Journal of Vertebrate Paleontology 22(1):110121, March 2002 2002 by the Society of Vertebrate Paleontology

LOCOMOTOR EVOLUTION IN CAMELS REVISITED: A QUANTITATIVE ANALYSIS OF PEDAL ANATOMY AND THE ACQUISITION OF THE PACING GAIT
CHRISTINE M. JANIS, JESSICA M. THEODOR*, and BETHANY BOISVERT Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island 02912, ChristineJanis@Brown.edu

ABSTRACTExtant camelids (llamas and camels) are unique among wild mammals in their regular employment of a pacing gait. They also have a unique foot morphology, assumed to be an adaptation for this mode of locomotion: their feet are secondarily digitigrade, with the loss of hooves and the addition of a broad foot pad. We examined 22 measurements of the metapodials and phalanges of camelids and ruminants with bivariate and multivariate analyses, including 18 genera of extinct camelids from the Tertiary of North America. Extant camelids and ruminants were clearly distinguishable from each other. Most extinct camelids showed some morphological features typical of extant forms, ve out of eighteen clustered with the extant camelids. Pacing may have evolved independently within the subfamilies Camelinae and Protolabinae. Additionally, evolutionary change towards a condition resembling that of extant camelids also occurred within the subfamilies Stenomylinae and Miolabinae. These parallel changes in camelid locomotor anatomy occurred in the late Oligocene or early Miocene, preceding the formation of widespread open grassland habitats in the late Miocene.

INTRODUCTION Camelids, represented today by camels and llamas, are fascinating and little-studied animals. Camelids are artiodactyls, and they probably represent the extant sister-group to ruminants (Webb and Taylor, 1980), although some molecular studies would place them in a more basal position within the Artiodactyla (Gatesy et al., 1999; but see Norris, 1999). Camelids are unique among artiodactyls in their secondarily digitigrade foot posture, derived from an ancestral unguligrade condition, with a splay-toed foot and the typical ungulate hooves replaced by a broad foot pad. This foot morphology is characterized by metapodials that are splayed at their distal end (Fig. 1A), and also by the derived condition of the loss of the interdigital ligaments, allowing for the divergence of the third and fourth digits (Webb, 1972). Extant camelids are also distinguished from all other wild mammals by their mode of locomotion, employing a true pacing gait (i.e., a running pace, Hildebrand, 1976). The pace resembles the trot, in which pairs of fore and hind legs are moved together, with a period of suspension between the movement of each fore-/hindlimb pair during which all four feet are off the ground. However, in the trot, contralateral pairs of fore and hind legs are moved simultaneously (e.g., left fore with right hind), whereas the pace involves ipsilateral pairs of legs (e.g., left fore with left hind). The pace prevents the fore and hind leg on the same side from interfering with each other during fast locomotion, allowing a longer stride length, and hence a faster and more efcient mode of locomotion than the trot (Howell, 1944; Webb, 1972; Gauthier-Pilters and Dagg, 1981). Three distinct types of pace gait can be distinguished in extant Camelus: a slow pace, where the animal may be supported for four legs during some part of the locomotory cycle; a medium pace, where the animal is only ever supported by two legs; and a fast pace, where there are times during the cycle when no legs are on the ground (Gauthier-Pilters and Dagg, 1981). The
* Present address: Ilinois State Museum, Research and Collections Center, 1011 East Ash Street, Springeld, Illinois 62703. Present address: 265 Blackberry Hill Road, Berwick, Maine 03901.

fast pace is the one that would be termed a running pace by Hildebrand (1976). With the exception of some long-legged domestic dogs, and some breeds of domestic horses (e.g., standardbreds, used in harness races), camelids are the only mammals that use this type of pacing gait in place of a trot. Some long-legged mammals employ a slower, walking pace, also seen in camelids, in which there is no period of suspension. The walking pace, used by some long-legged ungulates (e.g., giraffe and gerenuk) and the cheetah, is actually a modied fast version of the regular lateral walk of mammals and is not the same as the running pace of camelids (Hildebrand, 1976). Many long-legged mammals, including camelids, giraffe, and cheetah, also employ a lateral rotary gallop (involving ipsilateral pairs of limbs being moved in sequence), instead of the transverse gallop (involving contralateral pairs of limbs) seen in most mammals. Thus, while camelids are not unique in their use of lateral gaits, they differ from other wild mammals in their use of the running pace. Webb (1972) provided an extensive discussion of the advantages and disadvantages of the pacing gait in camelids. A prime disadvantage is reduced lateral stability. Webb considered the development of the broad foot pad and splay-footed digitigrade stance to be adaptations to mitigate this instability, and listed other morphological features that would aid in increasing lateral stability. Camelids have a narrow chest with broad, at ribs. They also have enlarged the areas of attachment for the proximal limb abductors, whose action would prevent the body from collapsing towards the unsupported side. These areas include a relatively large scapular spine and acromion process in the shoulder girdle for attachment of the trapezius and deltoid muscles; a large deltopectoral crest on the humerus for the insertion of the deltoids; and a broadened greater trochanter of the femur for the insertion of the gluteals and vastus lateralis. To this list we add a laterally expanded ridge on the dorsal ilium for the origin of the tensor fascia latae, and transverse processes of the lumbar vertebrae that are more robust and more horizontal in position than in ruminants, for the attachment of the longissimus dorsi. To trace the evolution of the pacing gait in camelids, Webb (1972) used evidence from both limb morphology and a fossil-

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TABLE 1. Species Camelids 19 Camelus bactrianus 20 Camelus dromedarius 21 Lama glama 22 Lama guanicoe 23 Lama pacos 24 Vicugna vicugna Tragulids 25 Hyemoschus aquaticus 26 Tragulus javanicus Girafds 27 Giraffa camelopardalis 28 Okapia johnstoni Cervoids 29 Alces alces 30 Antilocapra americana 31 Axis porcinus 32 Capreolus capreolus 33 Cervus elaphus 34 Elaphurus davidianus 35 Mazama americana 36 Moschus moschiferus 37 Odocoileus virginianus 38 Rangifer tarandus Bovids 39 Boselaphus tragocamelus 40 Capra hircus 41 Cephalophus sylvicultor 42 Damaliscus pygarus 43 Gazella gazella 44 Kobus leche 45 Ourebia ourebi 46 Ovis aries 47 Rupicapra rupicapra 48 Saiga tatarica 49 Sylvicapra grimmia 50 Taurotragus oryx FIGURE 1. Right metatarsals of (A) a Pliocene camelid, Hemiauchenia vera, with fully modernized limb morphology (B) a ruminant artiodactyl, the Pleistocene reindeer Rangifer tarandus and (C) the late Miocene protoceratid Synthetoceras tricornatus (modied from Frick, 1937; Frick and Taylor, 1968; and Patton and Taylor, 1971). Specimens measured of extant artiodactyls. Specimen no. AMNH AMNH AMNH AMNH AMNH AMNH 14113 14107 35235 143242 6240 468742

