Evolution of South American Mammalian Predators Borhyaenoidea Anatomical and Palaeobiological Implications (CHRISTINE ARGOT)

Zoological Journal of the Linnean Society

, 2004,

140

, 487–521. With 11 figures

© 2004 The Linnean Society of London,

Zoological Journal of the Linnean Society,

2004,

140

, 487–521

487

Blackwell Science, Ltd

Oxford, UK

ZOJZoological Journal of the Linnean Society

0024-4082The Lin-nean Society of London, 2004? 2004

140

?

487521Original Article

C. ARGOTEVOLUTION OF BORHYAENOIDEA

*Current address: Institut für Spezielle Zoologie und Evolutionsbiologie, Erbertstraße 1, 07743 Jena, Germany.E-mail: [email protected]

Evolution of South American mammalian predators (Borhyaenoidea): anatomical and palaeobiological implications

CHRISTINE ARGOT*

Laboratoire de Paléontologie UMR 8569 du CNRS, Muséum national d’Histoire naturelle, Paris, France

Received September 2002; accepted for publication October 2003

The evolution of South American carnivorous marsupials, the borhyaenoids, has been investigated through the func-tional analysis of postcranial adaptive traits and palaeobiological data. There is evidence that the evolutionary his-tory of Borhyaenoidea proceeded from a noncursorial ancestor. The locomotion and habits of the early Palaeocene

Mayulestes ferox

probably approached a generalized plesiomorphic pattern for marsupial locomotion, i.e. primarilyterrestrial with secondary arboreal adaptations. An exceptionally rich early Miocene Patagonian fauna has yieldedvarious morphological predator types, from scansorial ambusher to terrestrial, incipiently cursorial, taxa. The mostspecialized borhyaenoid was the powerful sabretooth

Thylacosmilus atrox

that survived until the late Pliocene. Theevolution from a scansorial pattern towards a cursorial trend, illustrated by

Borhyaena tuberata

, and towards theprobable development of postlactational parental care in

Thylacosmilus

, required by its dental specialization and kill-ing strategy, suggests a modification of the selective pressures and predatory activities of the group over evolutionarytime. © 2004 The Linnean Society of London,

Zoological Journal of the Linnean Society

, 2004,

140

, 487–521.

ADDITIONAL KEYWORDS: Cenozoic – functional anatomy – Metatheria – postcranial skeleton.

INTRODUCTION

The superfamily Borhyaenoidea includes the marsu-pial predators that inhabited South America duringthe Tertiary while the continent was isolated. Thissuperfamily has been revised by Marshall (1976,1977a, 1978a, 1979, 1981) on the basis of dentalremains, and unites ‘dog-like’ taxa (Hathlyacynidae,Prothylacinidae, Borhyaenidae, Proborhyaenidae) and‘sabretooth’ taxa (Thylacosmilidae). More recently, thediscovery of the earliest representative (so far as isknown) of the superfamily,

Mayulestes ferox

, from theearly Palaeocene of Tiupampa (Bolivia), added thenew family Mayulestidae (Muizon, 1998). The mostcommon remains of borhyaenoids are teeth and jaws,and less than one third of the 35 known genera arerepresented by both skulls and postcranial remains.

Dental morphology has therefore been used to deter-mine the various taxa in most cases.

Borhyaenoids maintained a position at the top of theSouth American food pyramid throughout the Ceno-zoic. They possessed a dental functional complexrelated to a hypercarnivorous diet, a complex thatappeared several times independently in many othergroups of mammals, especially thylacinids (see detailsin Muizon & Lange-Badré, 1997; Muizon, 1999). How-ever, despite such superficial resemblances shared bysome borhyaenoids and Australian thylacinids, due toa predatory mode of life, the phylogenetic analysesperformed all reached the conclusion (irrespective ofthe methodology used) that borhyaenoids are moreclosely related to South American didelphoids than tothylacinids, this latter family being more closelyrelated to dasyuroids (Marshall, 1977b; Archer, 1982;Szalay, 1982).

The borhyaenoid specimens examined were as fol-lows:

Mayulestes ferox

MHNC 1249 (Tiupampan, earlyPalaeocene, Bolivia);

Sipalocyon gracilis

PU 015154,MACN 691–703, MACN 5938–49;

Cladosictis pata-

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gonica

PU 015046, PU 015170, PU 015702;

Prothy-lacinus patagonicus

PU 015700, MACN 706–720;

Borhyaena tuberata

PU 015701, PU 015120, MACN2074–78, MACN 6203–6265 (these four taxa: San-tacrucian, early Miocene, Argentina);

Lycopsis longi-rostris

UCMP 38061 (Laventan, middle Miocene,Colombia);

Thylacosmilus atrox

FMNH P14531,FMNH P14344 (Huayquerian, late Miocene, Argen-tina). Intraspecific variation and variation related tosex or age were impossible to assess for these taxa.Three taxa are less well known:

Sipalocyon

, wherecomplete long bones, girdles, and the major part of theaxial skeleton are unknown;

Borhyaena

, in whichmost of the thoracolumbar and caudal vertebrae, thepelvic girdle and the hindlimb (except femur) areunknown; and

Thylacosmilus

, where scapula, ulna,innominate, and most of the thoracolumbar vertebraeand all caudals are unknown.

This paper has developed from studies of the post-cranial adaptations of various borhyaenoids (Argot,2001, 2002, 2003a, b, c; in press), and is an attempt todefine the structural pattern characterizing thesemetatherians. Moreover, because the structural-functional solution of a lineage appears to be highlydependent on its ancestry, the evolutionary history ofBorhyaenoidea is traced from its oldest known repre-sentative,

Mayulestes ferox

. This paper also reviewsthe existing literature dealing with habitats and fau-nas associated with borhyaenoids, in order to placethese carnivorous marsupials within their palaeoeco-logical framework.

Institutional abbreviations: FMNH, Field Museumof Natural History, Chicago, USA; MACN, MuseoArgentino de Ciencias Naturales ‘Bernardino Rivada-via’, Buenos Aires, Argentina; MHNC, Museo de His-toria Natural de Cochabamba, Cochabamba, Bolivia;PU, Peabody Museum of Yale University, New Haven,USA; UCMP, University of California, Museum ofPalaeontology, Berkeley, USA.

ROOTS

The oldest borhyaenoid known is

Mayulestes ferox

fromTiupampa (Santa Lucía Formation, south-centralBolivia), a locality that has yielded a marsupial-richand taxonomically diverse vertebrate fauna (Pascual &Ortiz Jaureguizar, 1991; Muizon, 1992; Marshall

et al

.1995; Muizon, 1998; Muizon & Cifelli, 2000). The Tiu-pampan Land Mammal Age (Pascual & Ortiz Jau-reguizar, 1990) is now commonly accepted to be earlyPalaeocene, about 63–64.5 Mya (Flynn & Swisher,1995; Marshall

et al

., 1995; Muizon, 1998).The Tiupampa fauna includes only marsupials and

placentals, with no indication of nontribosphenic taxa(Table 1). By contrast, the slightly younger Punta Peli-gro fauna, which represents the oldest Tertiary fauna

from Patagonia (the Peligran is about 61–62.5 Mya:Flynn & Swisher, 1995) includes a monotreme, sug-gesting biogeographical relationships with Australiaand presumably Antarctica, and a multituberculatebelonging to an endemic late Mesozoic

-

early CenozoicSouth American or Gondwanan radiation (Bonaparte

et al

. 1993; Flynn & Swisher, 1995). The mammalfauna of Laguna Umayo (Peru), close to the Creta-ceous–Palaeocene boundary (although the age of thisfauna is still a matter of debate), contains some teethand jaw fragments of marsupials and condylarths(Flynn & Swisher, 1995). The Chulpas fauna, alsofrom the Umayo Formation but slightly younger thanthe Laguna Umayo fauna, contains marsupials andnotoungulates (Flynn & Swisher, 1995). These faunasare much less diverse than that of Tiupampa and theirtaxa remain poorly known. Therefore, in the SouthAmerican faunas from the Cretaceous

-

Cenozoic tran-sition, the mammalian adaptive types are marsupials

Table 1.

List of Tiupampan mammals (Santa Lucía For-mation, Bolivia) from Muizon (1992, 1998) and Muizon &Cifelli (2000, 2001)

GONDWANADELPHIA LEPTICTIDA

MICROBIOTHERIA

Palaeoryctidae?Microbiotheriidae cf.

Cimolestes

sp.

Khasia cordillierensis

PANTODONTADIDELPHIDA Alcidedorbignyidae

DIDELPHIMORPHIA

Alcidedorbignya inopinata

Pucadelphydae

Pucadelphys andinus

NOTOUNGULATA

Andinodelphys cochabambensis

Henricosborniidae or Oldfielthomasiidae

?Didelphidae Undetermined taxon

Incadelphys antiquusMizquedelphys pilpinensis

PANAMERIUNGULATA

Tiulordia floresi

MioclaenidaeJaskhadelphydae Kollpaniinae

Jaskhadelphys minutus Molinodus suarezi

Mayulestidae

Tiuclaenus minutus, T. cotasi, T. robustus

Mayulestes ferox Andinodus boliviensisAllqokirus australis Pucanodus gagnieri

Family incertae sedis

Simoclaenus sylvaticusSzalinia gracilis

ARCHIMETATHERIA

Peradectidae

Peradectes

cf.

austrinum

SUDAMERIDELPHIA

Caroloameghiniidae

Roberthoffstetteria

nationalgeographica

EVOLUTION OF BORHYAENOIDEA

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and placentals, the latter being represented mainly byvarious native ‘ungulates’ (notoungulates, condy-larths), whose low-crowned cheek teeth indicatebrowsing herbivores more adapted to forested than toopen habitats (Pascual & Ortiz Jaureguizar, 1990).This period corresponds to the earliest phase of isola-tion of the continent, and here begins the most autoch-thonous part of the history of mammals in SouthAmerica (Pascual & Ortiz Jaureguizar, 1990).

Placentals and marsupials of the early Tertiary ofSouth America are commonly presumed to have dis-persed southward from North America, various taxasuggesting biogeographical relationships with NorthAmerica, and possibly other parts of Laurasia, duringthe Cretaceous

-

Cenozoic transition (Muizon, 1992;Pascual & Ortiz Jaureguizar, 1992; Bonaparte

et al

.,1993; Muizon

et al

., 1997; Flynn & Wyss, 1998). Forexample, the Tiupampa ‘condylarths’ (Kollpaniinae)and the litopterns are related to the North AmericanMioclaenidae, but they do not show close relationshipswith the other South American ‘ungulates’ (Astrapoth-eria, Pyrotheria, Notoungulata) (Muizon & Cifelli,2000). By contrast, the marsupials of Tiupampa moreclosely resemble those known from the late PalaeoceneItaboraí fissures of Brazil, suggesting that they werepart of an endemic radiation on the South Americancontinent and therefore that they arrived before the‘condylarths’ and pantodonts (Pascual & Ortiz Jau-reguizar, 1991, 1992; Muizon, 1992; Muizon & Cifelli,2001).

Within the Tiupampa fauna, the placentals wereherbivorous and partly omnivorous, whereas the mar-supials were insectivorous-frugivorous, omnivorous,and carnivorous, an ecological distribution unique toSouth America (Pascual & Ortiz Jaureguizar, 1991).The metatherian fauna includes the oldest skulls andskeletons of undisputed marsupials of the Americancontinent,

Mayulestes ferox

,

Pucadelphys andinus

and

Andinodelphys cochabambensis

, whose adaptationshelp to shed light on the evolutionary history of vari-ous metatherian groups (Muizon & Argot, 2003).

Several specimens of

Pucadelphys

and

Andinodel-phys

were found with the majority of bones articu-lated, suggesting little postmortem dismemberment.The abundance of frogs throughout the deposits wherethe mammals have been found suggests that theylived near the bank of a river, and were trapped anddied as a result of a catastrophic flood (Marshall

et al

.,1995). A sudden flood is likely to have affected terres-trial species more so than arboreal ones, and it is sig-nificant that

Pucadelphys andinus

is both the leastarboreally adapted taxon among the Tiupampan met-atherians known from postcranial remains (Muizon &Argot, 2003), and the most abundant mammal speciesof this fauna (Marshall & Sigogneau-Russell, 1995),with 20 specimens found to date (C. de Muizon, pers.

comm.). By contrast,

Mayulestes ferox

is known from asingle specimen and is the most arboreal of the threeTiupampan metatherians.

The locomotion and habits of these three taxa wereprobably more similar to those of living dasyuridsthan to those of living didelphids, the former beingmore predaceous and faster animals. It has beenhypothesized that the Tiupampan metatherians rep-resent a generalized plesiomorphic pattern for marsu-pial locomotion, i.e. primarily terrestrial, withsecondary arboreal adaptations more or less empha-sized, which is especially true for

Pucadelphys

and

Andinodelphys

(Muizon & Argot, 2003).

Mayulestes

ischaracterized by more specialized arboreally adaptedtraits (Muizon, 1998; Argot, 2001, 2002, 2003a). Theclimbing ability facilitates escape into an arboreal ref-uge and also makes accessible sources of food andcover that are denied to strictly terrestrial mammals(Wemmer, 1977). Hence, these activities were proba-bly selected by the marsupial taxa in order to avoidattack by terrestrial nonmammalian predators(mainly crocodiles), and to access the potentialitiesprovided by a forested milieu.

Mayulestes

is separated by more than 45 Myr fromthe other borhyaenoids examined, and is muchsmaller. It weighed less than 1 kg (probably less than500 g), a size at which an animal may be arboreal orscansorial but not cursorial, may be both predator andprey, and always has to deal with many obstacles, evenwhen moving on the ground. By contrast, the Miocenetaxa were larger, ranging from the size of a cat (

Sipal-ocyon

) to that of a jaguar (

Thylacosmilus

) (Argot,2003b, c; in press). Therefore, it is likely that Mayule-stidae are totally distinct from the later lineages thatgave birth to the Miocene taxa; unfortunately, veryfew borhyaenoid taxa are known from the period inbetween.

An unusual family of Borhyaenoidea, the Probo-rhyaenidae, is known from a few specimens that datefrom the Eocene and Oligocene, at a time when therepresentatives of other borhyaenoid families are rare(Marshall, 1978a). During the Casamayoran (earlyEocene, about 10 Myr after

Mayulestes

), a probo-rhyaenid known from postcranial elements hadalready reached the size of the Santacrucian

Borhyaena

and

Prothylacinus

(J. Babot, pers. comm.).At the same time, the family Borhyaenidae is repre-sented by one taxon,

Angelocabrerus daptes

. Similarin size to

Borhyaena tuberata

according to dental mea-surements, it may represent an early specialized off-shoot within the family, the massive P3 suggestinghyaena-like habits (Savage, 1977; Marshall, 1978a).The origins of Proborhyaenidae are unknown and therepresentatives of this family reached the size of verylarge bears and became extinct at the end of the Oli-gocene (Deseadan), simultaneously with very large

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herbivorous mammals. The differentiation and extinc-tion of these gigantic predators and herbivores appearto be a conspicuous South American example of coevo-lution, their extinction being interpreted as the effectof decisive climatic-environmental changes (Bond &Pascual, 1983). Considering the fact that during theearly Eocene two large proborhyaenid taxa alreadycoexisted, and that the late Palaeocene Itaboraí fis-sures of Brazil have yielded

Patene simpsoni

and

Nem-olestes

sp., representatives of two distinct families(Hathlyacynidae and Borhyaenidae, respectively:Marshall, 1978a, 1981), it may be hypothesized thatearly radiations, as yet unresolved, occurred withinBorhyaenoidea.

DETERMINATION OF FUNCTIONAL-ADAPTIVE CHARACTERS

Although it has been shown that some regions of thepostcranial skeleton can help to shed light on the sys-tematics of various groups (see Szalay, 1994; for ananalysis of metatherians based on tarsus evidence), itis extremely difficult to clarify the affinities betweenborhyaenoid families because of the poor sample ofspecimens known from postcranial elements. How-ever, it is possible to determine whether a commonstructural pattern can be detected from studying thevarious responses by borhyaenoids to adapting to dif-ferent modes of locomotion and hunting strategiesunder common phylogenetic constraints. Analysis of

Mayulestes

and of another Tiupampan metatherian,

Pucadelphys

(Muizon, 1998; Argot, 2001, 2002, 2003;Muizon & Argot, 2003) permits appraisal of possibleancestral retentions as well as of early specializationsthat occurred in the oldest borhyaenoid known.

Two features, a long axial neural process and strongsagittal ventral crests on the axis, C3, and C4, arecommon to all borhyaenoids observed, and are proba-bly related to their predatory habits. These two fea-tures are present in

Mayulestes

but not in

Pucadelphys

, and therefore could be qualified asancestral retentions for borhyaenoids.

Axial neural process

A long and robust neural process of the axis (Fig. 1) ispresent in

Mayulestes

,

Cladosictis

,

Prothylacinus

,

Borhyaena

and

Lycopsis

. This feature is unknown in

Sipalocyon

and its presence is uncertain in

Thyla-cosmilus

, since the posterior part of the process is bro-ken. However, its thinness and the orientation of theposterior margin (vertical above the postzygapophyses)in

Thylacosmilus

suggest a relatively reduced poste-rior extension of the process compared with theMiocene borhyaenoids. A long neural process is alsopresent in marsupials like

Dasyurus

and

Thylacinus

,

and in all placental carnivores that feed upon preysmaller than themselves, and shake it when biting theneck, e.g. in felids (Pellis & Officer, 1987) and mustel-ids (Poole, 1974). By contrast, this posterior extensionis not found in carnivores that prey upon animalsbigger than themselves or scavenge like wolves andhyaenas.

