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Locomotor Correlates of the Scapholunar of Living and Extinct Carnivorans

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Locomotor Correlates of the Scapholunar of Living and Extinct Carnivorans Received: 4 February 2019 Revised: 21 May 2019 Accepted: 26 May 2019 DOI: 10.1002/jmor.21024 RESEARCH ARTICLE Locomotor correlates of the scapholunar of living and extinct carnivorans Rachel H. Dunn | Candice Cooper | Joshua Lemert | Natalie Mironov | Julie A. Meachen Department of Anatomy, Des Moines University, Des Moines, Iowa Abstract The relationship of carpal morphology to ecology and habitat is under studied in car- Correspondence Julie A. Meachen, Department of Anatomy, nivorans and more generally in mammals. Here, we use 3D-scanning techniques to Des Moines University, 3200 Grand Ave., Des assess the usefulness of a carpal bone, the scapholunar, in carnivorans to reflect ecol- Moines, IA 50312. Email: [email protected] ogy and habitat, and to reconstruct the ecology of five extinct carnivorans from two fossil sites: Rancho La Brea and Natural Trap Cave. We 3D-scanned scapholunars Funding information NSF EAR-SGP, Grant/Award Number: and measured articular surface areas and angles between articular facets using 1425059; Des Moines University GeoMagic and Rhino 3D-software. We analyzed the difference in these metrics using multivariate analysis of variance and discriminant function analysis. Results show that the scapholunar reflects ecological signal, with clear groupings of cursorial carnivorans and grappling/climbing carnivorans; however, phylogenetic signal was also present in the results with hyaenids, canids, and large felids in distinct mor- phospaces. Extinct species Miracinonyx trumani (American cheetah) and Smilodon fatalis (sabertooth cat) showed surprising results with M. trumani grouping with pantherines instead of Acinonyx or Puma, suggesting it runs but still retains the ability to grapple prey. S. fatalis groups with pantherines, but also shows some unique adap- tations, suggesting it had a different range of wrist motion than living cats. Overall, the scapholunar is a good indicator of ecology and functional morphology and can be another tool to use in modern and fossil carnivorans to reconstruct extinct ecologies and locomotor behaviors. KEYWORDS carpals, ecometrics, locomotion 1 | INTRODUCTION Palmqvist, 2014a, 2014b; Meachen, Dunn, & Werdelin, 2016; Meachen & Roberts, 2014; Meachen-Samuels & Van Valkenburgh, Functional morphology is the well-tested idea that body shape is corre- 2009; Meloro, 2011; Polly, 2010; Samuels, Meachen, & Sakai, 2013; lated with the forces an animal's body is subjected to each day, for Van Valkenburgh, 1985; Van Valkenburgh, 1987; Walmsley, Elton, example: running, climbing, or digging. Much work has been done on Louys, Bishop, & Meloro, 2012). Of all the limb elements, carpals and carnivoran functional morphology, and many studies have shown that tarsals are the least developed for reconstructing locomotor modes carnivoran postcranial morphology correlates well with locomotor mode, and environments, since they have been understudied and often over- looked compared with long bones. However, carpals and tarsals are habitat use, and prey-killing behavior (e.g., Martín-Serra, Figueirido, & potentially useful as they reflect wrist and ankle mobility, and there- Rachel H. Dunn and Julie A. Meachen are co-lead authors. fore locomotor mode, substrate use, and overall environment in which Journal of Morphology. 2019;1–10. wileyonlinelibrary.com/journal/jmor © 2019 Wiley Periodicals, Inc. 1 2 DUNN ET AL. an animal lives (Polly, 2010). Carpals and tarsals are also useful for Our goal is to assess the scapholunar bone as a proxy for locomo- paleontological fossil assemblages because they are diagnostic ele- tor mode or habitat use in carnivorans, using 3D-scans and surface ments and are likely to be fossilized. Higher fossilization probability is area dimensions. We will compare our results in modern species with due to their hard, compact nature (more cortical and less spongy known functional morphological and ecological data to determine bone), and because they contain less nutritional value (fat), so are less how well the scapholunar bone reflects functional morphology. likely to be destroyed by carnivores preburial (Darwent, Lyman, Because of its location and articulation with several other carpals, we Haglund, & Sorg, 2001; Marean & Spencer, 1991). hypothesize that the scapholunar will be highly indicative of locomo- Tarsals have been used with success to capture environmental tor ecology. Then, using modern species as a baseline, we aim to variables in several groups. Polly (2010) analyzed calcanea using linear reconstruct the individual locomotor modes of several extinct species measurements and gear ratios in carnivores, and found a strong corre- of carnivores