AMERICAN MUSEUM Novitates

PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH’ STREET, NEW YORK, NY 10024

Number 3330, 24 pp., 10 figures, 2 tables April 26, 2001

Basicranial Anatomy of the Living Linsangs Prionodon and Poiana (Mammalia, Carnivora, Viverridae), with Comments on the Early Evolution of Aeluroid Carnivorans

ROBERT M. HUNT, JR.!

CONTENTS

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' Research Associate, Division of Paleontology, American Museum of Natural History; Professor, Geological Sciences, and Curator, Vertebrate Paleontology, University of Nebraska, Lincoln, NE 68588-0549.

AMERICAN MUSEUM NOVITATES NO.

ABSTRACT

The living Asian linsang, Prionodon pardicolor, shares marked anatomical similarities in basicranium and dentition with the extinct Oligocene aeluroid, Palaeoprionodon lamandini, from the Quercy fissures, France. The living African linsang, Poiana richardsoni, is similar yet slightly more derived in basicranial traits relative to Prionodon pardicolor, and also has basicranial and dental features indicating a relationship to the living genets (Genetta). The basicranial and auditory anatomy of a series Palaeoprionodon-Prionodon-Poiana can be in- terpreted as a morphocline showing the progressive alteration of the form of the petrosal and auditory bulla from the plesiomorphic aeluroid state in the Quercy fossils to a derived con- dition typical of the linsangs (Prionodon, Poiana) and living genets (Genetta). The basicranial anatomy of Genetta, including the structure of the petrosal and auditory bulla, is typical of other species of the Viverridae. The other lineages of living viverrids are believed to have undergone a similar transformation in their basicranial anatomical pattern from the plesiom- orphic state present in Oligocene aeluroids, exemplified by Palaeoprionodon, to the modern patterns typical of the living subfamilies (including the endemic Malagasy viverrid genera).

1

INTRODUCTION

African and Asian linsangs of the family Viverridae are living, nocturnal aeluroid car- nivorans, occupying forested environs in the Old World tropics (fig. 1). The African lin- sang (Poiana Gray, 1864) is represented by one or at most two species in west Africa. Poina richardsoni and P. leightoni are dis- tributed from Liberia to northern Zaire, and the island of Fernando Po (Bioko), according to Rosevear (1974). They are considered here as a single species, P. richardsoni, following Pocock (1908), who recognized leightoni as a subspecies of richardsoni. The Asian lin- sangs (Prionodon Horsfield, 1822) are con- sidered to be more diverse: one species (the spotted linsang, P. pardicolor) is found from Nepal to Indochina, and a second species (the banded linsang, P. linsang) reported from Thailand and the Malay Peninsula into Sumatra, Java, and Borneo (Nowak, 1991). Linsangs nest above ground and eat insects, small vertebrates, and some plant material (Rosevear, 1974).

The Old World linsangs are of particular interest because of their evident anatomical similarity in cranial and dental features to one of the oldest fossil representatives of the aeluroid Carnivora, Palaeoprionodon laman- dini, from the Oligocene fissure deposits of Quercy, France (Teilhard de Chardin, 1915; Gregory and Hellman, 1939). A recent study of Palaeoprionodon and other closely related primitive aeluroids (Stenoplesictis, Stenoga- le, Proailurus) from the Oligocene and early Miocene of western Europe identified a ple-

siomorphic basicranial pattern common to these aeluroid genera (Hunt, 1998). As a re- sult, I became interested to learn whether liv- ing linsangs have retained throughout the mid- and later Cenozoic the archaic basicra- nial pattern of these Quercy aeluroids, and in particular, whether they retain the pattern found in Palaeoprionodon, which has often been allied with the Asian linsangs of the genus Prionodon (Teilhard de Chardin, 1915, Gregory and Hellman, 1939).

The living African and Asian linsangs are rare animals: Prionodon pardicolor and P. linsang are listed as endangered (by the Con- vention on International Trade in Endangered Species, and by the U.S. Department of the Interior). Although the eastern population of Poiana richardsoni is not reported as endan- gered, the western population is listed by the IUCN (international Union for Conservation of Nature) as of indeterminate status (No- wak, 1991); whether these eastern and west- erm groups are in contact through the tropical forest belt is uncertain—Rosevear (1974) considered them among the rarest of African mammals. Therefore, the opportunity to dis- sect the auditory region and describe the ba- sicranial anatomy of both Poiana _ richard- soni and Prionodon pardicolor was fortu- itous and timely. Are the linsangs “‘living fossils’??? This study considers the possibility that linsangs are relicts of the Oligocene ae- luroid fauna, preserving a basicranial mor- phology from a time when the Aeluroidea were in an initial phase of their great Eur- asian radiation.

2001 HUNT: AELUROID CARNIVORE EVOLUTION 3

Fer Tsang (Poiana hare ony and the Eurasian localities that have aaa fossils of the Oligocene aeluroid Palaeoprionodon. 1, Palaeoprionodon lamandini, Quercy fissures, France; 2, Hsanda Gol, Mongolia (?Palaeoprionodon); 3, Poiana richardsoni leightoni (western area), P. r. richardsoni

(eastern area); 4, Prionodon pardicolor (northern area), Prionodon linsang (southern area).

ABBREVIATIONS h hypoglossal (condyloid) foramen ic internal carotid artery Anatomical L middle lacerate foramen m mastoid

A alisphenoid P petrosal a “apron’’ of petrosal plf posterior lacerate foramen ac alisphenoid canal (posterior opening) pp paroccipital process of the exoccipital BO basioccipital R rostral entotympanic BS basisphenoid rp rugose surface of petrosal promonto- Cc common opening for the hypoglossal and rium for attachment of the caudal en-

posterior lacerate foramina in Poiana totympanic in Nandinia d depression in basisphenoid for internal SQ squamosal

carotid loop i ectotympanic E caudal entotympanic tf flange of the ventral process thinned by F facet on petrosal promontorium for ec- appression of the caudal entotympanic

totympanic tt tensor tympani fossa fo foramen ovale Vv ventral process of the petrosal promon- ef postglenoid foramen torium

+ AMERICAN MUSEUM NOVITATES NO. 1

x line of caudal entotympanic attachment to ectotympanic ZL contact of ectotympanic flange with pe-

trosal promontorium

Institutional

AMNH~ American Museum of Natural History,

New York (Department of Mammalo- gy)

FMNH ~ Field Museum of Natural History, Chi- cago (Department of Mammals) MNHN Muséum National d’ Histoire Naturelle,

Paris

CRANIAL AND DENTAL COMPARISONS

Cranial measurements of Prionodon, Poiana, and two skulls of Quercy Palaeo- prionodon illustrate their similarity in size and proportion (table 1). All four skulls have a basilar length of ~6—7 cm and display a similar form (figs. 2, 3): a slender, tapering rostrum; a gradually ascending forehead; and relatively large, wide orbits in which the an- terior part is floored by the maxilla (fig. 3). The braincase is conspicuously expanded rel- ative to the narrow rostrum, and the surface of the braincase indistinctly registers the to- pography of the neocortex. The cerebrum has not grown backward to cover the cerebellum in Prionodon and the Quercy skulls, and this is reflected in a distinct separation between the anterior and posterior parts of the brain- case (a constriction in the skull occurs be- tween the two regions). In Poiana there is a somewhat greater posterior overgrowth of the cerebellum by the cerebrum than in Prionodon. A triangular occiput is common to all four skulls; in the midline the vermis of the cerebellum produces a low elevation dorsal to the foramen magnum. A cranial en- docast of Prionodon pardicolor has been de- scribed and figured by Radinsky (1975), comparing it with that of Poiana and other living viverrids.

In the living linsangs and in the plesio- morphic Quercy (Palaeopriondon, Steno- plesictis) and St.-Gérand (Stenogale) aelu- roids, the foramen rotundum, orbital fissure, and optic foramen are deeply recessed in the sphenoid in a common elliptical depression located in the posteroventral orbital wall. In these carnivorans, the interorbital partition

(formed by the right and left orbitosphe- noids) is thin and narrow at this locus and probably represents the primitive aeluroid condition for the emergence of cranial nerves V,, V>, and the optic nerve from the brain- case. The optic foramen lies in close prox- imity to the orbital fissure in these aeluroids, in contrast to many arctoid carnivorans in which the optic foramen is placed farther for- ward along the orbital wall.