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MCZ 6041 MCZ 3828 AMNH 70016 MCZ 38015 MCZ 1661 MCZ 1776 MCZ 1703 MCZ 29806 MCZ 36679 MCZ 8733 MCZ 49626 MCZ 6343 MCZ 59435 AMNH 5141 MCZ 6948 MCZ 42210 MCZ 58312 MCZ 5001 MCZ 54415 MCZ 56848 MCZ 5011 MCZ 50943 AMNH 24193 MCZ 5007 MCZ 5012 MCZ 1702

ized trackway attributed to the Miocene camelid genus Protolabis. He described features of the phalangeal anatomy of Protolabis and Michenia, noting changes in phalangeal proportions and articular surfaces that he considered to be correlated with the digitigrade stance typical of pacing camelids. A camelid phylogeny, in which Protolabis was placed as basal to later camelids, indicated the earliest evolution of the pacing gait. We seek to quantify the unique features of camelid limb anatomy, and to compare camelids analytically with ruminant artiodactyls to see if the two fall into statistically distinguishable groups. We also examine a broader range of fossil camelids to determine which taxa display morphology similar to that of extant camelids, which might be more like ruminants, and which represent intermediate states. By examining a larger diversity of taxa we can rene the estimation of the time at which camels may have rst adopted a pacing gait. Finally, the availability of a comprehensive cladogram of fossil camelids (Honey et al., 1998) enables us to plot these morphological changes on a phylogeny, and determine if these morphological changes evolved in parallel. MATERALS AND METHODS We made measurements on single individuals of all six species of extant camelids (Table 1), 26 species of extant ruminants (Table 1), and 18 taxa of extinct camelids from the Tertiary of

North America (Table 2) from the American Museum of Natural History, New York (AMNH) and the Museum of Comparative Zoology, Harvard University (MCZ). The fossil camelid data also came from single individuals, the availability of which formed the basis for our choice of taxa. The extant taxa selected depended primarily on the availability of the specimens that could provide the complete range of morphological measures in a single individual. However, we restricted our inclusion of bovid species to approximately equal numbers in comparison to the available cervoids, in order to avoid the possible phylogenetic bias that might occur if the majority of included species represented a single family. The bovid species were selected to represent a variety of body sizes and ecomorphological types. The fossil taxa are specimens from the Department of Vertebrate Paleontology and the Frick Collection at the AMNH, with the exception of Floridatragulus, which was from the MCZ. We also took measurements of the extinct Miocene protoceratid Synthetoceras tricornatus as representative of a more primitive artiodactyl limb morphology. We chose Synthetoceras for this comparison for reasons of taxonomic afliation, degree of morphological specialization, and body size. Synthetoceras serves here as a representative of a more generalized type of limb morphology than the cursorially-derived camelids and ruminants, not as an outgroup taxon for a phylogenetic analysis. Protoceratids are an extinct artiodactyl family, usually considered to be related to camels (Patton and Taylor, 1971; Webb and Taylor, 1980), but more recent workers have thrown some doubts on this afnity and suggested that they may in fact be basal ruminants (Joeckel and Stavas, 1996; Norris, 2000). Thus phylogenetically they could be considered as intermediate be-

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TABLE 2. Morphological characteristics of extinct camelids. Key: Mets: metatarsals. C cameline-like; L lamine-like; R ruminantlike; R/L; morphology in between that of ruminants and lamines; L/C morphology in between that of lamines and camelines. Note that Honey et al. (1998) considered Aepycamelus priscus (taxon 14) to belong to a separate genus from other species of Aepycamelus. Met. length length of metatarsals in comparison with extant artiodactyls. All specimen numbers refer to AMNH specimens unless otherwise noted. A # beside the specimen no. indicates a eld number. Taxon 1 Poebrotherium Stenomylinae 2 Pseudolabis 3 Miotylopus 4 Stenomylus (Not assigned to subfamily) 5 Floridatragulus 6 Gentilicamelus Miolabinae 7 Paramiolabis 8 Miolabis 9 Nothotylopus Protolabinae 10 Tanymykter 11 Michenia 12 Protolabis (Not assigned to subfamily) 13 Oxydactylus Camelinae 14 A. priscus Camelinae (Lamini) 15 Aepycamelus 16 Hemiauchenia Camelinae (Camelini) 17 Procamelus 18 Titanotylopus Specimen no. 6520 41942 36446 14226 MCZ 7784 7510 652-39# 24199 68554 36584 39628 400-2988# 17620 14188 9109 38179 75003 10703 Mets. fused? no partial fully mostly no partial partial no partial mostly mostly fully partial fully fully fully fully fully Mets. splayed? no slight slight slight/mod slight no slight slight no no/slight mod/fully fully no mod/fully fully fully fully fully Met. length long medium long long short medium medium medium medium medium long very long long long very long very long medium long PCA R R/L R/L R/L R R/L R/L R/L L L L L L C C C C C Ternary plot R R R R/L R/L R/L L R L/C R/L L L R R/L C L L L/C

tween camelids and ruminants. Protoceratids are derived cranially, and later forms (synthetoceratines) had characteristic sling-shot nasal horns. However, postcranially they retain primitive features such as short, unfused metapodials with incomplete distal metapodial keels. It might seem that a more basal taxon would be preferable to determine primitive artiodactyl limb anatomy, such as the Eocene Diacodexis, or an oreodont. However, the problem with both of these taxa is that they are small animals, and larger animals such as the camelids and ruminants under study might be expected to have differences in their limb anatomy simply because of their larger size, and further, they retains full-sized lateral digits, a primitive condition not found in any of the taxa in our analysis. Synthetoceras is of comparable size to the camelid and ruminant taxa compared in Figures 1 and 2 (body mass estimated at around 150 to 200 kg). Some suids are fairly large and retain a relatively primitive postcranial anatomy, and the same is also true for some extinct oreodonts. But these artiodactyls are more distantly related to camels and ruminants than protoceratids, and might be expected to have their own anatomical specializations, making them less appropriate for comparison. The following measurements were taken on all specimens, as allowed by preservation. Measurements were taken of the lengths (maximum articular length) and the diameter (at the midshaft, of both anteroposterior and mediolateral dimensions) of the tibia, metatarsal, and metacarpal, and of the length and diameters of the three hindfoot phalanges. Additional measurements were taken on articular surfaces of the phalanges. These included the extension onto the volar surface of the distal articular surface of the proximal and medial phalanges (Fig. 2.1 and 2.3) and the width and the depth of the carinal groove on the proximal articular surface of the proximal phalanx (Fig. 2.2). All measurements are listed in the appendix. In the fossil taxa we also noted whether or not the metapodials were fused, and if they had splayed distal ends, as in extant camelids (Table 2).

