Functional Anatomy of the Forelimb of Plesiotypotherium achirense (Mammalia, Notoungulata, Mesotheriidae) and Evolutionary Insights at the Family Level

Fernández-Monescillo, Marcos; Quispe, Bernardino Mamani; Pujos, François; Antoine, Pierre-Olivier

doi:10.1007/s10914-016-9372-7

Functional Anatomy of the Forelimb of Plesiotypotherium achirense (Mammalia, Notoungulata, Mesotheriidae) and Evolutionary Insights at the Family Level

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Published: 09 January 2017

Volume 25, pages 197–211, (2018)
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Functional Anatomy of the Forelimb of Plesiotypotherium achirense (Mammalia, Notoungulata, Mesotheriidae) and Evolutionary Insights at the Family Level

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Marcos Fernández-Monescillo¹,
Bernardino Mamani Quispe²,
François Pujos¹ &
…
Pierre-Olivier Antoine³

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Abstract

In the present work, we provide muscular reconstruction and we infer functional properties of the forelimb of Plesiotypotherium achirense, a fossil mesotheriid notoungulate from the late Miocene of Achiri (Bolivia). This locality has yielded the widest sample ever available for the forelimb of a mesotheriid. In addition, we propose a qualitative comparison of the forelimb (osteology and myology) at the family level, including the Miocene–Pleistocene mesotheriines Mesotherium cristatum, Plesiotypotherium achirense, Caraguatypotherium munozi, Plesiotypotherium casirense, and Pseudotypotherium sp, and the late Oligocene trachytheriine Trachytherus alloxus. Functional properties are consistent with a digging ability and a “scratch-digger” lifestyle for Mesotheriidae. In general, there are only slight differences among the comparison sample, except for Mesotherium cristatum, which reflect significant osteological modifications, likely to help increasing the moment arm while scratch-digging. These features are mainly observable on scapulae (distal border caudally displaced) and humeri (deltoid crest distally oriented and crista supracondylaris lateralis laterally projected).

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Introduction

Mesotheriidae is a family of South American native ungulates, assigned to the extinct order Notoungulata. Mesotheriidae includes Trachytheriinae, Oligocene in age, paraphyletic, and mostly represented by Trachytherus Ameghino, 1889 (see Billet et al. 2008), and Mesotheriinae, documented from the early Miocene (Colhuehuapian South American Land Mammal Age [SALMA]; Paz et al. 2011) to the late early Pleistocene (Ensenadan SALMA; e.g., Mesotherium cristatum Serres, 1867).

Croft (2007) considered that mesotheriines differ from other notoungulates in possessing: (i) hypselodont teeth, (ii) a large diastema between incisors and cheek teeth, and (iii) characteristic trilobed upper molars. Shockey et al. (2007) provided a short history of the group. Representatives of this family have been successively considered as transitional forms between rodents and “pachyderms” (Serres 1867), as rodents (Gervais 1867, 1869), and as prosimian primates (Ameghino 1891, 1906) before their ordinal affinities were set among Notoungulata. Accordingly, the hypothesized lifestyle of these taxa has always been disputed, ranging from aquatic (Serres 1867), running-hopping (Loomis 1914), “scratch digging” (Sydow 1988) sensu Hildebrand (1974, 1985), or cursorial and semiaquatic (Bond et al. 1995). The most recent studies interpreted a scratch-digging way of life and a highly conservative postcranial skeleton for Mesotheriidae as a whole (Shockey et al. 2007; Shockey and Anaya 2008). According to these authors, Mesotheriidae were probably semifossorial animals that could dig in pursuit of food and/or for building dens.