An alisphenoid canal is present, its poste- rior opening placed a few millimeters ante- rior to the foramen ovale. In Prionodon and Poiana the maxillary branch of the trigemi- nal nerve (V,) exits the braincase through the small foramen rotundum in the cranial wall and emerges within the alisphenoid canal. Both V, and the blood vessels traveling in the canal exit the skull directly below the or- bital fissure at the anterior opening of the ca- nal, which sometimes is confused with the true foramen rotundum.? This arrangement is also true of Genetta. Palaeoprionodon, al- though somewhat damaged in the orbital re- gion, appears to have been very similar to the living linsangs in the configuration of the orbital wall and the placement of these fo- ramina (Hunt, 1998: fig. 4A).

The palate of the linsangs and Palaeo- prionodon 1s triangular in ventral view, with a narrow anterior part that expands to its maximum width between the upper carnas- sials (fig. 2B). The upper dentition of these genera is delicate: the incisors are uniform in

? My identification of these foramina follows the in- terpretation put forward earlier by Pocock (1916a), based upon his detailed skull dissections. In many car- nivoran species, including the living linsangs, V, passes through the cranial wall via a small foramen that opens into the alisphenoid canal (this canal always lies external to the braincase and has anterior and posterior aper- tures). Pocock regarded the hidden internal opening in the cranial wall for V, as the true foramen rotundum, and the more visible external opening that transmits V,, once it has joined with the vessels of the alisphenoid canal, as the anterior aperture of the alisphenoid canal. Thus, in some carnivorans with an alisphenoid canal (alar canal of Miller et al., 1964), the foramen rotundum cannot be seen when looking at the orbit, but remains entirely hidden by the bony exterior wall of the alisphe- noid canal. However, in some pinnipeds (e.g., otariid Zalophus) the alisphenoid canal does not incorporate the true foramen rotundum for V, but remains a separate bony tube, and in this case the anterior opening of the alisphenoid canal and the foramen rotundum actually ap- pear as separate openings visible in the posterior orbit.

2001

HUNT: AELUROID CARNIVORE EVOLUTION

Fis. 12.

Skulls of the Quercy Palaeoprionodon (MNHN Qu 9370), the Asian linsang Prionodon

pardicolor (AMNH 163595), and the African linsang Poiana richardsoni (AMNH 51438), from left to right. (A) dorsal view; (B) ventral view. Scale bar in this and all subsequent figures is 1 cm.

shape and size and are arranged in a trans- verse row (I3 is only slightly larger than the interior incisors). P1-3 are thin bladelike teeth; Prionodon still retains a plesiomorphic double-rooted Pl, whereas Pl in Poiana and Genetta is single-rooted. P4 is a typical shearing carnassial with a small cuspate pro-

tocone and diminutive parastyle. The M1 is not present in the Palaeoprionodon skulls but, based on placement of the alveoli, prob- ably was similar in form to M1 in the lin- sangs where this tooth is a small narrow tri- angle with a prominent parastyle. However, M1 in Prionodon retains a distinct paracone

6 AMERICAN MUSEUM NOVITATES NO. 1

Fig. 3.

Skulls of the Asian linsang Prionodon pardicolor (AMNH 163595, above) and African

linsang Poiana richardsoni (AMNH 51438, below) in lateral view. Figures 3—10 are stereophotographs.

and metacone and is not as narrow as in Poiana, in which the paracone-metacone are subsumed in a thin crest and are no longer distinct cusps. I have not observed M2 in any of the living linsangs, but a vestigial M2 oc- curs in some individuals of Palaeopriono- don, and M2 has been reported in some spec- imens of Poiana richardsoni (Ewer, 1973; Rosevear, 1974). In the linsangs, the palatal choanae are closed (floored by bone) for 4— 5 mm posterior to the Mls, whereas in Pa- laeoprionodon this closure is not present.

In the mandible, the premolars (p2-4) of the living linsangs are thin bladelike teeth, each with anterior and posterior cingulum cusps and a posterior accessory cusp; in the Quercy genus the form of p3-4 is like that of the linsangs, but the p2 is usually reduced in size and thus often lacks these additional cusps. Remarkably, Prionodon shows the same reduction in size of p2 (relative to p3) seen in Palaeoprionodon, but the reduced p2 does not occur in Poiana. The p2 of Poiana is tall, not low, and in this trait, and in the form of the entire premolar row, it is clearly like that of the genets. The p1 is double-root- ed in Prionodon but is reduced to a single- rooted tooth in Poiana and Genetta.

There is a very close correspondence of ml form in Prionodon and Palaeopriono-

don: both have a tall trigonid with the para- conid-protoconid shearing blade set apart from a well-developed, conical, posterolin- gually directed metaconid, accompanied by a reduced, low, slightly basined talonid. But an even more striking similarity exists in the form of m2 in these two genera. The m2 of the Quercy genus is distinguished by a small low trigonid, in which the metaconid is set well apart (posterolingually displaced) from the protoconid-paraconid and separated from them by a prominent valley (Hunt, 1998: fig. 6h). This same derived form of m2 occurs in Prionodon pardicolor, but in the single in- dividual of Poiana richardsoni that I was able to examine, the m2 trigonid lacks the strongly displaced metaconid, and has the three trigonid cusps closely grouped as the points of an equilateral triangle. Neither Pa- laeoprionodon nor the species of living lin- sangs retain an m3.

Among the living viverrids, the taxa most closely resembling the linsangs in dentition, body form, and pelage are the genets (Ge- netta genetta and related species, Kingdon, 1977). Genets appear to be African linsangs scaled to larger size, differing only in such minor features as retention of M2 and in sub- tle variation in pelage patterns.

Thus, initial comparison of cranial and

2001 HUNT: AELUROID CARNIVORE EVOLUTION =,

TABLE 1 Comparative Cranial Measurements (in mm) of Prionodon pardicolor, Palaeoprionodon lamandini, and Poiana richardsoni (Carnivora, Viverridae).

TAXON Prionodon Paleoprionodon lamandini Poiana pardicolor richardsoni Measurement AMNH 163595 Qu 9348 Qu 9370 AMNH 51438 Basilar length 60.2 67.4 PLT 61.2 Rostral width 13.8 14.8 14.9 12.0 Braincase, greatest width 24.1 26.9 27.8 24.7 Palatal width between P4 paracones 1207 14.7 16:5" 11.8 Width between postorbital processes 13.8 ei 1S 3 16.8 Width between mastoid processes 21.8 24.6 24.9 21.4 Width between condyloid foramina 8.7 9.6 10.1 92k Ectotympanic, length 6.8 8.8 8.9 6.6 Ectotympanic, width at center Sel 4.6 4.9 3:9 Length, anterior auditory region?@ 58 8.1 ee2 5.6 Length, posterior auditory region’ 7.0 6.6 6.9 9:2 Condylobasal length 64.3 70.0 74.1 65.2 Condylobasal length’ 68.0 (Prionodon pardicolor, N = 7) 71.3 (Prionodon linsang, N = 9)

Condylobasal length’ 67.6 (Poiana richardsoni, N = 7)

“Measured between infraorbital foramina. > Estimated measurement.

“ Condyloid foramina are placed within the posterior lacerate foramina. ¢ Measured from apex of ventral promontorial process to anterior limit of ectotympanic. ¢ Measured from the apex of the ventral promontorial process to the posterior limit of the caudal entotympanic

chamber of the bulla. ‘From Pocock (1933). & From Rosevear (1974).

dental anatomy of the linsangs with the Quercy fossils suggests the possibility of re- lationship, one in which Prionodon is most similar to Palaeoprionodon; Poiana is more derived in its morphology, showing many correspondences with Genetta—the basicran- ium provides particularly relevant informa- tion on the nature of this relationship.

