The Clavicles of Smilodon fatalis and Panthera atrox(Mammalia: Felidae) from Rancho La Brea,Los Angeles, California

Adam Hartstone-Rose,1* Ryan C. Long,2 Aisling B. Farrell,2 and Christopher A. Shaw2

1Department of Biology, Penn State University Altoona, 1600 Ivyside Park, Altoona PA 166012Research and Collections, George C. Page Museum, 5801 Wilshire Boulevard, Los Angeles, CA 90036

ABSTRACT The Rancho La Brea collections at theGeorge C. Page Museum in Los Angeles, California, con-tain the largest single inventory of Smilodon fatalisremains representing virtually every bone in the skele-ton. Eighteen clavicles of two distinctive shapes havebeen recovered from historical and recent excavations atRancho La Brea. In this study, we identify these speci-mens to species through comparison of their morphologyand morphological variability with clavicles found inmodern felids. This study includes a reevaluation ofclavicles that have been previously assigned to S. fatalis,which are more likely to be those of Panthera atrox, andthe description of pantherine cat clavicles. A previouslyundescribed sample of clavicles not only includes someof the same pantherine morph but also 10 specimens,herein assigned to S. fatalis, which are morphologicallydistinctive and significantly smaller than the previouslydescribed specimens. In addition, we report unexpectedvariations between clavicles of Panthera leo and P.tigris: the clavicles of P. leo closely resemble those of thelarge Rancho La Brea clavicle morph—which presum-ably belongs to P. atrox—thus supporting a P. leo/P. atrox clade. We report distinctive morphology of theclavicles of Acinonyx jubatus. Possible functional andphylogenic significance of felid clavicles is suggested.J. Morphol. 273:981–991, 2012. � 2012Wiley Periodicals, Inc.

KEY WORDS: Smilodon fatalis; Panthera atrox;Felidae; clavicle; functional morphology; pectoral girdle

INTRODUCTION

Clavicles are reduced or absent in most mem-bers of the order Carnivora. In no carnivoran spe-cies do the clavicles come in contact with the acro-mion process or the manubrium. When present (asin felids), the bone is imbedded in the muscles ofthe shoulder, connected by fibrous tissue to thescapula and to the sternum by a ligamentous band(Field and Taylor, 1950; Evans, 1993; Cerny andCizinauskas, 1995). Extant felid species retain thebone (deep to and the dividing border of the clavo-trapezius and clavodeltoideus mm.), whereas manyadult caniforms have lost the bone altogether(Cerny and Cizinauskas, 1995). Adaptive advan-tages to reduction or loss of the clavicles mayinclude freeing the shoulder movement to increasestride, linear (rather than arcuate) excursion of

the shoulder joint, and restriction of pectoral limbmovements to the sagittal plane for increased cur-soriality (Jenkins, 1974; Cerny and Cizinauskas,1995). Greater absorption of impact from running/landing by pectoral limb muscles might also befacilitated by clavicle reduction.

Machairodontinae cats are the sister subfamilyto the Felinae cats, and thus, it is likely that theyalso retained the clavicle. Furthermore, Smilodonfatalis is thought to be an ambush predator, andbehavioral and biomechanical aspects of its preycapture and killing behaviors deduced by skeletalmorphology (Spoor, 1985; Spoor and Badoux, 1986;Anyonge, 1996; Meachen-Samuels and Van Val-kenburgh, 2010) indicate less cursorial limb useand more dependence on pectoral limbs for captur-ing and killing. Therefore, they likely retainedtheir clavicles unless there was great selectivepressure on ancestral machairodonts toward cur-soriality or another type of pectoral girdle remodel-ing took place. However, the felid clavicle is oftenoverlooked—even in the curation of modern skele-tons in the great museums of the world—and veryfew collections of machairodonts are completeenough to expect to find this vestigial bone.

One exception to this is the remarkably detailedfossil sample from the asphalt deposits at RanchoLa Brea—considered by many to be the richestsource of late Pleistocene terrestrial fossils known(e.g., Akersten et al., 1983; Shaw and Quinn,1986), and the significant collections from thereform the standard for the Rancholabrean LandMammal Age in the scheme of North Americanvertebrate paleontology (Savage, 1951; Savageet al., 1954). The radiometric dates for the extinct

*Correspondence to: Adam Hartstone-Rose, Department of Biol-ogy, Penn State University Altoona, 3000 Ivyside Park, Altoona, PA16601. E-mail: Adam.Hartstone-Rose@psu.edu

Received 13 January 2012; Revised 5 March 2012;Accepted 8 March 2012

Published online 17 May 2012 inWiley Online Library (wileyonlinelibrary.com)DOI: 10.1002/jmor.20036

JOURNAL OF MORPHOLOGY 273:981–991 (2012)

� 2012 WILEY PERIODICALS, INC.

biota have ranged from 11,000 to 45,0001 yearsBP (Marcus and Berger, 1984; O’Keefe et al.,2009). Felid remains are abundant and well-stud-ied, with at least 80 individuals of Panthera atrox(Stock and Harris, 1992) and 2100 individuals ofS. fatalis (Miller, 1968; Shaw and Tejada-Flores,1985) inventoried in the collections at the GeorgeC. Page Museum, Los Angeles, California. Morethan 166,000 fossil bones are identified in theS. fatalis collection alone, with specimens that rep-resent virtually every skeletal element in the body(Shaw and Tejada-Flores, 1985; Shaw, 2001).

