Muscular Reconstruction and Functional Morphology of the Forelimb of Early Miocene Sloths (Xenarthra, Folivora) of Patagonia
Article first published online: 28 NOV 2012
Copyright © 2012 Wiley Periodicals, Inc.
The Anatomical Record
Volume 296, Issue 2, pages 305–325, February 2013
How to Cite
Toledo, N., Bargo, M. S. and Vizcaíno, S. F. (2013), Muscular Reconstruction and Functional Morphology of the Forelimb of Early Miocene Sloths (Xenarthra, Folivora) of Patagonia. Anat Rec, 296: 305–325. doi: 10.1002/ar.22627
- Issue published online: 25 JAN 2013
- Article first published online: 28 NOV 2012
- Manuscript Revised: 12 OCT 2012
- Manuscript Accepted: 12 OCT 2012
- Manuscript Received: 16 JUN 2012
- PIP-CONICET. Grant Number: 1054
- PICT. Grant Number: 0143
- UNLP. Grant Number: N647
- National Geographic Society
- National Science Foundation
- functional morphology;
- substrate preferences;
- Santa Cruz Formation
- Top of page
- MATERIALS AND METHODS
- QUALITATIVE FUNCTIONAL MORPHOLOGY
- LITERATURE CITED
Early Miocene sloths are represented by a diversity of forms ranging from 38 to 95 kg, being registered mainly from Santacrucian Age deposits in southern-most shores of Patagonia, Argentina. Their postcranial skeleton differs markedly in shape from those of their closest living relatives (arboreal forms of less than 10 kg), Bradypus and Choloepus. In order to gain insight on functional properties of the Santacrucian sloths forelimb, musculature was reconstructed and a comparative, qualitative morphofunctional analysis was performed, allowing proposing hypotheses about biological role of the limb in substrate preferences, and locomotor strategies. The anatomy of the forelimb of Santacrucian sloths resembles more closely extant anteaters such as Tamandua and Myrmecophaga, due to the robustness of the elements, development of features related to attachment of ligaments and muscles, and conservative, pentadactylous, and strong-clawed manus. The reconstructed forelimb musculature was very well developed and resembles that of extant Pilosa (especially anteaters), although retaining the basic muscular configuration of generalized mammals. This musculature allowed application of powerful forces, especially in adduction of the forelimb, flexion and extension of the antebrachium, and manual prehension. These functional properties are congruent with both climbing and digging activities, and provide support for proposed Santacrucian sloths as good climbing mammals, possibly arboreal or semiarboreal, being also capable diggers. Their climbing strategies were limited, thus these forms relied mainly on great muscular strength and curved claws of the manus to move cautiously on branches. Anat Rec, 2013. © 2012 Wiley Periodicals, Inc.
Xenarthrans form one of the most conspicuous placental clades of South America (see Gaudin and McDonald,2008; Delsuc and Douzery,2008) and comprise two major groups, Cingulata and Pilosa (Fig. 1). Cingulata includes armadillos, pampatheres and glyptodonts, and Pilosa includes anteaters (Vermilingua) and sloths (Folivora). Anteaters are represented today by three genera, the small and fully arboreal silky anteater Cyclopes (about 0.5 kg), the semiarboreal Tamandua (about 5 kg) and the terrestrial giant anteater Myrmecophaga (about 35 kg; Nowak,1999). Living sloths, represented only by the two fully arboreal genera Bradypus (three-toed sloth) and Choloepus (two-toed sloth), are folivorous animals that weigh less than 10 kg and inhabit tropical forests (Nowak,1999; Chiarello,2008). The fossil record of anteaters is scarce, but that of fossils sloths is extraordinarily rich and diverse, especially during the Early Miocene Santacrucian Age of South America, and the Pleistocene of South and North America.
The fluvial deposits of the Santa Cruz Formation along the southernmost Atlantic shore of Patagonia (around 18–16 Ma, Perkins et al.,2012) contain a very well-preserved vertebrate fauna of Santacrucian Age that facilitates detailed paleobiological and paleoecological studies (Vizcaíno et al.,2010, 2012; Kay et al.,2012). The fauna includes a diversity of sloths in addition to anteaters, armadillos, glyptodonts, notoungulates, litopterns, astrapotheres, marsupials, primates, rodents, frogs, lizards, and birds.
In this contribution, we refer to the sloths recovered from Santacrucian deposits as “Santacrucian sloths” without intending any systematic or ecological connotations, as is true of similar expressions, commonly used in the literature, such as “extant sloths” and “Pleistocene sloths.” Santacrucian sloths are represented by megatherioids (Megatheriidae and Megalonychidae) and Mylodontidae, and the following genera are recorded (McKenna and Bell,1997): the megatheriids Planops and Prepotherium, the megalonychids Eucholoeops and Megalonychotherium, the basal megatherioids Hapalops, Analcimorphus, Schismotherium, Pelecyodon, and Hyperleptus, and the mylodontids Nematherium and Analcitherium. Nothrotheriids have not been reported from Santacrucian Miocene beds. For this study, we followed the phylogenetic proposal of Gaudin (2004; see Fig. 1).
Several authors suggest characterizing each taxon in a community by mean of three ecological parameters: body mass, diet, and substrate preference—including locomotion—(Andrews et al.,1979; Van Couvering,1980; Kay and Madden,1997; Reed,1998; Vizcaíno et al.,2006,2008,2010; Kay et al.,2012).
The diversity of Santacrucian sloths includes small and medium-sized forms (e.g., about 40 kg for Hapalops) and large forms (95 kg for one specimen of Nematherium, Vizcaíno et al.,2010; Bargo et al.,2012; see also Toledo et al., in press). The masticatory apparatus of Santacrucian sloths suggest that megatherioids were mainly folivorous while mylodontids could have ingested other fibrous items, such as fruits and tubers (Bargo et al.,2009,2012).
In her PhD dissertation, White (1993a) performed a comprehensive morphometric analysis of limb function of Santacrucian sloths, using multiple functional indices of the fore-and hind limb to discriminate locomotor modes. Her results were partially incorporated in subsequent publications (White, 1993b, 1997). Some genera were classified as arboreal or semiarboreal (Hapalops, Eucholoeops, among others) and Nematherium as probably more terrestrial. White (1997) remarked that none of the Santacrucian sloths were suspensorial. Using a similar morphometric approach focused on the forelimb of the Santacrucian sloths, Toledo et al., (2012) expanded the comparison to other groups, including extant marsupials, carnivorans, pangolins, rodents and tubulidentates, and described morphometric similarities between the forelimb of fossil sloths and digging animals such as anteaters, pangolins, aardvarks, and wombats. A preliminary quantitative and qualitative morphofunctional analysis of the overall skeleton of Santacrucian sloths performed by Bargo et al., (2012) obtained similar results. However, no detailed qualitative, morphofunctional studies involving soft tissue reconstruction of the appendicular apparatus of Santacrucian sloths have been published. Such qualitative morphofunctional approaches provide valuable paleobiological information about substrate preference (e.g., arboreal and terrestrial), locomotion and postural habits (e.g., climber and runner), and use of substrate (digger).