BASICRANIAL ANATOMY OF PALAEOPRIONODON

I have been able to study the basicranial anatomy of two skulls of Palaeoprionodon lamandini from Quercy, France, in the col- lections of the Muséum National d’ Histoire Naturelle, Paris. Both preserve the basicran- ium in very good condition: MNHN Qu 9348 retains both ectotympanic bones (one in the life position, demonstrated by the placement of the ectotympanic crura in sock- ets in the squamosal bone), and MNHN Qu

9370 preserves one ectotympanic—this bone is absent from the opposite side, allowing a full view of the petrosal and middle ear in this species. Detailed descriptions of the ba- sicranial structure of these two skulls are pre- sented in Hunt (1998). Here I illustrate Qu 9348 (fig. 4), and compare it with the basi- crania of the living linsangs.

The hallmark of the auditory region of Pa- laeoprionodon is a large, centrally placed, blocky petrosal, whose promontorium ex- tends below the plane of the basioccipital to form a prominent ventral process (fig. 4, V). This process buttresses the lateral margin of the basioccipital. The apex of the promon- torium with its ventral process divides the auditory region into anterior and posterior parts. The anterior part is covered by the crescent-shaped ectotympanic bone: the tip of the anterior crus rests in a small depres- sion in the squamosal; internal to this is a

8 AMERICAN MUSEUM NOVITATES NO. 1

broader concavity for the anterior face of the ectotympanic. The posterior crus is attached to the post-tympanic process of the squa- mosal that forms the anterior face of the mas- toid process.

The petrosal promontorium is so large in these early aeluroids that the posterior limb of the inwardly tilted ectotympanic crescent makes contact with the petrosal (fig. 4C, Z). This contact is marked by a prominent facet on the surface of the promontorium, imme- diately lateral to the ventral process (fig. 4B, F). This distinctive juxtaposition of ectotym- panic against the robust petrosal is an im- portant anatomical characteristic of the ge- nus.

However, it is the posterior part of the au- ditory region behind the promontorium that displays a striking plesiomorphic morpholo- gy unique to Palaeoprionodon among fossil aeluroids. Many living aeluroids (particularly felids and viverrids) have a greatly length- ened auditory region behind the promonto- rium, and this elongated space is occupied by a markedly inflated bony entotympanic cap- sule, the caudal entotympanic of Van der Klaauw (1922). In contrast, the earliest- known aeluroid crania from Quercy (Palaeo- prionodon, Stenoplesictis) and St.-Gérand (Stenogale) have short posterior auditory re- gions of very small volume, which would have been covered by a small, uninflated caudal entotympanic (Hunt, 1998). It is true that in the fossil Quercy crania no ossified caudal entotympanic element has been pre- served that would establish its actual size and shape. However, although the posterior au- ditory region remains open and uncovered in these Quercy aeluroids, the rim of the ecto- tympanic and the surfaces of the petrosal and surrounding basicranial bones demonstrate conclusively that a small plesiomorphic cau- dal entotympanic was present (fig. 4B, x and black triangles). It was either too loosely at- tached to remain with the skull during fos- silization or was formed of an unossified connective tissue, such as cartilage, which decayed and was not preserved.

Among the living aeluroids, only the Af- rican palm civet, Nandinia binotata, retains a cartilaginous caudal entotympanic in the adult (fig. 5). This is the most plesiomorphic caudal entotympanic known among living

aeluroids (Hunt, 1987: 32): a small, uninflat- ed hyaline cartilage that encloses a posterior auditory space of very small volume. When Nandinia’s caudal entotympanic is removed from the auditory region, its perimeter of at- tachment to the ectotympanic, petrosal, and rostral entotympanic is marked by character- istic ridges and rugose surfaces. Because the areas for the attachment of the caudal ento- tympanic to the ectotympanic and petrosal in Palaeoprionodon are nearly identical to the same areas in Nandinia (compare figs. 4 and 5A), it is virtually certain that a connective tissue element of similar form and dimen- sions, either fibrous or cartilaginous, formed the caudal entotympanic in Palaeopriono- don. This presumably cartilaginous entotym- panic would have covered the posterior au- ditory region, forming its floor, and then, as in young Nandinia, extended forward as a strip of tissue along the medial rim of the ectotympanic (fig. 5B, C). In both Nandinia and Palaeoprionodon there is a gap between the inner margin of the ectotympanic and the rostral entotympanic. This strip of connective tissue would fill this gap, intervening be- tween the inner edge of the ectotympanic and the ventral edge of the rostral entotympanic (compare figs. 4B, C and 5B, C); the rostral entotympanic is preserved as a small osseous wedge, separated from the ectotympanic, in some Quercy Palaeoprionodon (fig. 4, R). This condition can be observed in both ju- veniles and young adults of Nandinia (fig. 5, R).

Thus, the auditory bulla of Palaeoprion- odon was made up of three ontogenetic ele- ments: (a) a small, wedge-shaped, osseous rostral entotympanic in the anterointernal corner of the auditory region; (b) a slightly inflated (widened) bony ectotympanic cres- cent applied to the surface of the petrosal; and (c) a fibrous or cartilaginous caudal en- totympanic element of small size, covering a posterior auditory area of very small volume. Palaeoprionodon exhibits a plesiomorphic aeluroid auditory cachet, identified by the form of the petrosal and its ventral process, the ectotympanic resting against the robust promontorium, and particularly by the mod- est volume of the posterior chamber of the bulla enclosed by an unexpanded and unos- sified caudal entotympanic.

2001 HUNT: AELUROID CARNIVORE EVOLUTION 9

Fig. 4. The basicranium of Palaeoprionodon (MNHN Qu 9348) from Quercy: (A) ventral, (B) posteroventral, and (C) posterolateral views. In (B) small black triangles indicate line of attachment of the caudal entotympanic to the margin of the petrosal. For abbreviations in this and subsequent figures, see pages 3-4.

10 AMERICAN MUSEUM NOVITATES

5 : a. a ih, a -—

Fig. 5.

juvenile female from Akenge, Zaire (AMNH 51450), ventral view; (B) medial view of AMNH 51450; (C) neonate, from Medje, Zaire (AMNH 51472). The ectotympanic is separated from the osseous rostral

entotympanic by an intervening strip of connective tissue representing the anterior continuation of the caudal entotympanic.

Basicranium and auditory region of the living African aeluroid Nandinia binotata. (A),

2001

BASICRANIAL ANATOMY OF PRIONODON AND POIANA

A skull of Prionodon pardicolor was made available for dissection by the Depart- ment of Mammalogy, American Museum of Natural History. It is a female collected in 1938 from Mt. Victoria, Chin Hills, Burma, at an elevation of 2800 m (AMNH 163595). The form and size of the skull and the ex- pression of many anatomical details are ex- tremely similar to those of the Quercy Pa- laeoprionodon, and this is reflected in the ge- neric name initially given to the fossil taxon by Filhol (1880: 1579). Previous studies have emphasized the anatomical similarities between Prionodon and Palaeoprionodon (Teilhard de Chardin, 1915; Gregory and Hellman, 1939), but did not include a com- parison of their basicranial anatomy. A\I- though relevant distinctions can be found be- tween the two genera, the basicranial ana- tomical pattern of the living Prionodon par- dicolor, including construction of the auditory bulla, shows an evident relationship to the pattern in Palaeoprionodon.

For comparison with the Asian linsang Prionodon, a skull of the African linsang, Poiana richardsoni, was also made available for study—its auditory bulla already partially dissected. It is a male collected in 1910 from Medje, Zaire (AMNH 51438), at an un- known elevation in the northeastern part of the west African rain forest (Allen, 1924).

Figure 6 compares the basicrania of the Asian linsang (Prionodon pardicolor, AMNH 163595) and the African linsang (Poiana richardsoni, AMNH 51438). In gen- eral the two linsangs share a similar anatom- ical pattern. Some differences are evident: (a) the condyloid (hypoglossal) foramen remains separate from the posterior lacerate foramen in Prionodon, but is incorporated in that fo- ramen in Poiana; and (b) the ossified caudal entotympanic element of the auditory bulla is more inflated in Poiana than in Prionodon, and in the former has grown forward over the ectotympanic and backward toward the paroccipital process to a greater degree than seen in Prionodon. In both of these charac- ters, Prionodon is the more plesiomorphic taxon.