A unique set of geologic circumstances are re-sponsible for the accumulation of fossils at RanchoLa Brea, involving a complex system of faultingwithin the Newport-Inglewood fault zone (Quinnet al., 2000). It is defined by folding and dipping ofsubsurface strata containing structural traps filledwith petroleum, and migration of degraded petro-leum (asphalt) to the ground surface as the resultof up-dip leakage from oil sands (Wright, 1987)and/or along fractures and fissures within clayeysiltstones (Quinn et al., 1997). The extraordinaryoccurrence of fossils at Rancho La Brea is due forthe most part to the presence of asphalt (Shaw,2007), which in addition to trapping the organismsnear the vent also preserves the remains. At thesurface, ‘‘stratiform’’ deposits develop aroundactive vents and may produce rather sticky, sheet-like deposits in which animals and plant partsbecome mired and their remains (some of whichare incredibly delicate like the fleshy tissue ofleaves and the iridescent color of insects) becomeperfectly preserved by asphalt saturation (Shawand Quinn, 1986; Quinn, 1992). Where dischargefrom a single asphalt vent occurs for several thou-sand years, a significant deposit of petroleum satu-rated sediment and fossil remains of plants andanimals could accumulate into the typical cone-shaped deposits (Woodard and Marcus, 1971) thatcommonly occur at Rancho La Brea. Shallow, later-ally extensive fossil deposits have also been foundthat indicate a shorter period of accumulation(Shaw and Quinn, 1986). Since 2008, the Project23 excavation has clearly challenged our interpre-tations of ‘‘typical deposits’’ at Rancho La Brea,making it necessary to reevaluate our understand-ing of the mode of accumulation for some of thesedeposits (Harris et al., 2011).

The heyday of excavation activities at Rancho LaBrea occurred between 1905 and 1915, when tens ofthousands of fossils were removed from the site byworkers from many institutions, foreign and domes-tic. The Natural History Museum of Los AngelesCounty (LACM) was given exclusive privilege toexcavate the site for two years (1913–1915) afterwhich 23 acres of land containing the most exten-sive fossil deposits were donated to the County ofLos Angeles. During the two years of excavation bythe LACM, more than one million specimens were

recovered, which comprises the Hancock Collectionat the George C. Page Museum. Unfortunately,early excavators concentrated their efforts on fos-sils of larger plants and animals and were on aquest to find ‘‘perfectly preserved’’ items, so theyrarely noticed or collected remains of smaller organ-isms or noted important information pertaining togeology and taphonomy. Pit 91 was reopened in1969 to rectify these collecting biases (Shaw, 2007).New excavation techniques were developed in ac-cordance with established paleontological andarchaeological methods to intensely sample andcarefully record biologic and geologic data (Shaw,1982). The methodology has evolved and beenrefined over the past 42 years and has been adaptedto the new excavation of the Project 23 deposits.

Careful sampling of Pit 91 and the Project 23deposits have facilitated the recovery of fossil itemsrarely recovered in the early excavations, includingsome hyoid elements, baculae, auditory ossicles, andclavicles. In many cases, these fossil bones of extinctspecies are only known from Rancho La Brea.

Purportedly Machairodontine felid clavicles havebeen figured in the literature only once; fourclavicles from Rancho La Brea assigned by Mer-riam and Stock (1932) to S. fatalis:

Four specimens. . . represent felid clavicles and arepresumably to be referred to Smilodon. . . .It is possi-ble that one or more of these specimens should beassigned to Felis atrox, but the numerical representa-tion of the sabre-tooth in the collections from RanchoLa Brea makes it more probable that they belong tothe latter form.(Merriam and Stock, 1932; p. 108)

These four specimens, however, along with fourothers of similar size and morphology (Fig. 1A–H)since found in the collection from early excavations(Hancock Collection), are all strikingly similar to,although somewhat larger than those of Pantheraleo (Fig. 1 AA and BB). Although Merriam andStock noted the statistical likelihood that theseclavicles belong to Smilodon (the saber-toothedcats are much more numerous than their confami-lials at Rancho La Brea, and in the absence ofother large felid clavicles, it would be parsimoni-ous to assume that any monomorphic samplewould belong to S. fatalis), modern excavationmethods (see Shaw, 1982) for S. fatalis-rich Pit 91and Project 23 have not recovered similarclavicles. These excavations, however, have yielded10 smaller and morphologically distinct felidclavicles (Fig. 1I–R) that we believe likely tobelong to S. fatalis. The previously described speci-mens, supplemented by the other large specimensrecovered from the collection probably represent-ing clavicles of P. atrox.

Recently, several small clavicles have been foundin the bulk matrix sorted from Rancho La Brea’sPit 91 and Project 23 excavations. These smallclavicles are already more numerous (n 5 10) than

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the larger felid clavicles (n 5 8) from all earlyRancho La Brea excavations. These finds promptedthe present investigation into both the specificidentification of the new clavicles and reevaluationof the large felid clavicle morph previouslyassigned to S. fatalis.