Although the M. obliquus capitis caudalis originateson the axial neural process and inserts on the trans-verse processes of the atlas, providing rotation andshaking movements of the head, it seems that themorphology of the atlas and axis is not directlyrelated. The transverse processes of the atlas areindeed ovoid in shape in all borhyaenoids except

Thy-lacosmilus

, in which they are extended posteriorly(Argot, in press). This condition is similar to thatobserved in both

Hyaena

and

Smilodon

, two taxawhere the axial neural process is different. Accordingto anatomical data, the posterior extension of theatlantal transverse processes is probably related tothe pull of M. scalenus, a powerful flexor of the neck.

Sagittal ventral crests on the axis, third and fourth cervicals

These crests (Fig. 1) form strong triangular processes,a feature that characterizes borhyaenoids. In thePalaeocene

Mayulestes

the ventral process is incipienton the axis (a condition possibly related to its smallsize); the other cervicals are unknown. Although incip-ient processes can also be observed in modern taxalike

Thylacinus cynocephalus

,

Canis lupus

and pred-atory viverrids like

Poiana richardsoni

, their distribu-tion among taxa and development does not reach thatobserved in the Miocene borhyaenoids where they arepresent in all members. The development of these pro-cesses was either related to the pull exerted by thelong flexors of the neck (Mm. longus capitis and longuscolli), or to the presence of strong ventral ligamentsnot observed in modern taxa, equivalent to the dorsalligamentum nuchae. In

Thylacosmilus

the attachmentof the M. longus capitis forms rugose scars on the basi-cranium, in front of the foramen magnum. These flex-ors probably acted as strong depressors of the head,useful in increasing bite strength, and their develop-ment is therefore probably related to carnivoroushabits.

Two features, an elongate deltopectoral crest and anasymmetrical metacarpophalangeal joint on thepollex, are present in most borhyaenoids observed andrelated to manipulation of the forelimb.

Deltopectoral crest length

In all Miocene borhyaenoids, the deltopectoral crest(Fig. 2) is extremely long (i.e.

>

60% of the humerus

EVOLUTION OF BORHYAENOIDEA

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length). It is particularly strong in two medium tolarge-sized borhyaenoids that exhibit arboreal capa-bilities (

Prothylacinus) or manipulate heavy prey(Thylacosmilus). In these two taxa the crest is promi-nent anteriorly and ends distally with a strong tuber(Argot, 2003b; in press). This condition has no equiv-alent in living marsupials. The proximal anterior pro-jection of the crest is obviously related to thedevelopment of the greater tubercle (that protrudesanteriorly in all borhyaenoids in which it is known:Fig. 2, top), but not the shape of the distal end. InLycopsis and Cladosictis the crest is extremely long butnot prominent distally. Similarly, in the AustralianThylacinus the insertion of the pectoralis is extremely

long but the crest is not prominent. In Sipalocyon andBorhyaena the humerus is fragmentary. In Mayulestes(Fig. 2A) the crest is relatively shorter than in theother borhyaenoids (55% of the humerus length) butan allometric effect cannot be discarded. In living mar-supials, the M. deltoideus pars acromialis inserts onthe proximal third of the crest (anterolateral deltopec-toral area), the pectoralis along the whole crest (anter-omedial side). Although the crest does not appear to beparticularly strong in living Carnivora, the insertion ofthe pectoralis is extremely long in taxa where the fore-limb retains skilful manipulative capabilities, e.g.felids and ursids (Argot, 2003b). This suggests thatborhyaenoids also had good manipulative capabilities.

Figure 1. Skull and cervical vertebrae in lateral left view, showing the anteroposterior extension of the axial neural pro-cess, and the development of strong ventral triangular processes on the axis, C3, and C4 (arrowed). A, Borhyaena tuberataPU 015701 (the fourth cervical is unknown) modified from Sinclair (1906). B, Lycopsis longirostris UCMP 38061 modifiedfrom Marshall (1977a). C, Prothylacinus patagonicus PU 015700 (the sixth and seventh cervicals are unknown) modifiedfrom Sinclair (1906). D, Cladosictis patagonica PU 015046 (skull) and PU 015170 (cervicals) modified from Sinclair (1906).E, Thylacosmilus atrox FMNH P 14531 (skull, modified from Riggs, 1934), and FMNH P 14344 (cervicals). F, axis in May-ulestes ferox MHNC 1249. The natural curvature of the cervical area is preserved only in Lycopsis (B) and Cladosictis (D).Scale bars: 50 mm in A-E, 5 mm in F.

E

prominent ventral processes

F

incipient ventral process

D

BC5

axial neural processC7

C7

C7

C7

C

A

492 C. ARGOT

© 2004 The Linnean Society of London, Zoological Journal of the Linnean Society, 2004, 140, 487–521

Metacarpophalangeal joint of the pollexThe very asymmetrical, trochlear-shaped metacar-pophalangeal joint of the pollex (Fig. 3) ofborhyaenoid taxa in which it is preserved seems tohave no equivalent. On the proximal phalanx, theouter (radial) articular facet is transversely narrowbut is dorsoventrally long, and exhibits a longer arcof curvature than the inner (ulnar) condyle, which iswider and shorter. This asymmetry is reflected onthe distal epiphysis of Mt I and the articulation indi-cates that flexion-extension of the pollex did nottake place in a strict parasagittal plane. This condi-tion is found in Sipalocyon, Cladosictis (Argot,2003c), and Lycopsis (three taxa very different insize, age and adaptations). In Thylacosmilus, thedistal epiphysis of the first metacarpal is not tro-chlear-shaped as in these three genera, and theproximal phalanx is unknown. However, the distalarticular facet of Mc I is much more asymmetricalthan in the other metacarpals and also suggests thatthe pollex was pseudo-opposable (Argot, in press).This condition is unknown in the other borhyaenoidsexamined because of lack of elements, and no

borhyaenoid has yet been found with a metacar-pophalangeal joint similar to that of the other dig-its. Hence, the acquisition of hand dexterity mayhave had an important influence on the evolution offeeding and foraging strategy of Borhyaenoidea.

The use of the forepaws in grasping prey and pin-ning it to the ground seems to be a feature that hasevolved several times within various orders of mam-mals (Eisenberg & Leyhausen, 1972; Iwaniuk et al.,1998). According to Eisenberg & Leyhausen (1972), itis present in both the Dasyuridae and those eutherianspecies, like felids, which are arboreally adapted andretain some grasping ability in the forepaw. Where theforepaw is still employed in grasping, some ability topronate and supinate it is retained. By contrast, dig-itigrade viverrids that have little ability to pronate orsupinate the forelimbs (e.g. Civettictis, Viverra, Ich-neumia and Fossa) never employ them in manipulat-ing prey during feeding.

The combination of these two groups of characters(cervical morphology and forelimb dexterity) is notfound in any other group of mammals. Other postcra-nial features vary within the Borhyaenoidea according

Figure 2. Humerus in proximal (top) and lateral (bottom) views, showing the variable development of the greater tubercleand deltopectoral crest. A, Mayulestes ferox MHNC 1249. B, Prothylacinus patagonicus PU 015700. C, Thylacosmilus atroxFMNH P 14531. D, Lycopsis longirostris UCMP 38061. E, borhyaenoid UCMP 39250. Not to scale.

lessertubercle

delto-pectoral

crestlength

lateralepicondylarcrest

C DA B E

humeral head

greater tuberclebicipital groove

EVOLUTION OF BORHYAENOIDEA 493


Figure 3. General morphology of the manus in various borhyaenoids, focusing on the first metacarpal and associated proximalphalanx, showing the asymmetrical metacarpophalangeal joint. A, Cladosictis patagonica PU 015046 (manus as found inmatrix); proximal phalanx in dorsal and proximal views, Mc I is in dorsal and ventral views. B, Sipalocyon gracilis PU 015154(manus as found in matrix); proximal phalanx in proximal view. C, Lycopsis longirostris UCMP 38061 (association of phalangesis conjectural); proximal phalanx in dorsal, ventral and proximal views, Mc I in dorsal, ventral and distal views. D, Thylacosmi-lus atrox FMNH P 14531 (association of phalanges is conjectural); Mc I in dorsal, ventral and distal views. Not to scale.

Mc I

proximal phalanx

ungual phalanx

I

I

II

II

III

III

IV

IV

VV

V

IV

IV

III

III

II

II

I

I

Mc I unknown

B

innerarticular facet

outer articular facet

proximalphalanx

Mc I

A

C D

transverse axisof proximal epiphysis

transverse axisof distal epiphysis

proximal phalanx unknown

494 C. ARGOT


to the mode of locomotion and substrate used. Some ofthese characters, like the curvature of the posteriorborder of the ulna, the development of the medial epi-condyle and of the lateral epicondylar crest of thehumerus, and the orientation of the ectal facet on thecalcaneum indicate the primary locomotor category(arboreal or terrestrial) that characterizes a taxon(Table 2).

Humeroulnar jointIn extant taxa, the morphology of the humeroulnarregion (Fig. 4) reflects the stability of the elbow joint.In Prothylacinus the humeroulnar joint is poorly sta-bilized compared with Borhyaena, in which thehumeral trochlea is narrower and more concave pos-teriorly, with a medial margin that is more prominentanteroposteriorly as seen in distal view (Fig. 4, top).

This condition suggests arm movements morerestricted to a parasagittal plane in Borhyaena. Seenin distal view, the humeral trochlea is also betterdeveloped anteroposteriorly in Cladosictis than inProthylacinus, which suggests the need for better sta-bilized movements in the former, smaller taxon. Thedistal extremity of the humerus of Lycopsis is poorlypreserved, but the humeral trochlea is shallower thanin Borhyaena, and on the ulna the anconeal process isless prominent anteriorly. In the Palaeocene Mayule-stes, the trochlear notch on the ulna is extremely open,which precludes well-stabilized movements.

Medial epicondyle and lateral epicondylar crest of the humerusThe medial epicondyle is prominent (i.e. the distancebetween the medial lip of the trochlea and the apex of

Figure 4. Distal extremity of the humerus in anterior (top) and distal (middle) views, and ulna (bottom) in lateral view,showing: (1) the presence or absence of the entepicondylar foramen; (2) the protrusion of the medial epicondyle of thehumerus; (3) the curvature of the posterior border of the ulna. A, Mayulestes ferox MHNC 1249. B, Cladosictis patagonicaPU 015702. C, Prothylacinus patagonicus PU 015700. D, Borhyaena tuberata MACN 2074–78 (humerus) and PU 015701(ulna). E, Lycopsis longirostris UCMP 38061. Not to scale.

A B C D E

medial epicondyle capitulum trochlea

entepicondylarforamen



the medial epicondyle represents more than 30% ofthe transverse width of the distal humeral extremity)in Mayulestes, Cladosictis and Prothylacinus (Fig. 4).This distance is reduced in the three borhyaenoidsthat are primarily terrestrial (Borhyaena, Lycopsisand Thylacosmilus). In living taxa, the medial epi-condyle, where the deep flexors of the digits originate,is not prominent in the most terrestrial forms thatexhibit reduced manipulative capabilities of the hand,whatever the group considered (Argot, 2001, 2003b, c).

The entepicondylar foramen is absent in two taxa,Borhyaena and Thylacosmilus. Landry (1958) sug-gested that cursorial and ungulate mammals mighthave lost the entepicondylar foramen in relation toreduced abduction of the humerus. This could fit wellwith its absence in Borhyaena, the most terrestrialborhyaenoid examined (Argot, 2003b) but not inThylacosmilus which apparently had powerfuladductors.

In all borhyaenoids the lateral epicondylar crest iswell-developed. Its length relative to that of thehumerus is unknown for Sipalocyon and Borhyaena,for which there is no complete humerus known. How-ever, the preserved part of the crest of Borhyaena sug-gests that it was relatively reduced compared toProthylacinus. This is consistent with a reduced crestin the most terrestrial living marsupials examined(e.g. Metachirus, Thylacinus). However, a correlationbetween the reduction of the crest and of the flexormass originating from the medial epicondyle is notestablished in all taxa. For example, the crest isextremely well-developed in Thylacosmilus and Proth-ylacinus, whereas the medial epicondyle is much lessprominent in the sabretooth form than in Prothylaci-nus. This could relate to the numerous and antagonistmuscular demands placed upon the crest.

Posterior border of the ulnaA convex posterior border of the ulna (Fig. 4), charac-teristic of Mayulestes, Sipalocyon, Cladosictis and Pro-thylacinus, suggests arboreal capabilities. Asexplained in the study of the forelimb of Mayulestes(Argot, 2001), this condition indicates the combinedaction of the extensors and flexors of the forearm (tri-ceps brachii caput longum, biceps brachii and brachi-alis), while they exert powerful tractions both to flexthe arm to bring the body of the animal closer to thevertical support, and to pull the body up against grav-ity (see also Szalay & Sargis, 2001: 183–184). Astraight or concave posterior border of the ulna ispresent in Lycopsis and Borhyaena withinborhyaenoids as well as in Thylacinus, i.e. in preda-tory mammals that are primarily terrestrial and mayexhibit an incipient cursoriality. The last step, i.e. aposteriorly concave ulna, is achieved in modern canidsand hyaenids (Argot, 2003b).

Orientation of the ectal facet of the calcaneumThis facet (Fig. 5) is orientated medially in Mayulestes(Argot, 2002) and Lycopsis, a condition which suggeststhat in a resting posture the plantar side of the footfaced medially in these two taxa, as when appressedagainst a curved support. In contrast, it is orientateddorsally in Borhyaena, which suggests that in a rest-ing posture the plantar side of the foot lay on a hori-zontal support. The inclination of this facet isintermediate in Sipalocyon and Thylacosmilus.

The orientation of the femoral head, the width of thefemoral condyles and the shape of the tibia denote var-ied mechanical adaptive solutions related to distinctpostures and/or hunting strategies:

Orientation of the femoral headThe femoral head is much more prominent proximallyin Thylacosmilus (Fig. 6I) than in the otherborhyaenoids. A similar orientation is also found inbears and suggests the possibility of erect, semibipe-dal postures while attacking particularly large prey, inorder to allow the predator to encircle the prey’s neckwith its forelimbs (Argot, in press). However, all sabre-tooth forms that are expected to perform similarthroat attacks on large prey do not exhibit a similarorientation of the femoral head (e.g. in Smilodon theorientation of the femoral head and the height of thegreater trochanter are much more similar to a felidpattern: Argot, in press). It seems, therefore, that thepeculiar nature of loading exerted on the hindlimbmusculoskeletal system clearly results in adaptivemodifications within inherited constraints, which aredistinct between Thylacosmilus and Smilodon.

Femoral condylesBoth femoral condyles are approximately equivalentin size in most borhyaenoids, except in Borhyaena inwhich the medial condyle is wider than the lateral one.Although the medial condyle of Mayulestes is poorlypreserved in both femora known, in distal view the lat-eral condyle is wider than the medial one, but the dif-ference is not so emphasized as in didelphids,microbiotheriids and phalangeriformes. In thesegroups, the lateral condyle is approximately twice aswide as the medial one whereas in dasyuromorphs,the condyles are equivalent in width. The relativewidth of the femoral condyles emphasizes the natureof motions that are possible between the thigh and thecrus, and the nature of loading in the knee joint (see inparticular Szalay & Sargis, 2001). Unequal-sized fem-oral condyles reflect the locomotor repertoire of highlyarboreal marsupials, or of marsupials that likely havean arboreal ancestor, like Metachirus within Didel-phidae (Argot, 2002). It is likely that the loading at theknee joint was more similar between Mayulestes and

496 C. ARGOT


Tab

le 2

. Lis

t of

mor

phol

ogic

al p

ostc

ran

ial

char

acte

r st

ate

fou

nd

in B

orh

yaen

oide

a. A

bbre

viat

ion

s: A

Til

, ast

raga

loti

bial

lat

eral

fac

et; A

Tim

, ast

raga

loti

bial

med

ial

face

t; C

, cer

vica

l ve

rteb

ra;

L, l

um

bar

vert

ebra

; T, t

hor

acic

ver

tebr

a

May

ule

stes

fero

xS

ipal

ocyo

ngr

acil

isC

lad

osic

tis

pata

gon

ica

Pro

thyl

acin

us

pata

gon

icu

sB

orh

yaen

atu

bera

taL

ycop

sis

lon

giro

stri

sT

hyl

acos

mil

us

atro

xC

omm

ents

on

char

acte

rs

Axi

al n

eura

l pr

oces

san

tero

post

erio

rly

lon

g?

ante

ropo

ster

iorl

ylo

ng

ante

ropo

ster

iorl

ylo

ng

ante

ropo

ster

iorl

ylo

ng

ante

ropo

ster

iorl

y lo

ng

ante

ropo

ster

iorl

y lo

ng

post

erio

r pro

tru

sion

re

late

d to

po

wer

ful

exte

nso

rs a

nd

rota

tor

of th

e h

ead

Sag

itta

l ve

ntr

al

cres

ts o

n t

he

axis

, C

3, C

4

inci

pien

t on

th

e ax

isst

ron

g an

d pr

omin

ent

stro

ng

and

prom

inen

tst

ron

g an

d pr

omin

ent

stro

ng

and

prom

inen

tst

ron

g an

d pr

omin

ent

stro

ng

and

prom

inen

tpr

otru

sion

rel

ated

to

pow

erfu

l n

eck

flex

ors

Del

tope

ctor

al c

rest

shor

t (d

oes

not

re

ach

th

e la

tera

l ep

icon

dyla

r cr

est)

?lo

ng

lon

g an

d pr

omin

ent

dist

ally

lon

glo

ng

lon

g an

d pr

omin

ent

dist

ally

lon

g in

sert

ion

of t

he

pect

oral

is r

elat

ed

to m

anip

ula

tive

ca

pabi

liti

es

Met

acar

poph

alan

geal

join

t of

th

e po

llex

?as

ymm

etri

cal

and

troc

hle

ar-

shap

ed

asym

met

rica

l an

d tr

och

lear

-sh

aped

??

asym

met

rica

l an

d tr

och

lear

-sh

aped

asym

met

rica

l bu

tn

ot t

roch

lear

-sh

aped

pseu

do-o

ppos

able

po

llex

rel

ated

to

gras

pin

g ab

ilit

y

Med

ial

epic

ondy

le

len

gth

exp

ress

ed a

s a

perc

enta

ge o

f th

e di

stal

hu

mer

us

wid

th

33%

?32

%33

%25

%28

%18

%m

edia

l pr

otru

sion

re

late

d to

pow

erfu

l h

and

flex

ors

and

then

to

gra

spin

g ab

ilit

yL

ater

al e

pico

ndy

lar

cres

t/H

um

eru

s le

ngt

h

33%

?31

%40

%?