In both genera there is an alisphenoid ca-

HUNT: AELUROID CARNIVORE EVOLUTION 11

nal; a postglenoid foramen is absent, indi- cating loss of the vein exiting the cranium at that point to supply the external jugular ve- nous drainage (which is present in Palaeo- prionodon); the form and placement of the glenoid fossa for the mandible and its rela- tion to the auditory bulla and foramen ovale is the same; the mastoid region is not devel- oped as a prominent process or shelf; the ec- totympanic (anterior) chamber of the bulla lies directly in front of the caudal entotym- panic (posterior) chamber; and the ectotym- panic bone is a slightly expanded element resting on the petrosal promontorium.

Pocock (1916b) and Bugge (1978) de- scribed the path of the internal carotid artery in the auditory region of a number of viver- rids but did not include the linsangs. The in- ternal carotid artery in both genera takes es- sentially the same course: it enters the audi- tory region about midway along the length of the bulla—the point of entrance can be observed at the posterior end of the ventral process of the promontorium (fig. 6). The ar- tery runs between the flanged ventral process and the caudal entotympanic (remaining ex- ternal to that element, hence extrabullar), next travels along the lateral surface of the ventral process, and then follows the ventral edge of the rostral entotympanic, turning me- dially to enter the cranial cavity at the middle lacerate foramen. It is partially or entirely en- closed in a bony tube along the ventral bor- der of the rostral entotympanic. (Pocock [1916b] mistakenly thought that the rostral entotympanic of viverrids was part of the ec- totympanic bone.) The anteriorly directed ar- tery makes an abrupt 180° change in course at its anterior terminus in the auditory re- gion—here the artery forms a loop nested in a depression in the basisphenoid, turning backward to enter the middle lacerate fora- men. Thus, during its passage through the auditory region, the internal carotid artery never takes an intrabullar course: the artery does not penetrate the caudal entotympanic element to enter the posterior chamber of the bulla, and because it remains confined to the edge of the rostral entotympanic, it does not enter the anterior bulla chamber.

Prionodon has a robust, blocky petrosal centrally situated in the auditory region (fig. 7). Its promontorium is elevated to form a

V2 AMERICAN MUSEUM NOVITATES NO. 1

Fig. 6.

Basicrania of Prionodon (AMNH 163595, A) and Poiana (AMNH 51438, B) in ventral

view. The bony floor of the posterior chamber of the auditory bulla has been removed on one side in each individual to show the ectotympanic resting on the petrosal promontorium, and the size of the posterior chamber formed by the caudal entotympanic. Note the more expanded or inflated posterior

chamber in Poiana relative to Prionodon.

well-developed ventral process (V) that but- tresses the edge of the basioccipital (fig. 7B). The margins of the basioccipital are bent downward and applied to the medial face of the petrosal. Although the posterior face of the promontorium is more smoothly rounded in the Asian linsang, the form of the Prion- odon petrosal is much like that of Palaeo- prionodon. However, in Prionodon, the ven- tral process of the promontorium has a some- what more derived appearance than seen in the Quercy genus: it is apparent that the liv- ing Asian linsang has modified the blocky

ventral process of Palaeoprionodon, reshap- ing it into a low, laterally compressed flange tightly applied to the basioccipital. This flange becomes even more prominently de- veloped and bladelike in other genera of liv- ing viverrids (e.g., Genetta, Civettictis), but remains in an incipient state in Prionodon. In Poiana the promontorium and the flange are similar to these features in Prionodon, but the condition of the flange in Poiana is slightly more derived and begins to approach the more developed petrosal flange observed in such living viverrids as Genetta.

2001 HUNT: AELUROID CARNIVORE EVOLUTION 13

> i Pe,

Fig. 7. Dissection of the auditory region of Prionodon pardicolor (AMNH 163595) in oblique lateral view. The posterior chamber of the bulla has been opened (A), revealing the inflected dorsal margin of the caudal entotympanic applied to the petrosal, and the ectotympanic resting on the promontorium anterior to the round window. Removal of the ectotympanic and rostral entotympanic (B) allows an unrestricted view of the petrosal promontorium with its robust ventral process forming an incipient flange buttressing the edge of the basioccipital. Note that the caudal entotympanic covers the ventral

process of the promontorium when in place.

The degree of thinning of the ventral pro- cess of the petrosal in living viverrids (re- sulting in the eventual development of the bladelike flange) is an index of the amount of caudal entotympanic expansion. As the

auditory bulla of viverrids evolved, the pos- terior chamber increased in volume by ex- pansion of the caudal entotympanic element. During this process of relative growth, ap- plication of the enlarging caudal entotym-

14 AMERICAN MUSEUM NOVITATES NO. 1

panic to the petrosal promontorium altered the form of the ventral process in both Prion- odon and Poiana.

In the Quercy aeluroid, Palaeoprionodon, the unossified caudal entotympanic was sim- ilar in form to the cartilaginous entotympanic of Nandinia (fig. 5; also Hunt, 1987: figs. 6, 7B, 15—16), based upon a comparison of the well-preserved auditory anatomy of MNHN Qu 9348 and 9370 with that of Nandinia. The caudal entotympanic was a small, unex- panded element that covered the posterior auditory region behind the ectotympanic. Al- though it extended anteriorly along the me- dial rim of the ectotympanic to form part of the medial wall of the bulla, it did not alter the form of the ventral process of the pro- montorium. But in Prionodon, the anteriorly migrating and enlarging caudal entotympan- ic, accompanied by ossification of the ele- ment, compressed the ventral process to cre- ate the incipient flange. Continued enlarge- ment and anterior growth of the caudal en- totympanic chamber eventually produced the more derived flange observed in Poiana and in other living viverrids. The conversion of the ventral process of the promontorium in Poiana into an incipient flange proceeds from the posterior part of the process for- ward, and the creation of the flange is caused by the margin of the caudal entotympanic el- ement pressing only into the posterior part of the process, while not advancing craniad. This demonstrates that an advancing caudal entotympanic element can produce such a flange as it enlarges by a process of relative growth.

It is interesting that in a juvenile Poiana richardsoni (AMNH 51440) the ectotympan- ic is even larger in proportion to the caudal entotympanic than in the adult, and the rel- ative size of these two bulla elements in this juvenile effectively duplicates the size of the ectotympanic and (hypothetical) caudal en- totympanic elements in Palaeoprionodon. AMNH 51440 also shows that the caudal en- totympanic in a juvenile is confined to the posterior auditory region behind the ventral process of the promontorium and has not ini- tiated any significant forward growth in or- der to cover the ectotympanic. This is also true of Prionodon pardicolor.

The Asian linsang Prionodon and _ the

Quercy Palaeoprionodon share a similarly shaped ectotympanic bone, inclined inward toward the midline to the same degree, and resting on the promontorium. The posterior limb of the ectotympanic is directly applied to the surface of the promontorium immedi- ately anterior to the round window. Contact is made over a linear distance of ~3—4 mm in Prionodon (fig. 6, Z), but in the Quercy carnivore the contact is restricted to the lat- eral part of the promontorium at the location of the facet (fig. 4, Z). In Prionodon this con- tact extends farther medially, creating a more complete partition between the anterior and posterior chambers of the bulla. Both Poiana and Prionodon share this more internally ex- tended application of the ectotympanic rim to the promontorium (fig. 6, Z), which seems to be a derived trait, whereas the condition in the Quercy genus is considered to repre- sent the initial (rudimentary) application of the ectotympanic to the petrosal. Also, the ectotympanic in Prionodon is relatively and absolutely smaller than in Palaeoprionodon (table 1), so that in the Quercy genus the large ectotympanic and massive petrosal combine to produce an anterior bulla cham- ber of somewhat greater volume relative to the Asian linsang.

Just as in the Quercy genus, a small, wedge-shaped bony rostral entotympanic fits tightly into the anterointernal corner of the auditory region in Prionodon. Along its ven- tral margin runs the internal carotid artery, enclosed in a bony tube, with the exception of a short section of the lateral wall of the tube that is not ossified and is closed by con- nective tissue. The medial rim of the ecto- tympanic is inflected, and contacts and fuses with the edge of the rostral entotympanic.