MATERIAL AND METHODS

All the fossil clavicles from Rancho La Brea (three left andfive right of the large morph and three left and seven right ofthe small morph) were compared to modern clavicles of nine

felid genera: 15 species (Fig. 1 and Table 1) from the collectionsof the Carnegie Museum of Natural History (CM; Pittsburgh,PA), the Field Museum (FMNH; Chicago, IL), the Natural His-tory Museum of Los Angeles County (LACM; Los Angeles, CA),the Smithsonian National Museum of Natural History (USNM;Washington, DC), and the University of California Museum ofVertebrate Zoology (UC MVZ; Berkeley, CA). All Acinonyx, Neo-felis, and Panthera skeletons from each of these institutionswere examined for the presence of clavicles. Some specimens ofsmall felid taxa (including Puma) were added to this sample toexpand taxonomic interspecific diversity. Although photographsand digital caliper measurements were collected on all claviclesavailable, when both sides were present in a single specimen(see results section for a discussion of bilateral symmetry), the

Fig. 1. Anterior view of Rancho La Brea felid clavicles (A–R) and representative specimens of comparative species (S-BB). Ster-nal end is right and ventral border is up (some specimens have been digitally flipped to accommodate this orientation). A–H, RLBLarge Morph (Panthera atrox?); I–R, RLB Small Morph (Smilodon fatalis?); S, Lynx rufus; T, Neofelis nebulosa; U, Puma concolor;V1 and V2, Acinonyx jubatus—V2 is a superior edge view (perpendicular to the other images), showing the unique fold of the acro-mial end only seen in this taxon; W, Panthera uncia; X, P. onca; Y, P. pardus; Z, P. tigris; AA and BB, P. leo. Scale is in centimeters.Specimen numbers are as follows: A, LACM HC 30080; B, LACM HC 30081; C, LACM HC 30082; D, LACM HC 30091; E, LACMHC I-2; F, LACM HC I-3; G, LACM HC I-4; H, LACM HC I-5; I, LACM RLP R63606; J, LACM RLP R63607; K, LACM RLPR63608; L,LACM RLP R63609; M, LACM RLP R63610; N, LACM RLP R63611; O, LACM RLP R63612; P, LACM RLP R63215; Q,LACMP23-3469; R, LACMP23-2119; S, UC MVZ 10605; T, USNM 399291; U, USNM 152237; V1 and V2, USNM 52039; W, USNM252543; X, USNM 141897; Y, USNM 156284; Z, USNM 174981; AA, LACM M-1144; BB, USNM A22705.

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TABLE 1. Sample

Common name Species Specimen Sex

Cheetah Acinonyx jubatus USNM 251793 FemaleUSNM 395137 FemaleUSNM 521058 FemaleUSNM 520539 Male

Caracal Caracal caracal USNM 583895 ?Ocelot Leopardus pardalis USNM 241582 ?

USNM 240018 FemaleUSNM 256918 Male

Margay Leopardus wiedii USNM 397232 FemaleCanadian Lynx Lynx canadensis USNM 188731 ?Bobcat Lynx rufus LACM RLB-Comp. 30995 ?

UC MVZ 10605 ?UC MVZ 125927 ?USNM 144517/A49939 ?USNM 306264 ?USNM 14416/A49938 FemaleUSNM 292038 FemaleUC MVZ 165916 MaleUSNM 292037 MaleUSNM 398557 Male

Clouded Leopard Neofelis nebulosa USNM 198705 FemaleUSNM 399290 FemaleUSNM 399291 FemaleFMNH 54304 Male

Lion Panthera leo CM 1461 ?FMNH 15530 ?LACM M-1144 ?USNM 172677 FemaleCM 1825 MaleFMNH 1443 MaleFMNH 31121 (0-14-09) MaleFMNH 60788 MaleUSNM A22705 Male

Jaguar Panthera onca USNM 155603 ?USNM 141897/A49762 Female

Leopard Panthera pardus LACM Mam. 31068 ?USNM 013357/A16609 ?USNM 155403/155454 MaleUSNM 156284 MaleUSNM 396948 Male

Tiger Panthera tigris USNM A49773 ?CM 18227 FemaleCM 59939 FemaleFMNH 60760 FemaleUSNM 174981 FemaleUSNM 396137 FemaleUSNM 49740 Female

Snow Leopard Panthera uncia LACM Mam. 90729 ?FMNH 127297 FemaleUSNM 252543 Female

Leopard Cat Prionailurus bengalensis USNM 201069 FemaleUSNM 260779 Male

Flat-Headed Cat Prionailurus planiceps USNM 360975 FemaleUSNM 395254 Female

Puma/Mountain Lion Puma concolor LACM Mam. 85438 ?PED-039-1 ?UC MVZ 81547 ?UC MVZ 12690 FemaleUC MVZ 186058 FemaleUC MVZ 33556 FemaleUC MVZ 33560 FemaleUSNM 155400 FemaleUC MVZ 175988 MaleUC MVZ 186059 MaleUC MVZ 198447 MaleUC MVZ 216773 MaleUC MVZ 33557 MaleUSNM 152237 Male