The paleontological site of Achiri is located in the Pacajes Province of La Paz Department, Bolivia (Fig. 1). This fauna comes from the Mauri Formation (Unit IV), with a late Miocene age constrained by ⁴⁰Ar/³⁹Ar dating for the underlying Ulloma Formation (10.35±06 Ma; Marshall 1992). The Achiri site was first reported in the 1970s (Villarroel 1974; Saint-André 1993), and then excavated by distinct international teams (e.g., IFEA-GEOBOL missions during the 1990s; Saint-André 1993). Our working group, encompassing Bolivian, Argentinian, Spanish, and French paleontologists and geologists, has worked at Achiri during the period 2011–2015. Four decades of fieldwork have resulted in an unparalleled sample of craniomandibular and postcranial material referable to mesotheriids in Achiri, especially for the forelimb, and deposited in several scientific institutions (e.g., MNHN-Bol and MNHN). In Achiri, Mesotheriidae are documented by Plesiotypotherium achirense Villarroel, 1974, and Plesiotypotherium majus Villarroel, 1974, the former species being widely dominant over the latter in terms of referred specimen abundance.

Qualitative comparisons of the mesotheriid appendicular skeleton were already undertaken by several authors beginning in the last century (Cattoi 1943; Villarroel 1974; Croft et al. 2004; Flynn et al. 2005; Shockey et al. 2007; Cerdeño et al. 2012), but to our knowledge, no work has focused on soft tissue and morphological reconstruction for any mesotheriine thus far. Nevertheless, the comparative studies by Cattoi (1943) and Shockey et al. (2007) have included some muscular indications on postcranial elements, both qualitative and quantitative in the latter reference.

This work aims at (i) reconstructing the osteological and muscular forelimb configuration and inferring the locomotor abilities of the notoungulate Plesiotypotherium achirense, according to an unparalleled forelimb sample recovered from Achiri, and (ii) assessing the forelimb osteological changes at the mesotheriid level and discussing how the inferred morpho-functional properties have evolved for the different taxa analyzed.

Material and Methods

Institutional Abbreviations

FLMNH, Florida Museum of Natural History (with UF indicating FLMNHN specimens), Gainesville, USA; GEOBOL, (former) Servicio Geológico de Bolivia, La Paz, Bolivia; IFEA, Institut Français d’Etudes Andines, La Paz, Bolivia; MACN, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia,” Buenos Aires, Argentina; MNHN, Muséum national d'histoire naturelle, Paris, France (specimens referred to as PAM or SAL in the text, respectively); MNHN-Bol, Museo Nacional de Historia Natural de Bolivia, La Paz, Bolivia; SGO, Museo Nacional de Historia Natural, Santiago, Chile.

Specimens from Achiri

Plesiotypotherium achirense is the type species of Plesiotypotherium (abbreviated below as Pl.). The holotype originates from 3-4 km to the west of Achiri village in the place known as Cerro Balcunani (Villarroel 1974). In this study we include also the fossils of Pl. achirense recovered from other sites located in the same area: Hanko Hakke, Jakka Pukara, Cerro Pisakeri, and Virgen Pata (see Saint-André 1993). The type material of Pl. achirense was described by Villarroel (1974); we added to the original descriptions the unpublished fossils housed in the MNHN and in the MNHN-Bol. The forelimb fossil material is the most abundant known for any mesotheriid (see material list in Online Resource 1).

Plesiotypotherium majus also originates from the Achiri area, with a hypodigm collected between Pirapi Grande and Pirapi Chico southeast to Achiri (Villarroel 1974). We were not able to make any comparison with Pl. majus, because it is documented only by craniomandibular and hind limb remains. To our knowledge, no forelimb specimen has been assigned to this taxon, either originating from early field campaigns or from our own fieldwork.

Comparison Material (Other Mesotheriidae)

We compared with other mesotheriids in order to scrutinize evolutionary changes of the forelimb osteological features, and to infer their functional anatomical evolution at the family level. We include in the comparison the trachytheriine Trachytherus alloxus Billet et al. 2008, from the late Oligocene of Salla, Bolivia (Billet et al. 2008). Mesotheriines included within the present study are: Mesotherium cristatum from the Pleistocene (Ensenadan) of Paraná basin and La Plata River, Argentina; Pseudotypotherium sp. from the Pliocene (Montehermosan) of Monte Hermoso Formation, Buenos Aires Province, Argentina (Rovereto 1914; Cattoi 1943); Caraguatypotherium munozi Flynn et al., 2005, from the middle Miocene (pre-Huayquerian and post-Friasian) of Lower Huaylas Formation, Caragua, northern Chile (Flynn et al. 2005); and Plesiotypotherium casirense Cerdeño et al., 2012, from the late Miocene of Casira, Potosí Department, Bolivia.