A principal components analysis was conducted using the 22 morphological variables described above. Two principal components were extracted using a Varimax rotation as implemented in StatView 5.0. Missing data points for Synthetoceras, Miotylopus, Paramiolabis and Floridatragulus were estimated using regression equations (Appendix), while Tragulus was excluded because of two missing data points. To visualize differences in foot posture and proportions we used a ternary diagram to examine the proportions of the phalanges, following the methods outlined by Gatesy and Middleton (1997:310). We made no attempt to collect data for all extant ruminant taxa, nor have we corrected our data for phylogenetic biases. RESULTS General Features of Extant Camelid Foot Morphology Figures 1 and 2 show some general differences in foot morphology between camelids, ruminants, and protoceratids. Metapodial Morphology The primitive condition is for relatively short metapodials. The primitive tragulid ruminant Hyemoschus has metatarsals that are approximately six times longer than their average mid-shaft width. Metapodials are longer in all extant ruminants and camelids, although certain montane bovids have secondarily shortened metapodials (Scott, 1985). Extant Rangifer and Lama (the llama) both have metatarsals that are about eleven times as long as their width. Note that metapodial length tends to scale with negative isometry (Bertram and Biewener, 1990), except in Giraffa (the giraffe) which has exceedingly long metapodials, with metatarsals around twenty times as long as their width. Other primitive character states, seen in both Hyemoschus and Synthetoceras, are as follows: small side toes (short, complete or partial digits 2 and 5) are present; metapodials 3 and 4 are unfused and not splayed at their distal ends; and the metapodials lack complete distal keels. Extant camelids and ruminants are both derived with respect to these conditions, but in different ways. Both have fused metapodials; all extant ca-

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FIGURE 2. Phalangeal morphology of (A) a camelid, (B) a ruminant and (C) a protoceratid. All phalanges are right pedal phalanges, all scale bars are 1 cm. Taxa are the same as Figure 1. (1) Anterior (volar) view of proximal phalanx. (2) Posterior (plantar) view of proximal phalanx. (3) Anterior view of medial phalanx. (4) Anterior view of ungual phalanx. (5) Lateral view of ungual phalanx.

melids and almost all fossil taxa retain only digits 3 and 4 (Honey et al., 1998), whereas small side toes may be retained in the Cervidae and Moschidae, but are lost in members of other extant ruminants. Ruminants are derived in possessing complete distal metapodial keels that act to lock the foot in the unguligrade position (Webb and Taylor, 1980; Janis and Scott, 1987). Camelids lack complete keels, but have the derived feature of distally splayed metapodials (Fig. 1; Webb, 1972). Proximal Phalanx Morphology Camelids have a relatively long proximal phalanx, with a length of about ve times that of the diameter. The relative length in ruminants is shorter, with a length around four times that of the diameter (Fig. 2.1). The condition in Synthetoceras resembles the ruminant one: thus, the camelid condition is likely derived. In camelids, the distal articular surface of the proximal phalanx is extended up onto the volar surface (Fig. 2.1). This extension is not found in ruminants or in Synthetoceras, so the camelid condition is likely the derived one. The extent of the distal articular surface (not gured) is also greater on the plantar side in camelids than in Synthetoceras, but in ruminants it actually appears to be less extended than in Synthetoceras. Thus, in this morphology both camelids and ruminants appear to be modied from the probable primitive condition. The camelid morphology would allow for a greater degree of extension of the medial phalanx on the proximal one in association with a digitigrade foot posture. In contrast, the restriction of the artic-

ular surface in ruminants would serve to limit mobility between the proximal and medial phalanges, perhaps in association with a more derived unguligrade foot posture. The carinal groove on the posterior border of the proximal articulation of the proximal phalanx in camelids is relatively wider and shallower than in ruminants and Synthetoceras (Fig. 2.2). Additionally, the proximal articular surface of camelids is relatively smooth, with little surface relief, and is broader in the mediolateral direction than in the anteroposterior one. Synthetoceras has a relatively deep carinal groove, and a squareshaped articular surface with higher relief. If Synthetoceras represents the more primitive condition, the derived camelid condition could be interpreted as reecting a less stabilized metapodial-phalangeal joint in conjunction with a digitigrade foot posture. The ruminant condition differs from the camelid one in the opposite direction from that of Synthetoceras. The articular surface is longer anteroposteriorly, the carinal groove is deepened, presumably in association with the complete metapodial keels, and the articular surface is deeper, allowing for more interlocking of the joint. Medial Phalanx Morphology The medial phalanx of camelids is relatively shorter in comparison to the width (about two and a half as long as it is wide) than in ruminants (about three times as long as wide; Fig. 2.3). However, the medial phalanx of Synthetoceras is also short, so this may represent the primitive condition. The distal articular surface has only a slight extension onto the volar surface in both camelids and Synthetoceras, whereas in ruminants this surface is extended (Fig. 2.3). The derived ruminant condition is presumably related to a greater extension of the ungual phalanx on the medial one with an unguligrade foot posture that is more highly stabilized than in Synthetoceras. The proximal articular surface of the medial phalanx (not gured) is longer in the mediolateral direction than in the anteroposterior direction in camelids, with little surface grooving. The articular surface is more square in shape and more deeply depressed in both Synthetoceras and ruminants, with extensive relief in the ruminant condition. The derived condition in camelids probably represents greater mobility between proximal and medial phalanges. Ungual Phalanx Morphology The ungual phalanx of camelids is relatively short and at, with a very shallow, relatively at articular surface. In ruminants, the phalanx is long, distally pointed, and high in relief, with extensive depressions on the articular surface (Fig. 2.4, 2.5). The morphology of the ungual phalanx in Synthetoceras is similar to the ruminant condition, but with less extensive relief on the articular surface. The differences between camelids and ruminants would again reect foot posture. The longer and deeper ungual phalanx of ruminants is encased within a hoof, and the deep relief on the articular surface reects greater restriction of interphalangeal mobility with an unguligrade foot posture. Relative Metapodial Lengths Figure 3 shows a plot of metatarsal length against the anteroposterior diameter of the metatarsal, including measurements for the long-legged, so-called giraffe antelope, the gerenuk, Litocranius walleri, and the dibatag, Ammodorcas clarkei, (taken from Scott, 1985). Metatarsal diameter was chosen as a proxy of body size, because the diameters of distal limb bones provide better estimates of body mass in artiodactyls than length measurements (Scott, 1990). Additionally, the mass of extant camelids can be estimated reliably from the correlations of limb diameters with body mass derived from ruminants (Scott, 1990). However, metatarsal diameter does not here provide a perfect proxy of size: for example, as shown in Figure 3, the metatarsal of Giraffa has a greater diameter than that of

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FIGURE 3. Bivariate plot of the length of the metatarsal against the anteroposterior diameter of the metatarsal. Key to symbols: Open triangles bovid ruminants; half-tone triangles cervids, moschid and antilocaprid ruminants; half-tone squares the giraffe antelope Litocranius (52) and Ammodorcas (53); black squares tragulid ruminants; black triangles girafd ruminants; open circles fossil camelids; half-tone circles extant lamines; black circles extant camelines; See Table 2 for key to numbers for extinct camelid taxa and Table 1 for extant taxa.