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right side was used for interspecific and interindividual analy-ses. As none of the fossil specimens can be reliably assigned tothe same individual, and given the overall rarity of theseclavicles, all fossil specimens were included in these analyses asseparate individuals. Even though it is possible that some ofthe left and right clavicles from the same fossil localities mightrepresent a single individual, for statistical purposes, we ana-lyzed all the fossil specimens as separate individuals.Because of their relative size and overall morphology, as well

as the number of specimens recovered, we excluded all nonfelidRancho La Brea taxa as possible contenders for the taxonomicassignment of the 18 clavicles (see the Discussion section, forcomments on the exclusion of Canis dirus and other species).Seven measurements were taken on each clavicle sampled

(Fig. 2): total maximum length, acromial end maximum dorso-ventral width, acromial end anteroposterior thickness, longmidpoint dorsoventral width, long midpoint anteroposteriorthickness, sternal end dorsoventral width, and sternal end ante-roposterior thickness. These variables were then log trans-formed for comparisons in the JMP 9.0 software package (SASInstitute).Variation between and within species was compared for bilat-

eral symmetry and interspecific variation using bivariate plotsas well as principal components analysis and canonical discrim-inant function analysis. Sexual dimorphism could not be statis-tically assessed due to the scarcity of these vestigial bones evenin the most complete museum collections and informationalincompleteness of the comparative sample (see Results section).

RESULTS

In all, clavicles from 65 individuals representinga total of 15 extant species were measured in addi-tion to the 18 fossil clavicles. We found significantdifferences between species and remarkable mor-phological consistency within species (Fig. 1 andTable 2). One example is the difference betweenthe clavicles of P. leo and P. tigris; these speciesare generally morphologically quite similar inmost aspects of their cranial and postcranial skele-tons (e.g., some crania can be difficult to assign tospecies even by those with the most experience,and most postcranial elements are nearly identicalbetween the species), yet their clavicles are easily

distinguishable: those from P. leo are consistentlylarger and more curved than are those from P.tigris.

Given the variation we have found between spe-cies, the morphology of the large morph Rancho LaBrea clavicles (previously assigned to Smilodon byMerriam and Stock, 1932) was strikingly similarto those of P. leo. Acromial width was relativelyhigh in both the Rancho La Brea large morph andP. leo samples. This resulted from a rounded acro-mial flaring that was most pronounced in the pan-therines (particularly in P. leo), although it wasalso encountered in other felines. Within the sam-ple of P. leo clavicles, five of the seven measure-ments taken displayed higher standard deviationsthan in the large fossil morph (Table 2). Althoughit is possible that some of these specimens repre-sent paired clavicles from the same individual(e.g., three were found in Pit 3), the overall mor-phological and relative size similarities are clear.

Fig. 2. Measurements taken. Left clavicle of P. leo (USNM172677) anterior view (top) and inferior view (bottom). Acromialis to the left. A, length; B, acromial width; C, acromial thick-ness; D, mid-shaft width; E, mid-shaft thickness; F, sternal endwidth; G, sternal end thickness. Scale is in centimeters.

TABLE 1. (Continued)

Common name Species Specimen Sex

Rancho La Brea Large Morph LACM HC 30080LACM HC 30081 No DataLACM HC 30082 No DataLACM HC 30091 Pit 16LACM HC I-2 Pit 3LACM HC I-3 No DataLACM HC I-4 Pit 3LACM HC I-5 No Data

Rancho La Brea Small Morph LACM RLP R63215LACM RLP R63606LACM RLP R63607LACM RLP R63608LACM RLP R63609LACM RLP R63610LACM RLP R63611LACM RLP R63612LACM P23-2119LACM P23-3469

See methods for collection abbreviations

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P. atrox is estimated to average about 1.25 timesthe size of the largest of extant cats (Stock andHarris, 1992), therefore, if relative body size istaken into account, the large fossil clavicles repre-sent the expected proportional size compared withP. leo clavicles.

P. tigris, with the largest body size of living cats(Sunquist and Sunquist, 2002), was expected to ex-hibit clavicles of a size between those of P. atroxand P. leo. Instead they fell closer to the range ofthe smaller pantherines. The 10 Rancho La Breasmall morph clavicles show somewhat more varia-tion in size and shape than the larger fossils,although they tend to be substantially smaller andstraighter than the pantherines clavicles (espe-cially those of P. leo, and P. tigris). Likewise, theyare very different than the clavicles of the smallermodern felids which tend to be very thin and rela-tively curved. Furthermore, although they are sim-ilar in overall length to the medium size modernfelids they can be distinguished by their generallywider and more spatulate acromial end. This isparticularly distinctive in comparison to theclavicles of Puma which exhibit an acromial endthat is not notably flared at all—a vital distinctiongiven that Puma was a diagnostic candidate dueto its presence at the site. It can be definitivelyruled out for attribution of any of the fossil speci-mens both qualitatively and statistically.