While some methodological approaches, such as ecomorphology, attempt to infer biological attributes directly from form, the study of the causal relationship between form and biology requires, as an intermediate step, inferences on function. That is, investigation of the relationship between form and function (form-function paradigm of Radinsky,1987) is followed by consideration of the relationship between function of any particular feature of an organism and the biological role of that function. Such investigations follow the definitions proposed by Bock and von Wahlert (1965) and Plotnick and Baumiller (2000). According to these authors, function refers to the role(s) that a feature performs in the context of a particular organism, including physical emergent properties of its form. The suite of functions that a feature's form can perform is defined by Oxnard (1984) as the averaged biomechanical situation. Biological role is the utilization of the function by an organism to perform one or more particular activities (i.e., a single function can perform several biological roles). Conceptual differences between function and biological role can be more properly described with a non-biological example: function of bicycle pedals is to spin the wheel of the bicycle. In one context, the role of this function is to propel the bicycle forward on the ground, but in a different context, the same function of spinning the wheel may perform a different role, such as generating electricity. Following Bock and von Wahlert (1965), information on biological role must be obtained in the context of actualistic approaches.
The goal of this contribution is to provide hypotheses on the biological roles of the forelimb of Santacrucian sloths based on the reconstruction of musculature and inferences on function, and the functional properties of the limb joints.
MATERIALS AND METHODS
- Top of page
- MATERIALS AND METHODS
- QUALITATIVE FUNCTIONAL MORPHOLOGY
- LITERATURE CITED
The fossil sloths studied here (Fig. 2) include several specimens collected by expeditions during the 19th and early 20th centuries, housed in museums of Argentina and the United States of America, and material recovered by the Museo de La Plata-Duke University joint expeditions over the last decade that belongs to the Museo Regional Provincial P. M. J. Molina (Río Gallegos, Argentina). Santacrucian sloths specimens are listed in Table 1. As forelimb remains are not known for some genera (Planops, Megalonychotherium, Hyperleptus, and Analcimorphus), the analysis focused only on Hapalops, Pelecyodon, Schismotherium, Eucholoeops, Prepotherium, Nematherium, and Analcitherium. Extant mammals studied (housed in mammalogy collections from Argentina and the USA) are listed in Table 2.
|Folivora indet.||MPM-PV 3458|
|Megalonychidae||Megalonychidae indet||AMNH 9249; AMNH 9494; AMNH 94754|
|Eucholoeops ingens||FMNH 13125; FMNH 13280; MPM-PV 3401; MPM-PV 3451|
|Eucholoeops cf. fronto||MPM-PV 3403|
|Eucholoeops sp.||MPM-PV 3651; MPM-PV 3402|
|Megatheriidae||Prepotherium potens||YPM-VPPU 15345; YPM-VPPU 15412; YPM-VPPU 15676|
|Basal megatherioidea||Hapalops angustipalatus||YPM-VPPU 15562|
|Hapalops elongates||FMNH 13123; FMNH 13133; YPM-VPPU 15011; YPM-VPPU 15155; YPM-VPPU 15160; YPM-VPPU 15597|
|Hapalops indifferens||YPM-VPPU 15110|
|Hapalops longiceps||YPM-VPPU 15523|
|Hapalops platycephalus||YPM-VPPU 15536; YPM-VPPU 15564|
|Hapalops ponderosus||YPM-VPPU 15520|
|Hapalops rectangularis||AMNH 9222; FMNH 13143|
|Hapalops ruetimeyeri||FMNH 13130|
|Hapalops sp.||AMNH 9252; MPM-PV 3462; FMNH 13209; FMNH 15103; MLP 34-III-5-1; MPM-PV 3400; MPM-PV 3404; MPM-PV 3412; MPM-PV 3467; YPM-VPPU 15005; YPM-VPPU 15129; YPM-VPPU 15183; YPM-VPPU 15184; YPM-VPPU 15264; YPM-VPPU 15313; YPM-VPPU 15411; YPM-VPPU 15414; YPM-VPPU 15533; YPM-VPPU 15535; YPM-VPPU 15537; YPM-VPPU 15618; YPM-VPPU 15628; YPM-VPPU 15675; YPM-VPPU 15677; YPM-VPPU 15836|
|Schismotherium fractum||AMNH 9244|
|Pelecyodon arcuatus||AMNH 9240|
|Mylodontidae||Analcitherium sp.||FMNH 13131|
|Nematherium angulatum||FMNH 13129|
|Nematherium sp.||YPM-VPPU 15374; YPM-VPPU 15893|
|Bradypodidae||Bradypus sp.||AMNH 42454; 42838; 74136; 74137; 97315; 133437; 135474; 209940; 211663; 261304|
|Megalonychidae||Choloepus sp.||AMNH 16873; 35483; 70440; 90269; 139772; 139773; 209941; 265952|
|Myrmecophagidae||Myrmecophaga tridactyla||AMNH 1020; 100068; 100139;FMNH 15966|
|Tamandua sp.||AMNH 23432; 23436; 23437; 23565; 23567; 96258; 211659; 211660|
|Cyclopidae||Cyclopes didactylus||AMNH 4780; 167845; 171297; 204662; 213188; FMNH 61853|
|Dasypodidae||Priodontes sp.||AMNH 130387; 208104; FMNH 25271; 72913|
|Cabassous chacoensis||MLP 1-183|
|Chaetophractus villosus||MLP 821; MPL 785|
|Dasypus novemcinctus||MLP 1.I.03.76; 1.I.03.72.|
|Hapalops||Stem Megatherioidea||39.799 kg|
Institutional acronyms: AMNH, American Museum of Natural History, New York, USA; FMNH, Field Museum of Natural History, Chicago, USA; MLP, Museo de La Plata, La Plata, Argentina; MPM-PV, Museo Regional Provincial “Padre M. Jesús Molina”, Río Gallegos, Argentina; YPM-VPPU, Yale Peabody Museum, Vertebrate Paleontology, Princeton University Collection, New Haven, USA.
Based on previous anatomical descriptions of fossil and extant Pilosa (Ameghino,1891; Scott, 1903–1904; Taylor,1978, 1985; Mendel,1979, 1981; De Iuliis, 2003; McDonald,2003; McDonald and De Iuliis,2008), qualitative descriptions of functionally relevant skeletal features (such as articular surfaces and attachment sites for ligaments and muscles) of the forelimb of Santacrucian sloths are provided.
The analysis was performed by visual comparison with homologous elements of extant sloths (Bradypus and Choloepus), anteaters (Myrmecophaga, Tamandua, and Cyclopes), and armadillos (mainly Priodontes, but also Cabassous and Chaetophractus, see Appendix B), based on anatomical descriptions of extant mammals (Lessertiseur and Saban, 1971; Polly, 2007; De Iuliis and Pulerá, 2010), including humans (Gray,1918, revised edition of 2000). To avoid confusion and redundancy of anatomical terms, we follow the nomenclature of muscles and ligaments to that used by De Iuliis and Pulerá (2010) for mammals in general, and Mendel (1979, 1981) and Taylor (1978) for sloths and anteaters respectively. In relation to muscle and ligament attachment sites, we used the term enthesis, defined by Mariotti et al., (2007) as a simple surface irregularity, or osteoproductive/erosive formation, both produced by the bone as a response to mechanical loads related to movement and exerted by tendons and/or ligaments.
