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Climbing Adaptations of an Enigmatic Early Arctoid Carnivoran: the Functional Anatomy of the Forelimb of Amphicynodon leptorhynchus From the Lower Oligocene of the Quercy Phosphorites (France)

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Abstract

This paper provides a detailed description and the functional anatomy of the forelimb of an early Oligocene genet-sized arctoid carnivoran, Amphicynodon leptorhynchus, to infer its probable lifestyle. This work represents the first insights into the functional anatomy of the postcranial skeleton and palaeoecology of an emblematic member of the first radiation of arctoid carnivorans, the poorly known Amphicynodontidae, a group very likely related to bears. So far, the Amphicynodontidae have only been studied on the basis of their cranial and dental remains. The fossil site of Itardies (MP23, lower Oligocene), in the Quercy Phosphorites (France), have yielded hundreds of postcranial remains attributed to Am. leptorhynchus, allowing a complete analysis of its locomotor behaviour in comparison to a large sample of extant carnivorans showing diverse lifestyles. The anatomy of the forelimb of Am. leptorhynchus indicates well-developed climbing skills and grasping abilities. Thus, this early arctoid was probably living mostly in trees, moving on the ground basically for foraging as observed in small modern climbing carnivorans such as the red panda or the kinkajou, although some other climbing carnivorans can also live in rocky areas.

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taken from Tarquini et al. (2019)

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taken from Tarquini et al. (2019)

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taken from Tarquini et al. (2019)

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Data Availability

All data generated or analysed during this study are included in this published article and its Supplementary Information files.

Code Availability

Graphs were created in R Version 3.6.2 with the ggplot2 package.

References

  • Aguilar JP, Legendre S, Michaux J (1997) Actes du congres BiochroM’97. Mémoires et travaux de l’Institut de Montpellier de l’école pratique des hautes études, Montpellier

  • Antón M, Salesa MJ, Pastor JF, Peigné S, Morales J (2006) Implications of the functional anatomy of the hand and forearm of Ailurus fulgens (Carnivora, Ailuridae) for the evolution of the “false-thumb” in pandas. J Anat 209:757–764

    Article  PubMed  PubMed Central  Google Scholar 

  • Argot C (2001) Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. J Morphol 247:51–79

    Article  CAS  PubMed  Google Scholar 

  • Argot C (2003) Functional adaptations of the postcranial skeleton of two Miocene borhyaenoids (Mammalia, Metatheria), Borhyaena and Prothylacinus, from South America. Palaeontology 46:1213–1267

    Article  Google Scholar 

  • Argot C (2004) Evolution of South American mammalian predators (Borhyaenoidea): anatomical and palaeobiological implications. Zool J Linn Soc 140:487–521

    Article  Google Scholar 

  • Astruc JG, Escarguel G, Maranda B, Simon-Coinçon R, Sigé B (2000) Floor-age constraining of a tectonic paroxysm of the Pyrenean orogen. Late middle Eocene mammal age of a faulted karstic filling of the Quercy phosphorites, south-western France. Geodinamica Acta 13:271–280

    Article  Google Scholar 

  • Barone R (2010) Anatomie Comparée des Mammifères Domestiques, Tome 1, Ostéologie. Éditions Vigot, Paris

    Google Scholar 

  • Bonis L de (1974) Premières données sur les carnivores fissipèdes provenant des fouilles récentes dans le Quercy. Palaeovertebrata 6:27–32

    Google Scholar 

  • Bonis L de, Gardin A, Blonde C (2019) Carnivora from the early Oligocene of the ‘Phosphorites du Quercy’ in southwestern France. Geodiversitas 41:601–621

  • Carbone C, Mace GM, Roberts SC, Macdonald DW (1999) Energetic constraints on the diet of terrestrial carnivores. Nature 402:286-288

    CAS  PubMed  Google Scholar 

  • Carbone C, Teacher A, Rowcliffe JM (2007) The costs of carnivory. PLoS Biology 5:e22