FIGURE 4. Principal components analysis of pedal morphological variables. Key as for Figure 3, except star Synthetoceras, and Litocranius and Ammodorcas are not included.

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the extinct camelid Titanotylopus, but other skeletal elements indicate that the latter is the larger taxon. In comparing extant forms, it can be observed that Giraffa is highly aberrant in its extremely long metatarsals, but the related Okapia (the okapi) clusters with the other ruminants. Additionally, note that camelids are relatively long-legged in comparison with most ruminants, especially at larger body sizes, although they do not fall completely outside of the range of extant ruminants. The two species of Camelus are long-legged in comparison with the majority of ruminants of a similar size (i.e., body mass of around 500 kg), but are of comparable proportions to the moose, Alces. Many of the extinct camelids are longer-legged than extant camels, with extremely long metapodials in comparison with any living ruminant except Giraffa. This is especially true in the size range corresponding to body masses of around 200 500 kg. These extinct camelids include not only those taxa traditionally considered as giraffe camels, such as Aepycamelus, but also the taxa Hemiauchenia and Protolabis. The smaller camels, mainly Eocene or Oligocene in age, cluster with the extant ruminants and lamines. The larger ones (extinct members of the tribe Camelini) have metatarsals of similar length to Camelus and Alces. Our data on Protolabis shows it to have relatively long metapodials, although Honey et al. (1998) claimed that the metapodials are not very long in this genus, only equal (or less than) in length to the basal length of the skull. However, Honey et al. (1998) also stated that the metapodials of Protolabis are relatively shorter in more derived species. Our specimen is a fairly early one, from the early Hemingfordian Running Water Formation, so perhaps this specimen is primitive in its long metatarsals. Figure 3 also illustrates possible differences in scaling exponents of the metatarsals between camelids and ruminants. Scott (1985) noted a breakpoint in the scaling of metatarsal lengths in extant bovids: metatarsal length scales allometrically below a body size of around 200 kg, but at greater mass there is little increase in absolute metatarsal length. This breakpoint in limb length scaling has been attributed to the physical demands of support at larger body size (Bertram and Biewener, 1990). Note that in Figure 3 the breakpoint occurs at a metatarsal width of about 2.8 cm; ruminants with metapodials of this size are Elaphurus davidianus and Cervus elaphus, which both have body masses of around 200 kg. The members of the tribe Camelini (Camelus, Procamelus, and Titanotylopus) appear to obey the same scaling laws that apply to the majority of ruminants. Their metatarsals are around the same absolute length as smaller taxa such as Protolabis. However, metatarsal length in other large extinct taxa, principally the members of the tribe Lamini, Aepycamelus and Hemiauchenia, have metatarsal lengths that appear to fall along a continuation of the scaling exponent that applies to the smaller artiodactyls, as does Giraffa. Why the giraffe and some larger camelids should be exempt from the scaling rules that appear to affect ruminants and members of the tribe Camelini is not clear. Additionally, preliminary data suggest that, unlike any ruminant or camelid, Giraffa is unique in having a metatarsal that is longer than the tibia. Principal Components Analysis Figure 4 shows the results of the principal component analysis using the dimensions described in the Materials and Methods section. The rst principal component (PC1) accounts for 78.5% of the variance. The loadings on PC1 are all positive, and almost all are close to unity (Table 3). Thus this axis clearly discriminates taxa based on body size. Some shape inuence is involved, as seen in the slightly lower loading for the length of

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TABLE 3. Factor loadings for variables used in the principal components analysis. Factor loading Variable Tibia length Tibia diameter, mediolateral Tibia diameter, anteroposterior Metatarsal length Metatarsal diameter, mediolateral Metatarsal diameter, anteroposterior Metacarpal length Metacarpal diameter, mediolateral Metacarpal diameter, anteroposterior Proximal phalanx length Proximal phalanx diameter, mediolateral Proximal phalanx diameter, anteroposterior Proximal phalanx distal articular extension Proximal phalanx carinal groove depth Proximal phalanx carinal groove width Medial phalanx length Medial phalanx diameter, mediolateral Medial phalanx diameter, anteroposterior Medial phalanx distal articular extension Ungual phalanx length Ungual phalanx diameter, mediolateral Ungual phalanx diameter, anteroposterior Factor 1 0.931 0.967 0.950 0.900 0.950 0.954 0.872 0.940 0.957 0.905 0.957 0.973 0.746 0.732 0.882 0.906 0.949 0.904 0.802 0.547 0.879 0.765 Factor 2 0.196 0.146 0.044 0.202 0.142 0.019 0.300 0.181 0.128 0.344 0.123 0.093 0.418 0.309 0.334 0.016 0.027 0.362 0.479 0.737 0.155 0.581

the ungual phalanx (Table 3), which is the variable that separates Giraffa from the other taxa on this axis. This results in Giraffa scoring more positively on this axis than the much larger extinct camelid Titanotylopus. When Giraffa is removed from the analysis, the loading of the ungual phalanx length variable on PC1 is similar to the other variables, and the other taxa are more evenly spread out along PC1 in accordance with their body masses. The second principal component explains 9.3% of the variance. This axis clearly separates the camelids (negative loadings) from the ruminants (positive loadings). Giraffa has near zero loadings on PC2, similar to the tragulids, while Okapia clusters with the other ruminants. PC2 also contains a size component, in that larger ruminants (except Giraffa ) have higher positive loadings, and larger camelids have higher negative loadings. This may reect greater locomotor specializations in larger taxa, or somehow reect a size component in PC2. Variables with high positive values on PC2 (i.e., ruminant features) are as follows: the length and anteroposterior diameter of the ungual phalanx, the anteroposterior diameter of the medial phalanx, the length of the volar extension of the distal articular surface on the medial phalanx, and the depth of the carinal groove on the proximal phalanx. As previously discussed, these articular features reect the limitation of interphalangeal mobility, and the large ungual phalanx reects its enclosure within a hoof. Variables with high negative values (i.e., camelid features) are as follows: the length of the volar extension of the distal articular surface on the proximal phalanx, the length of the proximal phalanx, the width of the carinal groove on the proximal phalanx, and the length of the metacarpal. These articular features reect increased interphalangeal mobility. The length of the proximal phalanx may be related to a general elongation of the limb proximal to the foot pad. Thus PC2 appears to be primarily an axis of digitigrady (negative loadings) versus unguligrady (positive loadings). The length of the metacarpal (high negative values on PC2) reects the fact that all living and extinct camelids have fore- and hind limbs of approximately equal length. In ruminants, equally-proportioned forelimbs and hind limbs are seen only in animals living in more open habitats, that make habitual use of the trot