Muscular reconstruction in fossil taxa relies extensively on knowledge of the musculature of extant relatives (Bryant and Seymour,1990). However, in many cases, as indeed occurs for fossil sloths, the fossil taxa are so dissimilar to their extant relatives that the latter cannot serve as functional analogues. In such cases, it becomes essential to identify alternative analogues in order to infer soft tissue reconstructions and formulate functional hypotheses (see Vizcaíno et al.,2008); to this end, extensive reference to other xenarthrans such as anteaters and cingulates was required for muscular reconstruction in the Santacrucian sloths. The muscular reconstruction was performed by identifying bony features related to entheses of tendons and/or ligaments in extant sloths, anteaters, and armadillos, and investigating fossil sloths for homologous features. Formalized specimens of extant sloths and anteaters for dissection are scarce or unavailable. Therefore, we based our reconstruction largely on muscular descriptions of extant xenarthrans in the literature (Macalister,1869, 1875; Humphry,1869–1870; Windle and Parsons,1899; Jouffroy, 1971; Mendel,1979, 1981; Taylor,1978, 1985).
As described by Bryant and Seymour (1990) for carnivorans, the degree of certainty in muscular reconstruction decreases distally along the forelimb. Muscular entheses on the distal half of the zeugopodium are not readily recognized. Most of the entheses on the manus/autopodium are undoubtedly related to attachment of ligaments, precluding confident reconstruction of the musculature of the part of the forelimb. In extant Pilosa, several muscles attach on the manus by common tendons, fasciae, and aponeuroses (Macalister,1869, 1875; Humphry,1869–1870; Mendel,1979, 1981, 1985).
Muscular reconstruction allowed us to make qualitative inferences on the mechanical capabilities (i.e., function) of the appendicular apparatus of Santacrucian sloths. These inferences were based on previous works on extant Pilosa (Taylor,1978, 1985; Mendel,1979, 1981, 1985; Nyakatura et al.,2010) and other mammals (Argot,2001; Szalay and Sargis,2001; Sargis,2002; Candela and Picasso,2008), and mechanical analogues when needed. The interface between function and biological role was the averaged biomechanical situation (Oxnard,1984), which integrates functional information of each feature and element in a mechanical profile. In this sense, the functional analyses performed here may be considered as a qualitative biomechanical analysis. Finally, the biological significance of functional features, that is, the biological role, is discussed.
- Top of page
- MATERIALS AND METHODS
- QUALITATIVE FUNCTIONAL MORPHOLOGY
- LITERATURE CITED
Comparative Description of the Forelimb Elements and Muscular Reconstruction
In the next section, we describe the forelimb elements of Santacrucian sloths, focusing on functionally significant feature such as articular surfaces and entheses of ligaments and muscles. The description includes comparison with homologous elements of extant sloths, anteaters, and armadillos mentioned in the previous section and inferences on the presence and relative development of specific muscles and ligaments.
This element (Fig. 3) is preserved in specimens of Eucholoeops (MPM-PV 3402, 3403), Hapalops (MPM-PV 3400, 3412; YPM-VPPU 15562, 15005; FMNH 13143), and Pelecyodon (AMNH 9240), although the latter is a submature specimen and the scapula lacks its epiphyseal portions.
The general shape of the scapula of Hapalops, Eucholoeops, and Pelecyodon is slightly triangular, similarly to that of Choloepus and not as trapezoidal as that of Bradypus (Fig. 3e,f). The vertebral border in the scapula of Santacrucian sloths is not as inclined anteriorly as in Bradypus. Eucholoeops shows the greater expansion of the vertebral border, although the scapular protractor/retractor musculature in the Santacrucian sloths was apparently less well developed than in extant anteaters and the giant armadillo Priodontes. The cranial or supraspinous border is straight as in Tamandua, Myrmecophaga, and Priodontes (Fig. 3h–j), whereas in extant sloths and in Cyclopes (Fig. 3g) it is convex, which maximizes the attachment area for the m. levator scapulae and rhomboideus anterior. The medial surface of the scapula bears a rugose and subdivided but shallow fossa, which serves as the attachment site of the m. subscapularis (Fig. 3l). The scapular spine is tall and well developed, suggesting a robust m. trapezius. The supraspinous and infraspinous fossae, respectively, the origin sites of the mm. supraspinatus and infraspinatus, are well developed and similar in dimension, as in Myrmecophaga, Tamandua, Priodontes, and Dasypus. The infraspinous fossa is slightly larger but not to the degree as occurs in extant sloths and Cyclopes.
The secondary scapular spine is not as prominent as in anteaters and the armadillos Priodontes and Cabassous. Similarly, the postscapular fossa is less expanded, suggesting relatively smaller mm. teres major and triceps longus (Fig. 3k). In Eucholoeops, it is more developed than in Hapalops, and it is smaller in Pelecyodon, which resembles Bradypus in this regard.
The acromion process is rarely preserved. In Eucholoeops (MPM-PV 3402, 3403) Choloepus, it does not project anteriorly beyond the glenoid fossa, in contrast to the condition in Hapalops (MPM-PV 3400, 3412). The supraglenoid tubercle is prominent, indicating a very well developed m. biceps brachii. The glenoid fossa is piriform in anteroventral view and its anterior half curves ventrally together with the coracoid process. The latter is robust and mediolaterally expanded (Eucholoeops MPM-PV 3402), indicating strong development of the coraco-acromial ligament and mm. biceps brachii and coracobrachialis. In some specimens of Hapalops (YPM-VPPU 15562 and 15005) there is evidence of fusion between the anterior border of the acromion and the coracoid process (Fig. 3b), indicating a robust m. deltoideus, but not one as well developed as in Priodontes and Cabassous. The posterior border of the coracoid process is fused with the scapular border to form a coraco-scapular foramen, as occurs in other xenarthrans. The foramen is larger in Eucholoeops (e.g., MPM-PV 3402) than in Hapalops.
The clavicle of Santacrucian sloths is poorly known due to the scarcity of well preserved remains. In the few specimens that preserved a clearly identifiable clavicle (e.g., YPM-VPPU 15011, MPM-PV 3402, and MPM-PV 3467), the bone is slender and sigmoidal. It is more robust and bent than that of Choloepus; in Bradypus the clavicle is reduced to a ligamentous arch. The scapular end of the clavicle is rugose, but it is not clear whether this feature represents the origin enthesis of the clavicular portion of m. deltoideus, to attachment sites for ligaments, or both.
The humerus of the Santacrucian sloths is robust and massive (Figs. 4 and 5), especially that of the mylodonts Analcitherium and Nematherium, compared with that of extant sloths (Figs. 4e,f and 5g,h). In robustness and development of features associated with muscular enthuses, it resembles more the humerus of Myrmecophaga, Tamandua and the armadillos Priodontes and Cabassous.
The humeral head is sessile, posteriorly inclined and subspherical (Fig. 4). The tuberosities are lower than the humeral head. The greater tuberosity bears prominent entheses for well developed mm. supra- and infraspinatus (Figs. 4j and 5l,m). The lesser tuberosity is very robust and projects medially (especially in the Santacrucian mylodontids, Figs. 2c and 4c), suggesting a very well developed m. subscapularis. The bicipital groove is wide and shallow at this level, indicating that the origin tendons of the m. biceps were not particularly thick.