32%

33.5

%re

duce

d in

th

e m

ost

terr

estr

ial

taxa

En

tepi

con

dyla

r fo

ram

enpr

esen

tpr

esen

tpr

esen

tpr

esen

tab

sen

tpr

esen

tab

sen

tab

sen

t in

th

e m

ost

terr

estr

ial

taxa

Pos

teri

or b

orde

r of

th

e u

lna

con

vex

con

vex

con

vex

con

vex

stra

igh

tst

raig

ht

?co

nve

x bo

rder

re

late

d to

po

wer

ful

lim

b fl

exor

sO

rien

tati

on o

f th

e ca

lcan

eal

ecta

l fa

cet

med

ial

inte

rmed

iate

inte

rmed

iate

?do

rsal

med

ial

inte

rmed

iate

para

llel

to

the

plan

tar

side

of

the

foot

Ori

enta

tion

of

the

fem

oral

hea

dn

ot p

rom

inen

tpr

oxim

ally

?n

ot p

rom

inen

tpr

oxim

ally

not

pro

min

ent

prox

imal

lyn

ot p

rom

inen

tpr

oxim

ally

not

pro

min

ent

prox

imal

lypr

omin

ent

prox

imal

lypr

oxim

al p

rotr

usi

on

rela

ted

tooc

casi

onal

ere

ct

post

ure

sF

emor

al c

ondy

les

late

ral

con

dyle

w

ider

equ

ival

ent

in

wid

theq

uiv

alen

t in

w

idth

equ

ival

ent

in

wid

thm

edia

l co

ndy

le

wid

er[d

amag

ed]

equ

ival

ent

in w

idth

refl

ects

th

e w

eigh

t lo

adin

g in

th

e kn

ee j

oin

tT

ibia

sh

ape

sigm

oid

?st

raig

ht

stra

igh

t?

stra

igh

tsi

gmoi

dsi

gnifi

can

ce u

ncl

ear



An

ticl

inal

ver

tebr

aL

3 or

L4

?T

?11

T?1

1?

T11

no

anti

clin

alpo

siti

on r

elat

ed t

o th

e fl

exib

ilit

y of

th

e ba

ckF

emor

ofibu

lar

arti

cula

tion

prob

ably

pre

sen

tac

cord

ing

to

late

ral f

emor

al

con

dyle

prob

ably

ab

sen

tac

cord

ing

to l

ater

al

fem

oral

co

ndy

le

?ab

sen

t?

?ab

sen

tpr

esen

ce r

elat

ed t

o la

tera

l w

eigh

tlo

adin

g in

th

e kn

ee j

oin

t

Tib

ioas

trag

alar

joi

nt

shar

p an

gle

betw

een

AT

il

and

AT

im

face

ts

shar

p an

gle

betw

een

A

Til

an

d A

Tim

fac

ets

shar

p an

gle

betw

een

AT

il

and

AT

im

face

ts

shar

p an

gle

betw

een

AT

il

and

AT

im

face

ts

?sh

arp

angl

e be

twee

n

AT

il a

nd

AT

im

face

ts

shar

p an

gle

betw

een

AT

il

and

AT

im f

acet

ssh

arp

angl

e pr

imar

ily

suit

ed

for

flex

ion

-ex

ten

sion

Cal

can

eofi

bula

r fa

cet

pres

ent

pres

ent

[cal

can

eum

da

mag

ed]

?[c

alca

neu

m

dam

aged

]ab

sen

tpr

esen

tpr

esen

ce r

elat

ed t

o la

tera

l w

eigh

t lo

adin

g in

th

e an

kle

Per

onea

l pr

oces

spr

esen

t an

d pr

omin

ent

late

rall

y

pres

ent

but

redu

ced

pres

ent

but

redu

ced

?ab

sen

tab

sen

tpr

esen

t bu

t re

duce

dla

tera

l pr

otru

sion

re

late

d to

in

crea

sed

le

vera

ge o

f th

e M

. pe

ron

eus

lon

gus

Hal

lux

?w

ell- deve

lope

d?

vest

igia

l?

wel

l-de

velo

ped

vest

igia

lgr

aspi

ng

abil

ity

reta

ined

or

lost

Su

pras

pin

ous

foss

atr

ian

gula

r in

ou

tlin

e?

oval

to

quad

ran

gula

rov

al t

o qu

adra

ngu

lar

oval

to

quad

ran

gula

rov

al t

o q

uad

ran

gula

r?

sign

ifica

nce

u

ncl

ear

An

gle

betw

een

sc

apu

lar

spi

ne

and

vert

ebra

l bo

rder

obtu

se (

>90∞

)?

perp

endi

cula

rpe

rpen

dicu

lar

perp

endi

cula

rpe

rpen

dicu

lar

?re

late

d to

rot

ator

y fo

rces

exe

rted

on t

he

scap

ula

Ori

enta

tion

of

the

iliu

mpr

omin

ent

dors

ally

?al

ign

ed w

ith

th

e is

chiu

mal

ign

ed w

ith

th

e is

chiu

m?

alig

ned

wit

h t

he

isch

ium

?si

gnifi

can

ce u

ncl

ear

Ilia

c n

eck

len

gth

16.5

% o

f th

e in

nom

inat

e le

ngt

h

?13

% o

f th

e in

nom

inat

e le

ngt

h

4.5%

of

the

inn

omin

ate

len

gth

?11

% o

f th

e in

nom

inat

e le

ngt

h?

shor

t n

eck

rela

ted

to r

edu

ced

shea

rin

g fo

rces

An

teri

or in

feri

or il

iac

wea

kbr

oad

and

rou

ghbr

oad

and

rou

ghbr

oad

and

rou

ghbr

oad

and

rou

gh[d

amag

ed]

?or

igin

of

M. r

ectu

s fe

mor

is s

pin

eA

ceta

bulu

mov

al i

n o

utl

ine

rou

nde

d in

ou

tlin

ero

un

ded

in

outl

ine

rou

nde

d in

ou

tlin

ero

un

ded

in

outl

ine

[dam

aged

]?

oval

sh

ape

= pr

imit

ive

met

ath

eria

n

patt

ern

Tor

sion

of

the

fem

ur

yes

?n

on

on

oye

sn

osi

gnifi

can

ce u

ncl

ear

Gre

ater

tro

chan

ter

hei

ght

mu

ch h

igh

erth

an t

he

fem

oral

hea

d

?as

hig

h a

sth

e fe

mor

al

hea

d

as h

igh

as

the

fem

oral

h

ead

slig

htl

y h

igh

erth

an t

he

fem

oral

hea

d

as h

igh

as

the

fem

oral

hea

dm

uch

low

erth

an t

he

fem

oral

hea

dpr

obab

ly r

elat

ed t

o th

e sh

ape

and

orie

nta

tion

of

the

glu

teal

fos

saP

rim

ary

loco

mot

or

cate

gory

scan

sori

alpr

obab

ly

scan

sori

alsc

anso

rial

am

bush

ersc

anso

rial

am

bush

erte

rres

tria

l, in

cipi

entl

y cu

rsor

ial

terr

estr

ial

wit

h

reta

ined

gra

spin

g ab

ilit

y

terr

estr

ial

ambu

sher

May

ule

stes

fero

xS

ipal

ocyo

ngr

acil

isC

lad

osic

tis

pata

gon

ica

Pro

thyl

acin

us

pata

gon

icu

sB

orh

yaen

atu

bera

taL

ycop

sis

lon

giro

stri

sT

hyl

acos

mil

us

atro

xC

omm

ents

on

char

acte

rs

498 C. ARGOT


Figure 5. Calcaneum in dorsal (top) and anterior (bottom) views, showing the orientation of the ectal facet (arrowed).Abbreviations: CaA, calcaneoastragalar facet; CaCu, calcaneocuboid facet; CaFi, calcaneofibular facet; Su, sustentacularfacet. A, Mayulestes ferox MHNC 1249. B, Lycopsis longirostris UCMP 38061. C, Sipalocyon gracilis PU 015154. D, Thy-lacosmilus atrox FMNH P 14344. E, Borhyaena tuberata MACN 2074–78. Not to scale.

EDCBA

orientation of the ectal facet

Su Su

Su

CaA

Su

peronealprocess

peroneal process

CaFiCaFi

CaFi

CaA CaA

CaA

probable attachmentof a calcaneocuboidligament

CaCuCaCu

living arboreal forms than between Mayulestes andyounger borhyaenoids, especially Borhyaena in whichthe wide medial condyle suggests a medial displace-ment of the load line and more parasagittal move-ments of the crus.

Shape of the tibiaIn borhyaenoids, only Mayulestes and Thylacosmilushave a sigmoid tibia (Fig. 7A, D). A peculiar sigmoidcurvature characterizes the tibia of didelphids, micro-biotheriids and caenolestids. This condition probablyrepresents a primitive therian or pretherian featureand this curvature is not likely to be reliably indica-tive of functional attributes that can be related to sub-strate preference or locomotor mode (Szalay & Sargis,2001: 166, 206–209). Moreover, a relation between asigmoid tibia and asymmetrical femoral condyles can-not be ascertained. For example, Thylacosmilus andThylacinus exhibit a sigmoid tibia with femoralcondyles subequal in width, whereas in the smallMayulestes the sigmoid tibia is associated with aslightly wider lateral condyle.

The position of the anticlinal vertebra, the presence/absence of a femorofibular contact, the tibioastragalarjoint, the development of the calcaneofibular facet, ofthe peroneal process and of the first metatarsalappear to be related both to the locomotion and to theevolutionary history of Borhyaenoidea. For these char-acters, the case of Mayulestes and other Tiupampanmetatherians is therefore of particular importance, inorder to determine the ancestral state of thesefeatures.

Anticlinal vertebraThe anticlinal vertebra is L3 or L4 in Mayulestes. It islikely to be an ancestral retention, as it is L2 in thetwo other Tiupampan metatherians, Pucadelphys andAndinodelphys (Muizon & Argot, 2003), whereas it is athoracic vertebra in Miocene borhyaenoids, T?11 inCladosictis and Prothylacinus, and T11 in Lycopsis.The anticlinal is unknown in Sipalocyon. InBorhyaena, this condition is unclear because of thepoorly preserved axial skeleton, but the orientation oflumbar neural processes suggests that the anticlinalwas a lumbar vertebra (Argot, 2003b). The two lastlumbars are known for Thylacosmilus, and their ver-tical neural processes suggests that there was no anti-clinal vertebra in this taxon, as in Smilodon (Argot, inpress). The flexibility of the lower back of the twosabretooth taxa appears to be noticeably less than intheir closer relatives. In the lumbar and posterior tho-racic regions, the M. longissimus dorsi (the most pow-erful extensor of the back) originates by powerfultendons either from the apex of neural processes(which are then usually inclined anteriorly), or morelaterally, from the mammillary processes. In this lat-ter case, the neural processes usually stand vertical(Argot, 2003a). The forces generated by these symmet-rical muscular attachments primarily act to stretch orstabilize the vertebral column (Shapiro & Jungers,1994), but also contribute substantially to body pro-pulsion by additive sagittal spine movements allowedby thin and strongly inclined neural processes (Schill-ing & Fischer, 1999). Therefore, the position of theanticlinal vertebra and the inclination of the posteriorneural processes is related to the flexibility of theback.



Femorofibular articulationThe fibula exhibits a broad and distinct articular facetwith the femur in didelphids, phalangeriformes andmicrobiotheriids. By comparison, this facet is reducedin dasyuromorphs. In Mayulestes, the lateral expan-sion of the lateral femoral condyle suggests a femoro-fibular contact in contrast to Sipalocyon, although inthe latter taxon the fibular head is prominent proxi-mally. In Cladosictis and Lycopis, a potential contactbetween the two bones cannot be ascertained becauseof their poor state of preservation. However, the fibu-lar head of Cladosictis, Sipalocyon and Lycopsis is

more prominent proximally than in Prothylacinus andThylacosmilus. The absence of femorofibular articula-tion as observed in Prothylacinus and Thylacosmilus(Fig. 7B, D) is likely to be a derived feature amongmetatherians (Haines, 1942; Barnett & Napier, 1953;Szalay, 1994).

Tibioastragalar jointA sharp angle between the lateral and medial astraga-lotibial facets is observed in all borhyaenoids, in Puca-delphys and in various Palaeogene Itaboraian taxa

Figure 6. Innominate in lateral right view and proximal extremity of the femur in anterior view in various borhyaenoids,showing: (1) on the innominate, the general shape and orientation of the ilium, and the development of the anterior inferioriliac spine; (2) on the femur, the height of the greater trochanter and the orientation of the femoral head. A, E, Mayulestesferox MHNC 1249. B, F, Cladosictis patagonica PU 015702. C, J, Lycopsis longirostris UCMP 38061. D, G, Prothylacinuspatagonicus PU 015700. H, Borhyaena tuberata PU 015701. I, Thylacosmilus atrox FMNH P 14531. Not to scale.

iliumprominentdorsally

A

B

C

D

acetabulumantero-inferior iliac spine(m. rectus femoris origin)

iliacus fossa

iliacblade

I

gluteal fossashort iliac neck

greater trochanter

F

HG

J

L6

E

500 C. ARGOT


(Szalay, 1994). As emphasized by Szalay (1994: 329)this pattern is primarily suited for flexion-extensionrather than abduction and inversion and therefore,the tibioastragalar joint of borhyaenoids is anatomi-cally more severely constrained than in many livingmarsupials like didelphids, phalangeriformes andmicrobiotheriids. A perpendicular angle between themedial and lateral astragalotibial facets, present in allthe borhyaenoids examined whatever the adaptivefeatures of the other parts of the skeleton, may repre-sent a minor modification of an ancestral metatheriancondition (Szalay, 1994).

More recently, Szalay & Sargis (2001: 203) sug-gested that a narrow astragalotibial lateral facetbordered by a sharply angled astragalotibial medialfacet (which reflects the exceptionally deep tibialmedial malleolus), a narrow astragalofibular facet, ahuge astragalar medial plantar tuberosity (ampt),and a proximodistally long sustentacular facetextending dorsal to this ampt together represent theprimitive sudameridelphian pattern. This patterncan be observed in all borhyaenoids despite thealteration of surrounding elements, especially modi-fications to the calcaneoastragalar articulation (par-ticularly to the orientation of the ectal facet), or tothe orientation of the tibial malleolus, which inMayulestes exhibits a torsion relative to the proxi-mal epiphysis (Muizon, 1998; Argot, 2002). This fea-

ture is unknown in the other borhyaenoids forwhich a complete tibia is known (Cladosictis, Proth-ylacinus, Lycopsis, Thylacosmilus). This conditionmight be related to the capability to invert andevert the foot in Mayulestes, which is consistentwith the orientation of the ectal facet of the calca-neum and suggests the ability to walk on irregularsupports.

Calcaneofibular facetIn borhyaenoids, the calcaneofibular contact is exten-sive in Sipalocyon and Thylacosmilus (Fig. 5C, D) andconsidered an ancestral therian condition (Szalay,1994: 209). However, this may represent a secondarilyextended contact, since in the oldest borhyaenoidknown, Mayulestes, the calcaneofibular facet issmaller than in Sipalocyon. Despite the absence offemoro-fibular contact in Thylacosmilus, the wide cal-caneofibular facet suggests that the fibula in thistaxon is still distally a weight-bearer of importance. InProthylacinus, the calcaneum is unknown. The pres-ervation of the calcaneoastragalar facet in Borhyaenaand Cladosictis does not allow us to know if there isalso a calcaneofibular facet. In Lycopsis, althoughslightly damaged, the general shape of the calcaneoas-tragalar facet does not suggest the presence of a cal-caneofibular facet.

Figure 7. Tibia and fibula, underlining the general shape of the tibia. A, Mayulestes ferox MHNC 1249. B, Prothylacinuspatagonicus PU 015700. C, Lycopsis longirostris UCMP 38061. D, Thylacosmilus atrox FMNH P 14344. Not to scale.

A B C

deep tibial malleolus

D

fibula

no femoro-fibularcontact

convexmedialside



Peroneal processIn many Palaeogene taxa, the peroneal process (Fig. 5)is well-developed (Szalay, 1994: 199), and so it is inPucadelphys and Mayulestes. In the otherborhyaenoids this process is reduced compared withMayulestes. In Lycopsis and Borhyaena no process isobservable, in contrast to Sipalocyon in which it isreduced but present. In Prothylacinus, the calcaneumis unknown. The reduction of the peroneal process is acommon event which occurred at least two or threetimes in the Metatheria (Szalay, 1994: 345). Function-ally, a laterally extended peroneal process potentiallyincreases the leverage of the M. peroneus longus, anabductor of the hallux.

HalluxA powerful grasping hind foot with a widely divergenthallux (Fig. 8) characterizes both the didelphid-micro-biotheriid and the primitive syndactylan patterns(Szalay, 1994). The reduction of the hallux appears inboth dasyuromorphs and borhyaenoids. This is aderived pattern in both cases, the taxa characterizedby a vestigial (or absent) hallux being closely relatedto those that exhibit a normally developed Mt I. This isthe case in Dasyuridae (all the Dasyurus species donot have a reduced hallux), and in borhyaenoids: theMt I of Sipalocyon and Lycopsis is fully developed, incontrast to that of Prothylacinus and Thylacosmilus,where it is vestigial. However, the development of thefirst metatarsal does not appear to be correlated withthat of the peroneal process, which is prominent inSipalocyon but not in Lycopsis.