Bilateral Symmetry

Across all seven of the measurements, theextant taxa represented by both clavicles (N 5 42individuals) are relatively bilaterally symmetricalwith r2 values ranging from 0.9859 for Log TotalLength to 0.8531 for Log Sternal End Thickness.The sternal end is the most variable part of the

clavicle and has the least consistent size and shapevarying from hook-shaped to rounded to practicallyunossified (i.e., cartilaginous in some specimensand with minimal cortical bone in others). Whenthis variable is excluded from the bilateral symme-try comparisons, the next lowest correlation hasan r2 value of 0.8923 (acromial end thickness).Given that this bone is vestigial and has no articu-lation to any other bone, we regard this amount ofsymmetry as high.

Sexual Dimorphism

Unfortunately, the scarcity of clavicles in mod-ern felid collections precluded adequate known sexdistributions, and therefore, sexual dimorphismcould not be excluded as a possible explanation forthe dimorphism exhibited in the fossil claviclesample. Although it would have been particularlyinteresting to compare the two fossil morphs tosexual dimorphism in tigers and lions, none of themuseums have clavicular specimens assigned tomale tigers, and only one of the lion specimenswas recorded as a female. This leaves the possibil-ity that the size difference seen between the mod-ern lions and tigers and in the two fossil morphs(Fig. 1 and Table 2) is the result of sexual dimor-phism. However, the single female lion in our com-parative sample has among the largest clavicles,and the differences between the clavicles of thetwo large modern pantherines and the two fossilmorphs seems to far exceed the levels of sexualdimorphism exhibited in other skeletal elements ofmodern felids. The clavicles of male and femalecheetah and pumas (n ratios of 1:3 and 5:6, respec-tively) do not appear to exhibit very high levels ofsexual dimorphism—for only three of the sevenmeasurements are the male cheetah clavicles

TABLE 2. Basic morphometrics

Species (figure symbol) N Total Length W Acr. T Acr. W Mid. T Mid. W Stern. T Stern.

Acinonyx jubatus (A) 4 30.5 (2.8) 5.8 (1.0) 4.1 (1.0) 4.1 (0.6) 1.3 (0.3) 3.0 (0.8) 2.0 (0.7)Caracal caracal (c) 1 30.2 4.2 1.2 3.1 1.2 1.6 1.5Leopardus pardalis (p) 3 28.8 (5.0) 5.2 (2.4) 0.8 (0.2) 2.1 (0.4) 1.2 (0.1) 1.8 (0.6) 1.3 (0.2)Leopardus wiedii (w) 1 22.5 2.6 0.6 1.5 1.0 1.2 1.4Lynx canadensis (l) 1 30.1 2.7 1.2 2.3 1.2 1.9 1.7Lynx rufus (r) 10 29.4 (3.2) 3.0 (0.5) 1.1 (0.2) 2.1 (0.3) 1.4 (0.3) 1.4 (0.3) 1.3 (0.3)Neofelis nebulosa (N) 4 30.0 (3.8) 2.8 (0.4) 1.2 (0.1) 2.6 (0.3) 1.3 (0.2) 1.4 (0.5) 1.2 (0.2)Panthera leo (L) 9 78.6 (8.9) 11.6 (2.6) 2.9 (0.8) 6.8 (1.4) 4.1 (1.0) 6.1 (2.0) 4.1 (0.8)Panthera onca (O) 2 45.7 (9.5) 8.1 (2.7) 1.7 (0.3) 3.9 (0.1) 2.2 (0.4) 2.6 (0.9) 1.9 (0.4)Panthera pardus (P) 5 51.8 (7.6) 6.8 (2.3) 1.8 (0.4) 3.3 (0.6) 2.4 (0.5) 2.4 (0.9) 2.0 (0.5)Panthera tigris (T) 7 58.8 (5.4) 10.1 (3.4) 2.6 (0.6) 4.7 (0.7) 3.1 (0.3) 2.7 (0.9) 2.5 (0.8)Panthera uncia (U) 3 33.1 (4.4) 6.7 (0.9) 1.6 (0.3) 2.8 (0.4) 1.5 (0.2) 1.8 (0.2) 1.5 (0.4)Prionailurus bengalensis (b) 2 17.7 (5.1) 1.6 (1.0) 1.1 (0.0) 1.1 (0.40 0.7 (0.1) 0.9 (0.1) 0.8 (0.0)Prionailurus planiceps (/) 2 18.0 (1.6) 2.4 (0.2) 0.8 (0.2) 1.5 (0.2) 0.8 (0.0) 1.0 (0.2) 0.9 (0.2)Puma concolor (m) 11 47.8 (7.4) 5.0 (0.9) 2.2 (0.6) 4.4 (1.3) 2.4 (0.4) 2.6 (0.6) 2.1 (0.5)Rancho La Brea Large Morph (X) 8 90.4 (7.6) 15.1 (3.6) 3.9 (0.4) 8.6 (1.6) 5.3 (0.9) 5.7 (0.9) 4.6 (0.7)Rancho La Brea Small Morph (*) 10 38.4 (6.9) 8.0 (3.0) 2.1 (0.4) 4.7 (0.8) 2.7 (0.8) 2.0 (0.8) 1.5 (0.5 )

Mean (and standard deviations) of clavicular total length, and widths (W) and lengths (L) at the midshaft (Mid.), acromial (Acr.)and sternal (Stern.) ends by species.As with all analyses presented, when available, the right side is used.