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gait, instead of using the bound or gallop for speeds faster than a walk (Scott, 1985). In contrast, animals living in closed habitats have forelimbs that are shorter than the hind limbs (Scott, 1985). Among the fossil camelids, Poebrotherium and Floridatragulus fall fairly close to the ruminants, although with slightly less positive scores. Stenomylus, Gentilicamelus, Miolabis, Miotylopus, Paramiolabis, and Pseudolabis fall in the morphospace between ruminants and lamines. Michenia, Oxydactylus, Nothotylopus, Protolabis, and Tanymykter cluster with extant lamines. Aepycamelus, Aepycamelus priscus, Hemiauchenia, Procamelus, and Titanotylopus cluster with extant camelines (Table 2). The third principal component (not shown) explains 3.4% of the variance. This component appears to be a giraffe axis, separating Giraffa from the other taxa. The variables with high loadings on PC3 are long metapodials, a short ungual phalanx, a short extension to the distal articular surface on the proximal phalanx, and a wide and deep carinal groove on the proximal phalanx. The separation of the giraffe from other taxa appears to be a result of its similarity to extant camelids in limb length, but with an unguligrade foot posture and the anomalous condition (for unguligrady) of a short ungual phalanx. Ternary Diagram The ternary diagram of phalangeal lengths clearly separates out all extant camelids from all ruminants (with the exception of Giraffa, which here out-camels Camelus!; Fig. 5). Camelids score higher on length of the proximal phalanx and lower on the other two axes (lengths of medial and ungual phalanges, respectively) than ruminants. As with the PCA, Okapia clusters with other ruminants, towards the high end of the ruminant range, while Hyemoschus falls within the low end of the ruminant range, as do Moschus and Saiga in this analysis. Synthetoceras clusters within the ruminants. Again, as with the PCA, the extant camelines fall further from the ruminants than do the extant lamines. In this analysis, the following fossil taxa cluster with the ruminants: Miolabis, Miotylopus, Oxydactylus, Poebrotherium, and Pseudolabis (although Miotylopus and Oxydactylus are situated at the edge of the ruminant morphospace). The following taxa fall in the morphospace between ruminants and lamines: Aepycamelus priscus, Floridatragulus, Gentilicamelus, Stenomylus, and Tanymykter. Finally, Hemiauchenia, Michenia, Nothotylopus, Paramiolabis, Procamelus, and Protolabis cluster with lamines, and Aepycamelus clusters with camelines (Table 2). As in the PCA (Fig. 4), Titanotylopus again is more derived along the camelid trend in morphospace than any extant form, here falling close to the giraffe. DISCUSSION Figure 6 illustrates the only comprehensive phylogeny of camelids, and additionally shows the chronological range of these taxa (both from Honey et al., 1998). The fossil taxa have been identied in terms of varying degrees of foot posture that resembles the condition in extant camelids (see also Table 2). The most primitive camelid, Poebrotherium, shows no evidence of limb features like those of extant camelids, clustering with the ruminants in every analysis. Note that while it tends to fall close to less derived ruminants such as the tragulids on the PCA and the ternary plot, its metatarsals are relatively long, even in comparison with similar-sized ruminants (Fig. 3). Thus, if Poebrotherium can be taken as the primitive camelid condition, we can see that the original camelid morphological design was for moderately long legs with an unguligrade limb posture. But primitive camelids lack the additional cursorial limb specializations (fused metapodials, complete distal metapodial

FIGURE 5. (A) Ternary plot of phalangeal lengths. (B) Close up of ternary plot. Key as for Figure 4.

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FIGURE 6. Phylogeny of camelids (modied from Honey et al., 1998; only taxa considered in this paper shown). The rectangles show chronological ranges of taxa. Key: Unshaded (white) rectangle, no foot morphological adaptations towards extant camelid condition; lightly-shaded rectangles, some modications towards foot morphology like extant camelids; heavily shaded rectangles, numerous morphological features like that of extant camelids, but not with full suite of morphological adaptations; and black rectangles, foot morphology unequivocally like that of extant camelids.

keels) of extant ruminants, although these features are also absent in the ruminants contemporaneous with Poebrotherium, such as Hypertragulus and Leptomeryx (Webb and Taylor, 1980). All other camelids show some evidence of the acquisition of a derived limb morphology, more like that of extant camelids, although in some taxa this is relatively slight. For example, Floridatragulus is unlike most camelids in having relatively short metapodials (Fig. 3), and clusters with ruminants on the PCA (Fig. 4), but falls in the morphospace between ruminants and lamines on the ternary plot (Fig. 5; Table 2). On the other end of the scale, the more derived camelids that are included within extant phylogenetic bracket in the Camelinae (Aepycamelus, Hemiauchenia, Procamelus and Titanotylopus ) are indistinguishable in pedal morphology from living taxa. It can be inferred with condence that these taxa possessed the pacing behavior of extant camelids. Pacing was also probably the locomotor mode for the more primitive cameline Aepycamelus priscus. This animal differs in its morphology from extant camelids only by a slight displacement on the ternary plot towards somewhat longer medial and ungual phalanges, although its metapodials are also somewhat less distally splayed than the more derived camelids. However, a suite of characteristics identical to that of extant camelids is seen in the protolabine Protolabis, which has also evolved elongated metatarsals convergently with some of the

xn more derived camelids. Independent evidence for pacing in Protolabis exists in the form of a fossilized trackway (Webb, 1972). If the phylogeny of Honey et al. (1998) is correct, this would imply that pacing behavior evolved twice within camelids. In this phylogeny the genus Oxydactylus, which does not show extensive modications towards a condition like that of extant camelids, is placed as the sister-taxon to the Camelinae. If this phylogenetic position of Oxydactylus is incorrect, more extensive modications towards extant camelid limb anatomy might be a shared derived feature of the Protolabinae and the Camelinae. However, other protolabines (Tanymykter and Michenia ) are less like extant camelids in their limb anatomy than Protolabis, implying convergence on camelines within the protolabine lineage whatever the phylogenetic position of Oxydactylus. Of equal interest is the fact that some convergence on extant camelid morphology, although not attaining the fully derived condition, is seen within two other camelid lineages. This trend is seen both within the Stenomylinae (attaining the most derived condition in Stenomylus) and the Miolabinae (attaining the most derived condition in Nothotylopus). Note that the taxon that we here refer to as Nothotylopus may actually represent the taxon sometimes called Homocamelus, that Honey et al. (1998) refer to as Miolabine sp. Both are derived members of the Miolabinae, so in fact the precise identication of this specimen is not important. As there is no modern analog for this type of