Measurements and Indices

The measurement abbreviations are indicated in Online Resource 2. The measurements were taken with a digital caliper of 150 mm. Quantitative data were analyzed using the software package PAST, version 3.11 (Hammer et al. 2001). The summary of the measurements appear in the Online Resource 3. Biological indices have been used often in biological and paleontological studies in order to infer locomotor abilities (e.g., Maynard Smith and Savage 1956; Elissamburu and Vizcaino 2004; Shockey et al. 2007; Croft and Anderson 2008). The biological indices, derived from the ones used for the forelimb in Croft and Anderson (2008), are indicated in Table 1 and the biological index values are in Table 2.

Table 1 Biological indices used in this study

Full size table

Table 2 Biological indices for forelimb bones of the mesotheriid notoungulates analyzed in the current work

Full size table

Anatomical Description

The anatomical descriptions follow the terminology of Schaller (2007) using primarily the terms of the Nomina Anatomica Veterinaria (Waibl et al. 2005), and De Iuliis and Pulerà. (2010) as illustrated in Figs. 2 and 3. We use the following anatomical terms of direction: medial, lateral, cranial (dorsal in the manus), caudal (plantar in the manus), proximal, and distal. We made comparison with extant animals of similar osteological structures with well-known myology and functional anatomical abilities (Taylor 1978; McEvoy 1982; Ebensperger and Bozinovic 2000; Candela and Picasso 2008; Ercoli et al. 2014). In addition, we have compared with extant animals of different locomotor lifestyles including cursorial (Gregory 1912), natatorial (Polly 2007), or scansorial (Cartmill 1974).

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

Description of Forelimb Osteology and Myology

Scapula

The scapular body is rectangular. The main muscles (m.) involved in the fixation of the glenohumeral joint are the m. supraspinatus, m. infraspinatus, and m. subscapularis (Fig. 4; Davis 1949). In addition, there is evidence of a preserved clavicle in both Pl. achirense (MNHN ACH 26, 34) and the derived species Mesotherium cristatum (MNHN PAM 2) among mesotheriids. In lateral view (Fig. 2a,c), a marked spine runs along the transverse axis bifurcating cranially into a slender acromion (processus hamatus) and caudally into a broad metacromion (processus suprahamatus). The acromion coincides with the origin for the pars acromialis of the m. deltoideus and the metacromion with the omotransversarius (Larson 1993; Muizon 1998; Argot 2001). Proximally in the spine is attached the pars scapularis, and distally the m. trapezius (Fig. 4). The fossa infraspinata is slightly covered by the border of the spine cranially and by the caudal scapula; both lean over the fossa. The fossa supraspinata is rectangular and relatively larger than the fossa infraspinata, which is triangular in shape (Cattoi 1943). Accordingly, the supraspinatus muscle was probably more developed than the m. infraspinatus. The nutrient canal is located proximally in the fossa infraspinata, and below the suprahamatus process (metacromion) (Fig. 2c). In proximal view (Fig. 2b), the pear-like cavitas glenoidale is laterally convex and slightly medially convex. The lateral side is variable, from convex (MNHN ACH 34), straight (MNHN-Bol-V 8407), to concave (MNHN-Bol-V 12659 and 11690). The proximal cranial border is acute and ends in the supraglenoid tuberosity (tubercululum supraglenoidale), slightly ventrally projected. In this tuberosity inserts the m. biceps brachii. Craniomedially is the strongly developed and mediocranially oriented coracoid process, where the m. coracobrachialis is attached. In caudal view, the m. teres minor is inserted in a marked triangular facet on the tuberculum infraglenoidale of the scapular neck. Likewise, the caput longum of the m. triceps brachii inserts longitudinally in the caudal border of the scapula. In medial view, two surfaces inflated caudally and cranially to the fossa subscapularis coincide with the insertion of the m. subscapularis (Fig. 4).