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larger those of the females (and only a maximumof 27% larger: acromial end thickness), and malepumas are on average larger than female pumasfor only five of the seven measures (and only 37%larger for total length). Whereas the larger morphof fossil clavicles are at least 89% (for acromialend AP thickness) and up to 240% (for sternal endthickness) larger than the small morph in allseven measures. Furthermore, the qualitative dif-ferences between the large and small morphs ofthe Rancho La Brea specimens exceed those foundwithin any of the modern felid species. In otherwords, the large Rancho La Brea specimens lookvery much like the clavicles of modern panther-ines, whereas the small Rancho La Brea morph

looks very different than any modern felid. There-fore, evidence suggests that the dimorphism in theRancho La Brea felid clavicle morphology exhib-ited is not sexual but taxonomic.

Principal Component Analyses

Variation was analyzed for all seven log-trans-formed variables in principal components analysesincluding specimens from all modern individualsand all the fossils (Figs. 3 and 4 and Tables 3 and4). Independent principal component analyses weredone with subsets of the sample (e.g., large catsonly, pantherines only), but the eigenvector load-ings and resulting bivariate plots were so similarto those resulting from the whole-sample analysesthat these results are not included in this article.

As expected, the first principal component (PC1) accounts for most of the variation (nearly 85%;Table 3) and is predominantly a size measurementwith all variables loaded roughly equally and posi-tively (Table 4). On this axis, the lions and largefossil morphs clearly separate themselves from theother felids, with the tigers overlapping with,although falling toward the large-end of the rest ofthe cats. On this axis, the small Rancho La Breamorph overlaps the range of all of the medium sizefelids.

PC 2, accounting for nearly 5% of the morpho-logical variation (Table 3), separates the smallerfossil morph from the rest of the sample, althoughwith some overlap. On the basis of eigenvectorloadings (Table 4), PC 2 reflects an inverse rela-tionship between the sternal-end measurementsand the other shaft widths and thicknesses (totallength is not a strong factor in this axis). Thus,this axis reflects the observable shape peculiarityof highly pointed sternal ends seen in the RanchoLa Brea small clavicles relative to the other shaftmeasurements (Fig. 1I–P). Some of the other speci-mens in the sample, especially some of the tigers,also share this morphology, although not to theextent seen in the small fossil morph (Fig. 3).Thus, in this axis, the small Rancho La Breamorph appears to be the most distinct group.

The third principal component (accounting foran additional 4.62%; Table 3) does not separatethe fossil morphs, but rather it clearly separatesthe cheetahs from all other felids (Fig. 4)—

Fig. 3. Bivariate plot of PC 1 and PC 2. See Table 2 for key.90% density eclipses for P. leo (1), P. tigris (2) and the small (3)and large (4) Rancho La Brea morphs are shown for graphicalpurposes (see text).

Fig. 4. Bivariate plot of PC 2 and PC 3. See Table 2 for key.90% density eclipses for P. leo (1), P. tigris (2), the small (3) andlarge (4) Rancho La Brea morphs, and Acinonyx are shown forgraphical purposes (see text).

TABLE 3. Principal component percentages

Eigenvalue Percent Cum percent

PC 1 5.9267 84.667 84.667PC 2 0.3474 4.963 89.630PC 3 0.3233 4.618 94.248PC 4 0.1599 2.284 96.532PC 5 0.1158 1.655 98.187PC 6 0.0738 1.054 99.240PC 7 0.0532 0.760 100.000

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although some of the cougars approach them onthis axis—a finding that should likely be viewedas support for their molecular phylogenetic affinity(Johnson et al., 2006). On the basis of eigenvectorloadings (Table 4), this axis reflects an inverserelationship between acromial-end thickness andall other measurements. Thus, PC 3 is quantita-tively driven by the qualitatively peculiar cheetahacromial fold (Fig. 1V2). Unlike all other felids, allcheetah clavicles contain a distinctive folding onthe superficial side of the acromial end whichresults in a hook-shaped groove.

The fourth principal component (not figured),accounting for an additional 2.28% of the variationmay reflect some interesting variation based onthe eigenvector weightings (reflecting an inverserelationship between all three of the widths andthe other four variables; Table 4), but none of thefelid groups are statistically distinguishable alongthis axis. The other principal components (also notfigured), accounting for the remaining 3.47% of thevariation (Table 4), do not discriminate any of thefelid groups.

Discriminant Canonical Analyses

In a discriminant canonical analysis of the loga-rithmically transformed seven variables for thesample (Fig. 5), more than 85% of the specimensare correctly assigned to their taxonomic group.The two Rancho La Brea fossil morphs wereincluded in this analysis as separate taxa distinctfrom the modern species. Of the 12 specimens mis-classified, two small species were misclassified ascongeners (a Leopardus pardalis misclassified asL. wiedii, and a Lynx canadensis misclassified asL. rufus). Similarly, one of the L. rufus specimensis misclassified as Caracal caracal. The only largemodern species that have significant misclassifica-tions are Panthera pardus (with single specimensmisclassifying as P. tigris and L. rufus), andP. tigris (with single specimens misclassifying asP. pardus and Puma concolor). One P. concolormisclassified as Neofelis nebulosa, and all theremaining misclassifications involved the fossiltaxa. Only one of the small Rancho La Brea speci-mens sorted anomalously (as N. nebulosa), and the