The postcranial skeleton of Mayulestes appears to bedifferent from that of the Miocene taxa especially atthe level of the pectoral and pelvic girdles (Figs 6, 9):

Development of the supraspinous fossaIn three Santacrucian borhyaenoids (Cladosictis,Borhyaena and Prothylacinus) and in Lycopsis thesupraspinous fossa (Fig. 9) is roughly rectangular inoutline, the anterior border joining the scapular neckat a right angle to the scapular spine. In contrast, inMayulestes this fossa is subtriangular and the ante-rior border does not join the scapular neck at such anextreme angle. The functional significance of thesupraspinous fossa outline is unclear and, according toanatomical data on modern didelphids, cannot bedirectly related to the development of the M.supraspinatus.

Angle between the scapular spine and the vertebral border and posterior extension of the caudal angleThe angle between the scapular spine and the verte-bral border (Fig. 9), which represents the relative ori-entation of the lever arms of Mm. trapezius and

serratus anterior, affects the efficiency of the scapulain bearing rotatory and tensile forces (Oxnard, 1963,1968). It is therefore related to substrate preference.In Mayulestes (Fig. 9C), this angle is obtuse (100–110 ∞), i.e. when the spine is orientated vertically, thehighest point of the scapula is located at the postero-dorsal angle of the infraspinous fossa. This conditionis usually related to a posteriorly extended caudalangle. It clearly differs from that of the Mioceneborhyaenoids, in which the scapular spine and the ver-tebral border are approximately perpendicular. Inthese taxa, as well as in the modern taxa Thylacinusand Metachirus, the caudal angle is not extended pos-teriorly. An obtuse angle between the scapular spineand the vertebral border and a posteriorly extendedcaudal angle are found in arboreal and fossorial taxa(Maynard Smith & Savage, 1956; Roberts, 1974),whereas a more quadrangular scapula is found in ter-restrial to cursorial taxa (Jolly, 1967; Taylor, 1974).

The particular shape of the scapula of Mayulestes isnot found in the other borhyaenoids, or in the two otherTiupampan metatherians known from postcranialskeletons, Pucadelphys and Andinodelphys (Muizon &Argot, 2003). It probably represents an early special-ization that reflects arboreal habits. It is more similarin outline to the scapula of arboreal primates (such aslemurs) than to that of Miocene borhyaenoids, and isconsistent with the posteriorly convex ulna and wideopen trochlear notch that also indicates clear arborealcapabilities (Muizon, 1998; Argot, 2001).

Orientation of the ilium relative to the ischiumIn all the borhyaenoids in which the pelvis is known(i.e. Mayulestes, Cladosictis, Prothylacinus and Lycop-sis), the ilium is quadrangular in outline. The glutealfossa is broad and orientated laterally, whereas theiliac fossa is reduced to a narrow ventral strip, in con-trast to what is observed in most living marsupials.However, the ilium of Thylacinus and Metachirus isalso quadrangular, quite similar to that observed inborhyaenoids. Within Borhyaenoidea, whereas theilium and ischium are aligned in Cladosictis, Prothy-lacinus and Lycopsis, the ilium protrudes dorsallyabove the dorsal ramus of the ischium in Mayulestes(Fig. 6A), and the functional significance of this fea-ture is unclear. Unfortunately, the left part of the pel-vis and the sacrum are unknown in Mayulestes, whichprecludes the accurate orientation of the pelvic girdle.

Iliac neck lengthThe iliac neck is variable within Borhyaenoidea. It ismuch longer in Mayulestes (16.5% of the totalinnominate length) than in Prothylacinus (4%); it isintermediate in Cladosictis and Lycopsis (11–13%)(Fig. 6). A short iliac neck may be related to the sta-bility of the pelvic girdle and to the reduction of

502 C. ARGOT


shearing forces exerted on the ilium (Davis, 1964).Its potential relation to the orientation of the iliumis unclear.

Anterior inferior iliac spineThis spine is extremely well-developed in all Mioceneborhyaenoids (Fig. 6). The prominent and rugose scar,

where the M. rectus femoris (the biarticular head ofthe quadriceps) originates, is approximately as long asthe iliac neck in the genera where it can be observed(i.e. the four Santacrucian taxa). The innominate ofThylacosmilus is unknown, and it is very damaged inLycopsis. By contrast, this spine is very weak in thePalaeocene Mayulestes. Functionally, the developmentof a prominent scar in living macroscelidids that

Figure 8. General morphology of the pes in various borhyaenoids, showing the variable development of the first meta-tarsal. Abbreviations: As, astragalus; Ca, calcaneum; Cu, cuboid; Ec, ectocuneiform; En, entocuneiform; Mc, mesocunei-form; Mt I, first metatarsal; Mt III, third metatarsal; Na, navicular. A, Cladosictis patagonica PU 015046. B, Sipalocyongracilis PU 015154. C, Prothylacinus patagonicus PU 015700. D, Lycopsis longirostris UCMP 38061. E, Thylacosmilus atroxFMNH P 14344. Not to scale.

EnMc

Na

Ca

Cu

EcNa

McEn Ec

Cu

Ca

As

As

Na

En

Mc

EcCu

CBA

Mt I

Mt I

Mt I

Mt I

Mt III

vestigial

vestigial

E

I

II

IIIIV

V

D

articulation with Mt I

En



exhibit jumping ability suggests a relationshipbetween this tuberosity and the role of the rectus fem-oris in the type of locomotion performed. However, thepotentially different role of this muscle inborhyaenoids compared to living placental Carnivora(where the spine is reduced compared with the fossils)is unclear.

AcetabulumIn Mayulestes the acetabulum is oval in outline andthe articular facet is strongly constricted at the ilio-ischial suture. The dorsal margin is concave in dorsalview and the anterior part of the articular facet pro-trudes laterally. This condition is more similar to thatobserved in the living Australian marsupials than in

Figure 9. Scapula in lateral view showing variations in the shape of the supraspinous fossa and in the angle between thescapular spine and the vertebral border. A, Borhyaena tuberata PU 015701. B, Lycopsis longirostris UCMP 38061. C, May-ulestes ferox MHNC 1249. D, Prothylacinus patagonicus PU 015700. E, Cladosictis patagonica PU 015170. The scapularspine is broken and the acromion in unknown in all specimens except Mayulestes. Not to scale.

A B C

triangularsupraspinousfossa

angle betweenthe scapular spineand the vertebral border

D E

scapular notch

504 C. ARGOT


the Miocene borhyaenoids. This morphology alsoclearly indicates that Mayulestes was not as adaptedto leaping as various modern marsupials [e.g.Metachirus, Antechinomys, Perameles, or the livingcaenolestids (Szalay & Sargis, 2001)]. The morphologyobserved in Mayulestes, as well as in Pucadelphys,may reflect an ancestral condition. In the Miocenetaxa, the articular facet is more rounded in outlineand is not constricted at the ilio-ischial suture.

Torsion of the femurIn Mayulestes and Lycopsis the femur is twistedmediolaterally along its proximodistal axis, so that thehead projects anteromedially rather than medially rel-ative to the distal femur. The transverse axes of bothepiphyses form an angle of 30–40∞, whereas they areparallel in the other borhyaenoids. Among living mar-supials, a torsion is also found in Sarcophilus and Thy-lacinus. The functional significance of this torsion isunclear. It might be related to the orientation of theacetabulum, but the acetabulum of Lycopsis is toopoorly preserved to be compared with that of Mayule-stes (in which the position of the acetabulum relativeto the vertebral column is unknown).

Greater trochanter heightThe greater trochanter (Fig. 6) is clearly higher thanthe femoral head in Mayulestes, whereas it is partic-ularly low in Thylacosmilus (Argot, in press). Thischaracter intergrades in the other borhyaenoids, sinceit is slightly higher in Borhyaena, as high as the fem-oral head in Lycopsis, as high or slightly lower in Pro-thylacinus and Cladosictis. A low greater trochanter isalso present in ursids and hyaenids and might berelated to the shape and orientation of the glutealfossa. However, the absence of innominate in Thylaco-smilus, as well as the uncertain orientation of theinnominate in Mayulestes relative to the vertebral col-umn do not allow a test of this hypothesis.

Therefore, it seems that a peculiar association ofcharacters - a long axial neural process; strong ven-tral processes on the axis, C3 and C4; a long andstrong deltopectoral crest; a well-developed lateralepicondylar crest; a pseudo-opposable pollex; a tibio-astragalar joint medially constrained; a long tail witha muscular base; an intermembral index (humerus +radius + McIII length/femur + tibia + MtIII length)between 75 and 78% - represents a pattern common toall Borhyaenoidea (Table 2). However, each taxonexamined evolved characteristic specializations. May-ulestes and Cladosictis, characterized by arborealadaptive traits, probably occupied a civet-like eco-morph. Prothylacinus and Thylacosmilus were likelyambush predators, the former also exhibiting distinct

arboreal adaptive traits. Lycopsis and Borhyaena weremore terrestrial predators. However, some featurescharacterizing Lycopsis (the pseudo-opposable pollex,the nonreduced hallux, the short metatarsals and thepoorly stabilized calcaneoastragalar joint) indicatethat the animal was not a fast runner, suggesting thatit inhabited a densely forested environment. By con-trast, Borhyaena reveals a more specialized changetowards a cursorial pattern. The morphology of thegirdles appears to be variable within Borhyaenoidea,especially between Mayulestes and the laterborhyaenoids. The specializations of Mayulestes areconsistent with the hypothesis that the Tiupampanmetatherians had already experienced some endemicevolution on the South American continent (Pascual &Ortiz Jaureguizar, 1991, 1992; Muizon, 1992; Muizon& Cifelli, 2001).

PALAEOBIOLOGY AND EVOLUTION OF LOCOMOTION

Borhyaenoids with postcranial remains are knownfrom four places: (1) Tiupampa, early Palaeocene,south-central Bolivia (Mayulestes ferox); (2) SantaCruz Formation, end of early Miocene, Patagonia,Argentina (Sipalocyon gracilis, Cladosictis patagon-ica, Prothylacinus patagonicus and Borhyaena tuber-ata); (3) La Venta, middle Miocene, Colombia (Lycopsislongirostris); (4) Andalgalá and Corral Quemado For-mations, late Miocene, north-western Argentina (Thy-lacosmilus atrox). Habitat characteristics aresummarized for each place and the diet and huntingbehaviour of the borhyaenoid taxa are discussed.

HABITAT

The Tiupampa beds were deposited in channels of alarge meandering river on a flat alluvial flood plain(Marshall et al., 1995). In addition to mammals, theyhave yielded abundant remains of frogs, turtles,snakes and crocodiles: Amphibia (Anura, Gym-nophiona), Reptilia [Chelonia, Squamata (Lacertiliaand Ophidia) and Crocodilia] (Muizon, 1998). Thepresence of several taxa of crocodiles attests to a warmand moist climate, probably subtropical and relativelyequable (Pascual & Ortiz Jaureguizar, 1990). The lateCretaceous-early Cenozoic interval was dominated bywarm, humid tropical-temperate forested environ-ments throughout South America (Flynn & Wyss,1998).

Sedimentological, palaeopedological and vertebratepalaeontological studies undertaken at Monte Obser-vación indicate that the Santa Cruz sediments weredeposited under warm, humid conditions, reflecting atemperate to subtropical coastal alluvial plain (Bown



& Fleagle, 1993; Genize & Bown, 1994). Most of themammals recorded (porcupines, echimyids, dasyproc-tids, anteaters and primates: see Table 3) also suggesta mild climate and a forested milieu (Patterson & Pas-cual, 1968). However, invertebrate fossil remains andtraces have been found in the Santa Cruz Formation(termite nests, scarabeid brood masses and cells pro-duced by digging bees) and indicate relatively openareas (Genize & Bown, 1994).

A preliminary palaeoecological interpretation of theSanta Cruz Formation, based on the analysis of 22 fos-siliferous horizons located between the Río Gallegosand the Río Coyle, notes six main trends between thelower and the upper horizons (Tauber, 1997): (1) a gen-eral decrease in taxonomic diversity; (2) a decrease indiversity within small-sized taxa (<500 g); (3) adecrease in the number of large taxa like Homalodo-therium and Theosodon; (4) a reduction of the mega-theriid and megalonychid average body size; (5) anincrease in taxonomic diversity of the glyptodonts andtoxodonts (which were supposedly grazers), and (6) anincrease in the number of taxa with euhypsodont teeth.

These elements suggest a shift in the climate as awarm and moist climate and a forested milieu transi-tioned to a drier climate with more open conditions(Tauber, 1997). To a very large extent, the Santa Cruzbeds are made up of volcanic and detrital materialderived from the rising Andes to the west, superim-posed on marine Patagonian deposits (Scott, 1932;Marshall et al. 1983). It appears likely that stochasticcatastrophic reductions in population size, with localand regional extinctions resulting from rapid pyro-clastic deposition, profoundly influenced the course ofmammalian evolution in this area (Bown & Fleagle,1993).

In the middle Miocene, the area of northern Ecua-dor, central and western Colombia, and western Ven-ezuela formed a peninsula, without land connectionwith Central America, and bordered on the south by aseaway extending into the upper Amazon basin (Kay& Madden, 1997: fig. 30.1). The La Venta area was sit-uated on the eastern lowland region of that peninsula,several hundred kilometres from the upper Amazonseaway. Like Tiupampa, this area was characterizedby a meandering system of flood plains. There is evi-dence for periodic flooding and for extensive evergreenrain forest cover, in relation to the high percentage ofarboreal species found (presence of forest-dwellingmarsupials, bats, lizards, and birds like gruiforms,pelecaniforms, and coraciiforms, whose modern ana-logues occur in fluvial wetlands, wooded swamps andfreshwater marshes: Rasmussen, 1997). The diversefreshwater fish fauna discovered indicates a heteroge-neous aquatic environment, including large and openrivers, marginal shallow waters, and even anoxic, tem-porary waters, i.e. a mosaic of biotopes typical of mod-

ern lowland meandering stream systems (Kay &Madden, 1997). The annual rainfall may have been atleast 2000 mm per year, and the environment wasmore probably a forest mosaic than an interruptedmultistratal evergreen forest (Kay & Madden, 1997).

Unfortunately, the composition of the flora ofMiocene tropical South America is still poorly under-stood. In Africa, open clearings are maintained withinforests by the destructive habits of tuskedmegaherbivores. Four large mammals of the LaVenta community (Huilatherium, Pericotoxodon,Xenastrapotherium and Granastrapotherium) hadtusks, and may have helped in creating and maintain-ing edge habitats within the forests (Kay & Madden,1997). Overall species diversity in the Monkey beds(the lowest part of the Villavieja Formation) is compa-rable to that of modern Neotropical South Americancommunities despite profound differences in taxo-nomic and palaeoecological composition. For example,the La Venta fauna includes endemic ungulates,sloths, and caviomorph rodents vs. hypsodont artio-dactyls, sciurid and murid rodents today (Flynn &Wyss, 1998).

The two specimens of Thylacosmilus atrox knownfrom postcranial remains have been found in the lateTertiary beds in and around the Santa María Valley ofthe Province of Catamarca, north-western Argentina(Riggs, 1934). They come from two different localities,the Corral Quemado and Andalgalá Formations,which are considered to be Huayquerian in age (i.e. c.6.8–9 Myr old) (Flynn & Swisher, 1995). This ageforms a part of the ‘Panaraucanian Faunistic Cycle’ ofArgentina divided into the Protoaraucanian subcycle(Friasian + Chasicoan) and the Araucanian subcycle(Huayquerian + Montehermosan) (Pascual, 1989; Pas-cual & Ortiz Jaureguizar, 1990). During the Pro-toaraucanian subcycle, most of the precedingmammalian taxa suggesting subtropical woodlands(e.g. platyrrhines, stegotheriine armadillos, palaeoth-entid and abderitid caenolestoid marsupials, echimyidand erethizontid rodents, and most of the tree-dwell-ing edentates) became rare or absent in Patagonia(Pascual & Ortiz Jaureguizar, 1990).

The Araucanian subcycle is predominantly charac-terized by cursorial and/or grazing mammals. There isa progressive increase of the high-crowned ungulates,the armoured xenarthrans (armadillos, pampatheresand glyptodonts) experience the greatest diversifica-tion ever recorded, and specialized lineages withinsome rodent families (Dinomyidae, Hydrochoeridae)develop the largest and most cursorial rodents everknown (Pascual & Ortiz Jaureguizar, 1990). Also, thepresence of Argyrolagidae, a peculiar lineage of rico-chetal marsupials, provides one more indication ofopen habitats (Pascual & Ortiz Jaureguizar, 1990).The fauna therefore suggests predominant savannah-

506 C. ARGOT


like environments. These widespread and variedplains have been distinguished as ‘la edad de las plani-cies australes’, the age of southern plains (Pascual &Ortiz Jaureguizar, 1990; Ortiz Jaureguizar, 1998).

DIET AND HUNTING BEHAVIOUR

Four questions may therefore be asked (paraphrasingVan Valkenburgh, 1985):

(1) How many species of predators coexisted withineach community?

(2) What was the array of prey available?(3) What is the diversity of locomotor morphologies

that evolved within predators (i.e. how many arborealand scansorial species, ambush and pursuit hunters,etc.)?

(4) How similar in morphology are the predatorsto each other (i.e. what is the potential for nicheoverlap)?

Contemporaneous borhyaenoids are expected to differin behaviour, body size, and/or structural morphology.However, the two last questions will be examined onlyin the case of the Santa Cruz fauna that includes fourtaxa known from postcranial remains, whereas asingle taxon is known from the three other localities(Tiupampa, La Venta and Catamarca province).