Humerus

In cranial view (Fig. 5h), salient features are the massive deltopectoral crest (tuberositas deltoidea), the greater tubercle (tuberculum majus), and the proximodistally elongated medial epicondyle or entepicondyle (epicondylus medialis). The well-developed deltopectoral crest hosts the insertion for both the m. deltoideus and the m. pectoralis (Shockey et al. 2007). In lateral, and medial view (Fig. 5c), the humerus has a sigmoid shaft with a constant diaphyseal width. The distal epiphysis is slightly laterally oriented in comparison to the proximal epiphysis because of the torsion of the diaphysis (Cattoi 1943). Proximally, the greater tubercle is highly projected over the humerus head. A deep and triangular facet is located cranial to both tubercles, for the insertion of the m. coracobrachialis (Cattoi 1943). The greater tubercle presents laterally a rounded and deep facet for the m. infraspinatus. Another rounded facet is located distal to this structure. It is delimited by the linea m. tricipitis, which marks the insertion of the pars caput laterale of the tricipitis brachii muscle. In lateral view (Fig. 5a), the greater tubercle is proximally projected. The pars acromialis and pars scapularis of the m. deltoideus attach into the deltoid crest. A wide insertion for both the m. triceps brachii caput accesorium and caput laterale is located distally in the medial humeral neck. In medial view (Figs. 4 and 5c), the large insertion for the m. supraspinatus is situated medial to the tuberculus majus. Lateral to the lesser tubercle inserts the m. subscapularis. Distal to it is the longitudinal and narrow tuberositas teres major in which the m. teres major and m. latissimus dorsi insert. Caudal to them and distal to the neck attaches the medial branch of the m. triceps brachii. In proximal view, cranial to the caput humeri and between the greater and the lesser tuberosity, is the caudally concave intertubercular groove (sulcus intertubercularis). In cranial view (Fig. 5h) the deltopectoral crest is well developed. All these structures determine a wide, laterally oriented deltopectoral plateau. The well-developed crista supracondylaris lateralis receives the m. supinator longus (supinatory muscle brachioradialis), the m. extensor carpi radialis, and m. extensor digitorum communis. Whereas the surface for the origin of the m. extensor carpi ulnaris is located distally, the distal epiphysis has a thick and rounded medial lip of the trochlea, caudocranially oriented and coinciding with the distal tip of the humerus. The rounded capitulum and the trochlea are continuous structures. Proximal to the capitulum there is a wide supratrochlear foramen. Medially, the medial epicondyle is broad, massive, and proximodistally oriented. Combined entheses of the main flexors of the forearm originate there (Fig. 6). Proximal to the entepicondyle appears a wide, proximodistally oriented entepicondylar foramen for the medial nerve and brachial artery (Cattoi 1943; Landry 1958). The most proximal facet of the entepicondyle is for the caput mediale accesorium of the m. triceps brachii (m. epitrocleo-anconeus or m. anconeus internus; Taylor 1978; Fisher et al. 2009; Ercoli et al. 2014). Distal to this is the m. pronator teres, and caudal to it is an oval surface for the m. flexor carpi radialis. Distally is an irregular surface assumed to host the origin of the caput humerale and mediale of the m. flexor digitorum profundum. Distal to it, in an oval surface, would lay the caput humerale and caput mediale of the m. flexor carpi ulnaris. The broad and massive origin area, completely distally oriented, is for the m. palmaris longus flexor, which flexes the carpals and the proximal phalangeal joints (Fig. 6; Waibl et al. 2005). The origin area for the m. anconeus (m. anconeus externum) is caudal to the epicondylar crest (crista supracondylaris lateralis) and it lays proximolateral to the supratrochlear foramen.