The deltoid and pectoral ridges are prominently developed (especially in the mylodonts Analcitherium FMNH 13131 and Nematherium YPM-VPPU 15347), forming a wide deltopectoral shelf that extends distally beyond the diaphyseal midlength (Fig. 5a–c,f,l) and indicating a great development of the mm. deltoideus and pectoralis major. The bicipital groove is narrower at this level, overlapped by the medial margin of the deltopectoral shelf. The posteromedial surface of the proximal third of the diaphysis bears strong entheses, indicating powerful mm. teres major and latissimus dorsi, and the posterolateral surface, near the proximal origin of the deltopectoral shelf, bears a well marked enthesis for the m. triceps externus (Fig. 5m). No distinguishable enthesis for m. brachialis was recognized.
The distal humeral epiphysis is wide, as in extant anteaters and Priodontes (Fig. 4q–t), Cabassous, and Chaetophractus. The elongated and rugose supracondylar ridge (Fig. 5a–c) resembles that of extant anteaters and armadillos such as Priodontes, Cabassous, and Chaetophractus, and suggests well-developed antebrachial flexor musculature, such as the m. brachioradialis (Fig. 5l). The ectepicondyle bears strong entheses for supinator and manual extensor muscles (mm. supinator, extensor carpi radialis, and ulnaris, extensor digitorum Fig. 5l). The entepicondyle is very well developed and projects markedly medially, as in extant anteaters and armadillos. The entepicondyle, also well developed, projects medially considerably more than in extant sloths. It resembles more that of Tamandua and Myrmecophaga and bears extensive origin entheses for powerful pronator and manual and digital flexor musculature (mm. palmaris longus, pronator teres, flexor carpi ulnaris and radialis, and flexor digitorum Fig. 5l). In contrast to Bradypus (Fig. 5g), the entepicondyle is pierced by a wide entepicondylar foramen, as in Choloepus, Tamandua, and Priodontes. The olecranal fossa is fairly shallow in all genera. The distal articular surface is wide, as in Tamandua, Myrmecophaga, and Priodontes, and comprises a comparatively large and globular lateral capitulum and a shallow medial trochlea. The capitulum resembles that of extant sloths (Fig. 4o,p), Tamandua and Myrmecophaga, lacking a lateral border termed capitular tail (in contrast to the condition in Priodontes, Fig. 4t, and Chaetophractus). The shallow trochlea resembles that of Bradypus, Tamandua, and Myrmecophaga, with an anteroposteriorly expanded medial margin. The capitulum and trochlea surfaces are of similar size in distal view.
The ulna of Santacrucian sloths is also robust compared to that of Bradypus and Choloepus (Fig. 6f,g). It resembles more that of extant anteaters (Fig. 6h–j), in contrast to the extremely robust form characteristic of extant armadillos (e.g., Priodontes, Fig. 6k, and Cabassous). The olecranon is strong and well developed in all genera and especially in Hapalops and Nematherium, but not as much as in armadillos (such as Priodontes), and bears very well marked entheses for very robust mm. triceps and anconeus (internus and externus) (Fig. 6l). The anterior border of the olecranon is posteriorly inclined en Eucholoeops and Prepotherium, whereas in Hapalops and Nematherium is more, it is more nearly aligned with the longitudinal diaphyseal axis. The semilunar notch is clearly delimited by a prominent coronoid process (especially in Eucholoeops and Prepotherium) and the anconeal process, as also occurs in Bradypus. The coronoid process bears a strong enthesis for the annular ligament and possibly also m. brachialis. A flat and elliptical radial notch lies on the lateral side of the coronoid process.
The ulnar diaphysis is robust and short compared to that of extant sloths, and more closely resembles that of extant anteaters. In Eucholoeops, Prepotherium (YPM-VPPU 15345) and Nematherium (FMNH 13129) it is straight, while in Hapalops and Pelecyodon (AMNH 9240) it is posteriorly convex. The diaphyseal diameter diminishes distally, as in extant sloths. Its medial surface bears a shallow fossa for the origin of the m. flexor digitorum profundus.
The distal epiphysis is robust and wide, resembling that of Tamandua. The interosseous margin at this level lacks a discrete facet for articulation with the radius. The styloid process is robust, wide and sessile, as in Bradypus, with a flat and anteromedially-facing distal facet for the cuneiform (“pyramidal” of Lessertisseur and Saban, 1971; “triquetrum” of Mendel,1981; “triquetal” of Polly, 2007; “triangular” in Gray,1918).
As noted for the previously described elements, the radius of Santacrucian sloths is short and robust (Figs. 7 and 8), resembling more that of Choloepus than that of Bradypus. The overall robustness of this element resembles the radius of Myrmecophaga and Tamandua. The diaphysis is medially convex.
The radial head is relatively large and elliptical in proximal view, as in Myrmecophaga and Tamandua (Fig. 7h,i), and differing from the small and circular radial head of Choloepus and Bradypus (Fig. 6e,f). The fovea for articulation with the humeral capitulum is rounded and the facet for articulation with the ulna is flattened. The bicipital tuberosity (“radial tuberosity” of Polly, 2007) is stout, indicating a very well-developed m. biceps brachii, and it is placed from the center of the semilunar notch at a similar distance from this point to the tip of the olecranon.
The diaphysis is very robust (Fig. 8a–d). It is proximally cylindrical in section but becomes more mediolaterally flattened, expanded, and curved medially in its distal third (particularly in Nematherium YPM-VPPU 15893), where it bears well-marked entheses that indicate powerful pronator-supinator (mm. supinator and pronator teres) and antebrachial flexor (m. brachioradialis) musculature (Fig. 8k–m), especially compared with extant sloths. The radius is sigmoidal, so that its proximal and distal epiphyses are offset (rather than longitudinally aligned), especially in Hapalops and Nematherium (Fig. 8b,d).
The distal epiphysis is wide (Fig. 7k–n), resembling that of Choloepus, with a well- developed and anteromedially placed styloid process. Several well-marked grooves for tendons of the carpal and digital extensor musculature are present (Fig. 8k), and indicate that these muscles were robust. The radial articular facet for carpal bones faces slightly posteriorly, and the facet for articulation with the distal end of the ulna is triangular and shallow.
Anterior Autopodium: Manus
Anterior articulated autopodia of Santacrucian sloths are known from few specimens (e.g., Eucholoeops FMNH 13125, Hapalops FMNH 15523, Nematherium FMNH 13129, and Eucholoeops MPM-PV 3402; Fig. 9). The manus (Fig. 9a) is markedly conservative when compared with that of extant sloths: it is pentadactylous, and without the reduction, loss, or fusion of elements that characterizes extant (as well as some extinct) sloths (Fig. 9b). Rather, it resembles more the configuration present in Myrmecophaga and Tamandua (Fig. 9c) and possesses all the elements typical of the ancestral mammalian condition (see Polly, 2007).
The proximal row of carpal elements, including the scaphoid (navicular of Gray,1918), lunar (lunate of Mendel,1981), and cuneiform, form a smooth and convex surface, with the scaphoid bearing a well raised medial rim. Distal carpals include well-developed unciform, magnum, trapezoid and trapezium. The metacarpals (Mcs) are robust, especially Mcs II and III. Mcs I-III are shorter than the others, a feature present in many Pilosa (McDonald,2003), although generic variation in relative length of Mcs III and IV is registered (Fig. 2). The first phalange of each digit is strong and massive, and bears dorsopalmarly elongated articular surfaces. The second phalange of each digit is longer and more gracile. The ungual phalanges (Fig. 9f), not as curved as those of extant sloths (Fig. 9d), are robust and well developed, with those of digits II-IV being largest. The subungual tuberosity is massive and rugose, indicating a potent flexor musculature (mm. flexor digitorum profundus).