Mayulestes feroxAccording to the taphonomy, only marsupials couldhave played the role of mammalian predators in Tiu-pampa (Table 1), and the two largest metatherianswere the borhyaenoids Mayulestes and Allqokirus (thelatter being probably as large as Mayulestes and car-nivorous too, but this taxon is poorly known). Thehindlimb of Mayulestes exhibits numerous differencescompared with that of arboreal living marsupials(didelphids and phalangeriforms), such as a greatertrochanter higher than the femoral head, a femoraltrochlea well-defined between sharper ridges, and ahigher femorometatarsal index, all features suggest-ing a faster locomotion than that practised by extanthighly arboreal marsupials, which fits well with activehunting strategies (Argot, 2002).

Mayulestes, as a predator, could have fed upon theabundant fauna of small insectivorous marsupialslisted in Table 1, except Andinodelphys (relativelylarger than the other forms although slightly smallerthan Mayulestes). Muizon (1998) also suggested thatomnivorous small mioclaenids like Tiuclaenus, Molin-odus or Pucanodus could have represented occasionalprey, as well as some Amphibia, like the leptodactylidfrog Estesius. It is also likely that Mayulestes couldhave fed upon eggs of crocodiles, turtles or birds. Itwas probably hunting the small condylarths and mar-supials on the ground, but was clearly able to climb

tree for resting, foraging for eggs or nesting birds, pur-suing some prey, or escaping its own predators such ascrocodiles.

Sipalocyon gracilis, Cladosictis patagonica, Prothylacinus patagonicus, Borhyaena tuberataIn sympatry, closely related species often differ mor-phologically in regard to features that reflect diet, for-aging strategy, or life history. The extent of suchdifferences is usually ascribed to the intensity of com-petition and predation and/or to the levels of foodresources and environmental stability (Van Valken-burgh, 1985; Wayne et al., 1989).

The Santacrucian mammalian fauna, one of themost diverse and rich vertebrate fossil assemblages inSouth America (Table 3), is characterized by variouselements: (1) the predominance and diversity ofrodents (exclusively Hystricognatha) and edentates(especially Tardigrada); (2) the quantity of smallrodent- and rabbit-like notoungulates, Hegetotheri-idae and Interatheriidae; (3) the first and last recordof the enigmatic burrowing Necrolestes; (4) the lastrecord of platyrrhine monkeys in Patagonia (Homun-culus patagonicus in coastal deposits); (5) the lastrecord of the poorly known litoptern family Adi-anthidae, and (6) the last occurrence of the notoungu-late family Notohippidae (Marshall et al., 1983).

Cladosictis was a short-legged predatory form. Theshoulder height was about 20–25 cm, and the bodymass is estimated at 4–8 kg (Argot, 2003c; see alsoFig. 10B). The proportions of the limbs recall those ofthe living South American tayra (Eira barbara),although Cladosictis had shorter legs than this mus-telid. The pseudo-opposable pollex, also found inSipalocyon, suggests skilful manipulative behaviour.Cladosictis was probably able to climb and certainlyspecialized more in taking smaller prey, arboreal orterrestrial (small mammals, reptiles, amphibians,invertebrates, eggs and birds) than Prothylacinus.Although Cladosictis exhibits the dental complexrelated to a carnivorous or hypercarnivorous diet(details in Muizon, 1999: 502), hathlyacynines are con-sidered to have a more generalized dentition than pro-thylacinids or borhyaenids (Marshall, 1981), whichmay ensure flexibility of food habits, as in extantomnivorous-carnivorous small canids.

Prothylacinus (Fig. 10D) was the size of a wolverine,weighing about 30 kg (Argot, 2003b). The forelimbemphasizes arboreal adaptations, while the hindquar-ters are powerfully built (especially the thighs), andthe axial skeleton is flexible. Prothylacinus was notdesigned for speed, relying instead on its ability toperform powerful jumps from a crouched position(Argot, 2003b). It appears to have been a much moretypical ambush predator than the other Santacrucian



borhyaenoids. This hunting strategy (the predatorlying still watching its prey move past, and running ashort distance towards it) involves taking advantageof a covered habitat (Kruuk & Turner, 1967). The com-bination of stout pelvis, long femur and short meta-tarsals probably improves the mechanical advantageof muscles stabilizing the trunk and hindlimbs whilethe forelimbs are working against some resistance,such as struggling prey. It is also known that pouncerson rodent-sized prey have large thigh muscles, whichdo most of the work in stride acceleration and take-off(Alexander, 1993).

The manipulative ability of its forearms also sug-gests ability to execute skilful attacks on small mam-

mals and birds. Moreover, the powerful musculature ofthe limbs and neck of Prothylacinus suggests that itmight have been able to drag larger prey to a safeplace, far from the large ground-dwelling borhyaenidslike Borhyaena or Arctodictis. The curved, dorsoven-trally deep claws probably functioned for graspingprey as well as for climbing. A study of extant jaguarsin Belize revealed that Dasypus (armadillo), Agouti(paca), and Mazama (brocket deer) account for 94% ofthe available terrestrial prey, with just over half (54%)of the identified prey consisting of armadillos(Rabinowitz & Nottingham, 1986). According to theseauthors, the armadillo is a particularly vulnerableprey species, due to its limited mobility, lack of effi-

Table 3. Generic list of Santacrucian mammals (coastal beds) from Patagonia, Argentina (from Scott, 1903a, 1903b, 1904,1905; Patterson & Pascual, 1968; Marshall, 1978a, 1979, 1981; Marshall et al., 1983; Bown & Fleagle, 1993; Rae et al., 1996;Fleagle et al., 1997; McKenna & Bell, 1997)

TRIBOSPHENIDA XENARTHRA LITOPTERNA RODENTIANecrolestidae Dasypodidae Proterotheriidae OctodontidaeNecrolestes Anantiosodon Diadiaphorus Acaremys

Peltecoelus Licaphrium SciamysPeltephilus Prothoatherium Echimyidae

GONDWANADELPHIA Stegotherium Proterotherium AdelphomysMICROBIOTHERIA Proeutatus Thoatherium StichomysMicrobiotheriidae Paraeutatus Macraucheniidae SpaniomysMicrobiotherium Prozaedyus Theosodon Chinchillidae

Stenotatus Adianthidae PliolagostomusDIDELPHIDA Vetelia Adianthus Prolagostomus

SUDAMERIDELPHIA Glyptodontidae NeoepiblemidaePolydolopimorphia Asterostemma ASTRAPOTHERIA PerimysParabderites Cochlops Astrapotheriidae Dasyproctidae

Sparassodonta Eucinepeltus Astrapotherium NeoreomysBorhyaenoidea Metopotoxus DinomyidaePseudonotictis Propalaehoplophorus NOTOUNGULATA OlenopsisPerathereutes Family incertae sedis Toxodontidae ScleromysSipalocyon Hapalops Adinotherium EocardiidaeCladosictis Eucholoeops Nesodon EocardiaAnatherium Planops Hyperotoxodon LuantusProthylacinus Megatheriidae Homalodotheriidae PhanomysLycopsis Prepotherium Homalodotherium SchistomysArctodictis Analcimorphus Notohippidae ErethizontidaeBorhyaena Hyperleptus Notohippus SteiromysAcrocyon Pelecyodon Interatheriidae

GLIRIMETATHERIA Schismotherium Epipatriarchus PRIMATESPaucituberculata Nothrotheriidae Interatherium PlatyrrhiniCaenolestoidea Xyophorus Protypotherium HomunculusStilotherium Megalonychidae HegetotheriidaePhonocdromus Megalonychotherium HegetotheriumPichipilus Mylodontoidea PachyrukhosAbderites AnalcitheriumPalaeothentes NematheriumTitanothentes MyrmecophagidaeAcdestis ProtamanduaPropalaeothentes

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cient defences, and muffled grunting that accompaniesits nocturnal foraging. Therefore, it seems clear thatapart from rodents, caenolestoids and some notoungu-lates, armadillos and semiarboreal sloths like Hapa-lops could have represented prey species forProthylacinus.

In the Santacrucian borhyaenoid radiation,Borhyaena (Fig. 10E) differs in having forelimb move-ments that were more restricted to a parasagittalplane, relatively reduced distal muscular mass of thelimb, restricted pronation-supination capabilities,and a digitigrade manus with relatively elongatemetacarpals, short phalanges, and blunt claws (Argot,2003b). Moreover, Stein & Casinos (1997) developedthe idea of an asynchrony in the evolution of the mam-

malian girdles: the mammalian pelvis would haveevolved cursorial features earlier than the therianscapula, cursoriality being related primarily to theadduction of the hindlimb. In this context, it is note-worthy that the hip joint of Prothylacinus retainsmore abductive capability than that of Borhyaena, acondition which is consistent with climbing behaviourthat requires a greater abductive range at the hip jointthan in runners. Moreover, the medial femoral condyleof Borhyaena, which is larger than the lateral one,suggests a medial displacement of the load line, per-haps reflecting a less abducted position of the femur inan obligate terrestrial animal.

Considering these structural modifications,Borhyaena may be qualified as the most cursorial

Figure 10. Skeletal reconstructions of various borhyaenoids. A, Mayulestes ferox, modified from Muizon (1998). B, Cla-dosictis patagonica. C, Lycopsis longirostris, modified from Marshall (1977a). D, Prothylacinus patagonicus. E, Borhyaenatuberata. Scale bars: 5 cm in A, 10 cm in B-E. The darkened areas represent the elements preserved. Lycopsis is drawn asfound in matrix.

A B

C

D E



taxon known amongst Borhyaenoidea, although itmust have been a much slower runner than any mod-ern form. Finding a cursorial form was not unexpectedwithin a group of highly carnivorous mammals.According to Stein & Casinos (1997), there is no highlypolytypic order of terrestrial mammals that does notcontain at least some taxa that would be consideredcursorial. Biomechanical evidence suggests that cur-sorial mammals could have arisen naturally beyond acertain body weight to maximize locomotor efficiency(Janis & Wilhelm, 1993; Stein & Casinos, 1997).

Based on its forelimb proportions, Borhyaena wasrelatively shorter-legged and with bones relativelymore robust and heavier than present-day pursuitpredators (Argot, 2003b). The forelimbs of Borhyaenawere probably able to perform movements notrestricted to a strict parasagittal plane as in allborhyaenoids known, a condition which would havebeen useful in hunting and overpowering small prey,and overturning rocks and logs. The searching behav-iour of striped hyaenas, adapted towards obtainingsmall food (insects, small vertebrates, fruits and car-rion) from the denser part of the vegetation withoutcooperation between individuals (Kruuk, 1976), islikely to resemble the foraging behaviour ofBorhyaena. Another similarity between theborhyaenoid and striped hyaenas is that the strongand powerful neck and anterior part of the trunk ofBorhyaena would be advantageous in lifting and car-rying heavy prey to denning areas, as striped hyaenasdo (Kruuk, 1976).

Borhyaena appears to have had the best stereo-scopic vision among Santacrucian borhyaenoids, theestimated overlap of left and right visual fields being50–70∞ (Savage, 1977), vs. 30–50∞ for Cladosictis andProthylacinus. The primitive nocturnal carnivoresthat cannot visually localize their prey seem to bemore dependent upon an immediate rush and/orambush strategy rather than employing a circuitousstalking approach (Eisenberg & Leyhausen, 1972);this fits well with the hunting strategy hypothesizedfor Prothylacinus. Concerning the apparently poorrunning ability of Borhyaena compared with livingcanids, it is noteworthy that among the Santa Cruzherbivores, only two litoptern families might be con-sidered as potentially cursorials, the Proterotheriidaeand Macraucheniidae. The slenderly built prot-erotheriids were of small to moderate size, and consti-tute the major Santacrucian stock of equid-likeanimals characterized by long, slender limbs, and feetthat have a very horse-like appearance (because ofreduced lateral digits), although the metapodials arenot particularly elongate (Scott, 1910). The macra-ucheniids are represented by a single Santacruciantaxon, Theosodon, one of the most common elements ofthe Santa Cruz fauna, characterized by a long and

graceful neck recalling the guanaco and llama, and bythe presence of a short proboscis (Patterson & Pascual,1968). The feet are functionally tridactyl and almostisodactyl (Scott, 1910). Theosodon’s shoulder heightwas approximately 100 cm (vs. 45 cm for the antelope-like proteroteriid Thoatherium), i.e. it was taller andespecially stouter than the modern llama. It isunlikely that Borhyaena could have preyed uponadults, but it was certainly able to attack juveniles.

During the Santacrucian, Sipalocyon, Cladosictis,Prothylacinus and Borhyaena coexisted with six otherborhyaenoids, all less well-known (Table 3): (1) twohathlyacynids smaller than Sipalocyon gracilis:Pseudonotictis pusillus and Perathereutes pungens; (2)the largest known hathlyacynid, Anatherium defos-sus, slightly larger than Cladosictis patagonica, butknown only from fragmentary mandibular rami; (3)the medium-sized prothylacynid Lycopsis torresi; (4)the medium-sized borhyaenid Acrocyon sectorius,smaller than Borhyaena tuberata and much rarer; (5)the very large and quite rare borhyaenid Arctodictismunizi. Adults of Arctodictis were the giants of theirtime, the largest post-Deseadan borhyaenoids known(Marshall, 1976). It has been suggested that thistaxon filled the adaptive zone for a large terrestrialcarnivore, available in South America since the disap-pearance of the very large proborhyaenids at the endof Deseadan (Marshall, 1976; Bond & Pascual, 1983).However, Arctodictis did not reach the size of thegigantic proborhyaenids, and evolved concurrentlywith new climatic and environmental conditions(Bond & Pascual, 1983).

Therefore, the diversity in body size among theborhyaenoids that coexisted during the Santacrucianis considerable. Moreover, the diversity in morpholog-ical adaptations is also important between Cladosic-tis, Prothylacinus and Borhyaena. Sipalocyon is toopoorly known to infer conclusions about its mode oflife, although the pseudo-opposable pollex suggests,like the deep and sharp ungual phalanges, potentialgrasping ability (Argot, 2003c).

Distinct adaptations are expected to make differentprey species available to each hunter, by virtue of sub-strate preference (habitat selection) and/or varioushunting strategies (Rosenzweig, 1966). However,other factors, although important to explain varia-tions in diet of sympatric predators, remain unavail-able for palaeoguilds, such as their speed andperseverance during running, or the way in which thedifferent reactions of prey interact with the huntingstrategy (Kruuk & Turner, 1967). Response to prey isactually a function of experience and of the stimuliemanating from the prey object itself (Eisenberg &Leyhausen, 1972): ungulates can simply flee, whereasground sloths can fight and exhibit defensive threatpostures. Moreover, the occupation of the same habitat

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at different times of the day is a factor impossible toassess for fossil forms.

How could these contemporaneous borhyaenoidshave shared prey? It is usually thought that large carn-ivores tend to eat large prey. With increase in bodymass, predators change the composition of their foodfrom small to larger prey (Carbone et al., 1999), thelatter being nevertheless far more scattered, moreactive, and thus less productive than the former (Gos-zczynski, 1986). Hence, numerous exceptions exist(Rosenzweig, 1968). The sharp claws of felids enablethem to overpower prey larger than themselves. Incontrast, because the limbs of living canids are modi-fied for cursorial locomotion, they use only the jaws asa prehensile killing organ, which limits the size of preywhich can be captured and killed by a solitary hunter(Kleiman & Eisenberg, 1973). Hence, solitary canidsusually exhibit greater opportunism and moreomnivorous tendencies than felids. This seems to havepermitted the development of traits that are rare infelids, such as peaceful communal feeding (a steptowards pack hunting), or extensive scavenging on thekills of larger predators (Kleiman & Eisenberg, 1973).

The general pattern exhibited by the postcranium ofProthylacinus and Borhyaena suggests quite similardifferences, since the forelimb of Prothylacinus indi-cates ability to manipulate while that of Borhyaenalacks great abductive ability, pronation-supinationcapabilities, and sharp claws, all features that restrictmanipulation. Rosenzweig (1966) found that activepredators tend to specialize in a certain size of prey,although other sized prey may be taken occasionallyas well. For example, wolves that hunt in packs pri-marily eat ungulates, coyotes eat rabbits and largerodents (and also birds, insects, fruit and carrion), andfoxes eat rodents and occasionally vegetable matter(Ewer, 1998). Small predators are usually solitaryhunters, must sustain predation pressure from largersympatric carnivores, tend to hunt small prey, and tobe partly omnivorous (Kleiman & Eisenberg, 1973), ashathlyacynids were supposed to be compared to pro-thylacinids and borhyaenids (Marshall, 1981). Rosen-zweig (1966) also argued that the coexistence of closelyrelated predatory species is maintained in large partby differences in body size, or that predators of similarsize occupy different habitats or exhibit differenthunting habits. Although the adaptive niches of fossilforms cannot be defined accurately, the difference insize between Cladosictis and Prothylacinus limitedthe competition, whereas the distinct adaptations ofProthylacinus and Borhyaena certainly also limitedinteractions.

The powerful neck and massive skull of Borhyaena,characterized by robust and prominent zygomaticarches, suggest that this taxon could have occasionallyscavenged, although its dentition does not suggest

that it was a specialist bone-crusher. Most carnivorestend to scavenge when an opportunity arises (Estes,1967; Viranta, 1996). A primarily scavenging mode oflife has two requirements: the presence of efficienthunters (or some other factor inducing high prey mor-tality), and that the prey be sufficiently large, becausesmall prey are usually consumed entirely by the pred-ators themselves (Viranta, 1996). Moreover, the occur-rence of bone-eating species depends on feedingopportunities (Van Valkenburgh, 1989). Santacrucianenvironmental conditions were probably not optimumfor this, since carcasses are more difficult to find indensely covered habitats and when climates are warmand moist, because of rapid decomposition.

