Elsevier

Geobios

Volume 68, October 2021, Pages 61-70
Geobios

Original article
Macrauchenia patachonica Owen, 1838: Limb bones morphology, locomotory biomechanics, and paleobiological inferences

https://doi.org/10.1016/j.geobios.2021.04.006Get rights and content

Highlights

  • Wide scapula movements could compensate for the reduced mobility of a short humerus.

  • Lowered head derived in freedom for forelimbs movement increasing the step length.

  • Limbs biomechanics increased the food encounter rate by improving acceleration.

  • Macrauchenia patachonica probably ran with the neck in a horizontal position.

  • The nasal retraction could be an adaptation for dust filtering.

Abstract

Macrauchenia patachonica Owen, 1838 was among the last and largest litopterns, an extinct order of South American native ungulates. Macrauchenia patachonica had anatomical peculiarities as extremely retracted nasals, enlarged cervical vertebrae, and limb bones proportions without good living analogs that lead to asking about its paleobiology. To quantitatively assess the strange combination of limb bone features in M. patachonica, we constructed an indicator of differences in anatomical adaptations for efficient running between forelimb and hind limb (IDFH). We also made a multivariate analysis using data on osteological ratios of living mammals and two other litopterns. We discuss several biomechanical and paleobiological implications of the striking differences between hind limb and forelimb design in M. patachonica. Our main suggestion is that M. patachonica, during fast locomotion, probably used a posture with the neck in a horizontal position.

Introduction

During the Cenozoic in South America, a large variety of endemic ungulates evolved in relative isolation (Buckley, 2015, Croft et al., 2020). South American native ungulates were organized into six orders: Astrapotheria, Litopterna, Notoungulata, Pyrotheria, Xenungulata, and Notopterna, and these orders were grouped as a separate placental superorder called Meridiungulata (McKenna, 1975, Bond et al., 1995, Schmidt and Ferrero, 2014, Welker et al., 2015). However, some alternative phylogenetic hypotheses must be considered, e.g., Pyrotheria within Notoungulata (Billet, 2011) and Panameriungulata (Muizon and Cifelli, 2000). Notoungulates and litopterns were among the South American survivors of the Great American Biotic Interchange (GABI) that peaked in the Late Pliocene at ca. 3 Ma. Both groups died out in the Late Pleistocene-Early Holocene (Westbury et al., 2017). Macrauchenia patachonica Owen, 1838 was among the last and largest litopterns with an estimated body mass of ca. 1,000 kg (Fariña et al., 1998).

The order Litopterna includes various families, with Macrauchenia patachonica belonging to Macraucheniidae. This family’s representatives are characterized mainly by the retraction of the nasals, the backward shift of the nares, and a complete dental formula (Scherer et al., 2009, Schmidt and Ferrero, 2014, Forasiepi et al., 2016). Another characteristic of the Macraucheniidae is an extended neck unique among the South American native ungulates (Webb, 1978). There are records of M. patachonica since the Ensenadan South American Land Mammal Age (SALMA; Middle Pleistocene) in Argentina and more abundantly for the Lujanian SALMA (Late Pleistocene-Holocene) in Argentina, Brazil, Uruguay, Paraguay, Chile, Peru, and Bolivia (Scherer et al., 2009). Molecular phylogenetics showed that Perissodactyla is the extant order most closely related to Litopterna (Buckley, 2015, Welker et al., 2015, Westbury et al., 2017). Also, morphological phylogenetics resulted in the nesting of litopterns and kin as successive stem-clades of crown Perissodactyla (Chimento and Agnolin, 2020).

The representatives of the family Macraucheniidae were generally reconstructed as long-necked high-level browsers (Webb, 1978). However, from morphological and isotopic data, it was suggested that M. patachonica was a mixed feeder that could have been eating a wide combination of leaves and grasses (MacFadden and Shockey, 1997). Another stable isotopes study of South American Quaternary mammals suggested that M. patachonica was probably a mixed feeder with a combination of C3 and C4 vegetation in its diet from wooded and more open C3 environments as well as mixed C3-C4 environment (Domingo et al., 2012). The oxygen isotope composition values pointed to water ingested from different water bodies (Domingo et al., 2012). Dietary patterns inferred by analyzing enamel microwear and the occlusal enamel index of the tooth of M. patachonica positioned it as a grazer that probably ingested sedimentary particles together with food items while feeding close to the ground (de Oliveira et al., 2020). Species distribution modeling suggests that M. patachonica had environmental suitability for subtropical/temperate ecosystems with relatively high aridity and relatively low temperatures with predominantly pasture vegetation (de Oliveira et al., 2020).