QUALITATIVE FUNCTIONAL MORPHOLOGY
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- MATERIALS AND METHODS
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The morphology of the vertebral border of the scapula of Santacrucian sloths indicates that the protractor/retractor and stabilizing musculature (m. serratus and m. levator scapulae) were not as developed as in extant anteaters and armadillos such as Priodontes, suggesting that the scapula was subjected to great mechanical stresses in protraction-retraction. Development of m. supraspinosus and morphology of glenoid fossa suggest that humeral ability for elevation and protraction was less developed that in extant sloths and Cyclopes. This apparently applies as well to external rotation of the humerus, which resembles the condition in Myrmecophaga, Tamandua, and Priodontes than arboreal xenarthrans. The robust scapular spine, indicating a powerful m. trapezius, suggests good ability for scapular retraction and stabilization, which contrasts with the implications derived from the morphology of the vertebral border.
In Hapalops, the m. deltoideus was more capable for humeral elevation than in Eucholoeops, as suggested by its more anteriorly expanded acromion. Moreover, the presence of an ossified acromio-coracoid arch in some specimens of Hapalops may reflect marked mechanical stress applied to the shoulder. The ventrally incurved anterior apex of the glenoid fossa would have acted as a stop for shoulder hyperextension and possibly in preventing dislocation in hyperflexed stances (Fig. 10), suggesting that the gleno-humeral joint was subjected to high mechanical stresses in flexed stances.
Although the origin enthesis of the clavicular portion of the m. deltoideus (clavodeltoideus) could not be determined (due, as noted above, to the scarcity of preserved clavicles), the presence of a well-developed clavicle may be inferred in all the Santacrucian genera analyzed here based on the expanded acromion and provides additional support for functional hypothesis concerning high mobility of the shoulder joint.
The posteriorly inclined and sub-spherical humeral head, together with little raised tuberosities, permitted wide mobility of the gleno-humeral joint, especially in protraction and abduction. Conversely, raised tuberosities restrict the mobility of humerus, especially in protraction and extension. The medially expanded lesser tuberosity improved leverage for the m. subscapularis during internal rotation and adduction of the humerus, but would also have stabilized the shoulder against hyperabduction. Additionally, the low tuberosities allowed the tendons of the mm. supra- and infraspinatus to gain extensive attachment around the humeral head, thus contributing to the structural integrity of the gleno-humeral joint.
The morphology of the deltopectoral shelf improved the lever arm of the mm. deltoideus and pectoralis major compared with the condition in extant sloths and anteaters, The shelf resembles more closely that of the armadillos Priodontes, Dasypus, and Chaetophractus, and indicates that these muscles conferred powerful humeral abilities in abduction and adduction and participated in arm retraction and internal rotation.
As indicated by the morphology of the supracondylar ridge, the well developed flexor musculature of the antebrachium allowed powerful flexion of the zeugopodium, especially in pronated and semipronated stances. The well-developed, medially protruding entepicondyle reflects great mechanical advantage of the powerful carpal and digital flexor musculature. Thus, the Santacrucian sloths, and particularly the mylodontids, were capable of relatively powerful autopodial prehension, much more so than are extant sloths. The Santacrucian sloths were similar in this regard to Myrmecophaga, but prehension was not as powerful as in Tamandua and Cyclopes. Among these muscles, the m. pronator teres is especially important because it (along with the m. brachioradialis) is involved in pronation and flexion of the antebrachium as well as in stabilization of the radio-humeral joint. Another powerful muscle arising from the entepicondyle is the m. anconeus, which is involved in the stabilization of the humero-ulnar joint in flexed stances and when the joint is in abduction. This muscle was comparatively more massive and powerful in Santacrucian sloths than in their extant relatives, suggesting greater requirement for joint stabilization in the former.
The shallow olecranal fossa indicates that full extension of the antebrachium was restricted in Santacrucian sloths, especially in those genera in which the anterior margin of the olecranon is more nearly aligned with the diaphysis (e.g., Hapalops and Analcitherium).
The morphology of the distal humeral joint, with a large globular capitulum lacking a capitular tail (as occurs in extant sloths, Myrmecophaga and Tamandua) and a flattened trochlea (resembling that of Bradypus, Myrmecophaga and Tamandua and differing from that of Choloepus), suggests that the capitulum, rather than the ulnar coronoid process, was the main point of transmission of mechanical loads between the zeugopodium and stylopodium during flexion. However, similar development of the capitulum and trochlea in distal view suggests that transmission of mechanical loads in antebrachial/zeugopodial extension was shared by the capitulum and trochlea. Additionally, the sphericity of the capitulum indicates good rotation of the radius on the capitulum during antebrachial/zeugopodial flexion.
The development of the olecranon increases the lever arm for the m. triceps. Thus, Santacrucian sloths were capable of very powerful antebrachial/zeugopodial extension, much more so than are extant sloths but less than the anteaters and cingulates analyzed here. Among the Santacrucian genera, Nematherium and Hapalops were capable of more forceful antebrachial extension than Eucholoeops and Prepotherium. The m. triceps also participates in the flexion of the shoulder when the antebrachium is fixed or flexed. The inclination of the anterior border of the olecranon indicates that the maximum lever arm for the m. triceps was achieved in a more extended stance in Eucholoeops and Prepotherium, whereas this was achieved in a semi-flexed stance in Hapalops. Thus, Nematherium and Hapalops were able to develop powerful forces in flexed stances, while Eucholoeops and Prepotherium were capable of improved strength in extended stances.
The morphology of the semilunar notch indicates a highly stabilized humero-ulnar joint restricted to flexion and extension, mainly in Eucholoeops and Prepotherium, with an extensive area of transmission of mechanical loads between the ulnar coronoid process and the humeral trochlea. However, the morphology of the anterior half of the trochlea apparently implies the opposite converse (see above), so it is clear that Santacrucian sloths showed a mosaic of functional features. Further, the weight of evidence indicates that the elbow joint of Santacrucian sloths, resembling slightly that of extant sloths, was more stable and restricted in its mobility than in extant anteaters. Among Santacrucian sloths, Prepotherium and Eucholoeops would have had a more stabilized elbow joint, although by way of distinct morphologies: Prepotherium through a deeper semilunar notch and Eucholoeops through a deeper humeral trochlea. Hapalops possessed a looser and more mobile elbow joint than that of Prepotherium and Eucholoeops, which were capable of postures involving greater antebrachial extension (Fig. 11).
The flattened radial notch suggests that rotational movements of the head of radius on the ulna (e.g., supination) were not mechanically stressed. This applies as well to the distal ulno-radial contact, based on the morphology of the distal facet. The robustness and orientation of the ulnar styloid process indicates that great mechanical loads were transmitted between the cuneiform and the ulna, especially during flexion and ulnar deviation.
The elliptical shape of the radial head and the morphology of the ulnar facets for the radius suggest supination in Santacrucian sloths, in contrast to the implications of form of the humeral capitulum. The robust bicipital tuberosity and its distance from the center of the semilunar notch, resembling more the condition of extant vermilinguas than of extant sloths, indicates a powerful lever arm for the m. biceps, a main flexor of the antebrachium.