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serves for the origin of an enlarged tensor fascia latae to aid in lateral stability, although the giraffe lacks the camelid feature in the scapula of a relatively large scapular spine and acromion process. This morphology of the ilium is not simply related to large size, because it is absent in other large ruminants such as Alces and Bison. The giraffe also resembles extant camelids in having a relatively narrow chest, but lacks the camelid-like broad, attened ribs. The giraffe is unique among all ruminants and camelids, including the extinct giraffe camels with highly elongated limbs, in having metapodials that are longer than the tibia. Additionally, there appears to be a peculiar morphology of the pedal sesamoid bones observed on mounted specimens in the Harvard Museum of Zoology. In ruminants (e.g., Bison), the distal sesamoids have their major articulation with the base of the medial phalanx. In contrast, Giraffa has relatively larger distal sesamoids that appear to have a greater articulation with the ungual phalanx, possibly acting as a posterior extension for the effective plantar surface of the ungual phalanx. CONCLUSIONS The peculiar foot morphology of present-day camelids, indicative of a secondarily digitigrade foot posture in association with a pacing mode of locomotion, may have evolved more than once within the lineage. The fully modern version of this morphology is seen not only in the extinct taxa closely related to the living camels and llamas, but also within the Protolabinae, the sister taxon to the Camelinae, where it may represent independent evolution. Fossilized trackways also support the hypothesis that the derived protolabine Protolabis had a running pace gait like that of extant camelids (Webb, 1972). Partial convergence on the foot morphology of extant camelids was also seen within the more primitive families Stenomylinae (primarily in the genus Stenomylus) and the Miolabinae (primarily in the genus Nothotylopus). However, some deviation from the more primitive condition (as exemplied by the extinct protoceratid Synthetoceras, or in extant tragulid ruminants) could be observed in all camelids studied with the exception of the most primitive taxon, Poebrotherium. We consider that most extinct camelids may have engaged in some types of lateral gaits, such as the lateral walk and the rotary gallop, observed in extant long-legged antelope and the giraffe. However, the running pace gait, unique to camelids among extant wild mammals, was probably used only by those taxa with a foot fully like that of extant camelids. The parallel emergence of more derived types of foot morphology among fossil camelids occurred in the late Oligocene to early Miocene times, preceding the development of more open savanna habitats in the North American late Miocene. ACKNOWLEDGMENTS We thank the following people for access to specimens in their collections. Maria Rutzmoser (Mammalogy) and Chuck Schaff (Vertebrate Paleontology) at the Museum of Comparative Zoology (Harvard University), and Dick Tedford (Vertebrate Paleontology) and Chris Norris (Mammalogy) at the American Museum of Natural History (New York). Thanks also to Dave Webb for discussions, Kay Earls for checking specimens on display, Brian Regal for the osteological drawings, Ian Tattersall for accommodations, and Mark Norell for being understanding of various problems. This project was funded in part by a Salomon Faculty Award (Brown University) to CMJ, and by Brown University undergraduate honors thesis funds to BB.

intermediate morphology, without associated trackways it is impossible to determine what the actual gait of these animals might have been. Stenomylus and Nothotylopus both lack the splaying of the distal ends of the metapodials seen in more derived camelids, and thus it seems unlikely that they had a digitigrade foot posture. Yet, on both the PCA and ternary plots, Stenomylus falls in the morphospace between the ruminants and lamines and Nothotylopus clusters with the lamines, indicative of changes in relative proportions of the foot bones in both taxa. Nothotylopus is more derived in its pedal anatomy than Stenomylus, but Stenomylus is more derived than the other stenomylines, Pseudolabis and Miotylopus. We also note that Stenomylus possesses other skeletal features like those of extant camelids that may be indicative of lateral stabilization, such as broad, at ribs and an expanded iliac crest. We were unable to determine the condition of these features in Nothotylopus. In contrast, the primitive camelid Poebrotherium, which possesses a ruminant-like foot morphology, shows little evidence of features promoting lateral stability. Poebrotherium lacks an expanded iliac crest, and has only a slight broadening of the anteriormost ribs (nos. 17, as seen on the mounted specimen in the American Museum of Natural History; Scott, 1940:630635). Perhaps these camelids of intermediate morphology used some types of lateral gaits (for example, the slow pace or lateral walk and the rotary gallop, as employed by present-day long-legged ruminants), but did not have the running pace gait of extant camelids. When Webb (1972) considered the evolution of pacing locomotion in camelids, he noted that the pacing trackways of Protolabis were middle Miocene (Barstovian) in age, and correlated the locomotor shift with the spread of open grassland habitats in North America. He pointed out that, in extant camelids, the pacing gait is adapted for long distance travel in open terrain, and interpreted the fossil record as supportive of the hypothesis that pacing rst evolved along with the open habitat grasslands. Figure 6 shows the chronological ranges of camelid taxa along with their phylogeny, and it is apparent that the trend towards a more derived morphology resembling that of extant camelids occurred at an earlier date than proposed by Webb. Consider those taxa where partial modications are attained. Stenomylus (Stenomylinae) rst appeared in the late Oligocene, and Nothotylopus (Miolabinae) and Tanymykter and Michenia (Protolabinae) in the early Miocene. Furthermore, some taxa possessing modications fully like those of extant camelids, Protolabis (Protolabinae) and Aepycamelus (Camelinae) also rst appeared in the early Miocene. Thus, both taxa with adaptations indicating a fully-derived pacing gait, and those with some sort of modications leading towards this gait, made their appearance before the spread of open savanna or grasslands (Jacobs et al., 1999). The signicance of this observation is unclear. One possible explanation is that more open habitats were present earlier in North America than previously considered, as also suggested by other workers (Webb, 1977; Janis, 1982; Leopold et al., 1992), although such habitats were not dominated by grass until later in the Miocene. Another interesting feature of this study is the observation of how different Giraffa is from other extant ruminants. We document here the convergences with camelids in certain aspects of foot morphology; but the giraffe also has other peculiar aspects of postcranial morphology, some convergent with the extant camelid condition and some unique. The description of giraffe morphology below is based on general osteological observations rather than on quantitative analysis, but nevertheless serves to highlight features that are deserving of further study. The giraffe resembles extant camelids in having an elongated and laterally projecting iliac crest, which presumably also