Macrauchenia patachonica had anatomical peculiarities including extremely retracted nasals resulting in the nostrils located at the top of its skull and posterior to the orbits with no match in living terrestrial mammals, and enlarged cervical vertebrae reminiscent of extant giraffes (MacFadden and Shockey, 1997). The morphology of the skull’s anterior part suggests that M. patachonica had a proboscis (MacFadden and Shockey, 1997), although there is an argument that Macraucheniidae lacked a proboscis and perhaps had a more Alces-like prehensile lip (Moyano and Giannini, 2018).

It has been highlighted previously that relative to its body mass, M. patachonica had a femoral length less than one standard deviation longer than the mammalian average, a tibial length that is about one standard deviation shorter than the mammalian average, and that the radius shows an unusual wide medial flange (Fariña et al., 2005). Also, Carrano (1997) suggested that M. patachonica had limb proportions that would not be expected in a cursorial mammal. All these features without good living analogs lead to question the locomotion and paleobiology of M. patachonica. Other features already discussed in the literature are the unusual bone strength for lateral bending of some large limb bones like the humerus and femur (Fariña et al., 2005). Based on this feature, it was suggested that M. patachonica was adapted to swerving behavior to avoid predators (Fariña et al., 2005). Therefore, M. patachonica presented striking differences among bone proportions between fore and hind limbs: the forelimb had a very short humerus in comparison with the ulna, which is usually attributed to animals that are good runners, while in the hind limb, the femur was only slightly larger than the tibia, which is usually considered not suitable for fast running (Hildebrand, 1987).

Several anatomical features have been identified as indicatives of efficient locomotion. Generally, fast-running vertebrates have proximally-placed muscle insertions on the limb bones, elongated distal parts of the limbs, digitigrade or unguligrade support, and the limb joint morphology restricts motion to a predominantly parasagittal plane. Additionally, fast-moving ungulates have a reduced number of metapodials, a reduced ulnar diaphysis, and a reduced or nearly absent fibula (Hildebrand, 1987). These features can be biomechanically explained: muscles proximally placed in the limbs and osteological reduction in distal elements reduce the leg moment of inertia (Alexander, 1982, Alexander, 1983). Therefore, the rotational kinetic energy of the limbs is also reduced when moving at a given angular speed (Minetti, 1998). This adaptation produces relatively less energy consumption during the oscillation of the limbs at a given speed (Marsh et al., 2004). Moreover, proximally-placed limb muscles allow to operate the bones through long tendons, suitable for the storage of elastic potential energy to be released during the propulsive phase of the stride (Alexander, 1988, Alexander, 2003, Christiansen, 2002, Blanco and Gambini, 2006). This implies that in a certain range of the animal speed, the muscles produce force during locomotion but they do little work, as most of the shortening occurs in the tendons (Roberts et al., 1997, Blanco and Gambini, 2006). From the above, it follows that there are several limb bone ratios such as metatarsus/femur, radius/humerus, metacarpus/humerus, and tibia/femur that could potentially influence adaptations for speed and efficient terrestrial locomotion (Christiansen, 2002). It was also suggested that the ratio of the lengths between the inlevers (e.g., olecranon process and calcaneal tuber) and outlevers of muscles is important for speed and efficiency (Christiansen, 2002).

Christiansen (2002) used various ratios between relevant osteological features as independent variables against running velocity in regression analyses for 76 running mammals. To quantitatively assess the strange combination of limb bone features in M. patachonica, we constructed an indicator of differences in anatomical adaptations for efficient running between forelimb and hind limb (IDFH) from Christiansen’s (2002) regression equations. For the sake of comparison, we calculated this indicator for the whole sample of 76 mammals in Christiansen (2002) and two other litopterns: Theosodon garrettorum, a representative of the Macraucheniidae, and Diadiaphorus majusculus, a representative of Proterotheriidae. We also made a multivariate analysis using all data on osteological ratios of the living mammals and the three litopterns.