What sort of efficient hunters could have killed largeprey? During the Santacrucian, the nonmammalianoccupants of the carnivore adaptive zone were large,flightless running birds, the phororhacoids, thatranged from Deseadan to Montehermosan (i.e. lastingc. 20 Myr: Marshall, 1978b). Three families areknown: the medium and large-sized Psilopteridae andPhorusrhacidae, rather lightly built and probablyswift runners, and the gigantic Brontornithidae,including ponderous forms with massive beaks(Patterson & Pascual, 1968; Marshall, 1978b). Thebiology of these birds is still poorly known. Much of therecorded material is fragmentary, and the associationof the elements is often questionable, which increasesthe difficulty of performing a comprehensive overview.

Amongst the best known taxa, Pelecyornis (Fig. 11)was a medium-sized bird, about 80–90 cm tall, with askull about 18 cm long, and a massive, deep beak.According to Ameghino (1895), the orientation of thearticular facets of the cervical vertebrae in Phororha-cos (structurally similar to, but larger than, those ofPelecyornis) suggests an important sigmoid curvatureof the neck: the head was probably placed in a restingposition in the same vertical axis as the scapula,which would have helped to support its weight. Themandible of Phororhacos longissimus suggests a skullabout 65 cm long. The tail of Pelecyornis was long andallowed lateral movement. The sternum is that of atypical carinate bird, supporting a prominent ventralkeel. The length of the wing equals that of the livingSouth American Cariama, a long-legged, long-neckedbird about 70 cm tall (Marshall, 1988). Cariama iscredited with the ability to run as fast as a trottinghorse (25 miles per hour); it spends most of its time onthe ground and is only capable of flight over short dis-tances (Sinclair & Farr, 1932; Marshall, 1978b, 1988).

The most striking difference between Pelecyornisand Cariama concerns the development of the beak,which is much greater in the fossil, although Cariamaalso exhibits carnivorous habits, feeding on smallmammals, birds, reptiles and insects (Sinclair & Farr,1932; Marshall, 1978b). Cariama usually seizes its



victim in its beak and hurls it to the ground with greatforce. Moreover, the inner claw of each foot is long,sharp and deeply curved, and is probably used to pinthe prey to the ground. This suggests ferocious habitsin the much larger phororhacoids. Patterson & Pas-cual (1968) even suggested that they could havepreyed on armadillos and glyptodonts, the Santacru-cian taxa being less heavily armoured than the Pleis-tocene ones.

Competition between phororhacoids and largeborhyaenoids cannot be excluded, but remains spec-ulative. It is usually considered that these largebirds replaced borhyaenoids in the later Tertiary inthe savanna grasslands of Argentina (Marshall,1978a), although some authors consider that the20 Myr of coexistence between borhyaenoids andphororhacoids resulted in resource partitioningrather than extinction (Patterson & Pascual, 1968;Bond & Pascual, 1983). Although the axe-like beakof these big birds suggests that they probably hadpredatory habits, there is little reason to think thatborhyaenoids were unable to kill a phororacoid,especially the relatively small psilopterids. Ecologi-cal theory predicts that if competition for a shared

resource occurs, guild members will either diverge intheir resource utilization or become extinct locally(Van Valkenburgh, 1985). However, it is still impos-sible to prove that borhyaenoids and phororacoidsexhibited microhabitat separation or differences inactivity pattern.

Because the partition of the specimens of Borhyaenawithin the various fossiliferous horizons of the SantaCruz Formations is poorly documented, it is difficult toestablish faunistic correlations precisely. PerhapsBorhyaena was more abundant in forested areas andthe flightless birds in grasslands. Alternatively,Borhyaena might have been present in both environ-ments, hunting under cover or in the open country atthe very edge of forests and scavenging on grasslands(the presence of carnivorous birds improving carcasspredictability). It may have sought out the nests ofgrassland birds as hyaenas do in African plains, wait-ing for the time when the ostrich eggs are left momen-tarily unguarded (Estes, 1967). Such a partition couldalso explain the relatively important variation in sizefound within the different specimens of Borhyaena(Marshall, 1978a) as it is well known that jaguarsfrom the grasslands of the Brazilian Pantanal can be

Figure 11. Pelecyornis australis, from the Santa Cruz Formation (end of early Miocene) of Patagonia, Argentina. A, skel-etal reconstruction modified from Sinclair & Farr (1932). Scale bar = 10 cm. B, life reconstruction modified from Scott(1932).

A B

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twice as heavy as those dwelling in the Amazonian for-est (Emmons, 1992).

Moreover, although these ground-dwelling birdswere certainly able to run fast, the way that theykilled prey with their strong beak acting as a weaponis still unclear. Therefore, it may also be suggestedthat borhyaenids killed prey and phororacoids scav-enged them. In fact, at typical kills, a definite rankorder among African open plains scavengers is main-tained, hyaenas coming first, then jackals, then vul-tures (Estes, 1967). Hyaenas and jackals predominateduring the night, and vultures during the day, andsome phororacoids might have played the role of mod-ern vultures. Moreover, while hyaenas and jackalsmay live largely as scavengers on the kills of purepredators (big cats), where such predators are scarcethey may be very active hunters (Estes, 1967). Assess-ing whether such opportunism was practised by fossilspecies remains speculative.

Lycopsis longirostrisThe La Venta fauna contains a diverse assemblage ofendemic ungulates and edentates that filled a varietyof niches as herbivores, as well as the earliest repre-sentatives of many clades of living South Americanmammals, including modern subfamilies of armadil-los, anteaters, bats, opossums and New World mon-keys (Flynn & Wyss, 1998). There was a highproportion of browsing species, a large number of frug-ivorous taxa, a large number of arboreal species(especially platyrrhines and some edentates), and thepresence of forest-dwelling marsupials, bats, lizardsand birds suggests that moist evergreen forests wereextensive (Kay & Madden, 1997). Remains of birdsfound at La Venta reveal the presence of Hoazinoides,a cuculiform whose modern relatives (turacos andhoatzins) underwent evolutionary development in footand wing structure in order to clamber about in trees(Rasmussen, 1997). Phororhacoids are unknown fromthis locality, perhaps reflecting the presence of exten-sive forests.

Lycopsis weighed about 15 kg, and the shoulderheight was about 35 cm (C. Argot, pers. observ.; seealso Fig. 10C). It was relatively longer-legged than theother borhyaenoids known from postcranial remains,but the intermembral index is similar to that of theother borhyaenoids (approx. 78%), in the same rangeas most felids and mustelids. Morphological analysisof the postcranial skeleton reveals that it was a pri-marily terrestrial form. The general shape of the scap-ula and ulna indicates in particular that Lycopsis wasclearly less adapted towards an arboreal life than Cla-dosictis or Prothylacinus. However, it does not exhibitfeatures suggesting an incipient cursorial specializa-tion, in contrast to Borhyaena. The development of the

musculature of the arm (especially Mm. spinati, pec-toralis and biceps brachii), as well as the pseudo-opposable pollex, nevertheless suggest that Lycopsismight have used its forelimb for a manipulative pur-pose, consistent with the capture of small prey. On thecalcaneum, the orientation of the calcaneoastragalarand sustentacular facets reduces the stability of thecalcaneoastragalar joint, a condition which probablyprecluded fast running.

Lycopsis is traditionally compared in the literaturewith Thylacinus (Marshall, 1978a), although func-tional analysis of the postcranial skeleton revealsclear differences, especially in the structural patternof the forelimb, the thylacine’s being more specializedtowards a cursorial trend. Despite this trend, Thylaci-nus is thought to have been more at home in dense for-ests than open plains, although this preference mayhave resulted from competition with dingos, Canislupus dingos, which are better adapted to open coun-try (Smith, 1982). However, the niche overlap betweenthe two species may have been overstated because ofdifferences in dentition and thus probably in diet(Johnson & Wroe, 2003). It has been suggested thatthe diet of the thylacine in the wild was composed ofsmall macropodids, echidnas, rats and birds (e.g. theTasmanian native hen Gallinula mortierii) - prey con-siderably smaller than itself, and better stalked thanpursued (Smith, 1982). However, such selection couldwell have resulted from human disturbance, as thetwo largest potential Tasmanian prey species of thethylacine, the emu and eastern grey kangaroo, werebeing decimated or eliminated by the 19th century,while the thylacine was restricted to marginal habi-tats (Johnson & Wroe, 2003).

Living in forested environments and without anycursorial specialized features, Lycopsis probablystalked small mammals, which were abundant at LaVenta during the Miocene. Direct evidence that it fedupon rodents exists, because in the body cavity of theholotype UCMP 38061, between the ribs and righttibia, several broken rodent bones and an upper molarof Scleromys colombianus have been found. Additionalrodent bones and an incisor were found immediatelyposterior to the pelvis and below the base of the tail(Marshall, 1977a). Scleromys colombianus weighedabout 2.5–3.5 kg (Walton, 1997). Rodents are well-diversified in the La Venta fauna (Table 4) and mayhave represented a diverse array of prey. Their closestliving relatives are generally forest dwellers (Walton,1997), except for caviids whose ever-growing cheek-teeth suggest grazing habits. Their presence suggeststhat the palaeoenvironment of La Venta was a sort ofecological mosaic, although the fossil caviids may alsonot have had exactly the same ecological requirementsas their modern relatives. Alternatively, the absence ofmodern caviids in the tropical regions may be ascribed



to various factors such as competitive exclusion (Wal-ton, 1997).

Lycopsis coexisted with a few larger borhyaenoids.These included Dukecynus magnus, poorly knownfrom a distorted partial skull, and an undeterminedlarge-sized borhyaenoid, known from very fragmen-tary postcranial and cranial fragments that do notallow a generic identification. Labelled ?Arctodictis byMarshall (1978a), the size of the fragments corre-sponds to that expected for D. magnus (Goin, 1997),but the determination is still in doubt. The lastundoubted borhyaenoid is Anachlysictis gracilis,which represents the first appearance of thylacosmil-ids (Goin, 1997). Its flat skull roof, and the absence ofpostorbital bar and of dorsal extension of the uppercanines suggest a predation strategy distinct fromthat of Thylacosmilus atrox. The systematic positionand borhyaenoid affinities of the enigmatic Hondadel-phys are still unclear (Goin, 1997). This taxon wassmaller than Lycopsis and probably omnivorous (Goin,1997). Hathlyacynids are unknown at La Venta,although they are known in later faunas. It may besuggested that Hondadelphys, intermediate in sizebetween Sipalocyon and Cladosictis, and sharing withthem similar dental specializations, filled a similar

ecological niche, which suggests a possible competitiveexclusion between the groups (Marshall, 1978a).

The nonmammalian predators of that fauna werecrocodiles, particularly well-diversified in terms oftaxonomic diversity, body size range, and presumedfeeding ecology (Langston & Gasparini, 1997). Theyincluded probable active terrestrial carnivores like thevery large and deep-skulled Sebecus and other sebe-cosuchians (Langston & Gasparini, 1997). Other taxahave been recorded, like Charactosuchus (Crocodyl-idae), Mourasuchus (Nettosuchidae, endemic to SouthAmerica), Balanerodus (Alligatoridae), and the abun-dant Gryposuchus (Gavialidae) (Langston & Gas-parini, 1997). The variety of crocodiles in the HondaGroup is astonishing, as it is unusual in modern fau-nas that more than three taxa frequent the samestretch of river (Langston & Gasparini, 1997). Theability of Lycopsis to invert its hind foot and graspbranches might have allowed it to occasionally escapethese predators. Similarly, some Australian carnivoreniches may have been occupied by reptiles (crocodiles,snakes and lizards) from the middle Tertiary to thePleistocene, although such reptiles were probablymuch more uncommon and geographically restrictedthan carnivorous marsupials (Wroe, 2002).

Table 4. Generic list of Laventan mammals from the Honda Group (Monkey beds) of La Venta, Colombia (from Hirschfeld,1985; Bown & Fleagle, 1993; Carlini et al., 1997; Dumont & Bown, 1997; Edmund & Theodor, 1997; Fleagle et al., 1997;Goin, 1997; Johnson & Madden, 1997; Kay & Madden, 1997; McDonald, 1997; McKenna & Bell , 1997; Walton, 1997; White,1997)

DIDELPHIDA XENARTHRA LITOPTERNA RODENTIADIDELPHIMORPHIA Dasypodidae Proterotheriidae DinomyidaeDidelphidae Anadasypus Prolicaphrium ‘Scleromys’Micoureus Pedrolypeutes Prothoatheri ‘Olenopsis’Thylamys Nanoastegotherium Megadolodus cf. Simplimus sp.Undetermined taxa Pampatheriidae Macraucheniidae Dasyproctidae

SUDAMERIDELPHIA Scirrotherium Theosodon NeoreomysSparassodonta Glyptodontidae MicroscleromysHondadelphidae Neoglyptatelus ASTRAPOTHERIA ErethizontidaeHondadelphys Asterostemma Astrapotheriidae ?Steiromys sp.

Borhyaenoidea Mylodontoidea Xenastrapotherium MicrosteiromysLycopsis Pseudoprepotherium Granastrapotherium EchimyidaeDukecynus Glossotheriopsis Acarechimys?Arctodictis Neonematherium NOTOUNGULATA CaviidaeAnachlysictis Megalonychidae Toxodontidae Prodolichotis

GLIRIMETATHERIA Undetermined taxon Pericotoxodon Undetermined taxaPaucituberculata Nothrotheriidae LeontiniidaeCaenolestoidea Undetermined taxa Huilatherium PRIMATESHondathentes Megatheriidae Interatheriidae Atelidae

Undetermined taxon Miocochilius NeosaimiriGONDWANADELPHIA Myrmecophagidae Cebupithecia

MICROBIOTHERIA Neotamandua MohanamicoMicrobiotheriidae StirtoniaPachybiotherium Undet. callitrichine

514 C. ARGOT


Thylacosmilus atroxThe highly specialized Thylacosmilus is the only largestrictly carnivorous borhyaenoid living in the Hua-yquerian fauna of northern Argentina. Although adetailed study of the evolution of amphicyonids sug-gests that increased specialization of predators mayoccur in a carnivore community as a result ofdecreased herbivore diversity (Viranta, 1996), thefauna associated with thylacosmilids does not clarifythe appearance of such specialized predators(Table 5). During the Huayquerian, notoungulates arerestricted to three families, Hegetotheriidae andMesotheriidae (small to medium-sized rodent-likeforms) and Toxodontidae (larger in size, similar to rhi-noceros and hippopotamus). It is possible that glypt-odonts and giant rodents took advantage of the declineof notoungulates to exploit new adaptive niches (OrtizJaureguizar, 1998). Thylacosmilids may have evolvedin coevolution with huge ground-sloths, notoungulates(toxodontids), perhaps some litopterns (macraucheni-

ids), and giant rodents (Pascual & Ortiz Jaureguizar,1990). However, it is unlikely that thylacosmilidsattacked the two former groups. Their most probableprey were thus mesotheriids (Notoungulata), macra-ucheniids (Litopterna), and dinomyids and hydrocho-erids (Rodentia).

The sabre-tooth adaptation is viewed as an exten-sion of the throat-bite, a learned behaviour in felids(Martin, 1980, 1989). A stab into the side of the neck,with the curvature exhibited by the canines, wouldbring the edge of the canine back under the carotidand jugular, their tearing resulting in almost instan-taneous death (Kurtén, 1952; Martin, 1980, 1989). Astab into the neck requires forelimbs powerful enoughto manipulate the prey and position it for the killingslash (Radinsky & Emerson, 1982). The dirk-toothedcats and nimravids whose postcranial skeletons areknown (Smilodon, Barbourofelis) exhibit like Thyla-cosmilus huge muscle attachments, massive proximallimb bones, and shortened distal segments of the leg

Table 5. Generic list of Huayquerian mammals from Argentina, slightly modified from Marshall et al. (1983)

DIDELPHIDA XENARTHRA LITOPTERNA RODENTIADIDELPHIMORPHIA Dasypodidae Proterotheriidae Octodontidae

Didelphidae Chorobates Brachytherium ?NeophanomysHyperdidelphis Doellotatus ?Diadiaphorus PhtoramysLutreolina Paleuphractus ?Eoauchenia PseudoplateomysThylatheridium Paraeuphractus Epecuenia Abrocomidae

Sparassocynidae Pampatheriidae Macraucheniidae ProtabrocomaSparassocynus Kraglievichia Macrauchenidia Echimyidae

GLIRIMETATHERIA Vassallia Promacrauchenia CarterodonSimpsonitheria Glyptodontidae Proechimys

Argyrolagidae Aspidocalyptus NOTOUNGULATA TrichomysMicrotragulus Coscinocercus Toxodontidae Chinchillidae

SUDAMERIDELPHIA Cranithlastus Pisanodon LagostomopsisSparassodonta ?Eleutherocercus Xotodon DinomyidaeBorhyaenoidea Eosclerocalyptus Mesotheriidae Diaphoromys

Notictis Glyptodontidium Pseudotypotherium ?PotamarchusBorhyaenidium Hoplophractus ?Typotheriopsis TelicomysStylocinus Peiranoa Hegetotheriidae TetrastylopsisEutemnodus Phlyctaenopyga Hemihegetotherium TetrastylusThylacosmilus Stromaphorus Paedotherium Caviidae

?Urotherium Raulringueletia CardiomysNothrotheriidae Tremacyllus ?CaviodonPronothrotherium Orthomyctera

Megatheriidae CARNIVORA PalaeocaviaPlesiomegatherium Procyonidae ErethizontidaePyramiodontherium Cyonasua Neosteiromys

Mylodontoidea HydrochoeridaeElassotherium ?CardiatheriumSphenotherus Kiyutherium

Myrmecophagidae ?ProcardiatheriumNeotamanduaPalaeomyrmidon



(arm, crus, and metapodials) (Merriam & Stock, 1932;Martin, 1980; Anyonge, 1996; Turner & Antón, 1997).In acquiring the strength to overpower large prey, itseems that sabretooth forms sacrificed speed andendurance.

