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      Opportunistic Feeding Strategy for the Earliest Old World Hypsodont Equids: Evidence from Stable Isotope and Dental Wear Proxies

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          Abstract

          Background

          The equid Hippotherium primigenium, with moderately hypsodont cheek teeth, rapidly dispersed through Eurasia in the early late Miocene. This dispersal of hipparions into the Old World represents a major faunal event during the Neogene. The reasons for this fast dispersal of H. primigenium within Europe are still unclear. Based on its hypsodonty, a high specialization in grazing is assumed although the feeding ecology of the earliest European hipparionines within a pure C 3 plant ecosystem remains to be investigated.

          Methodology/Principal Findings

          A multi-proxy approach, combining carbon and oxygen isotopes from enamel as well as dental meso- and microwear analyses of cheek teeth, was used to characterize the diet of the earliest European H. primigenium populations from four early Late Miocene localities in Germany (Eppelsheim, Höwenegg), Switzerland (Charmoille), and France (Soblay). Enamel δ 13C values indicate a pure C 3 plant diet with small (<1.4‰) seasonal variations for all four H. primigenium populations. Dental wear and carbon isotope compositions are compatible with dietary differences. Except for the Höwenegg hipparionines, dental microwear data indicate a browse-dominated diet. By contrast, the tooth mesowear patterns of all populations range from low to high abrasion suggesting a wide spectrum of food resources.

          Conclusions/Significance

          Combined dental wear and stable isotope analysis enables refined palaeodietary reconstructions in C 3 ecosystems. Different H. primigenium populations in Europe had a large spectrum of feeding habits with a high browsing component. The combination of specialized phenotypes such as hypsodont cheek teeth with a wide spectrum of diet illustrates a new example of the Liem’s paradox. This dietary flexibility associated with the capability to exploit abrasive food such as grasses probably contributed to the rapid dispersal of hipparionines from North America into Eurasia and the fast replacement of the brachydont equid Anchitherium by the hypsodont H. primigenium in Europe.

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          Most cited references23

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          Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo)ecology and (paleo)climate.

          A broad compilation of modern carbon isotope compositions in all C3 plant types shows a monotonic increase in δ(13)C with decreasing mean annual precipitation (MAP) that differs from previous models. Corrections for temperature, altitude, or latitude are smaller than previously estimated. As corrected for altitude, latitude, and the δ(13)C of atmospheric CO(2), these data permit refined interpretation of MAP, paleodiet, and paleoecology of ecosystems dominated by C3 plants, either prior to 7-8 million years ago (Ma), or more recently at mid- to high latitudes. Twenty-nine published paleontological studies suggest preservational or scientific bias toward dry ecosystems, although wet ecosystems are also represented. Unambiguous isotopic evidence for C4 plants is lacking prior to 7-8 Ma, and hominid ecosystems at 4.4 Ma show no isotopic evidence for dense forests. Consideration of global plant biomass indicates that average δ(13)C of C3 plants is commonly overestimated by approximately 2‰.
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            Global patterns in leaf 13C discrimination and implications for studies of past and future climate.

            Fractionation of carbon isotopes by plants during CO(2) uptake and fixation (Delta(leaf)) varies with environmental conditions, but quantitative patterns of Delta(leaf) across environmental gradients at the global scale are lacking. This impedes interpretation of variability in ancient terrestrial organic matter, which encodes climatic and ecological signals. To address this problem, we converted 3,310 published leaf delta(13)C values into mean Delta(leaf) values for 334 woody plant species at 105 locations (yielding 570 species-site combinations) representing a wide range of environmental conditions. Our analyses reveal a strong positive correlation between Delta(leaf) and mean annual precipitation (MAP; R(2) = 0.55), mirroring global trends in gross primary production and indicating stomatal constraints on leaf gas-exchange, mediated by water supply, are the dominant control of Delta(leaf) at large spatial scales. Independent of MAP, we show a lesser, negative effect of altitude on Delta(leaf) and minor effects of temperature and latitude. After accounting for these factors, mean Delta(leaf) of evergreen gymnosperms is lower (by 1-2.7 per thousand) than for other woody plant functional types (PFT), likely due to greater leaf-level water-use efficiency. Together, environmental and PFT effects contribute to differences in mean Delta(leaf) of up to 6 per thousand between biomes. Coupling geologic indicators of ancient precipitation and PFT (or biome) with modern Delta(leaf) patterns has potential to yield more robust reconstructions of atmospheric delta(13)C values, leading to better constraints on past greenhouse-gas perturbations. Accordingly, we estimate a 4.6 per thousand decline in the delta(13)C of atmospheric CO(2) at the onset of the Paleocene-Eocene Thermal Maximum, an abrupt global warming event approximately 55.8 Ma.
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              On the relationship between hypsodonty and feeding ecology in ungulate mammals, and its utility in palaeoecology.