remaining discrepancies surrounded the classifica-tions of the P. leo and large Rancho La Brea speci-mens with two P. leo grouping with large RanchoLa Brea specimens and one large Rancho La Breaspecimen classifying as P. leo. In other words, inthis analysis, these two groups interdigitated morethan any other pair of taxa reaffirming the mor-phological similarity of the two sets of claviclesand lending further support to the phylogeneticrelationship of the two taxa, if the large RanchoLa Brea clavicles belong to P. atrox. Importantly,there is no classification overlap between either ofthe large extant felids (P. leo and P. tigris) orbetween the fossil morphs.

When the discriminant canonical analysis isrerun without categorization of the fossil speci-mens, all the large Rancho La Brea specimens sortas P. leo. In fact, they do so with higher predictedprobability (Mean Prob 0.992, SD 0.014) than thetotal sample of modern P. leo specimens (MeanProb 0.949, SD 0.092). In other words, based onthe total sample, the large Rancho La Brea speci-mens are more securely sorted as P. leo than mostof the P. leo specimens are. As expected, the mor-

TABLE 4. Principal component eigenvectors of the logarithmically transformed variables, where extant individuals wererepresented by both clavicles, the right was used in all analyses

Variablea Eigenvectors PC 1 PC 2 PC 3 PC 4

A Total length 0.39242 20.03829 20.35867 20.25915B Width acromial 0.37208 0.51140 20.11918 0.60702C Thickness acromial 0.35561 0.12569 0.82614 20.33283D Width mid 0.38585 0.32792 0.07162 0.08758E Thickness mid 0.38579 0.15663 20.37059 20.47448F Width sternal 0.37139 20.58342 0.13692 0.46378G Thickness sternal 0.38139 20.49877 20.11591 20.07551

aCorresponding to those in Figure 2.

Fig. 5. Discriminant canonical plot of the log-transformedseven measurements for all felids. To reduce graphical clutter,only the 95% confidence region means eclipses for (1) P. leo, (2)P. tigris, (3) the small and (4) large Rancho La Brea morphs,and (5) Acinonyx are included. See Table 2 for key.

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phologically diverse and distinctive small RanchoLa Brea specimens do not sort consistently withany modern taxon. One specimen sorts with highprobability (0.99) as a P. uncia, but all others sortwith relatively low probability among five othertaxa with the most frequent classification beingP. onca—the most likely predicted attribution forsix of the 10 specimens, and the second most likelyfor two others. The classification of the small Ran-cho La Brea specimens is apparently drivenentirely by size as they are sorted entirely into me-dium size modern clavicle morphs—namelyP. onca, P. tigris (which has relatively smallclavicles for its size), P. uncia, Puma, and one speci-men being designated either Caracal (prob 0.78) orNeofelis (prob 0.22). Thus, the large Rancho LaBrea specimens, when sorted without independentcategorization, sort with very high probabilities asP. leo, whereas the small Rancho La Brea specimenssort with much more inconsistency although withslight, size-based, affinities mostly with P. onca.

As with the principal component analyses, themost distinct taxon in the discriminant functionanalyses is Acinonyx jubatus. That is, in an analysisof the biplot rays (not shown) the second canonicalaxis, like PC3, is driven by the acromial thickness(at the top) and total length (at the bottom). Thefirst canonical axis is primarily driven by acromialwidth and (to a lesser extent) sternal width (to theleft), and all other measurements, especially totallength and mid-shaft width (to the right).

As with the principal component analyses, sub-sets of the sample (e.g., large cats only, panther-ines only) were also examined using discriminantfunction analyses, and the results (not shown)were nearly identical to those of the whole sample.

DISCUSSIONThe Variable Presence of Clavicles inMuseum Collections

Not only are carnivoran clavicles rare in the fossilrecord but also they are surprisingly uncommon incollections of modern specimens as well. Althoughless than half of the postcranial specimens exam-ined did include clavicles, all feline cadavers thatwe examined retain the clavicle. Hyoid elementswere also missing from slightly less than half of thespecimens. Roughly, two-thirds of the instanceswhere specimens contained hyoid elements, clavicleswere also present. In fewer instances, clavicles werefound when no hyoid elements were present. There-fore, it seems plausible that clavicles were notextracted from the musculature before the musclemass was removed and discarded and the rest of theskeleton was processed. In every skeletonization offelines performed or directed by A. Hartstone-Rose,where recovery of the clavicles was attempted (N 521 including members of Felis, Lynx, Neofelis andPanthera), these bones were present.

Relative Abundance of Two Fossil Morphs inModern Excavations

With more than 2000 individuals of S. fatalisfound at Rancho La Brea, it can be assumed thatif clavicles of the size figured by Stock and Mer-riam were present in S. fatalis, many more wouldhave been found than the handful represented inour sample. From Pit 91, S. fatalis is the medium-to-large mammal species with the highest mini-mum number of individuals (MNI; from unpub-lished Page Museum database). Furthermore,modern Pit 91 (1969–2008) excavation and labora-tory work (screening and cleaning was not per-formed in early Rancho La Brea excavations)should have revealed many more of them. Theratios of small to large morphs from Pit 91 andProject 23 (the only excavations which would havelikely identified both, due to screening) are 8:0 and2:0, respectively, providing additional evidencethat the small morph is most likely that of S.fatalis.