from two late Pleistocene fossil sites: Natural Trap Cave, lation between temperature, ecoregion, and calcaneal morphology. and Rancho La Brea to determine what the scapholunar can teach us Panciroli, Janis, Stockdale, and Martín-Serra (2017) also found a clear about the behavior of these extinct organisms. link between calcanea and locomotor mode in extant and extinct car- nivorans. Astragali have been analyzed in apes to elucidate locomotor 2 | MATERIALS AND METHODS and substrate use differences in gorillas and other primates (Boyer, Yapuncich, Butler, Dunn, & Seiffert, 2015; Dunn, Tocheri, Orr, & Our sample comprises 34 scapholunars from five extinct species: Jungers, 2014). Canis dirus, Canis lupus sp., Panthera atrox, Smilodon fatalis, and Carpals have also been examined for locomotor traits. Multiple Miracinonyx trumani from Natural Trap Cave and Rancho La Brea; and studies have done qualitative examinations of carpal bones to assess 30 scapholunars from six extant species (Table 1). The specimens are their utility in locomotion and phylogeny (Argot, 2001; Lehmann, 1963; Salton & Sargis, 2008; Stafford & Thorington, 1998; housed at the following institutions: Kansas Museum of Natural His- Thorington & Darrow, 2000). Many of these studies found morpho- tory (KUM [modern], KUVP [fossil]), American Museum of Natural logical correlations between carpal morphology and locomotor mode; History (AMNH), University of Wyoming Geological Museum (UW), however, at least one found no correlation between carpals and loco- and Tar Pits Museum (TPM; for a complete list of all specimens with motor mode (e.g., Swiderski, 1991). Yalden (1970) did a qualitative museum catalogue numbers see Supporting Information Table S1). analysis of carnivore carpals and determined that there are differences Extant species were chosen either because they represent species in the carpals based on locomotor modes but did not give a quantita- most closely related to the extinct species of interest or are thought tive breakdown of these distinctions. Fewer studies have done quanti- to be most similar to them in purported locomotor category. For tative analyses on carpal bones (Almécija, Orr, Tocheri, Patel, & example, for the extinct species M. trumani, the American cheetah-like Jungers, 2015; Hamrick, 1997; Tocheri et al., 2003), and no quantita- cat, we chose both Puma concolor (closest genetic relative; Barnett tive analyses have been done on carnivoran carpals. This may be et al., 2005) and Acinonyx jubatus (purported ecomorph; Van Val- because these bones are small, rounded, and most of the useful infor- kenburgh, Grady, & Kurtén, 1990). Care was taken to avoid juveniles mation is from examining surface areas and curvatures, which are dif- whenever possible, although juvenile scapholunars were already ossi- ficult to quantify using traditional linear measurements. fied in the collections we had access to. We also took care to choose The scapholunar bone, a fusion of the ancestral mammalian scaph- both male and female specimens whenever possible. oid and lunate carpal bones, is found in a few taxonomic groups including tenrecoids, and carnivorans, among a few other taxa TABLE 1 Taxa included in this study (Salton & Sargis, 2008). This bone may be a good indicator of sub- Family Species N Locomotor mode strate use and locomotor mode because it is the largest bone in the Extant taxa carnivoran wrist and is one of the bones that make up the major joint of flexion and extension, with the radius being the other. The Canidae Canis lupus 6 Cursorial scapholunar also articulates with the magnum, unciform, trapezoid, Hyaenidae Crocuta crocuta 6 Cursorial and trapezium. Therefore, overall wrist mobility should be reflected in Hyaena hyaena 2 Cursorial its morphology. Salton and Sargis (2008) found that tenrecoids with Felidae Acinonyx jubatus 4 Cursorial arboreal habits had a larger trapezoid/trapezium and unciform, and Panthera leo 6 Grappler additionally that they had a larger articular surface of the radius. Puma concolor 6 Grappler/climber Yalden (1970) observed that the morphology of the scapholunar bone Extinct taxa was correlated with locomotor mode and habitat preference, for Canidae Canis dirus 5 example, he noticed that the distal end of a cheetah scapholunar Canis lupus 8 resembles that of canids and hyaenids—all cursors; but that the other Felidae Miracinonyx trumani 9 felids share affinities with mustelids and ursids—climbers and grap- Panthera atrox 7 plers. However, Yalden (1970) did not quantify these differences, nor Smilodon fatalis 5 did he examine any extinct species in his study. DUNN ET AL. 3 All data were collected from 3D-digital models generated with a between the articular facets for the trapezium and trapezoid is diffi- NextEngine 3D-Ultra HD-scanner, model 2020i following the cult to discern in felids, so we combined the
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