The Asian and African linsangs share the same form and spatial relationship of the ec- totympanic and rostral entotympanic. In both genera the inner margin of the ectotympanic contacts the ventral edge of the rostral en- totympanic. The two bulla elements fuse along this line without intervention of the caudal entotympanic, and when the ectotym- panic is carefully detached from the auditory region, the rostral entotympanic accompanies it, the two elements delicately attached along the inner rim of the ectotympanic bone (fig. 8). In both genera, the internal carotid artery

2001

HUNT: AELUROID CARNIVORE EVOLUTION 15

Fig. 8.

Rostral entotympanic fused to the inner margin of the ectotympanic in Prionodon (AMNH

163595), medial view, ventral at top. Dashed line indicates path of the internal carotid artery within the

ventral edge of the rostral entotympanic.

travels along the ventral edge of the rostral element and does not enter the middle ear cavity. The application of the relatively unexpanded ectotympanic to the small rostral entotympanic element in Prionodon and Poiana is an aeluroid character state also pre- sent in most other living viverrids, hence does not distinguish these genera.

The American Museum skulls of the Asian and African linsangs can be immediately separated by the different degree of expan- sion of the caudal entotympanic. Among all living viverrids, Prionodon pardicolor shows the closest correspondence to Palaeopriono- don in the small volume of its posterior bulla chamber (fig. 7). Measurements of the length of the posterior auditory region (table 1) in- dicate that P. pardicolor is proportionately similar to the Quercy genus, and differs in this regard from Poiana (fig. 9). There is less expansion or inflation of the caudal entotym- panic in Prionodon relative to Poiana, and during the ontogeny of these linsangs a pro- gressive increase in inflation of this element occurs (e.g., a juvenile of Poiana richard- soni, AMNH 51440, a male with milk teeth collected in 1914 at Niapu, Zaire, shows less inflation of the caudal entotympanic than in the adults).

In Prionodon the relative amount of cau- dal entotympanic inflation appears to in- crease from northwest to southeast over the geographic range of the genus. Skulls of Prionodon pardicolor from Sikkim (FMNH 35463, female; 35464, male) at the north- western geographic limit of the species dis- play the least inflation. Skulls of P. pardi-

color from Tonkin and Assam (FMNH 39175, 39176, 75814, all males) show an in- termediate degree of inflation. Skulls of Prionodon linsang from Borneo (FMNH 88606, male; 8371, female) at the southeast- ern limit of the genus in southeast Asia de- velop the most inflated caudal entotympanic chambers. Inspection of Prionodon linsang in other North American collections indicates that this species has a consistently more in- flated caudal entotympanic bulla than P. par- dicolor. In P. linsang the caudal entotym- panic has grown forward, nearly covering the medial border of the ectotympanic, whereas in P. pardicolor the caudal entotympanic re- mains largely posterior to the ectotympanic, migrating forward along its posterointernal margin in slight but varying degree in dif- ferent individuals.

An estimate of the relative amount of cau- dal entotympanic inflation in Prionodon and Poiana is further indicated by the relation- ship of the paroccipital process to the pos- terior wall of the caudal entotympanic. In plesiomorphic carnivorans (e.g., Nandinia, Daphoenus, Cynodictis, Amphicynodon, Mustelictis, nimravine cats), the paroccipital process is not applied to the bulla, but rather exists as a rodlike process diverging postero- ventrally from the exoccipital. In most living viverrids, including Poiana, posterior growth and expansion of the caudal entotympanic creates a firm contact between entotympanic and the paroccipital process of the exoccip- ital, and as a result the process has become broadened and dorsoventrally expanded into a thin sheet of bone that covers most of the

16 AMERICAN MUSEUM NOVITATES NO. 1

Fig. 9. view (compare with fig. 7). The posterior chamber of the bulla has been opened (A), showing the inflected dorsal margin of the caudal entotympanic applied to the petrosal, and the ectotympanic resting on the promontorium anterior to the round window. Removal of the ectotympanic and rostral entotym- panic (B) reveals the petrosal promontorium with ventral process produced as a flange buttressing the edge of the basioccipital. The flange is more developed in Poiana than in Prionodon, and the caudal entotympanic element is more inflated.

posterior bulla wall. A discrete rodlike par- occipital process no longer exists in these vi- verrids. But in Prionodon, only a minimal amount of posterior expansion of the poste- rior bulla chamber (formed by caudal ento- tympanic) has taken place, and there is mere-

Dissection of the auditory region of Poiana richardsoni (AMNH 51438) in oblique lateral

ly a rudimentary contact between the bulla and the base of the paroccipital process. Con- sequently, the base of the process is only weakly indented by the expanding bulla, and the tip of the process remains recognizable, diverging slightly ventrad from the bulla (Po-

2001

cock, 1933). In primitive aeluroids, such as Palaeoprionodon and the living palm civet, Nandinia, the unossified caudal entotympan- ic attaches near the base of the paroccipital process, and the process remains a rodlike structure, descending from the skull, and is not thinned and applied to the bulla wall.

According to this interpretation, Priono- don is arrested at an evolutionary stage of bulla development only somewhat more ad- vanced than Palaeoprionodon, and evidently derived from that stage. The principal mor- phological changes necessary to modify the bulla of the Quercy aeluroid to arrive at the bulla morphology of Prionodon involved os- sification of the caudal entotympanic that forms the posterior chamber of the bulla, ac- companied by a small amount of inflation of the chamber. The modest inflation of the cau- dal entotympanic in Prionodon resulted in a slight change in shape of the ventral process of the promontorium, creating a nascent con- figuration of the petrosal flange that became more prominently modified and developed in other living viverrids. The auditory anatomy seen in Prionodon can be explained as an intermediate morph between the character state found in Palaeoprionodon and that of Poiana.

DISCUSSION AND CONCLUSIONS

The basicranial anatomy of the Asian lin- sang, Prionodon pardicolor, is of particular significance in a consideration of the early evolution of aeluroid carnivorans. Previous- ly, a study of the oldest known fossil aelu- roids from Quercy and St.-Gérand (Palaeo- prionodon, Stenoplesictis, Stenogale, Hap- logale, Anictis) indicated the existence of a primitive morphology of the petrosal and au- ditory bulla common to several of these early aeluroid taxa (Hunt, 1998). Skulls with well- preserved basicrania are known for Palaeo- prionodon, Stenoplesictis, and Stenogale. The auditory regions of these fossil aeluroids compare in anatomical grade with the living archaic aeluroid, Nandinia binotata, but no connecting or intermediate morphological stage existed to link the archaic and the mod- ern basicranial types. The basicranium of Prionodon pardicolor, particularly the audi- tory bulla and petrosal, provides that critical

HUNT: AELUROID CARNIVORE EVOLUTION Fy.

link. Its auditory region not only can be de- rived from that of the Oligocene aeluroid, Palaeoprionodon, but also can be interpreted as a transitional state between the Quercy ge- nus and the living African linsang, Poiana. Both Prionodon and Poiana exhibit an early stage in the development of the modern vi- verrid auditory region found in living Ge- netta, which is similar to the auditory region of the other living viverrids.

Of particular importance is the form of the petrosal promontorium in Prionodon pardi- color and Poiana richardsoni (fig. 10): the ventral process of the promontorium is pro- duced as an incipient flange on the medial margin of the Prionodon petrosal. Poiana displays a similar but more developed flange. Yet both petrosals are very little modified from the plesiomorphic aeluroid state found in the Quercy Palaeoprionodon. Other ana- tomical features of the auditory region of these two living genera are correlated with the differing degree of development of the flanged ventral process—plesiomorphic char- acters in Asian Prionodon are consistently more derived in African Poiana: Prionodon pardicolor has (a) a modest inflation of the caudal entotympanic chamber of the bulla; (b) a discrete hypoglossal foramen separated from the posterior lacerate foramen; and (c) an independent paroccipital process—Poiana has a more developed petrosal flange, a more inflated caudal entotympanic, and has merged the hypoglossal with the posterior lacerate foramen. The greater amount of ex- pansion of the caudal entotympanic in Poiana has caused the paroccipital process to spread over the rear wall of the bulla, but in Prionodon, because there is less expansion of the bulla, a vestige of the independent pro- cess remains.