The stout and distally expanded radial diaphysis, reflecting very well developed mm. pronator teres and brachioradialis, also indicates powerful capacity for antebrachial flexion. The m. pronator quadratus, which also reflects radial diaphyseal expansion, is involved in maintaining the structural integrity of the distal zeugopodium when subjected to mechanical stresses tending to separate the ulna and radius. This was apparently especially important in Nematherium, in which the radial diaphysis is particularly expanded. The offset between the proximal and distal ends of the radius, owing to the sigmoidal form of its diaphysis, may have improved the mechanical advantage of the pronator and supinator musculature. The facet for articulation with the distal end of the ulna is triangular and shallow, indicating that movement between the distal ends of the radius and ulna were restricted and/or not subjected to marked mechanical loads. The morphology of the radial articular facet for carpal bones suggests that the wrist joint was capable of extensive flexion but only limited extension.
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The proximal row of carpal elements (scaphoid, lunar, and cuneiform) forms a smooth and convex surface, indicating good capabilities of rotation within the radial articular facet for carpal bones. The scaphoid bears a medial rim that acted as a stop for ulnar deviation of the manus (Fig. 9a). Although inferences cannot be made on the maximum degrees of flexion and extension, it is clear that the wrist was a very robust joint and well suited for performing activities under great mechanical loads. The robustness of the proximal phalanges, their dorsopalmarly elongated articular surfaces, and the robustness of the metapodials, indicate strong demands on the metapodium-proximal acropodial joints, the morphology of which suggests considerable articular stability and mobility restricted to flexion-extension. The development of the digital and carpal flexor musculature indicates very powerful manual/autopodial prehension and a role in preventing digital hyperextension during strenuous activities.
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Biological Role of Functional Features of the Forelimb
Now that inferences on function have been provided, we may hypothesize on the biological role of these functions. As noted in the Introduction, biological role is defined as the use or uses to which a given function is put to by an organism. Here we discuss the results of the muscular reconstruction and qualitative functional morphology and infer the biological role of the functional features described, mainly by comparison with knowledge on extant mammals.
Functional Features of Scapula
The ecological interpretation of the general shape of the scapula is complex. Oxnard (1963) claimed that because this element is supported entirely by muscles and it is not linked firmly to the axial skeleton, its shape should strongly reflect functional factors (see Nyakatura et al.,2010 on Choloepus). Argot (2001) recognized that didelphids with expanded vertebral borders are arboreal; whereas those with anteriorly sloped and less expanded borders are more terrestrial. Jolly (1967) explained that among arboreal forms the mm. serratus and rhomboideus require increased mechanical advantage because they must resist the rotation of the scapula during climbing. Additionally, Sargis (2002) linked locomotion on arboreal substrates with high demands on the mm. supraspinatus and deltoideus. According to Argot (2001), the development of the m. infraspinatus is related to the ability to move the forelimb to grasp supports in a three-dimensional space. However, Argot (2001) noted that the functional interpretation of the relative development of the supra- and infraspinous fossae is not readily discernible because of the multiplicity of mechanical demands related to several movements (including stabilization of the gleno-humeral joint). The development of the postscapular fossa, and hence of the humeral retractor muscles, has been considered as an indicator of digging habits (Hildebrand,1988; Monteiro and Abe,1999; McDonald,2003). Argot (2001) remarked that the function of the m. teres major as a humeral retractor is important both in digging and in climbing forms, acting as a forelimb retractor in the former and elevating the body in the latter. Thus, this feature, on its own, lacks utility as an ecological predictor.
Outlining, the functional features of the scapula of Eucholoeops and Hapalops suggest, on the one hand, less climbing ability than in extant sloths and Cyclopes and, on the other hand, less digging ability than in the extant anteaters and armadillos analyzed here.
Mobility of Gleno-Humeral Joint
Capabilities for humeral elevation and protraction were apparently not as well developed in Santacrucian sloths as in extant arboreal pilosans. Among the former, Hapalops would have had better humeral elevation capabilities and was perhaps a more agile climber than Eucholoeops, but the evidence is not determinant. Improved mobility of the gleno-humeral joint has been related to arboreal locomotion in several groups of mammals (Argot,2001 and Szalay and Sargis,2001 for Metatheria; Sargis,2002 for Tupaiidae, Candela and Picasso,2008 for Hystricognathi). The opposite condition, with movements restricted to the parasagittal plane by highly raised tuberosities (mainly the lateral one, see Argot,2001; Polly, 2007; Candela and Picasso,2008), is related to greater stabilization of the joint in terrestrial forms (Szalay and Sargis,2001). Argot (2001) remarked that some arboreal didelphids increase the lever arm of the m. subscapularis through a more medially expanded lesser tuberosity than in terrestrial didelphids; Sargis (2002) also remarked on the important function of the m. subscapularis during locomotion on vertical or strongly inclined supports.
The Santacrucian sloths had a more mobile shoulder joint than the terrestrial extant xenarthrans analyzed here, well equipped for high mechanical demands in flexion and retraction and suited with a well developed musculature for abduction and flexion. These functional features are consistent with both the mechanical contexts of digging and climbing (Fig. 12). Probably, a flexed stance of this joint was usual, especially in Hapalops and Eucholoeops, whereas in mylodontids (Analcitherium and Nematherium) the posture of the gleno-humeral joint, including a somewhat proximally longer greater tubercle of the humerus, was more extended, rendering it less suitable for humeral elevation.
Adduction and Retraction of the Forelimb
With regard to the biological role of a well- developed m. pectoralis, Argot (2001) noted that this humeral adductor can force both antebrachia and manus against a support during climbing (see also McEvoy,1982). Other muscles collaborating in this action are the mm. latissimus dorsi, teres major, and subscapularis, all of which are also well developed in Santacrucian sloths. Candela and Picasso (2008), however, indicated that powerful action of m. pectoralis in Hystricognathi rodents can be related to the mechanical context of climbing, digging, and even swimming. Thus, adduction of the humerus (and the entire forelimb) was more powerful in Santacrucian sloths, especially in Analcitherium and Nematherium, than in the extant xenarthrans analyzed here. This functional feature would have been involved mainly in climbing activities (Fig. 13), but also in digging. Humeral retraction, important during climbing and swimming, was more powerful than in extant sloths, resembling that of extant anteaters and armadillos. Among Santacrucian sloths it was strongest in Nematherium and Analcitherium, followed by Hapalops and then Eucholoeops.
Mobility of Elbow Joint
Restriction to full antebrachial extension, as indicated by the morphology of the olecranal fossa of Santacrucian sloths, is consistent with arboreal habits, as noted by Candela and Picasso (2008) for Hystricognathi rodents. The capitular tail, present in extant armadillos such as Priodontes and Chaetophractus, has been linked to enhancement of joint stabilization (see Argot,2001; Sargis,2002; Candela and Picasso,2008). Its absence in Santacrucian sloths thus suggests fewer requirements for stabilization, as compared with armadillos. However, there is evidence (morphology of semilunar notch and development of antebrachium flexor and extensor musculature) that the elbow joint of Santacrucian sloths was subjected to great mechanical stress. Argot (2001) noted that the morphology of the trochlea in arboreal didelphids indicates less stabilization, while full extension of the antebrachium appears to be restricted. The combination of these functional features resembles the condition in Santacrucian sloths, but also of other xenarthrans analyzed here (e.g., Tamandua and Myrmecophaga). In contrast, stabilization of the elbow joint and increased extension of the antebrachium are linked by Argot (2001), Sargis (2002) and Candela and Picasso (2008) to terrestrial forms with cursorial locomotor styles.