Other Mammals

The morphology of the small Rancho La Breamorph is most similar to felines when comparedwith those of rodents and rabbits (Sandstrom andSaltzman, 1944). There is no other claviculate spe-cies from Pit 91 with a high enough MNI toaccount for eight clavicles except perhaps canidsand lagomorphs, but based on the known shapeand size of this bone, they do not belong to speciesof any of these taxa. The clavicles are more numer-ous than the MNI for all mustelid species from Pit91 and are larger than mustelid clavicles, which, ifpresent, are normally less than 1 cm. (PamelaOwen: Pers. Com.). When present, Canis claviclesare normally oval in shape and generally less thana centimeter long (Schebitz and Wilkens, 1978;Evans, 1993; Cerny and Cizinauskas, 1995); quitedifferent than these small clavicles from Pit 91and Project 23, which reflect the general shape ofthe feline clavicle. Canid clavicles large enough tonotice as distinct bones are rare indeed (XiaomingWang: Pers. Com.). Thus, Canis dirus and C.latrans are not considered as possible candidatesfor these clavicles.

Our comparative study of feline cat clavicles,however, suggests that S. fatalis could have a clav-icle of this shape and size, and with no other possi-ble candidate represented in the collection, we areconfident in our assignment of these distinct skele-tal elements to S. fatalis.

Body size and weight of large pantherines, whencompared with respective clavicle sizes and mor-phologies, shows that the clavicle has beenreduced far more in P. tigris than in P. leo. This isunexpected because P. tigris is on average signifi-cantly larger than P. leo, although they are closely

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related. Furthermore, P. tigris is primarily a wood-land or jungle species, whereas P. leo more oftenhunts in open habitats. Therefore, if clavicularreduction is a consequence of increased cursorial-ity, we expected the opposite evolutionary trajec-tory. The phylogeny proposed by Johnson et al.(2006) pairs tigers and snow leopards. Our datasupports this conclusion due to the grouping oftiger clavicles with smaller pantherines in princi-ple component and discriminant canonical analy-ses, as well as in the smaller size they exhibitqualitatively. The large Rancho La Brea morph isherein assigned to P. atrox and clearly supports aclose relationship with P. leo casting doubt on theveracity of the recent hypothesis linking P. atroxto P. onca (Christiansen and Harris, 2009). Evi-dence suggests this large, robust, clavicular formis a synapomorphy of the P. atrox/P. leo group ofpantherine felids. Although we are not aware of aclavicle known from P. spelaea, it’s morphologywould help confirm this hypothesis.

It was unexpected to find that cheetahs (A. juba-tus) have clavicles at all, given that their postcra-nial anatomy displays profound convergence withcanids, and even more extreme cursoriality. Alsosurprising is that their clavicles exhibit such dis-tinct morphology. The size of the clavicle does notseem to be reduced much more than the otherfelines’ leading us to infer that, at least in thistaxon, cursorial adaptive changes in the pectoralgirdle lead to changes in the clavicle beyond sizereduction. Of course, canids and hyenids may havereduced their clavicles over longer evolutionarytime periods. Thus, such a highly cursorial carni-vore like the cheetah, having evolved over a rela-tively short time interval, might have a clavicleadapted to, rather than reduced by, changes inpectoral girdle morphology. Investigation of themorphology of the A. jubatus clavicle (particularlyin relation to the soft tissue associated with it) isbeyond the scope of this article but should includeconsideration of the acromial hook (mentionedabove) which may serve a structural purpose, ifnot a functional one. This morphology clearlymakes cheetah clavicles diagnostically distinctfrom all other felids.

To our knowledge, no other machairodontineclavicles have been identified. This leaves us withno basis for discussion of the evolutionary historyof this bone within the subfamily. The claviclessampled for P. tigris seem to show that within thefamily Felidae there are occurrences of very largecats with small clavicles, but the S. fatalisclavicles are the smallest we have seen relative tobody size. Considering the likely heavy forelimbuse by this species in hunting (Marean, 1989;Meachen-Samuels and Van Valkenburgh, 2010), itseems possible that S. fatalis or its antecedentsmay have had evolutionary developmental factorsin pectoral limb remodeling which required or led

to the further reduction of the clavicle. A deeperunderstanding of the evolutionary history of thisbone may require a sample of clavicles from morebasal machairodontine cats.

ACKNOWLEDGMENTS

For access to specimens, we thank John Harris,Antonia Tejada-Flores, Shelley Cox, and RichardReynolds from the George C. Page Museum,Xiaoming Wang and Jim Dines from the NaturalHistory Museum of Los Angeles County, Chris Con-roy from the University of California Museum ofVertebrate Zoology, Linda Gordon from the Smith-sonian National Museum of Natural History, andPamela Owen from University of Texas, Austin.The authors thank Graham Slater and one anony-mous reviewer for feedback on this manuscript.

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