There are other anatomical traits that sug- gest linsangs conserve a number of plesio- morphic viverrid features. Prionodon is more conservative in these features relative to Poiana.

For example, the surface of the neocortex of Prionodon and Poiana retains one of the simplest patterns among viverrids (Radinsky, 1975): there are only two major sulci, the coronolateral and suprasylvian, and in Prion- odon the cerebellum shows only a minimal

18 AMERICAN MUSEUM NOVITATES NO. 1

amount of overlap by the cerebrum, whereas in Poiana the amount of overlap is greater.

The perineal scent glands are absent in Prionodon pardicolor (Pocock, 1915a), but appear to be present in a rudimentary state in Poiana (Pocock, 1933: 970; Rosevear, 1974: 222). Pocock quite reasonably argued that the absence of perineal glands in such viverrids as Prionodon, Fossa, and Crypto- procta, as well as their absence in herpestids, felids, and hyaenids, indicated that the an- cestral aeluroid lacked such glands, which were later independently acquired in various viverrid lines. Pocock’s argument receives support from the observation that perineal glands differ in position and in anatomical detail in the various living viverrids that have these glands (the details of glandular struc- ture and position are presented in a series of papers by Pocock, 1915a, 1915b, 1915c, 1915d, 1915e; Pocock, 1915d, clearly pre- sents his rationale for the evolution of peri- neal glands.) Considering the array of ple- siomorphic basicranial features in Priono- don, the absence of perineal glands is in- structive. In Prionodon the placement of the penis in proximity to the scrotum, and the vulva to the anus, stands in contrast to their separation in viverrids with perineal glands, and appears to be plesiomorphic for aelu- roids, since this state also occurs in felids, herpestids, and Nandinia (but not in hyaen- ids).

Earlier studies of the linsangs by Mivart (1882) and Pocock (1915a) established that the color and pattern of the pelage and the external anatomy of the feet and rhinarium also supported a relationship between the Asian and African species. My own obser- vations of the pelage of the two genera are in agreement (brown with black markings, mostly spotted, with some striping on the shoulders, and rings around the tail). The ability to retract the claws is present in both genera, and the texture of the fur and their general appearance and behavior particularly reminds one of many of the small living fe- lids.

Finally, the pronounced similarity in de- tails of the dentition of Palaeoprionodon and Prionodon (form of m1, m2, reduction of an- terior premolars), and the retention of ple- siomorphic double-rooted P1/p1 in Priono-

don, also support a close relationship be- tween the Quercy genus and the Asian lin- sang.

G. G. Simpson (1945) had placed Prion- odon in a tribe, Prionodontini, and Poiana in the Viverrini closely related to Genetta. Such segregation of Prionodon essentially follows Pocock’s (1933) separation of the genus (as a subfamily Prionodontinae) following his discovery that perineal glands were absent in both sexes. Rosevear (1974) thought that the similarities between the Asian and African linsangs were convergent and without evi- dence of affinity. Here I would argue that the basicranial similarities, coupled with evident correspondence in size and form of these an- imals, their dental and cranial traits, and pel- age and external anatomy of the feet empha- sized by Pocock, suggest a phylogenetic af- finity among living Asian and African lin- sangs and genets, an affinity shared at a more basic level with the archaic aeluroids of the genus Palaeoprionodon. In this sense, then, because one of these living aeluroids, Prion- odon pardicolor, can be closely identified with an Oligocene genus from Quercy, and was much like it in size, body form, and in details of cranial and dental anatomy, this species of Asian linsang is reasonably con- sidered a “‘living fossil’’, a modern proxy for an Oligocene grade of aeluroid evolution that has shown little change in ~25-—30 million years.

The combined anatomical evidence sug- gests the existence of a clade that includes the Oligocene Palaeoprionodon as a ple- siomorphic stem taxon, and the more derived living genera, Prionodon, Poiana, and Ge- netta, as member taxa of a hypothetical mor- phocline. Gregory and Hellman (1939) placed both Prionodon and Palaeoprionodon in their subfamily Prionodontinae, and this subfamily I believe can reasonably incorpo- rate not only the Quercy Palaeoprionodon, but also the species of living linsangs and genets (table 2). Gregory and Hellman (1939: 335) thought that the skull of Palaeo- prionodon could represent the ancestor “‘of all the diverse subfamilies of the Viverri- dae’’. Study of the Quercy fossils suggests a more limited role for Palaeoprionodon near the ancestry of only the linsangs and genets. The viverrine viverrids (Viverra, Viverricula,

2001 HUNT: AELUROID CARNIVORE EVOLUTION 19

Fig. 10. Final stage of the dissection of the auditory bulla of Prionodon (AMNH 163595, A) and Poiana (AMNH 51438, B) in ventral view. Note the robust ventral process of the promontorium in Prionodon, only incipiently modified as a flange appressed against the basioccipital, hence similar to the form of the ventral process in Palaeoprionodon (compare with fig. 4). In Poiana the flange has been further modified as a thin blade and has been extended fore and aft to a greater degree than in Prionodon. The caudal entotympanic is more inflated in Poiana, broadly contacting the paroccipital process, whereas in Prionodon the caudal entotympanic is not as expanded, and the process still retains a vestige of its primitive rodlike form.

20 AMERICAN MUSEUM NOVITATES NO. 1

Civettictis) appear to be closely related to the Prionodontinae because of their marked sim- ilarity in dental and basicranial anatomy. But the other principal subfamilies of viverrids, the Paradoxurinae and Hemigalinae, proba- bly stem from other early aeluroids of Eo- cene or Oligocene age.

Pocock (1916b) astutely remarked that the Viverridae, as originally conceived by Flow- er (1869) and Mivart (1882), was ‘‘a hetero- geneous group including all the aeluroids which are not obviously cats or hyaenas’’. Part of this heterogeneity derived from inclu- sion of the mongooses in Viverridae; today, herpestids have been removed from Viverri- dae by general consensus (Gregory and Hell- man, 1939; Hunt, 1987, 1991; Wyss and Flynn, 1993; McKenna and Bell, 1997). Re- cent studies of the aeluroid Carnivora have recognized the morphologic uniformity of herpestids, as well as the living felids and hyaenids—a highly uniform basicranial mor- phology characterizes each family, and on- going molecular/biochemical studies also support the integrity of these groups (Wurster and Benirschke, 1968; Wurster-Hill and Gray, 1975; Wayne et al., 1989). But viver- rids are consistently seen as more diverse, an observation that would appear to be sup- ported by the variety of subfamilies and gen- era created for these carnivores by Pocock and other students, many genera including only a single species.

Are the viverrids a monophyletic group? What evidence exists to suggest that viver- rids are not simply a polyphyletic aggregate of primitive aeluroids? I would argue that three lines of evidence support monophyly: (a) the morphology of the basicranium, par- ticularly the ontogenetic development and adult form of the auditory bulla and petrosal (Hunt, 1974, 1987); (b) the general tendency to develop perineal glands in the family (Po- cock); and (c) molecular-biochemical evi- dence indicating relationship among genets, civets, and paradoxures (Wayne et al., 1989). But the tracing of living viverrid genera and species backward in time beyond the later Cenozoic has met with little recent success.

The relatively poor fossil record of viver- rids is in part responsible for this situation (Petter, 1974; Hunt, 1996a, for a summary of the viverrid fossil record). We know little of

the diversity that existed during the early his- tory of the family, confined as it is to the Old World, where much of the viverrid record of fragmentary jaws and teeth comes from ex- ceptional burial settings such as the fissure deposits at Quercy, La Grive, and Winter- shof-West, and the freshwater limestones of St.-Gérand and Oeningen. The few European viverrid fossils, coupled with a rather meager Asian record, make it difficult to determine if the living genera are of considerable anti- quity, or if the species diversity evident today in southeast Asia and Africa only recently came into existence.