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cirot E (1992) Etude phylogénétique de quelques genres d’Arctoidea de l’Oligocène eurasiatique: comparaison des données morphologiques et moléculaires. Doctoral dissertation, Poitiers

  • Cirot E, Bonis L de (1992) Révision du genre Amphicynodon, carnivore de l’Oligocène. Palaeontogr Abt A 220:103–130

    Google Scholar 

  • Davis DD (1949) The shoulder architecture of bears and other carnivores. Fieldiana Zool 31:285-305

    Google Scholar 

  • Davis DD (1964) The Giant Panda: A Morphological Study of Evolutionary Mechanisms. Chicago Natural History Museum, Chicago

    Google Scholar 

  • Durand-Delga M (2006) Sur la découverte des phosphorites du Quercy au renouveau de leur étude avec Bernard Gèze. Strata 13:25–36

    Google Scholar 

  • Ercoli MD, Prevosti FJ, Álvarez A (2012) Form and function within a phylogenetic framework: locomotory habits of extant predators and some Miocene Sparassodonta (Metatheria): locomotion in sparassodonts and extant predators. Zool J Linn Soc 165:224–251

    Article  Google Scholar 

  • Ercoli MD, Youlatos D (2016) Integrating locomotion, postures and morphology: the case of the tayra, Eira barbara (Carnivora, Mustelidae). Mammal Biol 81:464–476

    Article  Google Scholar 

  • Evans HE, Lahunta A de (2013) Miller’s Anatomy of the Dog. Elsevier Saunders, St. Louis

    Google Scholar 

  • Fabre AC, Cornette R, Slater G, Argot C, Peigné S, Goswami A, Pouydebat E (2013) Getting a grip on the evolution of grasping in musteloid carnivorans: a three-dimensional analysis of forelimb shape. J Evol Biol 26:1521–1535

    Article  PubMed  Google Scholar 

  • Fabre AC, Goswami A, Peigné S, Cornette R (2014) Morphological integration in the forelimb of musteloid carnivorans. J Anat 225:19–30

    Article  PubMed  PubMed Central  Google Scholar 

  • Fabre AC, Cornette R, Goswami A, Peigné S (2015) Do constraints associated with the locomotor habitat drive the evolution of forelimb shape? A case study in musteloid carnivorans. J Anat 226:596–610

    Article  PubMed  PubMed Central  Google Scholar 

  • Fabre AC, Marigó J, Granatosky MC, Schmitt D (2017) Functional associations between support use and forelimb shape in strepsirrhines and their relevance to inferring locomotor behavior in early primates. J Hum Evol 108:11–30

    Article  PubMed  Google Scholar 

  • Finarelli JA (2008) A total evidence phylogeny of the Arctoidea (Carnivora: Mammalia): relationships among basal taxa. J Mammal Evol 15:231-259

    Article  Google Scholar 

  • Fisher RE, Adrian B, Barton M, Holmgren J, Tang SY (2009) The phylogeny of the red panda (Ailurus fulgens): evidence from the forelimb. J Anat 215:611–635

    Article  PubMed  PubMed Central  Google Scholar 

  • Fujiwara S (2009) Olecranon orientation as an indicator of elbow joint angle in the stance phase, and estimation of forelimb posture in extinct quadruped animals. J Morphol 270:1107–1121

    Article  PubMed  Google Scholar 

  • Gebo DL, Rose KD (1993) Skeletal morphology and locomotor adaptation in Prolimnocyon atavus, an early Eocene hyaenodontid creodont. J Vertebr Paleontol 13:125–144

    Article  Google Scholar 

  • Gittleman JL (1985) Carnivore body size: ecological and taxonomic correlates. Oecologia 67:540–554

    Article  PubMed  Google Scholar 

  • Heinrich R, Houde P (2006) Postcranial anatomy of Viverravus (Mammalia, Carnivora) and implications for substrate use in basal Carnivora. J Vertebr Paleontol 26:422–435