              High-crowned (hypsodont) teeth are widely found among both extant and extinct mammalian herbivores. Extant grazing ungulates (hoofed mammals) have hypsodont teeth (a derived condition), and so extinct hypsodont forms have usually been presumed to have been grazers. Thus, hypsodonty among ungulates has, over the past 150 years, formed the basis of widespread palaeoecological interpretations, and has figured prominently in the evolutionary study of the spread of grasslands in the mid Cenozoic. However, perceived inconsistencies between levels of hypsodonty and dental wear patterns in both extant and extinct ungulates have caused some workers to reject hypsodonty as a useful predictive tool in palaeobiology, a view that we consider both misguided and premature. Despite the acknowledged association between grazing and hypsodonty, the quantitative relationship of hypsodonty to the known ecology of living ungulate species, critical in making interpretations of the fossil record, was little studied until the past two decades. Also, much of the literature on ungulate ecology relevant to understanding hypsodonty has yet to be fully incorporated into the perspectives of palaeontologists. Here we review the history and current state of our knowledge of the relationship between hypsodonty and ungulate ecology, and reassert the value of hypsodonty for our understanding of ungulate feeding behaviour. We also show how soil consumption, rather than the consumption of grass plants per se, may be the missing piece of the puzzle in understanding the observed correlation between diets, habitats, and hypsodonty in ungulates. Additionally, we show how hypsodonty may impact life-history strategies, and resolve some controversies regarding the relevance of hypsodonty to the prediction of the diets of extinct species. This in turn strengthens the utility of hypsodonty in the determination of past environmental conditions, and we provide a revised view of a traditional example of evolutionary trends in palaeobiology, that of the evolution of hypsodonty in horses and its correlation with the Miocene spread of grasslands in North America. © 2011 The Authors. Biological Reviews © 2011 Cambridge Philosophical Society.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                11 September 2013
                : 8
                : 9
                : e74463
                Affiliations
                [1 ]Steinmann-Institut für Geologie, Mineralogie und Paläontologie, University of Bonn, Bonn, Germany
                [2 ]University Hamburg, Biozentrum Grindel, Hamburg, Germany
                [3 ]Institut de Géochimie, Université de Lausanne, Lausanne, Switzerland
                [4 ]iPHEP UMR 7262 CNRS, Université de Poitiers, Poitiers, France
                University of Arkansas, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: TT GM TMK. Performed the experiments: TT GM TMK. Analyzed the data: TT GM TMK. Contributed reagents/materials/analysis tools: TV. Wrote the paper: TT GM TMK.

                Article
                PONE-D-12-06980
                10.1371/journal.pone.0074463
                3770545
                24040254
                7ccff45e-5ab0-43a7-9384-d0fab88f14d4
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 6 March 2012
                : 5 August 2013
                Page count
                Pages: 14
                Funding
                This study was partly financed by the Swiss National Science Foundation (SNF) grant 200021-100530/1 to TV and the Deutsche Forschungsgemeinschaft Emmy Noether-Program TU 148/2 to TT and KA-1525 4-1/4-2 and KA-1525 9-1, KA 1525 8-1 to TMK and is publication no. 44 of the DFG Research Unit 771 “Function and enhanced efficiency in the mammalian dentition–phylogenetic and ontogenetic impact on the masticatory apparatus”. The study was further funded by a research grant from the Fyssen Foundation (Paris, France) to GM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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