Because many early viverrids were prob- ably arboreal and thrived in subtropical to tropical forests, where skeletal remains often are infrequently preserved in the fossil re- cord, their past history could continue to re- main poorly known. However, as some vi- verrids occupied more open environments in semiarid to arid regions during the climatic cooling of the Neogene, particularly in tec- tonically active regions in south Asia and the African rift, where sedimentation in restrict- ed basins was taking place, the probability of preservation of these species increased and a modest record has developed in these set- tings. But the scarcity of viverrid fossils in these sedimentary environments suggests that they were never very abundant, with a species diversity probably similar to the pre- sent.

This perspective envisions the preserva- tion of Palaeoprionodon and other aeluroid fossils at Quercy as the chance result of the development of karst terrain in southern France in the Eocene and early Oligocene. Karst fissures serve as particularly effective traps for small carnivores. Indeed, the karst fissures at Quercy sample a rather diverse ae- luroid array of taxa [the early felids Proail- urus and Stenogale, a genet-like aeluroid Haplogale, the enigmatic aeluroids Steno- plesictis and Anictis (Teilhard de Chardin, 1915; Hunt, 1998)]. The Quercy “‘window”’ provides a brief, geographically limited glimpse into an aeluroid radiation that we know was not confined to western Europe but was probably unfolding throughout the Eurasian landmass, based upon the fossil ae- luroid record beginning to appear at eastern Asian localities such as Hsanda-Gol, Alag

2001

Tsab, and Ergil Obo (Dashzeveg, 1996). Pa- laeoprionodon is not necessarily the ances- tral viverrid, as Gregory and Hellman claimed, but is only one of a stem group of early aeluroids that includes Haplogale, Stenogale, Stenoplesictis, and Proailurus in Europe, and Asiavorator, Shandgolictis, Proailurus, and additional poorly known species in eastern Asia (Hunt, 1998). The plesiomorphic aeluroid basicranial pattern common to several of these genera suggests that the same pattern probably was shared by other early aeluroids distributed across Eur- asia at this time, many as yet unrepresented by cranial remains.

The abrupt appearance of Quercy aelu- roids at the beginning of the Oligocene, fol- lowing the Grande Coupure event in Europe, yet their complete absence in the Eocene fau- nas that precede that event, has suggested to several investigators that aeluroids immigrat- ed to Europe from elsewhere. It is possible that increasing continental aridity in central Asia during the Oligocene could have ac- companied the development and radiation of aeluroids in that region, leading eventually to their spread westward across the Eurasian landmass. The importance of the fossils that we can now view through the Quercy-Mon- golia “‘window”’ into early aeluroid evolu- tion is found in the similar dentitions of these geographically dispersed fossil species, and in the uniformity of the known basicranial patterns among various genera, the sum of the evidence indicating that these aeluroid fossils document an initial phase of the Eur- asian aeluroid diversification.

Of particular significance, however, is the fact that these Oligocene aeluroids do not in- clude clear and direct morphological ante- cendents to modern viverrid species (with the exception of Palaeoprionodon). The Oligo- cene aeluroids display an archaic basicranial pattern and hypercarnivorous dentitions that are much different from the derived auditory anatomy and dentitions of many living vi- verrids.

Within the Viverridae, several subgroups have been consistently recognized since the 19th century (Mivart, 1882; Gregory and Hellman, 1939; Simpson, 1945; McKenna and Bell, 1997): the subfamilies Viverrinae, Paradoxurinae, and Hemigalinae (table 2).

HUNT: AELUROID CARNIVORE EVOLUTION 21

TABLE 2 Classification of the Aeluroid Families Viverridae and Nandiniidae

Order Carnivora Bowdich, 1821 Division Aeluroidea Flower, 1869 Family Viverridae Gray, 1821

Subfamily Prionodontinae Pocock, 1933

Palaeoprionodon Filhol, 1880 Prionodon Horsfield, 1821 Poiana Gray, 1864

Genetta G. Cuvier, 1816

Subfamily Viverrinae Gray, 1821

Viverra Linnaeus, 1758 Viverricula Hodgson, 1838 Osbornictis Allen, 1919 Civettictis Pocock, 1915

Subfamily Euplerinae Chenu, 1852

Fossa Gray, 1864 Eupleres Doyere, 1835

Subfamily Cryptoproctinae Gray, 1864 Cryptoprocta Bennett, 1833

Subfamily Hemigalinae Gray, 1864 Hemigalus Jourdan, 1837 Diplogale Thomas, 1912 Chrotogale Thomas, 1912 Cynogale Gray, 1837

Subfamily Paradoxurinae Gray, 1864 Paradoxurus F. Cuvier, 1821 Paguma Gray, 1831 Arctictis Temminck, 1824 Arctogalidia Merriam, 1897 Macrogalidia Schwartz, 1910

Family Nandiniidae Pocock, 1929 Nandinia Gray, 1843

The Viverrinae most often include the genera Viverra, Viverricula, Civettictis, Osbornictis, Genetta, Poiana, and occasionally the Mal- agasy Fossa. All are restricted to or largely confined to Africa except for Viverra and Viverricula, which are found in southeast Asia (a large species of Viverra, however, oc- curred in Africa in the Plio-Pleistocene, see Petter, 1963; Hunt, 1996b). Viverrines are dentally conservative, maintaining a shearing carnassial pair and functional molars (M1-2, m1-2).

With the exception of the viverrids isolat- ed on Madagascar (Fossa, Eupleres, Cryp- toprocta; for a review see Petter, 1974), the

22 AMERICAN MUSEUM NOVITATES NO. 1

remaining living genera are found in south- east Asia and the islands of Indonesia and are placed in the subfamilies Paradoxurinae (Paradoxurus, Paguma, Arctictis, Arctogali- dia, Macrogalidia) and Hemigalinae (Hemi- galus, Diplogale, Chrotogale, Cynogale). Certain lines of evidence, such as the endo- cranial casts of viverrids studied by Radinsky (1975) suggest that the paradoxures may be made up of closely related genera. Both sub- families are composed of species that occupy forested settings; are largely nocturnal and arboreal; have perineal glands (reduced or lost in some males); are usually plantigrade, with the entire sole of the hindfoot in contact with the substrate; and have evolved modi- fied carnassials and molars in which the typ- ical shearing function is modified to a crush- ing mode, and the posterior molars can be quite small and reduced in size. Paradoxures and hemigalines seem to be geographically restricted relict species, derived from an ear- lier viverrid radiation in eastern Asia—an as- semblage of diverse taxa that survived in tropical-subtropical settings as these environ- ments became restricted to lower latitudes during mid- and late-Cenozoic global cool- ing. The climatic oscillations of the late Pli- ocene and Pleistocene probably contributed to the species diversity of the paradoxures and hemigalines. Lowering of global sea lev- el during glacial maxima provided land mi- gration routes from the Asian mainland southward to the islands of the Sunda shelf, permitting the movement of south Asian mammals into the islands of Indonesia. When warmer interglacial intervals flooded the Sunda shelf, creating the islands of Su- matra, Java, Borneo, and the numerous smaller satellite islands, the isolation of vi- verrid populations on these islands must have resulted in genetic fragmentation of once- continuous populations. With sufficient time and continued isolation, the fragmented pop- ulations could serve as a potential stockpile for the derivation of new viverrid species. The geographic restriction of paradoxures and hemigalines to forested tropical environ- ments virtually assures that this scenario oc- curred in Indonesia in the later Cenozoic. The more terrestrial viverrid species of Af- rica (Genetta, Civettictis) and southeast Asia (Viverra, Viverricula) are made up of con-

joined or geographically adjacent popula- tions that occur in spatial continuity over large geographic regions. The wide-ranging terrestrial character of these viverrids (al- though most climb well and utilize trees) suggests a genetic continuity over their rang- es, with less tendency to fragment into allo- patric species. Viverra-Viverricula comprises a group of similar, closely related species ex- tending from Nepal and eastern India to south China, Indochina, and continuing southward to Malayasia and the Indonesian islands. They differ little except in size. The large bush civet, Civettictis, despite its con- siderable geographic range from the southern border of the Sahara southward to Namibia and South Africa, exists as a single species (C. civetta) in both forest and savanna en- vironments. At least nine species of genets (Genetta) are said to occupy forests, grass- lands, and savannas over nearly all of Africa (Nowak, 1991); this species diversity has been called into question (Rosevear, 1974), because genets are known to be highly var- iable in size, pelage color, and even cranial characters (Allen, 1924). It is likely that a number of the named species may in fact be capable of interbreeding and are not repro- ductively isolated. Much of the variation ob- served among the genets may be the result of the widespread distribution of the species over the African continent, and the conse- quent adaptation of populations to local con- ditions. Kingdon (1977) notes that diversifi- cation in African genets has produced a num- ber of distinct ecological species adapted to particular environments (some of these spe- cies have produced hybrids in captivity). To what extent the diversification of African vi- verrids is due to the fluctuation in tropical forested environments during the Quaternary glacial episodes remains an interesting and unresolved question.