    Article  Google Scholar 

  • Henderson K, Pantinople J, McCabe K, Richards HL, Milne N (2017) Forelimb bone curvature in terrestrial and arboreal mammals. PeerJ 5:e3229

    Article  PubMed  PubMed Central  Google Scholar 

  • Hunt RM (2002) New amphicyonid carnivorans (Mammalia, Daphoeninae) from the early Miocene of southeastern Wyoming. Am Mus Novit 2002:1–41

    Google Scholar 

  • Iwaniuk AN, Pellis SM, Whishaw IQ (1999) The relationship between forelimb morphology and behaviour in North American carnivores (Carnivora). Can J Zool 77:1064–1074

    Article  Google Scholar 

  • Janis CM, Scott KM, Jacobs LL (1998) Evolution of Tertiary Mammals of North America: Volume 1, Terrestrial Carnivores, Ungulates, and Ungulate Like Mammals. Cambridge University Press, Cambridge, pp 73–246

  • Legendre S (1987) Les communautés mammifères d’Europe occidentale de l’Eocène supérieur et Oligocène : structures et milieux. Münch Geowis Abh A10:301–312

    Google Scholar 

  • McClearn D (1992) Locomotion, posture, and feeding behavior of kinkajous, coatis, and raccoons. J Mammal 73:245-261

    Article  Google Scholar 

  • McEvoy JS (1982) Comparative myology of the pectoral and pelvic appendages of the North American porcupine (Erethizon dorsatum) and the prehensile-tailed porcupine (Coendou prehensilis). Bull Am Mus Natl Hist 173:337–421

    Google Scholar 

  • Meng J, McKenna MC (1998) Faunal turnovers of Palaeogene mammals from the Mongolian Plateau. Nature 394:364-367

    Article  CAS  Google Scholar 

  • Morgan CC (2009) Geometric morphometrics of the scapula of South American caviomorph rodents (Rodentia: Hystricognathi): form, function and phylogeny. Mammal Biol, 74: 497-506

    Article  Google Scholar 

  • Oxnard CE (1968) The architecture of the shoulder in some mammals. J Morphol 126:249–290

    Article  CAS  PubMed  Google Scholar 

  • Peigné S, Bonis L de (2003) Juvenile cranial anatomy of Nimravidae (Mammalia, Carnivora): biological and phylogenetic implications. Zool J Linn Soc 138:477–493

    Article  Google Scholar 

  • Salesa MJ, Antón M, Peigné S, Morales J (2006) Evidence of a false thumb in a fossil carnivore clarifies the evolution of pandas. Proc Natl Acad Sci USA 103:379–382

    Article  CAS  PubMed  Google Scholar 

  • Salesa MJ, Antón M, Peigné S, Morales J (2008) Functional anatomy and biomechanics of the postcranial skeleton of Simocyon batalleri (Viret, 1929) (Carnivora, Ailuridae) from the late Miocene of Spain. Zool J Linn Soc 152:593–621

    Article  Google Scholar 

  • Samuels JX, Van Valkenburgh B (2008) Skeletal indicators of locomotor adaptations in living and extinct rodents. J. Morphol 269: 1387-1411

    Article  PubMed  Google Scholar 

  • Samuels JX, Meachen JA, Sakai SA (2013) Postcranial morphology and the locomotor habits of living and extinct carnivorans. J Morphol 274: 121-146

    Article  PubMed  Google Scholar 

  • Sargis EJ (2002) Functional morphology of the forelimb of tupaiids (Mammalia, Scandentia) and its phylogenetic implications. J Morphol 253:10–42

    Article  PubMed  Google Scholar 

  • Schaller O, Constantinescu GM (2007) Illustrated Veterinary Anatomical Nomenclature. Enke Verlag, Stuttgart

    Google Scholar 

  • Sigé B, Aguilar JP, Astruc JG, Mandarat B (1991) Extension au Miocène inférieur des remplissages phosphatés du Quercy. La faune de vertébrés de Crémat (Lot, France). Geobios, Lyon 24:497–502