Thus, the elbow joint of Santacrucian sloths was more stable and restricted in its mobility than that of extant anteaters, resembling somewhat that of extant sloths. Among Santacrucian sloths, the elbow joint was most highly stabilized in Prepotherium (by way of a deeper semilunar notch) and Eucholoeops (by way of a deeper humeral trochlea), while Hapalops had a looser, more mobile elbow joint that was slightly better-suited for climbing activities in flexed stances. These former two genera were more capable of extended postures of the antebrachium, a functional feature consistent with extension of the forelimb both during terrestrial locomotion and climbing.
Flexion of the Antebrachium
It is difficult to discern whether the great development of the antebrachial flexor musculature in Santacrucian sloths reflects arboreal or digging habits. Following Argot (2001 and references therein), supinator musculature can collaborate in adduction of the left and right manus against a support, acting jointly with other adductor muscles (Fig. 13). However, no clear correlation exists between development of the m. brachioradialis and carpal extensor musculature and locomotory habit. Candela and Picasso (2008) described a great development of this musculature in both arboreal and climbing forms of Hystricognathi rodents, but also noted it in swimming forms such as Myocastor coypus. The improvement in mechanical advantage for antebrachial flexion in Santacrucian sloths would be related to raising body weight when holding from a support (Fig. 12), suggesting arboreal habits. Argot (2001) described a more robust m. biceps brachii in arboreal didelphids than in terrestrial didelphids, linking this feature to powerful flexion for body support during climbing and to supination when the left and right manus are opposed on either side of a support (see McEvoy,1982).
Extension of the Antebrachium
The ecological significance of increased leverage for antebrachial extension in Santacrucian sloths is not clear. In general terms it is claimed that leverage of the m. triceps is strongly correlated with locomotor habit or style, but a wide variation in olecranon length has been reported (see Argot,2001; Szalay and Sargis,2001; Sargis,2002; Elissamburu and Vizcaíno,2004; Candela and Picasso,2008). Argot (2001) discussed functional implications of the m. triceps. In terrestrial forms, this muscle collaborates participates in supporting the body, in addition to providing propulsive power, by extending the antebrachium against body weight. In arboreal forms, however, body weight is supported mainly by the flexor musculature during climbing of arboreal supports. Moreover, in climbing forms the m. triceps acts in flexed stances (Argot,2001), but such postures are also common in small sized terrestrial mammals (Polly, 2007). Taylor (1974) noted that the m. triceps also supports body weight during headfirst descent of arboreal substrates. A further consideration is that a long olecranon improves the lever arm of the m. anconeus for stabilizing the elbow joint. Further, olecranon length is also related to the speed of antebrachial extension. However, the implications of the differences between Santacrucian and extant sloths cannot be addressed given that the reduced olecranon in extant forms is related to a minimal requirement for antebrachial extension, which is produced mainly as a response to gravity (White, 1993a,b).
As with other functional features, the curved ulnar diaphysis in Hapalops can be related to the mechanical context of arboreal locomotion as well as to that of digging. Argot (2001) related the posterior convexity of the ulna of some didelphids with the resultant of flexor (mainly m. biceps) and extensor forces (mainly m. triceps) applied to the ulnar diaphysis during climbing. Curvature of the ulnar diaphysis improves the lever arm of the m. triceps when the elbow is flexed, but strongly diminishes it when the antebrachium is extended (Argot,2001; Sargis,2002; Candela and Picasso,2008). Szalay and Sargis (2001) noted, as a general pattern among placental mammals, that arboreal forms possess a short and anteriorly directed olecranon, while terrestrial forms possess a straight or even posteriorly inclined olecranon. However, based on the numerous studies analyzing and describing digging capabilities in xenarthrans (see Vizcaíno et al.,2008 for a review), it is clear that biological roles (such as substrate use, Fig. 12) other than locomotion may be reflected at the morphology of the ulna.
Wrist Joint and Pronation-Supination Capabilities
The morphological evidence suggesting that great loads were borne by the wrist joint in Santacrucian sloths (especially Hapalops and Prepotherium) may be interpreted within the context of different biological roles: support and elevation of body weight during climbing and retraction of the forelimb during digging. With regard to pronation-supination, good abilities are described for arboreal mammals (Oxnard,1984; Sargis,2002; Candela and Picasso,2008), but the evidence for such abilities in Santacrucian sloths remains inconclusive. Pronation and supination perform the biological role of positioning the manus in different orientations during climbing. Argot (2001) noted that the radial head is more rounded in arboreal didelphids than in terrestrial didelphids. Additionally, elongated and subrectangular radial heads were described for terrestrial Hystricognathi by Candela and Picasso (2008) and for some terrestrial marsupials by Szalay and Sargis (2001). Notwithstanding, the significance of humeral capitular and radial head morphologies with regard to pronation-supination abilities is unclear.
The manual flexor musculature is poorly developed in terrestrial digitigrade cursors, whereas it is well developed in plantigrade mammals with climbing or digging capabilities (Lessertiseur and Saban, 1971), as is the case in Santacrucian sloths. Among the Hystricognathi rodents, Candela and Picasso (2008) described a powerful manual flexor musculature in both arboreal and digging forms. With regard to the functional features of the manus of Santacrucian sloths, the morphology of the metacarpals and phalanges does not provide evidence for drawing unequivocal ecological inferences, except that they were well suited for performing strenuous activities. According to Argot (2001), the form of the ungual phalanges provides important clues for inferring locomotory habit. We, however, consider that other factor influence their morphology in digging-capable forms. Concerning the musculature, in arboreal didelphids the powerful digital flexor musculature is involved not only in flexion but also in avoiding hyperextension of the digits (Argot,2001). This latter functional feature is also applicable to the mechanical context of digging, thus precluding its use as an unequivocal ecological predictor.
Climbing and Digging
As explained in previous paragraphs, many of the functional features of the forelimb of Santacrucian sloths are consistent with different biological roles within distinct but mechanically similar ecological contexts: digging and climbing (Fig. 12). The mechanical requirements for digging and climbing activities involve powerful adduction of the forelimb, enhanced stabilization of shoulder, elbow and wrist joints, and powerful forelimb retraction, manual prehension, and digital flexion. This leads to a highly interesting pattern: while ecologically climbing and digging have different contexts and biological significance, they are not, functionally, particularly dissimilar. The mechanical requirements of these activities overlap to varying degrees depending of the styles of climbing and digging. This has been recognized previously by several authors, such as White (1997), Argot (2001) and Toledo et al., (2012). Morphometric analyses performed by Toledo et al., (2012) on the forelimb of Santacrucian sloths revealed interesting morphometric similarities between these fossil sloths and an assemblage of extant digging mammals, of which many are also good climbers. These similarities were explained, in part, by variables functionally related to the mechanical contexts of both digging and climbing activities. An interesting hypothesis to be tested in future research is that, the more generalized taxa are being compared, the greater the degree of overlap between the mechanical requirements of digging and climbing (and hence the functional solutions to both problems).
Our results provide additional support for the paleobiological inferences of Santacrucian sloths proposed by White (1993a,b and 1997) on climbing habits and Toledo et al., (2012) on digging habits. The forelimb of these fossil sloths suggests that they were arboreal or semiarboreal forms with good digging capabilities, especially the mylodontids and Hapalops. As discussed in Toledo et al., (2012) and considering the inferred digging habits for Pleistocene ground sloths by Bargo et al., (2000), the evidence for good digging abilities in Santacrucian mylodontids would suggest a long phylogenetic history of digging habits for mylodonts.