Post-lactational parental care may have been a fac-tor of considerable importance in the evolution of spe-cialized techniques for killing large prey, for it permitsthe development of killing methods which are beyondthe capabilities of young animals, as well as of thosewhich require a considerable degree of experiencebefore they become fully effective (Ewer, 1969). Unfor-tunately, no fossil clues remain which suggest any-thing of that sort for Thylacosmilus, although it ishard to see how such complex predatory behaviourcould have developed in the young while they werestill unable to become specialized killers of prey largerthan themselves. One of the major differencesbetween dasyurids and felids in the development ofthe killing technique is that cats learn how to use skil-fully the innate repertoire of paw movements to posi-tion prey for the killing bite (Pellis & Officer, 1987),something Thylacosmilus was also expected to learn.By contrast, living dasyurids are not endowed withthe same variety of paw movements, although withexperience the forepaws can be used during frontalattacks by Dasyuroides in order to grasp and pin prey(Pellis & Officer, 1987). It has been suggested for Smil-odon that large kills were provided by a mature ani-mal, allowing young individuals whose canines hadnot yet reached their full development to feed uponthese kills (Hough, 1949). Similar behaviour in Thy-lacosmilus would suggest cooperation unknown inmodern marsupials.

An important aspect of hunting strategy concernsthe acuteness of senses. Savage (1977) determinedthe degree of stereoscopic vision for various preda-tors, and found that the estimated overlap of left andright visual fields was 30–50∞ in Thylacosmilus, a lowvalue compared with modern predators. It is notewor-thy that in the lion’s hunting methods, surprise is ofoverriding importance for initial capture and also forreducing the risk of self-injury. On the open plains,there is seldom enough cover for concealed stalking,so lions hunting by day must usually wait in highvegetation, often by a watering place, for game tocome to them (Estes, 1967). The Huayquerian savan-nah-like environments suggest quite similar huntingmethods for thylacosmilids, which are not equippedfor pursuit. Moreover, in the Ngorongoro crater, prob-ably 90% of kills are made at night (Estes, 1967).Although fossils do not carry traces of nocturnalhunting, this might account for the low stereoscopicvision of thylacosmilids. It may be significant thatThylacosmilus had evolved a specialized, unique(compared to other borhyaenoids) ear region, in

which the enlarged hypotympanic sinus is containedwithin a fully ossified, expanded auditory bulla. Thelarge and complex hypotympanic sinus increasesmiddle ear volume which prevents excessive dampingof sound energy transmission (Turnbull & Segall,1984). This condition is consistent with life in a quitearid environment (Hunt, 1974; Savage, 1977).Because sound absorption in air becomes greaterwith a decrease in humidity and an increase in tem-perature, selective pressures in warm arid environ-ments tend to favour mammals equipped with ahighly inflated bulla, providing a high degree of audi-tory sensitivity (Hunt, 1974). The inflated bulla ofThylacosmilus may have therefore favoured acutehearing, which could compensate for the poor stereo-scopic vision related to small eyes facing laterally.Because the auditory bullae of Thylacosmilus andSmilodon exhibit similar modelling, Turnbull & Seg-all (1984) suggested that they may reflect a similarrole related to hearing, one especially matched to thepeculiar demands of the sabretooth way of life. How-ever, this role is not yet understood.

During the Huayquerian, Thylacosmilus coexistedwith different dog-like borhyaenoids: (1) the small-sized hathlyacynids Notictis ortizi and Borhyaenid-ium musteloides (Marshall, 1981), which occur infaunas of the same age but from different Argentin-ian localities (Marshall, 1978a). Notictis was quitesimilar in dental structure to the contemporaneousdidelphid Lutreolina, whereas B. musteloidesappears to be more carnivorous than the contempo-raneous Didelphis pattersoni (Marshall, 1981); (2)the poorly known medium-sized Eutemnodus spp.(E. acutidens, E. americanus, E. propampinus), quitesimilar in size and dental structure to the Santacru-cian borhyaenid Acrocyon sectorius (Marshall,1978a); (3) the large-sized prothylacynid Stylocynusparanensis. This taxon is a relatively largeborhyaenoid, probably the most bear-like accordingto its dental specialization that suggests an omnivo-rous diet (Marshall, 1979). Therefore, during theLate Miocene and Pliocene, Thylacosmilus was with-out doubt the most specialized carnivorous mamma-lian predator, exhibiting a combination of charactersthat represents the culmination of a long evolution-ary history. No member of the superfamilyBorhyaenoidea, as far as is known, could seriouslycompete with it. Also of relevance is the fact thatpredatory phororhacoids became increasingly signifi-cant in the late Tertiary of South America (Mar-shall, 1994). Because Thylacosmilus was singularlyinadequate as a processor of bones (Goin & Pascual,1987) it would have probably left significant parts oflarge kill untouched, which suggests that the giantbirds were at least partly scavengers, in the absenceof ‘dog-like’ marsupial taxa.

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CONCLUSIONS

Borhyaenoids do not exhibit a constant and regularincrease in size and diversity during the 60 Myr oftheir development. While the oldest specimen knownis small, the largest borhyaenoids evolved during theEocene and Oligocene (i.e. between 54 and 24 Mya),before the main radiation of the superfamily. Thisradiation occurred during the Santacrucian (approx.17 Mya), together with a radiation of rodents andsmall notoungulates, which were potential prey forHathlyacynidae, Prothylacinidae and Borhyaenidae.As far as is known, borhyaenoids survived until theChapadmalalan (late Pliocene, 3.5–4 Mya), with themost specialized family of the group, the Thylacosmil-idae, having developed during the last 10 Myr. Theirevolution is thus characterized by various periods ofradiation and extinction, and by the development of abroad range of body plans, the marten-like Cladosictiscontrasting with the digitigrade Borhyaena and pow-erfully built Thylacosmilus.

All the borhyaenoids known from postcranial ele-ments appear to have possessed considerable strengthin the neck and forequarters, prehensile forepaws anda pseudo-opposable pollex, probably required to cap-ture struggling prey and/or to climb efficiently. Mayu-lestes is the oldest and only Palaeocene borhyaenoidknown from postcranial elements. It is distinct fromthe other taxa examined by its age, size and particularmorphology. Some of these features, particularly themorphology of the pectoral and pelvic girdles, arealready specialized, compared with those of the otherTiupampan metatherians (Muizon & Argot, 2003).Because of these specializations, the notion of primi-tive pattern does not make sense for Mayulestes. May-ulestidae appear totally distinct from the latePalaeocene lineages that gave birth to the Miocenetaxa, and in view of the still unresolved appearance oflarge Eocene taxa, it is suggested that early radiationsoccurred within the group.

The end of the Oligocene and late Miocene representtwo critical periods in the evolution of theBorhyaenoidea, probably in relation to global environ-mental changes. The post-Santacrucian climaticchanges in particular led to the rarefaction of subtrop-ical woodlands, which were replaced by savannah-likeenvironments (Pascual & Ortiz Jaureguizar, 1990).This occurred together with the simultaneous predom-inance of the sabretooth thylacosmilids and growingscarcity of the ‘dog-like’ taxa. The appearance of sabre-tooth taxa offers an interesting parallel with similarevolutionary developments that occurred within vari-ous other groups (Nimravidae, Felidae, Creodonta),demonstrating that this adaptation was not anunusual evolutionary track. The lifestyle and huntingand killing strategies of thylacosmilids are totally dis-

tinct from those of the ‘dog-like’ borhyaenoids,although the associated fauna does not explain thereasons for their appearance. Some dog-like taxa sur-vived in the northern parts of the continent, e.g. inColombia, probably because the environmental condi-tions in the equatorial tropics were less affected by thegradual global climatic zonation that occurred insouthern South America (Patterson & Pascual, 1968).

One question which has been posed concerns whyonly thylacosmilids survived and why the dog-liketaxa did not evolve greater cursoriality in the south-ern plains. It has been suggested that borhyaenoidswere gradually eliminated by placental carnivoransand didelphids that began to develop from the Hua-yquerian onward. At that time, the radiation of didel-phids was characterized by a tendency towards thedevelopment of carnivorous types, some of them veryspecialized, such as Hyperdidelphis or Sparassocynus(Simpson, 1974). These taxa might have occupied theadaptive zone of hathlyacynids, thus representing an‘endo-replacement’ (Goin, 1989). Concerning the ‘exo-replacement’ of marsupials by placentals, it has beensuggested that procyonids might have competed withthe omnivorous Lycopsis/Pseudolycopsis lineage, orreplaced it, as suggested by the successive occurrenceof Pseudolycopsis during the Chasicoan and Cyonasuaduring the Huayquerian (Marshall, 1978a). However,it is not clear why so few borhyaenoids survived dur-ing late Miocene-Pliocene, considering the arrayof potential prey, especially rodents and somenotoungulates.

Although much has been said about the extinction ofBorhyaenoidea due to competition with large ground-dwelling birds or other mammals (see Marshall,1978a), it is worth stressing the change in environ-mental parameters that occurred. During the San-tacrucian, borhyaenoids were abundant, reaching aclimax in variety of size and adaptations, apparentlywithout strong constraints on the rate and direction ofmorphological evolution, since all the mammalianpredatory ecological niches were vacated. The factthat the Santacrucian area was at first largelywooded, with a subtropical climate, may have influ-enced the evolution of the Borhyaenoidea, which werenot confined to the ground with the probable exceptionof Borhyaena (as far as we know from postcranial ele-ments). They were probably able to exploit all strata oftropical forests, a strategy which provides opportuni-ties for greater diversification in niche occupancy (Kle-iman & Eisenberg, 1973). While Palaeocene south-central Bolivia, early Miocene Patagonia, and middleMiocene Colombia were characterized primarily by asubtropical climate and forested environment, Thyla-cosmilus is the only borhyaenoid examined that didnot live in a densely covered milieu, and the savan-nah-like environments of the late Miocene-Pliocene



seem to have been less favourable to the dog-like taxa.With less than one third of the taxa recorded knownfrom postcranial skeletons, improved understandingof the locomotor evolution of Borhyaenoidea is criti-cally dependent on the discovery of further remains.More material is required in order to fully documentthe evolution of the ecomorphs that occurred withineach family.

ACKNOWLEDGEMENTS

For access to borhyaenoid specimens, I am grateful tothe following people and institutions: José Bonaparte(Museo Argentino de Ciencias Naturales ‘BernardinoRivadavia’, Buenos Aires), John J. Flynn (FieldMuseum of Natural History, Chicago), Patricia Hol-royd (Museum of Palaeontology, University of Califor-nia, Berkeley) and Mary Ann Turner (PeabodyMuseum, Yale University, New Haven). I thank Chris-tian Muizon for critically reviewing the first version ofthis manuscript, as well as Jean-Pierre Gasc, PascalTassy, and two anonymous reviewers for commentsthat helped improve the text. Financial support wasprovided by the Muséum national d’Histoire naturelle,Paris.

REFERENCES

Alexander R, McN. 1993. Legs and locomotion of Carnivora.Symposia of the Zoological Society of London 65: 1–13.

Ameghino F. 1895. Sur les oiseaux fossiles de Patagonie.Boletín del Instituto Geográphico Argentino 15: 1–104.

Anyonge W. 1996. Locomotor behaviour in Plio-Pleistocenesabre-tooth cats: a biomechanical analysis. Journal of Zool-ogy, London 238: 395–413.

Archer M. 1982. A review of Miocene thylacinids (Thyla-cinidae, Marsupialia), the phylogenetic position of the Thy-lacinidae and the problem of apriorisms in characteranalysis. In: Archer M, ed. Carnivorous marsupials. Sydney:The Royal Society of New South Wales, 445–476.

Argot C. 2001. Functional-adaptive anatomy of the forelimb inthe Didelphidae, and the palaeobiology of the Palaeocenemarsupials Mayulestes ferox and Pucadelphys andinus.Journal of Morphology 247: 51–79.

Argot C. 2002. Functional-adaptive analysis of the hindlimbanatomy of extant marsupials, and the palaeobiology of thePalaeocene marsupials Mayulestes ferox and Pucadelphysandinus. Journal of Morphology 253: 76–108.

Argot C. 2003a. Functional-adaptive anatomy of the axialskeleton of some extant marsupials, and the palaeobiol-ogy of the Palaeocene marsupials Mayulestes ferox andPucadelphys andinus. Journal of Morphology 255: 279–300.

Argot C. 2003b. Functional adaptations of the postcranialskeleton of two Miocene borhyaenoids (Mammalia, Metathe-

ria), Borhyaena and Prothylacinus, from South America.Palaeontology 46: 1213–1267.

Argot C. 2003c. Postcranial functional adaptations in theSouth American Miocene borhyaenoids (Mammalia, Met-atheria) Cladosictis, Pseudonotictis, and Sipalocyon. Alcher-inga 27: 303–356.

Argot C. in press. Functional-adaptive features of the postc-ranial skeleton of a sabertooth borhyaenoid, Thylacosmilusatrox (Metatheria), and palaeobiologic implications. Alcher-inga in press.

Barnett CH, Napier JR. 1953. The form and mobility of thefibula in metatherian mammals. Journal of Anatomy 87:207–213.

Bonaparte JF, Van Valen LM, Kramartz A. 1993. La faunalocal de Punto Peligro, Palaeocene inferior, de la provinciadel Chubut, Patagonia, Argentina. Evolutionary Mono-graphs 14: 1–61.

Bond M, Pascual R. 1983. Nuevos y elocuentes restos cra-neanos de Proborhyaena gigantea Ameghino, 1897 (Marsu-pialia, Borhyaenidae, Proborhyaeninae) de la EdadDeseadense. Un ejemplo de coevolucion. Ameghiniana 20:47–60.

Bown TM, Fleagle JG. 1993. Systematics, biostratigraphy,and dental evolution of the Palaeothentidae, Later Oligoceneto Early-Middle Miocene (Deseadan-Santacrucian) caenoles-toid marsupials of South America. Journal of Paleontology,Memoir 29: 1–76.

Carbone C, Mace GM, Roberts SC, MacDonald DW. 1999.Energetic constraints on the diet of terrestrial carnivores.Nature 402: 286–288.

Carlini AA, Vizcaíno SF, Scillato-Yané GJ. 1997. ArmoredXenarthrans: a unique taxonomic and ecologic assemblage.In: Kay RF, Madden RH, Cifelli RL, Flynn JJ, eds. Vertebratepaleontology in the Neotropics. The Miocene fauna of LaVenta, Colombia. Washington, DC: Smithsonian InstitutionPress, 213–226.

Davis DD. 1964. The giant panda. A morphological study ofevolutionary mechanisms. Fieldiana: Zoology Memoirs 3: 1–327.

Dumont ER, Bown TM. 1997. New caenolestoid marsupials.In: Kay RF, Madden RH, Cifelli RL, Flynn JJ, eds. Vertebratepaleontology in the Neotropics. The Miocene fauna of LaVenta, Colombia. Washington, DC: Smithsonian InstitutionPress, 207–212.

Edmund G, Theodor J. 1997. A new giant pampatheriidarmadillo. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ,eds. Vertebrate paleontology in the Neotropics. The Miocenefauna of La Venta, Colombia. Washington, DC: SmithsonianInstitution Press, 227–232.

Eisenberg JF, Leyhausen P. 1972. The phylogenesis ofpredatory behaviour in mammals. Zeitschrift für Tierpsy-chologie 30: 59–93.

Emmons LH. 1992. Les jaguars. In: Seidensticker J, LumpkinS, eds. Les félins. Paris: Bordas, 116–123.

Estes RD. 1967. Predators and scavengers. Natural History76: 20–29, 38–47.

Ewer RF. 1969. Some observations on the killing and eating ofprey by two dasyurid marsupials: the mulgara, Dasycercus

518 C. ARGOT


cristicauda, and the Tasmanian devil, Sarcophilus harrisii.Zeitschrift für Tierpsychologie 26: 23–38.

Ewer RF. 1998. The carnivores. Ithaca, NY: Cornell Univer-sity Press.

Fleagle JG, Kay RF, Anthony MRL. 1997. Fossil New Worldmonkeys. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ, eds.Vertebrate paleontology in the Neotropics. The Miocene faunaof La Venta, Colombia. Washington, DC: Smithsonian Insti-tution Press, 473–495.

Flynn JJ, Swisher CC III. 1995. Cenozoic South Americanland mammal ages: correlation to global geochronologies.Geochronology Time Scales and Global Stratigraphic Corre-lation, SEPM Special Publication 54: 317–333.

Flynn JJ, Wyss AR. 1998. Recent advances in South Ameri-can mammalian palaeontology. Trends in Ecology and Evo-lution 13: 449–454.

Genise JF, Bown TM. 1994. New Miocene scarabeid andhymenopterous nests and Early Miocene (Santacrucian)paleoenvironments, Patagonian Argentina. Ichnos 3: 107–117.

Goin FJ. 1989. Late Cenozoic South American marsupial andplacental carnivores: changes in predator-prey evolution.Fifth International Theriological Congress (Rome 22–29August 1989, abstracts of papers and posters) 271–272.

Goin FJ. 1997. New clues for understanding Neogene marsu-pial radiations. In: Kay RF, Madden RH, Cifelli RL, FlynnJJ, eds. Vertebrate paleontology in the Neotropics. TheMiocene fauna of La Venta, Colombia. Washington, DC:Smithsonian Institution Press, 187–206.

Goin FJ, Pascual R. 1987. News on the biology and taxonomyof the marsupials Thylacosmilidae (late Tertiary of Argen-tina). Anales de la Academia Nacional de Ciencias Exactas,Físicas y Naturales 39: 219–246.

Goszczynski J. 1986. Locomotor activity of terrestrial preda-tors and its consequences. Acta Theriologica 31: 79–95.

Haines RW. 1942. The tetrapod knee joint. Journal of Anat-omy 76: 270–301.

