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Paleoecological Inferences from Long Bone Microanatomical Specializations in Hippopotamoidea (Mammalia, Artiodactyla)

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Abstract

Hippopotamoids are herbivorous mammals that originated in the late middle Eocene. This taxon includes animals with a great variety of sizes and body proportions, from small and gracile forms with slender limbs to heavy massive ones. Many hippopotamoids have previously been considered semi-aquatic but recent studies have highlighted a diversity of ecologies. This study focuses on bone microanatomy, one of the various proxies that enable inferring the ecology of extinct taxa. The comparative analysis of the inner structure of the stylopod bones in various hippopotamoids, based on both transverse and longitudinal virtual sections, highlights a diversity of patterns and clarifies previously proposed hypotheses about the ecology of the sampled hippopotamoids. The filling of the medullary area by spongious deposits in the pygmy hippopotamus, Choeropsis liberiensis, appears associated with frequent incursions into the water by an animal that essentially forages in forests. The common hippopotamus, Hippopotamus amphibius, which spends most of the day submerged in water, shows a greater filling of the medullary area by spongious bone and a thicker cortex. These observations coupled with comparisons with diverse terrestrial and semi-aquatic mammals of various sizes confirm that semi-aquatic lifestyle and heavy weight-bearing are associated with similar microanatomical specializations causing an increase in bone mass. However, for a given mass, comparisons enable determining if an additional increase in bone compactness occurs, as in Hippopotamus amphibius, in which case a semi-aquatic lifestyle could be inferred. Accordingly, this study suggests an essentially terrestrial lifestyle for Microbunodon minimum, Bothriodon velaunus, Elomeryx borbonicus, Merycopotamus medioximus, Paenanthracotherium bergeri, and probably also Saotherium cf. S. mingoz, a slight degree of water dependence in Brachyodus onoideus, and a stronger one in Libycosaurus bahri and Hexaprotodon garyam, though less intense than in Hippopotamus amphibius. Comparisons with other large terrestrial and semi-aquatic taxa, and based on a large part of the diaphysis, are required to better decipher the microanatomical changes associated with a semi-aquatic lifestyle from those linked to loading in heavy quadrupedal mammals.

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Data Availability

3D image data (.tif format) obtained by micro-tomography of MNHN specimens will be permanently saved by the MNHN DSI and identified by the inventory number of the specimen. They will be visible as work carried out on the interface https://3dtheque.mnhn.fr/ and made available via the interface http://colhelper.mnhn.fr/. All 3D image data obtained by micro-tomography at the IC2MP (University of Poitiers) are permanently saved by PALEVOPRIM under the responsibility of the director of the research unit (currently: JRB). Inventory will be communicated upon request, and data will be made available depending on the policy of the original specimen repository institution. As for the other microtomographic scans, they will be available under request to the authors.

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Acknowledgments

We warmly thank J. Lesur, A. Verguin, C. Argot, and G. Billet (MNHN, Paris, France); F. Saragoza, A. Bonnet, and E. Magne (Musée Crozatier, Le Puy-en-Velay, France); D. Berthet and F. Vigouroux (Musée des Confluences, Lyon, France); E. Robert (Université Claude Bernard Lyon I, Lyon, France); L. Costeur and F. Dammeyer (Naturhistorisches Museum Basel, Basel, Switzerland); G. Garcia and M. Brunet (PALEVOPRIM, Université de Poitiers, Poitiers, France); C. Nékoulnang Djétounako, B. El-Hadj Mallah and M. Adoum, (Centre National de Recherche pour le Dévelopement, N’Djamena, Chad) with support of L. Andossa and M. Hassane Taïsso (Université de N’Djamena, Chad) for the loan of the hippopotamoid specimens. We thank A. Mazurier (IC2MP, UMR 7285 CNRS-UP, Poitiers, France), R. Lebrun (ISEM, plateforme MRI, Montpellier, France), M. Garcia Sanz (AST-RX platform, UMS 2700, MNHN), and the Steinmann-Institut (University of Bonn, Germany), for providing beamtime and support, and for performing scans and reconstructions. We are very grateful to L.N. Cooper (Northeast Ohio Medical University, USA) for sending us virtual sections of Merycopotamus and Microbunodon. We also thank F. Guy, X. Valentin, J. Surault (PALEVOPRIM), and A.-L. Charruault (ISEM) for their precious help for the preparation of the specimens before scanning, A. Gekme and L. Martin for borrowing and transporting some of the studied specimens, as well as the Mission Paléoanthropologique Franco-Tchadienne (MPFT, PI: M. Brunet) for providing access to the Chadian material. We also thank two anonymous reviewers for constructive comments that helped to improve the manuscript.

Funding

We acknowledge financial support from the ANR SPLASH (ANR-15-CE32-0010). AH also acknowledges financial support from the ERC-2016-STG-715300.

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Authors and Affiliations

  1. UMR 7179, Département Adaptations du Vivant, CNRS/Muséum National D’Histoire Naturelle, 57 rue Cuvier CP-55, 75005, Paris, France

    Alexandra Houssaye

  2. Laboratoire Paléontologie Evolution Paléoécosystèmes Paléoprimatologie, CNRS, Université de Poitiers - UFR SFA, Bât B35 - TSA 51106, 86073 Poitiers Cedex 9, Poitiers, France

    Florian Martin & Jean-Renaud Boisserie

  3. Centre Français Des Etudes Ethiopiennes, CNRS Et Ministère de L’Europe Et Des Affaires Étrangères, PO BOX 5554, Addis Ababa, Ethiopia

    Jean-Renaud Boisserie

  4. Institut Des Sciences de L’Evolution de Montpellier, Université Montpellier CNRS IRD EPHE, Montpellier, France

    Fabrice Lihoreau

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  1. Alexandra Houssaye
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  2. Florian Martin
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  4. Fabrice Lihoreau
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Correspondence to Alexandra Houssaye.

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Houssaye, A., Martin, F., Boisserie, JR. et al. Paleoecological Inferences from Long Bone Microanatomical Specializations in Hippopotamoidea (Mammalia, Artiodactyla). J Mammal Evol 28, 847–870 (2021). https://doi.org/10.1007/s10914-021-09536-x

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