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APPENDIX

Data used in statistical analyses, all measurements in cm. Key: L articular length; ML mediolateral diameter; AP anteroposterior diameter; Ext distal articular extension; GW width of carinal groove; GD depth of carinal groove; *estimated by regression. Taxa designated by numbers used in Tables 1 and 2. Data for 51, Synthetoceras, from AMNH 40231, 40241, 40243, and 40245. Tibia Taxon 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 Poebrotherium Pseudolabis Miotylopus Stenomylus Floridatragulus Gentilicamelus Paramiolabis Miolabis Nothotylopus Tanymykter Michenia Protolabis Oxydactylus Aepycamelus priscus Aepycamelus Hemiauchenia Procamelus Titanotylopus Camelus bactrianus Camelus dromedarius Llama glama Llama guanicoe Llama pacos Vicugna vicugna Hyemoschus aquaticus Tragulus javanicus Okapia johnstoni Giraffa camelopardalis Alces alces Antilocapra americana Axis porcinus Capreolus capreolus Cervus elaphus Elaphurus davidianus Mazama americana Moschus moschiferus Odocoileus virginianus Rangifer tarandus Boselaphus tragocamelus Capra hircus Cephalophus silvicultor Damaliscus pygarus Gazella gazella Kobus leche Ourebia ourebi Ovis aries Rupicapra rupicapra Saiga tatarica Sylvicapra grimmia Taurotragus oryx Synthetoceras L 22.47 30.23 28.82 21.85 *19.59 26.40 *24.07 27.93 37.85 36.93 31.77 44.65 38.50 52.30 36.50 48.10 44.50 50.36 47.94 43.59 30.16 33.45 29.05 25.39 12.36 10.07 33.60 61.90 46.99 26.95 19.42 23.69 45.72 36.83 19.96 19.97 31.52 36.94 37.50 21.74 25.38 27.69 22.20 31.59 20.82 20.17 26.84 22.43 17.43 39.70 *22.34 ML 1.95 2.32 2.11 1.69 *2.92 2.16 *2.04 2.57 3.23 3.03 2.64 3.45 2.65 4.35 3.25 3.90 4.62 5.53 5.46 5.01 3.16 2.94 2.82 2.66 1.31 0.73 3.83 6.56 4.37 2.17 1.23 1.77 4.82 3.76 1.62 1.22 2.37 3.19 3.96 1.86 2.66 2.15 1.71 2.65 1.54 2.05 1.59 1.89 1.82 4.35 *2.10 AP 1.41 2.58 2.75 1.81 *2.07 2.49 *1.98 2.59 3.85 3.12 2.60 3.18 2.64 3.18 3.22 3.43 3.92 5.11 4.47 4.27 2.76 2.96 2.59 2.49 1.67 0.87 3.50 5.77 4.89 2.77 1.78 1.91 5.48 3.51 1.80 1.12 2.59 3.36 4.36 2.04 3.46 2.12 1.83 3.04 1.78 2.10 1.68 2.01 1.50 4.41 *2.59 L 15.50 22.19 23.87 16.68 12.98 18.83 17.12 17.25 26.75 27.56 27.20 36.79 28.47 45.90 35.46 40.79 34.50 38.05 35.92 34.60 21.03 22.99 20.34 18.56 5.99 6.71 29.19 67.61 36.83 22.61 13.36 19.32 34.93 28.26 12.33 13.41 27.34 29.55 26.89 12.21 16.80 22.26 17.70 23.04 15.46 12.54 16.55 18.44 14.42 28.70 *15.39 Metatarsal ML 1.82 2.09 1.37 1.21 2.08 1.71 1.46 2.23 2.45 2.10 1.80 2.22 2.01 3.15 2.78 2.54 3.15 4.00 3.92 3.19 1.81 1.72 1.83 1.89 1.45 0.58 2.99 4.40 3.30 1.49 1.17 1.23 3.17 2.57 1.08 0.84 1.85 2.39 2.74 1.37 1.89 1.38 1.15 1.95 1.14 1.46 1.28 1.13 0.95 2.71 *1.51 AP 0.99 1.97 1.94 1.17 1.17 1.47 1.39 1.70 2.40 2.69 2.00 2.95 2.17 3.29 2.83 2.86 4.61 4.22 3.55 3.23 1.78 2.08 1.67 1.54 0.67 0.62 3.14 4.80 4.09 1.90 1.41 1.53 4.31 2.69 0.91 0.95 2.35 3.43 3.11 1.32 2.09 1.85 1.52 2.14 1.36 1.47 1.25 1.85 1.09 3.18 *1.63 L 13.07 22.28 *22.71 16.27 11.09 18.02 17.23 16.74 24.66 27.15 28.22 36.94 28.12 45.30 36.85 44.25 35.80 41.48 35.35 34.68 21.50 23.40 20.30 18.39 3.96 4.45 28.59 69.16 32.27 21.49 10.79 15.95 30.48 25.36 15.08 9.86 21.29 22.30 26.51 11.24 15.36 21.26 16.44 22.39 15.31 11.77 14.94 15.91 13.15 26.02 13.57 Metacarpal ML 1.49 2.27 *1.50 1.20 *2.31 1.98 1.42 2.71 2.91 2.48 1.89 2.40 2.57 3.22 3.26 2.55 3.87 4.72 4.48 3.69 1.98 2.14 1.98 2.19 1.39 0.55 3.15 5.00 3.54 1.62 1.22 1.82 3.49 2.76 1.21 0.96 1.95 2.43 3.10 1.64 2.05 1.55 1.27 2.03 1.09 1.71 1.48 1.38 0.86 3.02 1.64 AP 0.90 1.78 *1.75 1.07 1.01 1.53 1.38 1.76 2.32 2.36 2.11 2.86 2.01 3.37 3.18 2.94 4.00 4.35 3.72 3.09 1.76 2.22 1.65 1.50 0.38 0.33 3.46 4.80 3.30 1.59 1.10 1.19 3.72 2.34 1.25 0.74 1.88 2.40 2.52 1.09 1.51 1.42 1.10 1.65 0.99 1.31 1.06 1.36 0.83 3.72 1.39