    Article  Google Scholar 

  • Siliceo G, Salesa MJ, Antón M, Pastor JF, Morales J (2015) Comparative anatomy of the shoulder region in the late Miocene amphicyonid Magericyon anceps (Carnivora): functional and paleoecological inferences. J Mammal Evol 22:243–258

    Article  Google Scholar 

  • Stalheim-Smith A (1984) Comparative study of the forelimbs of the semifossorial prairie dog, Cynomys gunnisoni, and the scansorial fox squirrel, Sciurus niger. J Morphol 180:55–68

    Article  CAS  PubMed  Google Scholar 

  • Tarquini J, Morgan CC, Toledo N, Soibelzon LH (2019) Comparative osteology and functional morphology of the forelimb of Cyonasua (Mammalia, Procyonidae), the first South American carnivoran. J Morphol 280:446–470

    Article  PubMed  Google Scholar 

  • Tarquini J, Toledo N, Morgan CC, Soibelzon LH (2017). The forelimb of †Cyonasua sp. (Procyonidae, Carnivora): ecomorphological interpretation in the context of carnivorans. Earth Environ Sci Trans R Soc Edinburgh, 106:325-335

    Article  Google Scholar 

  • Tarquini J, Toledo N, Soibelzon LH, Morgan CC (2018) Body mass estimation for †Cyonasua (Procyonidae, Carnivora) and related taxa based on postcranial skeleton. Hist Biol 30:496–506

    Article  Google Scholar 

  • Taverne M, Fabre AC, Herbin M et al (2018) Convergence in the functional properties of forelimb muscles in carnivorans: adaptations to an arboreal lifestyle? Biol J Linn Soc 125:250–263

    Google Scholar 

  • Taylor ME (1970) Locomotion in some East African viverrids. J Mammal 51:42-51

    Article  Google Scholar 

  • Taylor ME (1974) The functional anatomy of the forelimb of some African Viverridae (Carnivora). J Morphol 143:307–335

    Article  CAS  PubMed  Google Scholar 

  • Taylor ME (1989) Locomotor adaptations by carnivores. In: Gittleman Jl (ed) Carnivore Behavior, Ecology and Evolution. Volume 1. Comstock Publishing Associates, Ithaca, pp 382–409

    Chapter  Google Scholar 

  • Toledo N, Bargo MS, Cassini GH, Vizcaíno SF (2012) The forelimb of early Miocene sloths (Mammalia, Xenarthra, Folivora): morphometrics and functional implications for substrate preferences. J Mammal Evol, 19:185-198

    Article  Google Scholar 

  • Tomiya S, Tseng ZJ (2016) Whence the beardogs? Reappraisal of the middle to late Eocene ‘Miacis’ from Texas, USA, and the origin of Amphicyonidae (Mammalia, Carnivora). R Soc Open Sci 3:160518

    Article  PubMed  PubMed Central  Google Scholar 

  • Trapp GR (1972) Some anatomical and behavioral adaptations of ringtails, Bassariscus astutus. J Mammal 53:549–557

    Article  Google Scholar 

  • Van Valkenburgh B (1987) Skeletal indicators of locomotor behavior in living and extinct carnivores. J Vertebr Paleontol 7:162–182

    Article  Google Scholar 

  • Van Valkenburgh B (1990) Skeletal and dental predictors of body mass in carnivores. In: Damuth J, MacFadden BJ (ed) Body Size in Mammalian Paleobiology. Estimation and Biological Implications. New York: Cambridge University Press, Cambridge, pp 181-205

    Google Scholar 

  • Vianey-Liaud M, Legendre S (1986) Les faunes des phosphorites du Quercy: principes méthodologiques en paléontologie des mammifères; homogénéité chronologique des gisements de mammifères fossiles. Eclogae Geologicae Helvetiae 79:917–944

    Google Scholar 

  • Vianey-Liaud M, Schmid B (2009) Diversité, datation et paléoenvironnement de la faune de mammifères oligocènes de Cavalé (Quercy, SO France) : contribution de l’analyse morphométrique des Theridomyinae Mammalia, Rodentia). Geodiversitas 31:909–941