Body size, one of the most important biological variables (see Smith and Savage,1955; Eisenberg,1981; Hildebrand,1988; Brown and West,2000 and references therein), must be carefully considered when inferring paleoecological features of fossil taxa (Andrews et al.,1979; Van Couvering,1980; Kay and Madden, 1997; Reed,1998; Vizcaíno et al.,2006, 2008, 2010; Kay et al.,2012). Previous works provide body mass estimates for many Santacrucian genera (White, 1993a,b; Croft,2000, 2001; Bargo et al.,2009, 2012; Toledo et al., in press). Although they differ in methodology and results, all generated estimates exceeding 40 kg for some genera and 100 kg for others (Table 3). Such values place Santacrucian sloths, along with the extinct giant lemurs of Madagascar (Megaladapis and Archaeoindris, see Jungers et al.,2002), among the heavier extant climbing mammals. As discussed by Toledo et al., (in press), most arboreal mammals are small-sized forms (Cartmill, 1985; Hildebrand,1988). However, many large felids and, in particular, ursids are very capable climbers, although they cannot be categorized as “arboreal.”
Following Hildebrand (1988) the arboreal substrate offer several advantages, such as food resources unavailable at ground level, shelter for resting, avoidance of predation, and more efficient locomotion when the ground is rough or flooded. However, arboreal locomotion entails its own difficulties, linked to two important mechanical aspects: avoidance of falling and movement through a three-dimensional and discontinuous substrate. Extant arboreal mammals exhibit panoply of locomotor and posture strategies for confronting these problems (Cartmill, 1985; Hildebrand,1988). Some of them leap or glide between supports (e.g., many acrobatic primates and marsupials), while others move more slowly by “reaching and bridging” (e.g., the extant sloths and the orangutan). Most arboreal forms rely on opposable digits, prehensile tails, curved claws, flexed stances, or different combinations of these features to hold onto supports. In addition, many arboreal mammals appose their hands the left and right manus on either side of a support, applying muscular force to counteract the torque and sliding components of body weight during climbing (Cartmill, 1985).
The body size estimates and overall functional features of the forelimb of Santacrucian sloths permit us to infer that their locomotor strategies on arboreal substrates were fairly limited when compared with extant sloths. Certainly, they were not well suited for leaping: their forelimb morphology increased the mechanical advantage of many muscles, optimizing force over speed and agility. There is no evidence of opposable digits, in contrast to many extant arboreal mammals such as primates and marsupials (Cartmill, 1985; Hildebrand,1988). In contrast to extant sloths that rely on their long forelimbs for “reaching and bridging” strategies (Hildebrand,1988) to move from one support to another, the comparatively short and robust forelimb of Santacrucian sloths, limited for antebrachium extension, precluded their application for such purposes, especially in Analcitherium, Nematherium, and Hapalops. Among the strategies employed by extant arboreal mammals to decrease the risk of collapse or breaking of the support is the distribution of body weight over two or more supports, as the extant sloths (Mendel,1979) and orangutan do (Hildebrand,1988). Santacrucian sloths were limited in this behavior, and hence were probably constrained to moving only on thicker and more resistant supports. An alternative biological role for powerful forelimb retraction may have been to pull more slender branches toward the body to access leaves as a food source. However, the forelimbs of Santacrucian sloths were especially well suited for apposing each manus on either side of a support and applying powerful adduction forces combined with curved digits equipped with prominent claws that could be powerfully flexed. Using the forelimbs in this manner, the Santacrucian sloths would have employed a climbing style similar to that of Tamandua and other slow climbing mammals, such as the koala Phascolarctos cinereus (Smith and Ganzhorn,1996; Nowak,1999; Toon and Toon,2004).
Several of the functional differences among the genera analyzed here may be related to variation in locomotion and posture. Eucholoeops, for example, may have employed a more agile climbing style. Given its more extendable elbow joint and greater shoulder mobility, it may have relied to a greater degree on extension of the forearm and distribution of its body mass over several supports. A more extendable forearm and mobile shoulder combined with its relatively smaller body mass may have allowed Eucholoeops to move over more slender supports than other Santacrucian sloths. Hapalops, which displays wide variation in body size (see Toledo et al., in press) and more flexed forelimbs, was restricted to thicker supports than Eucholoeops, but it was probably able to climb vertical branches because of its greater muscular force. Schismotherium and Pelecyodon are less readily categorizable due to insufficient functional information, but it is reasonable to suppose that their smaller body size allowed them to move over thinner branches. Among the larger genera, Prepotherium was probably the most terrestrial, based on its body mass being largest and more extended forelimb posture; extension of the forearm may have played a role in defense against predators. Mylodontids were probably the most able diggers owing to their powerful musculature. Given their body mass, they were probably mainly terrestrial, spending most of their time on the ground, possibly foraging by digging. Their powerful musculature may in any event have allowed them to climb over thicker branches, perhaps to rest and/or to avoid predation.
In summary, forelimb features of Santacrucian sloths allow us to infer that all were good climbers, but limited in their locomotor strategies on the supports, and diggers. They were probably slow climbers that relied on flexed stances, curved claws and a powerful musculature to move over thick branches, very similarly to extant slow climbing mammals such as Tamandua and Phascolarctos. Some locomotor and postural differences among the genera analyzed here may be proposed. Studies in progress on hindlimb functional properties will provide additional insight on their substrate preference and locomotory strategies and allow the formulation of more integrative ecological hypotheses.
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The forelimb of Santacrucian sloths differ from those of the extant tree sloths Bradypus and Choloepus. In the robustness of the elements, development of features related to attachment of muscles and ligaments, and pentadactylous and conservative manus, the Santacrucian sloths more closely resemble extant anteaters such as Tamandua and Myrmecophaga.
The forelimb musculature of Santacrucian sloths resembles that of extant Pilosa (especially anteaters), retaining the basic forelimb configuration of a generalized mammal.
The forelimb musculature of Santacrucian sloths was very well developed. Although there were minor differences among genera, the musculature allowed the application of powerful forces, especially in adduction of the forelimb, flexion and extension of the antebrachium and manual prehension, existing slight differences between genera.
These functional properties are congruent with both climbing and digging activities, and provide support for similar inferences in previous works.
Santacrucian sloths can be proposed as good climbing mammals, possibly arboreal or semiarboreal, and capable diggers. Their climbing strategies would have been limited, and thus these animals relied mainly on their great muscular strength and curved claws of the manus to move slowly over branches.
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The authors want to thanks M. Reguero and L. Pomi, D. Verzi and I. Olivares (MLP), W. Joyce and D. Brinkman (YPM), J. Flynn, N.B. Simmons, and C. Norris (AMNH), and W.F. Simpson and K.D. Angielczyk (FMNH) for kindly providing access to the collections under their care, and to the Dirección de Patrimonio Cultural of Santa Cruz Province and the Museo Regional Provincial P.M.J. Molina of Río Gallegos, for support during field work. The authors are especially grateful to G. De Iuliis for his valuable comments and corrections, and to J.L. White and one anonymous reviewer for greatly improving the quality of this work.
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- QUALITATIVE FUNCTIONAL MORPHOLOGY
- LITERATURE CITED
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