In summary, the morphology of M. patachonica is clearly unusual and it has led to contradictory interpretations of its moving abilities and paleoecology. Since Litopterna is such a peculiar order, we cannot assume that M. patachonica was necessarily similar to extant ungulates. Therefore, we applied new techniques to add information to the topic.

Section snippets

Morphology of Macrauchenia patachonica

Macrauchenia patachonica is a long-necked and long-limbed animal that earns its name based on the elongation of its cervical vertebrae (Lydekker, 1903). Its skull is elongated, and the orbits are completely encircled in bone and located behind the dental series (Scott, 1910; Fig. 1(B)). A very conspicuous feature in the skull of M. patachonica is its extremely retracted nasals (Fig. 1(C)), which result in the nostrils located at the top of the skull and posterior to the orbits (Burmeister, 1864

Results

The maximum running speeds of the three litoptern species obtained from Christiansen’s (2002) regression equations are shown in Table 3. The IDFH of Macrauchenia patachonica (46.05 for right limbs and 49.20 for left limbs) is close to four standard deviations higher than the mean value in living mammals (0.26 ± 11.93). The IDFH of Theosodon garrettorum (1.27) is in the range of living mammals, and the IDFH of Didiaphorus majusculus (23.73) is close to two standard deviations higher than the

Running capabilities

From a biomechanical model based on body mass estimate, measurements of the hind limb bones proportions and tibiae strength (Blanco et al., 2003), it was previously estimated that Macrauchenia patachonica top speed probably ranged between 14 m/s (50.4 km/h) and 27 m/s (97.2 km/h), with the most likely value around 18 m/s (64.8 km/h) (Blanco, 2004). Probably such speed is an overestimation due to the unusual robustness of the tibiae. Although, this result suggests that M. patachonica was capable

Conclusions

We proposed that Macrauchenia patachonica frequently engaged in running gaits in arid environments with the neck in a horizontal position, using the retracted nasals and related structures to minimize the inhalation of dust. This mode of locomotion would have been useful for seasonal migration but also for fighting between males. The biomechanics of its limbs probably also increased the food encounter rate by improving acceleration capabilities. It is possible that the overall biomechanical

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We thank PEDECIBA and ANII for providing financial support and Alejandra Rojas, responsible for the Project of the ANII (ANII_PR_PCTI_2009_15) “Fósiles de tu departamento, fósiles de Uruguay”, through which the replica of Macrauchenia patachonica that we measured was acquired. We also want to thank the editor-in-chief Gilles Escarguel, the associate-editors Darin A. Croft and Pierre-Olivier Antoine, and all reviewers, as they have allowed for significantly improving previous versions of the

References (88)

  • S.R. Moyano et al.

    Cranial characters associated with the proboscis postnatal-development in Tapirus (Perissodactyla: Tapiridae) and comparisons with other extant and fossil hoofed mammals

    Zoologischer Anzeiger

    (2018)
  • R.M. Alexander

    Size, shape, and structure for running and flight

  • R.M. Alexander

    Animal Mechanics

    (1983)
  • R.M. Alexander

    Elastic Mechanisms in Animal Movement

    (1988)
  • R.M. Alexander

    Principles of Animal Locomotion

    (2003)
  • R.M. Alexander et al.

    Allometry of the leg muscles of mammals

    Journal of Zoology

    (1981)
  • P.O. Antoine et al.

    A giant rhinocerotoid (Mammalia, Perissodactyla) from the Late Oligocene of north-central Anatolia (Turkey)

    Zoological Journal of the Linnean Society

    (2008)
  • A.G. Bannikov

    Die Saiga-Antilope (Saiga tatarica L.)

    A. Ziemsen Verlag, Wittenberg-Lutherstadt.

    (1963)
  • A.G. Bannikov et al.

    Saiga Biology

    (1961)
  • M.S. Bargo et al.

    Limb bone proportions, strength and digging in some Lujanian (Late Pleistocene-Early Holocene) mylodontid ground sloths (Mammalia, Xenarthra)

    Journal of Vertebrate Paleontology

    (2000)
  • H. Baur et al.