    Article  Google Scholar 

  • Wang B, Qiu Z (2003) Notes on early Oligocene ursids (Carnivora, Mammalia) from Saint Jacques, Nei Mongol, China. Bull Am Mus Natl Hist 279:116–124

    Article  Google Scholar 

  • Wang X, McKenna MC, Dashzeveg D (2005) Amphicticeps and Amphicynodon (Arctoidea, Carnivora) from Hsanda Gol Formation, central Mongolia and phylogeny of basal arctoids with comments on zoogeography. Am Mus Novit, 1–60

  • Wang X, Rothschild BM (1992) Multiple hereditary osteochondroma in oligocene Hesperocyon (Carnivora: Canidae). J Vertebr Paleontol 12:387–394

    Article  CAS  Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer Nature

  • Wilson DE, Mittermeier RA (2009) Handbook of the Mammals of the World, vol. 1. Carnivores. Lynx Editions, Barcelona

    Google Scholar 

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Acknowledgements

This research was funded by the French CNRS in the frame of the “Recherche coopérative sur programme : Phosphorites du Quercy”. This work is part of the master's thesis of AG, who received financial assistance for international mobility: ERASMUS+ grant from the Faculté des Sciences of the Université de Montpellier (France) and AMI grant from the French Ministry of Higher Education and Research and Innovation. The article is greatly indebted to all the people who worked with LdB in the locality Itardies. We thank the members of PALEVOPRIM (University of Poitiers) and the Museo Nacional de Ciencias Naturales-CSIC, where this paper was prepared, and especially Camille Grohé for our constructive discussions. Furthermore, we wish to acknowledge Nahuel Muñoz and an anonymous reviewer for their comments which greatly improved the paper. We thank the Anatomical Collections of the Museo Nacional de Ciencias Naturales-CSIC (especially its curator, Ángel Luis Garvía), and the Museo Anatómico de la Universidad de Valladolid for providing the large sample of skeletons of extant carnivorans used for comparison.

Funding

The research was funded by the French CNRS in the frame of the “Recherche coopérative sur programme: Phosphorites du Quercy”. This work is part of the master's thesis of AG, who received financial assistance for international mobility: ERASMUS + grant from the Faculté des Sciences of the Université de Montpellier (France) and AMI grant from the French Ministry of Higher Education and Research and Innovation.

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Authors and Affiliations

  1. Laboratoire de Paléontologie, Evolution, Paléoécosystèmes et Primatologie (PALEVOPRIM) UMR 7262 CNRS, Université de Poitiers, Poitiers, France

    Axelle Gardin & Louis de Bonis

  2. Departamento de Palaeobiología, Museo Nacional de Ciencias Naturales-CSIC, Madrid, Spain

    Manuel J. Salesa, Gema Siliceo & Mauricio Antón

  3. Departamento de Anatomía, Facultad de Medicina, Universidad de Valladolid, Valladolid, Spain

    Juan Francisco Pastor

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  1. Axelle Gardin
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  2. Manuel J. Salesa
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  3. Gema Siliceo
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  4. Mauricio Antón
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  5. Juan Francisco Pastor
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  6. Louis de Bonis
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Contributions

Louis de Bonis and Manuel J. Salesa designed the study. Louis de Bonis and Axelle Gardin made the descriptions of the forelimb of Am. leptorhynchus. Axelle Gardin analysed and interpreted the forelimb anatomy and draft the manuscript. All the authors revised and improved the writing of this manuscript.

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Correspondence to Axelle Gardin.

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Gardin, A., Salesa, M.J., Siliceo, G. et al. Climbing Adaptations of an Enigmatic Early Arctoid Carnivoran: the Functional Anatomy of the Forelimb of Amphicynodon leptorhynchus From the Lower Oligocene of the Quercy Phosphorites (France). J Mammal Evol 28, 785–811 (2021). https://doi.org/10.1007/s10914-021-09553-w

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