JANIS ET AL.LOCOMOTOR EVOLUTION IN CAMELS

APPENDIX Proximal phalanx Taxon 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 L 2.84 4.35 3.58 3.72 4.31 4.38 4.57 4.60 7.10 5.70 6.99 7.73 5.35 8.12 9.69 10.22 9.99 12.67 10.56 10.09 6.96 7.95 6.52 6.06 2.04 1.44 6.62 12.96 8.30 5.28 3.45 3.92 7.44 6.72 3.03 4.15 5.23 6.63 7.11 3.83 4.47 5.46 4.52 5.74 3.21 3.74 4.59 4.89 3.07 6.51 5.37 ML 0.71 0.97 0.96 0.68 0.93 1.03 0.77 1.24 1.54 1.32 0.92 1.31 1.05 1.70 1.77 1.71 1.95 2.38 2.40 2.14 1.23 1.45 1.10 1.06 0.85 0.41 2.32 3.57 2.51 0.95 0.75 0.78 2.29 2.06 0.81 0.63 1.33 1.60 2.31 1.10 1.76 0.98 0.89 1.37 0.83 1.23 1.09 0.92 0.63 2.17 1.67 AP 0.86 1.28 0.95 0.90 1.07 1.07 1.01 1.28 1.73 1.37 1.51 1.61 1.14 1.87 2.32 2.04 2.52 3.21 2.77 2.44 1.49 1.60 1.25 1.29 0.73 0.41 2.50 3.73 2.90 1.53 1.23 1.07 2.80 2.42 1.05 0.90 1.60 1.86 2.90 1.08 1.64 1.27 1.05 1.65 1.00 1.17 1.15 1.18 0.85 2.68 1.43 Ext 0.35 0.48 0.35 0.50 0.50 0.40 0.55 0.50 1.17 0.51 0.87 0.74 0.48 1.31 1.54 1.22 1.91 2.17 2.21 1.94 1.04 1.25 0.96 1.03 0.20 0.05 0.54 1.00 1.46 0.36 0.71 0.34 0.95 0.98 0.35 0.36 0.73 0.78 0.87 0.66 0.74 0.49 0.58 0.55 0.21 0.57 0.53 0.45 0.47 0.83 0.49 GW 0.22 0.32 0.38 0.29 0.37 0.34 0.37 0.49 0.63 0.47 0.59 0.65 0.45 0.87 0.83 0.74 0.85 0.97 1.02 0.82 0.67 0.67 0.58 0.48 0.34 0.56 1.55 0.69 0.19 0.13 0.31 0.65 0.68 0.17 0.44 0.49 0.65 0.59 0.30 0.20 0.31 0.18 0.27 0.21 0.34 0.32 0.25 0.22 0.51 0.31 GD 0.25 0.30 0.34 0.25 0.37 0.26 0.42 0.30 0.48 0.33 0.36 0.42 0.33 0.40 0.46 0.44 0.37 0.31 0.45 0.39 0.39 0.31 0.31 0.27 0.24 0.43 0.85 0.55 0.21 0.20 0.27 0.49 0.65 0.15 0.38 0.46 0.43 0.48 0.45 0.33 0.38 0.25 0.43 0.18 0.24 0.48 0.31 0.29 0.73 0.40 L 1.57 2.21 1.80 2.19 2.21 2.12 2.10 2.37 3.80 3.21 3.23 3.71 2.37 4.66 4.37 3.96 4.77 6.47 6.17 5.98 3.46 3.84 3.01 2.92 1.48 0.96 3.89 6.44 6.18 2.99 2.62 2.67 5.44 5.73 2.29 2.98 4.31 4.61 4.80 2.61 2.99 3.01 2.35 3.74 2.12 2.43 3.31 2.45 2.06 4.12 0.32 (Continued) Medial phalanx ML 0.66 1.01 0.85 0.67 0.98 0.87 0.85 1.06 1.59 1.12 1.05 1.18 1.13 1.78 1.82 1.83 2.01 2.52 2.64 2.81 1.37 1.56 1.50 1.14 0.75 0.31 2.08 3.78 2.17 1.01 0.91 0.84 2.12 1.81 0.81 0.60 1.32 1.59 2.25 1.00 1.27 1.03 0.72 1.41 0.64 1.05 0.84 0.82 0.67 2.14 1.97 AP 0.69 1.05 0.71 0.68 0.98 0.87 0.77 1.10 1.16 1.07 1.05 1.06 0.86 1.58 1.55 1.55 1.70 2.19 1.86 1.58 1.07 1.18 1.09 1.30 0.55 0.38 2.19 3.68 3.19 1.26 1.08 1.05 2.59 2.30 0.94 0.78 1.61 1.74 2.57 0.99 1.48 1.22 0.73 1.45 0.80 1.07 0.97 0.93 0.79 2.54 1.55 Ext 0.51 0.86 0.59 0.56 0.59 0.62 0.50 0.84 0.84 0.92 0.76 0.86 0.67 1.23 1.08 0.99 0.91 1.17 1.22 1.17 0.93 1.00 0.84 0.94 0.40 0.11 1.84 3.62 2.88 1.14 0.93 0.83 2.42 1.62 0.66 0.60 1.26 1.85 1.99 1.06 1.06 1.13 0.78 1.36 0.76 0.94 1.16 0.90 0.67 1.86 0.69 L 1.69 2.61 1.84 1.48 1.88 1.78 1.40 2.76 2.12 2.53 1.98 2.50 2.59 3.02 2.57 2.69 2.78 2.65 2.96 2.57 2.28 2.17 2.44 2.00 1.22 1.00 6.13 2.99 8.11 3.37 2.63 2.72 6.55 5.48 2.06 2.01 3.56 5.35 6.02 3.29 3.04 3.67 2.91 5.03 2.54 2.71 3.73 2.45 2.07 7.77 0.39 Ungual phalanx ML 0.48 0.70 0.67 0.64 0.71 0.72 0.58 0.93 1.18 0.91 0.81 0.98 0.87 1.44 1.45 1.24 1.65 1.68 2.24 1.90 1.07 1.24 1.19 1.05 0.59 0.26 1.81 1.90 2.24 0.66 0.77 0.66 2.06 2.05 0.66 0.55 1.05 1.97 1.68 0.50 0.81 0.78 0.64 1.11 0.55 0.70 0.72 0.59 0.64 1.68 1.98

121

AP 0.62 1.12 0.91 0.55 0.94 0.79 0.75 1.08 1.10 1.22 1.08 1.13 1.15 1.79 1.54 1.40 1.77 1.74 1.66 1.50 1.24 1.23 1.29 1.02 0.50 0.32 3.02 2.50 3.51 1.51 1.17 1.09 2.79 2.27 0.98 0.88 1.53 2.31 2.74 1.54 1.23 1.58 1.12 1.65 0.88 1.30 1.35 1.12 0.82 2.99 2.33