    Analysis of ratios in multivariate morphometry

    Systematic Biology

    (2011)
  • BBC Earth, 2018. Brutal Guanaco fight for dominance | Wild Patagonia | BBC Earth. Video file retrieved from...
  • M.B. Bennett

    Unifying principles in terrestrial locomotion: do hopping Australian marsupials fit in?

    Physiological and Biochemical Zoology

    (2000)
  • G. Billet

    Phylogeny of the Notoungulata (Mammalia) based on cranial and dental characters

    Journal of Systematic Palaeontology

    (2011)
  • R.E. Blanco

    Biomecánica de la carrera a alta velocidad: nuevos modelos para la estimación de limitantes del desplazamiento a alta velocidad en tetrápodos terrestres con miembros parasagitales y algunas de sus aplicaciones paleobiológicas

    (2004)
  • Bond, M., Cerdeño, E., López, G., 1995. Los ungulados nativos de América del Sur. In: Alberdi, M.T, Leone, G., Tonni,...
  • M. Buckley

    Ancient collagen reveals evolutionary history of the endemic South American ‘ungulates’

    Proceedings of the Royal Society B: Biological Sciences

    (2015)
  • H. Burmeister

    Descripción de la Macrauchenia patachonica

    Anales del Museo Público de Buenos Aires

    (1864)
  • N.R. Chimento et al.

    Phylogenetic tree of Litopterna and Perissodactyla indicates a complex early history of hoofed mammals

    Scientific Reports

    (2020)
  • D. Chong Díaz et al.

    Informe geológico del sitio de hallazgo de restos de vertebrados en el sector urbano de la ciudad de Calama, sector de Kamac Mayu

    (2004)
  • A. Christian

    Neck posture and overall body design in sauropods

    Fossil Record

    (2002)
  • P. Christiansen

    Locomotion in terrestrial mammals: the influence of body mass, limb length and bone proportions on speed

    Zoological Journal of the Linnean Society

    (2002)
  • T.F. Clancy et al.

    Differences in habitat use and grouping behavior between macropods and eutherian herbivores

    Journal of Mammalogy

    (1991)
  • A.B. Clifford et al.

    Case studies in novel narial anatomy: 3. Structure and function of the nasal cavity of saiga (Artiodactyla: Bovidae: Saiga tatarica)

    Journal of Zoology

    (2004)
  • C.F. Cooper

    II.–Baluchitherium osborni (? syn. Indricotherium turgaicum, borrissyak)

    Philosophical Transactions of the Royal Society of London, Series B, Containing Papers of a Biological Character

    (1924)
  • D.A. Croft et al.

    Splendid innovation: The extinct South American Native Ungulates

    Annual Review of Earth and Planetary Sciences

    (2020)
  • K. de Oliveira et al.

    Fantastic beasts and what they ate: Revealing feeding habits and ecological niche of late Quaternary Macraucheniidae from South America

    Quaternary Science Reviews

    (2020)
  • R.A. Fariña et al.

    Body mass estimations in Lujanian (late Pleistocene-early Holocene of South America) mammal megafauna

    Mastozoología Neotropical

    (1998)
  • R.A. Fariña et al.

    Swerving as the escape strategy of Macrauchenia patachonica Owen (Mammalia; Litopterna)

    Ameghiniana

    (2005)
  • Flores-Aqueveque, V., 2020. Contexto geológico del sitio Kamac Mayu. In: Martínez Rivera, I., Rojas Mondaca, O. (Eds.),...
  • A.M. Forasiepi et al.

    Exceptional skull of Huayqueriana (Mammalia, Litopterna, Macraucheniidae) from the late Miocene of Argentina: anatomy, systematics, and paleobiological implications

    Bulletin of the American Museum of Natural History

    (2016)
  • W. Franklin

    Family Camelidae (Llamas and Guanacos)

  • R. Frey et al.

    Skull, proboscis musculature and preorbital gland in the saiga antelope and Guenther’s dikdik (Mammalia, Artiodactyla, Bovidae)

    Zoologischer Anzeiger

    (1997)
  • R. Frey et al.

    A nose that roars: anatomical specializations and behavioural features of rutting male saiga

    Journal of Anatomy

    (2007)
  • Corresponding editors: Darin Croft, Pierre-Olivier Antoine.

    View full text