Hirschfeld SE. 1985. Ground sloths from the Friasian LaVenta fauna, with additions to the pre-Friasian Coyaimafauna of Colombia, South America. University Of CaliforniaPublications in Geological Sciences 128: 1–90.

Hough J. 1949. The habits and adaptation of the Oligocenesaber tooth carnivore, Hoplophoneus. Geological Survey Pro-fessional Paper 221-H: 125–137.

Hunt RM Jr. 1974. The auditory bulla in Carnivora: an ana-tomical basis for reappraisal of carnivore evolution. Journalof Morphology 143: 21–76.

Iwaniuk AN, Nelson JE, Ivanco TL, Pellis SM, WhishawIQ. 1998. Reaching, grasping and manipulation of foodobjects by two tree kangaroo species, Dendrolagus lumholtziand Dendrolagus matschiei. Australian Journal of Zoology46: 235–248.

Janis CM, Wilhelm PB. 1993. Were there mammalian pur-suit predators in the Tertiary? Dances with wolf avatars.Journal of Mammalian Evolution 1: 103–125.

Johnson SC, Madden RH. 1997. Uruguaytheriine astrapoth-eres of tropical South America. In: Kay RF, Madden RH,Cifelli RL, Flynn JJ, eds. Vertebrate paleontology in the Neo-

tropics. The Miocene fauna of La Venta, Colombia. Washing-ton, DC: Smithsonian Institution Press, 355–383.

Johnson CN, Wroe S. 2003. Causes of extinction of verte-brates during the Holocene of mainland Australia: arrival ofthe dingo, or human impact? Holocene 13: 1009–1016.

Jolly CJ. 1967. The evolution of the baboons. In: Vagtborg H,ed. The baboon in medical research, Vol. II. Austin, TX: Uni-versity of Texas Press, 23–50.

Kay RF, Madden RH. 1997. Paleogeography and paleoecol-ogy. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ, eds. Ver-tebrate paleontology in the Neotropics. The Miocene fauna ofLa Venta, Colombia. Washington, DC: Smithsonian Institu-tion Press, 520–550.

Kleiman DG, Eisenberg JF. 1973. Comparisons of canid andfelid social systems from an evolutionary perspective. Ani-mal Behaviour 21: 67–659.

Kruuk H. 1976. Feeding and social behaviour of the stripedhyaena (Hyaena vulgaris Desmarest). East African WildlifeJournal 14: 91–111.

Kruuk H, Turner M. 1967. Comparative notes on predationby lion, leopard, cheetah and wild dog in the Serengeti area,East Africa. Mammalia 31: 1–27.

Kurtén B. 1952. The Chinese hipparion fauna. Societas Sci-entiarum Fennica, Commentationes Biologicae 13: 1–82.

Landry SO. 1958. The function of the entepicondylar foramenin mammals. American Midland Naturalist 60: 100–112.

Langston W Jr, Gasparini Z. 1997. Crocodilians,Gryposuchus, and the South American gavials. In: Kay RF,Madden RH, Cifelli RL, Flynn JJ, eds. Vertebrate paleontol-ogy in the Neotropics. The Miocene fauna of La Venta, Colom-bia. Washington, DC: Smithsonian Institution Press, 113–154.

Marshall LG. 1976. Evolution of the Thylacosmilidae, extinctsaber-tooth marsupials of South America. Paleobios 23: 1–30.

Marshall LG. 1977a. A new species of Lycopsis(Borhyaenidae: Marsupialia) from the La Venta fauna (LateMiocene) of Colombia, South America. Journal of Paleontol-ogy 51: 633–642.

Marshall LG. 1977b. Evolution of the carnivorous adaptivezone in South America. In: Hecht MK, Goody PC, Hecht BM,eds. Major patterns in vertebrate evolution. New York, Lon-don: Plenum Press, 709–721.

Marshall LG. 1978a. Evolution of the Borhyaenidae, extinctSouth American predaceous marsupials. University Of Cal-ifornia Publications in Geological Sciences 117: 1–89.

Marshall LG. 1978b. The terror bird. Field Museum of Nat-ural History Bulletin 49: 6–15.

Marshall LG. 1979. Review of the Prothylacyninae, an extinctsubfamily of South American ‘dog-like’ marsupials. Fieldi-ana Geology N. S. 3: 1–50.

Marshall LG. 1981. Review of the Hathlyacyninae, an extinctsubfamily of South American ‘dog-like’ marsupials. Fieldi-ana: Geology N. S. 7: 1–120.

Marshall LG. 1988. Land mammals and the Great AmericanInterchange. American Scientist 76: 380–388.

Marshall LG. 1994. The terror birds of South America. Sci-entific American 270: 64–69.



Marshall LG, Muizon C, Sigogneau-Russell D. 1995.The locality of Tiupampa: age, taphonomy and mammalfauna. In: de Muizon C, ed. Pucadelphys andinus (Marsu-pialia, Mammalia) from the Early Palaeocene of Bolivia.Paris: Mémoires du Muséum national d’Histoire naturelle,11–20.

Marshall LG, Hoffstetter R, Pascual R. 1983. Mammalsand stratigraphy: Geochronology of the continentalmammal-bearing Tertiary of South America. Palaeoverte-brata, Mémoire extraordinaire 1–93.

Marshall LG, Sigogneau-Russell D. 1995. Postcranial skel-eton. In: Muizon C, ed. Pucadelphys andinus (Marsupialia,Mammalia) from the Early Palaeocene of Bolivia. Paris:Mémoires du Muséum national d’Histoire naturelle, 91–164.

Martin LD. 1980. Functional morphology and the evolution ofcats. Transactions of the Nebraska Academy of Sciences 8:141–154.

Martin LD. 1989. Fossil history of the terrestrial Carnivora.In: Gittleman JL, ed. Carnivore behaviour, ecology and evo-lution. London: Chapman & Hall, 382–409.

Maynard Smith J, Savage RJG. 1956. Some locomotoryadaptations in mammals. Zoological Journal of the LinneanSociety 42: 603–622.

McDonald HG. 1997. Xenarthrans: Pilosans. In: Kay RF,Madden RH, Cifelli RL, Flynn JJ, eds. Vertebrate paleontol-ogy in the Neotropics. The Miocene fauna of La Venta, Colom-bia. Washington, DC: Smithsonian Institution Press, 233–245.

McKenna MC, Bell SK. 1997. Classification of mammalsabove the species level. New York: Columbia UniversityPress.

Merriam JC, Stock C. 1932. The Felidae of Rancho La Brea.Carnegie Institution of Washington, DC Publications 422: 1–231.

Muizon C de. 1992. La fauna de mamiferos de Tiupampa(Palaeoceno Inferior, Formación Santa Lucía), Bolivia. In:Suarez-Soruco R, ed. Fosiles y facies de Bolivia, Vol. I: Ver-tebrados. Santa Cruz (Bolivia): Revista Técnica de YPFB,575–624.

Muizon C de. 1998. Mayulestes ferox, a borhyaenoid (Met-atheria, Mammalia) from the early Palaeocene of Bolivia.Phylogenetic and palaeobiologic implications. Geodiversitas20: 19–142.

Muizon C de. 1999. Marsupial skulls from the Deseadan (lateOligocene) of Bolivia and phylogenetic analysis of theBorhyaenoidea (Marsupialia, Mammalia). Geobios 32: 483–509.

Muizon C de, Argot C. 2003. Comparative anatomy of thedidelphimorph marsupials from the early Palaeocene ofBolivia (Pucadelphys, Andinodelphys, and Mayulestes).Palaeobiologic implications. In: Jones M, Dickman C,Archer M, eds. Predators with pouches: the biology of car-nivorous marsupials. Collingwood: CSIRO Publishing, 43–62.

Muizon C de, Cifelli RL. 2000. The ‘condylarths’ (archaicUngulata, Mammalia) from the early Palaeocene of Tiu-pampa (Bolivia): implications on the origin of the SouthAmerican ungulates. Geodiversitas 22: 47–150.

Muizon C de, Cifelli RL. 2001. A new basal ‘didelphoid’(Marsupialia, Mammalia) from the early Palaeocene of Tiu-pampa (Bolivia). Journal of Vertebrate Palaeontology 21: 87–97.

Muizon C de, Cifelli RL, Céspedez Paz R. 1997. The originof the dog-like borhyaenoid marsupials of South America.Nature 389: 486–489.

Muizon C de, Lange-Badré B. 1997. Carnivorous dentaladaptation in tribosphenid mammals and phylogeneticalreconstruction. Lethaia 30: 353–366.

Ortiz Jaureguizar E. 1998. Palaeoecología y evolución de lafauna de mamiferos de América del Sur durante la ‘edad delas planicies australes’ (Mioceno superior–Plioceno supe-rior). Estudios Geologicos 54: 161–169.

Oxnard CE. 1963. Locomotor adaptations in the primate fore-limb. Symposium of the Zoological Society of London 10:165–182.

Oxnard CE. 1968. The architecture of the shoulder in somemammals. Journal of Morphology 126: 249–290.

Pascual R. 1989. Late Cenozoic mammal dispersal betweenthe Americas: an overview of the South American evi-dences. Fifth International Theriological Congress (Rome22–29 August 1989, abstracts of papers and posters), 279–280.

Pascual R, Ortiz Jaureguizar E. 1990. Evolving climatesand mammal faunas in Cenozoic South America. Journal ofHuman Evolution 19: 23–60.

Pascual R, Ortiz Jaureguizar E. 1991. El ciclo faunisticocochabambiano (Palaeoceno temprano). Su incidencia en lahistoria biogeografica de los mamiferos sudamericanos. In:Suarez-Soruco R, ed. Fosiles y facies de Bolivia, Vol. I: Ver-tebrados. Santa Cruz (Bolivia): Revista Técnica de YPFB,559–574.

Pascual R, Ortiz Jaureguizar E. 1992. Evolutionary pat-tern of land mammal faunas during the late Cretaceousand Palaeocene in South America: a comparison with theNorth American pattern. Annales Zoologici Fennici 28:245–252.

Patterson B, Pascual R. 1968. Evolution of mammals onsouthern continents. V. The fossil mammal fauna ofSouth America. Quarterly Review of Biology 43: 409–451.

Pellis SM, Officer RCE. 1987. An analysis of some predatorybehaviour patterns in four species of carnivorous marsupials(Dasyuridae) with comparative notes on the eutherian catFelis catus. Ethology 75: 177–196.

Poole TB. 1974. Detailed analysis of fighting in polecats (Mus-telidae) using ciné film. Journal of Zoology, London 173:369–393.

Rabinowitz AR, Nottingham BG Jr. 1986. Ecology andbehaviour of the jaguar (Panthera onca) in Belize, CentralAmerica. Journal of Zoology, London 210: 149–159.

Radinsky L, Emerson S. 1982. The late, great sabertooths.Natural History 91: 50–57.

Rae TC, Bown TM, Fleagle JG. 1996. New palaeothentidmarsupials (Caenolestoidea) from the early Miocene ofPatagonian Argentina. American Museum Novitates 3165:1–10.

520 C. ARGOT


Rasmussen DT. 1997. Birds. In: In: Kay RF, MaddenRH, Cifelli RL, Flynn JJ, eds. Vertebrate paleontology inthe Neotropics. The Miocene fauna of La Venta, Colom-bia. Washington, DC: Smithsonian Institution Press,171–183.

Riggs ES. 1934. A new marsupial saber-tooth from thePliocene of Argentina and its relationships to other SouthAmerican predacious marsupials. Transactions of the Amer-ican Philosophical Society, N. S. 24: 1–31.

Roberts D. 1974. Structure and function of the primate scap-ula. In: Jenkins FA Jr, ed. Primate locomotion. New York:Academic Press, 171–200.

Rosenzweig ML. 1966. Community structure in sympatricCarnivora. Journal of Mammalogy 47: 602–611.

Rosenzweig ML. 1968. The strategy of body size in mam-malian carnivores. American Midland Naturalist 80: 299–315.

Savage RJG. 1977. Evolution in carnivorous mammals.Palaeontology 20: 237–271.

Schilling N, Fischer MS. 1999. Kinematic analysis oftreadmill locomotion of tree shrews, Tupaia glis(Scandentia: Tupaiidae). Zeitschrift für Säugetierkunde 64:129–153.

Scott WB. 1903a. Mammalia of the Santa Cruz beds:Edentata, Dasypoda. In: Scott WB, ed. Reports of thePrinceton University Expedition to Patagonia, 1896–1899,Vol. V, Part I, 1. Princeton University, 1–106, plates I-XVI.

Scott WB. 1903b. Mammalia of the Santa Cruz beds: Eden-tata, Glyptodontia and Gravigrada. In: Scott WB, ed. Reportsof the Princeton University Expedition to Patagonia, 1896–1899, Vol. V, Part I, 2. Princeton University, 107–227, platesXVII-XXXV.

Scott WB. 1904. Mammalia of the Santa Cruz beds: Eden-tata, Gravigrada. In: Scott, WB, ed. Reports of the Prince-ton University Expedition to Patagonia, 1896–1899, Vol. V,Part I, 3. Princeton University, 227–364, plates XXXVI-LXIII.

Scott WB. 1905. Insectivora and Glires. In: Scott, WB, ed.Reports of the Princeton University Expedition to Patagonia,1896–1899, Vol. V, Parts 2, 3. Princeton University, 365–499,plates LXIV-LXXI.

Scott WB. 1910. Litopterna of the Santa Cruz beds. In: Scott,WB, ed. Reports of the Princeton University Expedition toPatagonia, 1896–1899, Vol. VII, Part I. Princeton University,1–156, plates I-XX.

Scott WB. 1932. Nature and origin of the Santa Cruz fauna.In: Scott, WB ed. Reports of the Princeton University Expe-dition to Patagonia, 1896–1899, Vol. VII, Part 3. PrincetonUniversity: 193–238, plates A-K.

Shapiro LJ, Jungers WL. 1994. Electromyography of backmuscles during quadrupedal and bipedal walking in pri-mates. American Journal of Physical Anthropology 93: 491–504.

Simpson GG. 1974. Notes on Didelphidae (Mammalia, Mar-supialia) from the Huayquerian (Pliocene) of Argentina.American Museum Novitates 2559: 1–15.

Sinclair WJ. 1906. Marsupialia of the Santa Cruz beds. In:

Scott WB, ed. Reports of the Princeton University Expeditionto Patagonia, 1896–1899, Vol. IV, Part 3. Princeton Univer-sity, 333–460, plates XL-LXV.

Sinclair WJ, Farr MS. 1932. Aves of the Santa Cruz beds. In:Scott WB, ed. Reports of the Princeton University Expeditionto Patagonia, 1896–1899, Vol. VII, Part 2. Princeton Univer-sity, 157–191, plates XXI-XXXV.

Smith M. 1982. Review of the thylacine (Marsupialia,Thylacinidae). In: Archer M, ed. Carnivorous marsupials.Sydney: The Royal Zoological Society of New South Wales,237–253.

Stein BR, Casinos A. 1997. What is a cursorial mammal?Journal of Zoology, London 242: 185–192.

Szalay FS. 1982. A new appraisal of marsupial phylogenyand classification. In: Archer M, ed. Carnivorous marsupi-als. Sydney: The Royal Society of New South Wales. 621–640.

Szalay FS. 1994. Evolutionary history of the marsupials andan analysis of osteological characters. New York: CambridgeUniversity Press.

Szalay FS, Sargis EJ. 2001. Model-based analysis of postc-ranial osteology of marsupials from the Paleocene of Itabo-raí, Brazil, and the phylogenetics and biogeography ofMetatheria. Geodiversitas 23: 139–302.

Tauber AA. 1997. Paleoecología de la Formación Santa Cruz(Mioceno inferior) en el extremo sudeste de la Patagonia.Ameghiniana 34: 517–529.

Taylor ME. 1974. The functional anatomy of the forelimb ofsome African Viverridae (Carnivora). Journal of Morphology143: 307–336.

Turnbull WD, Segall W. 1984. The ear region of themarsupial sabertooth, Thylacosmilus: influence of thesabertooth lifestyle upon it, and convergence withplacental sabertooths. Journal of Morphology 181: 239–270.

Turner A, Antón M. 1997. The big cats and their fossil rela-tives. New York: Columbia University Press.

Van Valkenburgh B. 1985. Locomotor diversity within pastand present guilds of large predatory mammals. Paleobiol-ogy 11: 406–428.

Van Valkenburgh B. 1989. Carnivore dental adaptations anddiet: a study of trophic diversity within guilds. In: GittlemanJL, ed. Carnivore behaviour, ecology and evolution. London:Chapman & Hall, 410–436.

Viranta S. 1996. European Miocene Amphicyonidae – taxon-omy, systematics and ecology. Acta Zoologica Fennica 204:1–61.

Walton AH. 1997. Rodents. In: Kay RF, Madden RH, CifelliRL, Flynn JJ, eds. Vertebrate paleontology in the Neotropics.The Miocene fauna of La Venta, Colombia. Washington, DC:Smithsonian Institution Press, 392–409.

Wayne RK, Van Valkenburgh B, Kat PW, Fuller TK,Johnson WE, O’Brien SJ. 1989. Genetic and morphologi-cal divergence among sympatric canids. Journal of Heredity80: 447–454.

Wemmer CM. 1977. Comparative ethology of the large spottedgenet (Genetta tigrina) and some related viverrids. Smithso-nian Contributions to Zoology 239: 1–93.



White JL. 1997. Locomotor adaptations in Miocene xenar-thrans. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ, eds.Vertebrate paleontology in the Neotropics. The Miocene faunaof La Venta, Colombia. Washington, DC: Smithsonian Insti-tution Press, 246–264.

Wroe S. 2002. A review of terrestrial mammalian and reptil-ian carnivore ecology in Australian fossil faunas, and factorsinfluencing their diversity: the myth of reptilian dominationand its broader ramifications. Australian Journal of Zoology50: 1–24.

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