Ulna

The ulna is long and slender transversely, with a widened distal epiphysis. In lateral view (Fig. 7b), the caudal border is markedly convex, while the cranial border distal to the trochlear notch is straight. The olecranon is well developed, mediocranially oriented, with the proximal border of the olecranon caudocranially expanded (Fig. 7h). The massive proximal tubercle (tuber olecrani) has a rough surface for the attachment of the different folds of the m. triceps brachii: medially, a deep depression marks the origin of the medial head, cranially, the insertion area for the caput accesorium, and caudally, the caput lateralis (Fig. 5). The broad insertion for the m. anconeus is located in the lateral part of the olecranon, proximal to the trochlear notch. Lateral to the ulnar body, there is a transverse depression for the attachment of the m. abductor digiti I longus (m. abductor pollicis longus). In cranial view (Fig. 7h), the trochlear notch is laterally oriented due to the orientation of the anconeus process. The incisura radialis is markedly flat in the parasagittal plane. Distal to the coronoid process appears the attachment for the m. brachialis and m. biceps brachii. The pronator quadratus originates from a broad and triangular facet located cranially in the distal epiphysis. The ulnar body width is slender, while the distal epiphysis is inflated (Fig. 7h). In medial view, the origin for the caput mediale accesorium of the m. triceps brachii occupies the proximal border of the olecranon; in the medial part of the ulnar body, a triangular and longitudinal depression coincides with the insertion for the caput ulnare of the m. flexor digitorum profundus. The circunferentia articularis is oval and connects with the incisura ulnaris of the radius. Distocranially, the facies articularis carpi radii contacts the pyramidal and the pisiform.

Radius

The radius is flattened distocranially with well-developed radial head and distal epiphysis. The diaphysis is oval in cross section all along the bone. The proximal articular surface is oval and mediolaterally enlarged. It presents two depressed areas: the fovea capitis radii (lateral), facing the rounded trochlea humeri, and another one on the medial border, facing the capitulum. The dorsal border is rounded and continuous. In cranial view (Fig. 8b), the neck is elongate mediolaterally and flattened craniocaudally. The distal portion displays grooves for three tendons: for the m. abductor digitis I in the medial border, for the m. extensor carpi radialis just lateral to it, and finally for the m. extensor digitorum communis. In lateral view (Fig. 8f), the supinator muscle (m. supinator brevis) inserts in a concave surface distal to the radial head (Fig. 4). Distal to it is a depressed surface proximodistally elongated and located in the distal half of the shaft, which hosts the insertion for the m. pronator quadratus. In medial view (Fig. 8), in the distal epiphysis is a triangular insertion for the m. brachioradialis (Fig. 4). In dorsal view (Fig. 3d), the wide oval articular facets for the scaphoid and the lunar are visible distally. In distal view, distal to the neck appears the inflated surface of the bicipital tuberosity where the tendon for the m. biceps brachii inserts (Fig. 8f).

Manus

The manus of Pl. achirense is pentadactyl with bifid ungual phalanges (Villaroel 1974). The first digit is slender with a markedly slenderer Mc I. The largest metacarpal is the Mc II. Yet, in anatomical position, the Mc III reaches a more distal position than any other metacarpal (Fig. 9). The proximal phalanges of digits II-III are robust proximally and tapering/narrowing distally. Median phalanges show a similar pattern, although less pronounced. The phalanges show a palmar articular facet for a large sesamoid preventing the over extension of the digits (Shockey et al. 2007). Distal phalanges are bifid, with a deep median sagittal groove. Their height regularly diminishes distally, whereas their width increases. In dorsal view, in anatomical position the metacarpals have a fan-shaped pattern, as in other mesotheriids (see Shockey et al. 2007; Cerdeño et al. 2012), similar to what is observed in ursids or other terrestrial carnivorans.