfamily of oreodonts. Bull Am Mus Nat Hist 77:213–306

    Google Scholar 

  • Schultz CB, Falkenbach C (1968) The phylogeny of the oreodonts. Bull Am Mus Nat Hist 139:1–498

    Google Scholar 

  • Simpson GG (1953a) Evolution and geography. Oregon state system of higher education, Eugene

  • Simpson GG (1953b) The major features of evolution. Columbia University Press, New York

  • Simpson GG (1965) The geography of evolution: collected essays. Chilton, Philadelphia

    Google Scholar 

  • Stehli FG, Webb SD (1985) The great American biotic interchange. Plenum, New York

  • Sternberg LSL, Mulkey SS, Wright SJ (1989) Ecological interpretation of leaf carbon isotope ratios: influence of respired carbon dioxide. Ecology 70:1317–1324

    Google Scholar 

  • Stewart KM, Bowyer RT, Kie JG, Dick BL, Ben-David M (2003) Niche partitioning among mule deer, elk, and cattle: do stable isotopes reflect dietary niche? Ecoscience 10:297–302

    Google Scholar 

  • Slaughter BH (1981) A new genus of geomyoid rodent from the Miocene of Texas and Panama. J Vert Paleontol 1:111–115

    Google Scholar 

  • Straight WH, Barrick RE, Eberth DA (2004) Reflections of surface water seasonality and climate in stable oxygen isotopes from tyrannosaurid tooth enamel. Palaeogeogr Palaeoclimatol Palaeoecol (in press)

  • Tedford RH (1970) Principles and practices of mammalian geochronology in North America. In: Proc 3rd N Am Paleontol Conv, vol F, pp 666–703

  • Tedford RH, Skinner MF, Fields RW, Rensberger JM, Whistler DP, Galusha T, Taylor BE, Macdonald JR, Webb SD (1987) Faunal succession and biochronology of the Arikareean through Hemphillian interval (late Oligocene through earliest Pliocene epochs) in North America. In: Woodburne MO (ed) Cenozoic mammals of North America: geochronology and biostratigraphy. University California Press, Berkeley, pp 153–210

  • Thomasson JR, Nelson ME, Zakrzewski RJ (1986) A fossil grass (Gramineae: Chloridoideae) from the Miocene with Krantz anatomy. Science 233:876–878

    Google Scholar 

  • Tidwell WD, Nambudiri EVM (1989) Tomlinsonia thomassonii, gen. et sp. nov., a permineralized grass from the Upper Miocene Ricardo Formation, California. Rev Paleobot Palynol 60:165–177

    Article  Google Scholar 

  • Webb SC (1977) A history of savanna vertebrates in the New World. Part I: North America. Annu Rev Ecol Syst 8:355–380

    Article  Google Scholar 

  • Webb SD (1981) The Thomas Farm Fossil site. Plaster Jacket. Fl Mus Nat Hist 37:1–33

    Google Scholar 

  • Webb SD, Perrigo SC (1984) Late Cenozoic vertebrates from Honduras and El Salvador. J Vert Paleontol 4:237–254

    Google Scholar 

  • Whitmore FC, Stewart RH (1965) Miocene mammals and Central American seaways. Science 148:180–185

    Google Scholar 

  • Wood HE (1964) Rhinoceroses from the Thomas Farm Miocene of Florida. Mus Comp Zool Bull 130:361–386

    Google Scholar 

  • Woodring WP (1957) Geology and paleontology of Canal Zone and adjoining parts of Panama. US Geol Surv Prof Paper 306-A. US Gov Printing Office, Washington

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Acknowledgements

We thank Robert J. Emry of the USNM for permission to borrow and sample the fossils from the Gaillard Cut L.F. Isotopic preparation and analyses were done at the Center for Isotope Geoscience in the Department of Geological Sciences at the University of Florida. This is University of Florida Contribution to Paleobiology number 562.

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Authors and Affiliations

  1. Florida Museum of Natural History, University of Florida, Gainesville, FL, 32611, USA

    Bruce J. MacFadden & Pennilyn Higgins

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  1. Bruce J. MacFadden
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  2. Pennilyn Higgins
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Correspondence to Bruce J. MacFadden.

Appendices

Appendix 1

Table 3 shows data for individual bulk carbon and oxygen isotopic analyses.

Table 3 Data for individual bulk carbon and oxygen isotopic analyses
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Appendix 2

Table 4 shows serial isotopic analyses for two teeth of the large rhino Floridaceras whitei from the Miocene of Panama.

Table 4 Serial isotopic analyses for two teeth of the large rhino Floridaceras whitei from the Miocene of Panama
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MacFadden, B.J., Higgins, P. Ancient ecology of 15-million-year-old browsing mammals within C3 plant communities from Panama. Oecologia 140, 169–182 (2004). https://doi.org/10.1007/s00442-004-1571-x

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  • DOI: https://doi.org/10.1007/s00442-004-1571-x

Keywords

  • Carbon isotopes
  • Diet
  • Fossils
  • Miocene
  • Oxygen isotopes