The considerable diversity of paradoxures, hemigalines, and the viverrines Viverra and Viverricula, seems somehow linked to the episodic isolation of land areas in Indonesia and adjacent southeast Asia during the cli- matic oscillations of the late Cenozoic. On the other hand, the African viverrids Civet- tictis and Genetta, although widely distrib- uted over the continent and exhibiting evi- dent populational variation, are without the

2001

production of marked generic diversity equivalent to that seen in southeast Asian vi- verrids.

Malagasy viverrids include the cranially and dentally plesiomorphic species Fossa fossa and the highly derived and specialized Eupleres and Cryptoprocta, that are not in evidence anywhere outside Madagascar, and likely represent endemic lineages evolved in isolation on the island. An improved fossil record of viverrids from the Neogene of Eur- asia and Africa will be necessary to under- stand the origins of these diverse viverrid subgroups.

ACKNOWLEDGMENTS

I am grateful to Dr. L. Ginsburg, Muséum National d’Histoire Naturelle, Paris, for per- mission to study the crania of Quercy aelu- roids, and to Dr. N. Simmons, American Mu- seum of Natural History, New York, for the loan of the skulls of Prionodon and Poiana, and for allowing the dissection of the audi- tory regions of representative individuals. My thanks to Dr. Bruce Patterson, Field Mu- seum of Natural History, Chicago, for the opportunity to study the linsang material in their collections. For figure 1, I thank illus- trator Angie Fox, University of Nebraska State Museum, Lincoln.

REFERENCES

Allen, J. A.

1924. Carnivora collected by the American Museum Congo Expedition. Bull. Am. Mus. Nat. Hist. 47(3): 73-281.

Bugge, J.

1978. The cephalic arterial system in carni-

vores, with special reference to the sys- tematic classification. Acta Anat. 101: 45-61.

Dashzeveg, D.

1996. Some carnivorous mammals from the Paleogene of the Eastern Gobi Desert, Mongolia, and the application of Oli- gocene carnivores to stratigraphic cor- relation. Am. Mus. Novitates 3179: 14.

Ewer, R. FE

1973. The Carnivores. Ithaca, NY: Cornell

Univ. Press, 494 pp. Filhol, H.

1880. Sur la découverte de mammiféres nou-

veaux dans les dépdts de phosphates de

HUNT: AELUROID CARNIVORE EVOLUTION 23

chaux du Quercy. C. R. Acad. Sci., Par- is 90: 1579-1580. Flower, W. H.

1869. On the value of the characters of the base of the cranium in the classification of the Order Carnivora. Proc. Zool. Soc. London 1869: 4—37.

Gregory, W. K., and M. Hellman

1939. On the evolution and major classifica- tion of the civets (Viverridae) and al- lied fossil and recent Carnivora: a phy- logenetic study of the skull and denti- tion. Proc. Am. Philos. Soc. 81(3): 309-392.

Hunt, R. M., Jr.

1974. The auditory bulla in Carnivora: an an- atomical basis for reappraisal of carni- vore evolution. J. Morphol. 143: 21-76. Evolution of the aeluroid Carnivora: significance of auditory structure in the nimravid cat Dinictis. Am. Mus. Nov- itates 2886: 74 pp.

Evolution of the aeluroid Carnivora: vi- verrid affinities of the Miocene carni- voran Herpestides. Am. Mus. Novitates 3023: 34 pp. 1996a. Biogeography of the Order Carnivora. In J. Gittleman (ed.), Carnivore Behav- ior, Ecology and Evolution 2: 485-541. Ithaca, NY: Cornell Univ. Press. 1996b. Basicranial anatomy of the giant viver- rid from ‘E’ Quarry, Langebaanweg, South Africa. In K. Stewart and K. Seymour (eds.), Palaeoecology and Pa- laeoenvironments of Late Cenozoic Mammals: Tributes to the Career of C.S. Churcher: 588-597. Toronto: Univ. Toronto Press. Evolution of the aeluroid Carnivora: di- versity of the earliest aeluroids from Eurasia (Quercy, Hsanda-Gol) and the origin of felids. Am. Mus. Novitates 3252? -65..pp: Kingdon, J.

1977. East African Mammals: An Atlas of Evolution in Africa. Vol. II(A), Car- nivores. New York, NY: Academic Press, 476 pp.

Klaauw, C. J. van der

1922. Uber die Entwickelung des Entotym- panicums. Tijdschr. Ned. Dierk. Ver- een. 18: 135-174.

McKenna, M. C., and S. K. Bell

1997. Classification of Mammals Above the Species Level. New York: Columbia Univ. Press, 631 pp.

1987.

LOST.

1998.

24 AMERICAN MUSEUM NOVITATES NO. 1

Miller, M. E., G. C. Christensen, and H. E. Evans 1964. The Anatomy of the Dog. Philadelphia: W. B. Saunders, 941 pp. Mivart, S t. G. 1882. On the classification and distribution of the Aeluroidea. Proc. Zool. Soc. Lon- don 1882: 135-208. Nowak, R. M. 1991. Walker’s Mammals of the World (5th ed.) 2: 1149-1151. Baltimore: Johns Hopkins Univ. Press.

Petter, G.

1963. Etude de quelques Viverridés (Mam- miféres, Carnivores) du Pleistocéne in- férieur du Tanganyika. Bull. Soc. Géol. Fr. (ser. 7) 5: 265-274.

1974. Rapports phylétiques des Viverridés (Carnivores fissipédes). Les formes de Madagascar. Mammalia 38(4): 605— 636.

Pocock, R. I. 1908. Report upon a small collection of

Mammalia brought from Liberia by Mr. Leonard Leighton. Proc. Zool. Soc. London 1907: 1037-1046.

1915a. On some of the external characters of the genus Linsang, with notes upon the genera Poiana and Eupleres. Ann. Mag. Nat. Hist. 16: 341-351.

1915b. On the feet and glands and other exter- nal characters of the Viverrinae, with the description of a new genus. Proc. Zool. Soc. London 1915: 131-149.

1915c. On the feet and glands and other exter- nal characters of the paradoxurine gen- era Paradoxurus, Arctictis, Arctogali- dia, and Nandinia. Proc. Zool. Soc. London 1915: 387-412.

1915d. On some external characters of Gali- dia, Galidictis, and related genera. Ann. Mag. Nat. Hist. 16: 351-356.

1915e. On some of the external characters of the palm-civet (Hemigalus derbyanus, Gray) and its allies. Ann. Mag. Nat. Hist. 16: 153-162.

191l6a. The alisphenoid canal in civets and hy- aenas. Proc. Zool. Soc. London 1916: 442-445.

1916b. On the course of the internal carotid ar- tery and the foramina connected there- with in the skulls of the Felidae and Viverridae. Ann. Mag. Nat. Hist. 17: 261-269.

1933. The rarer genera of Oriental Viverridae. Proc. Zool. Soc. London 1933: 969— 1035: Radinsky, L. 1975. Viverrid neuroanatomy: phylogenetic

and behavioral implications. J. Mam- mal. 56(1): 130-150. Rosevear, D. R. 1974. The Carnivores of West Africa. Br. Mus. (Nat. Hist.) Publ. 723: 220-228. Simpson, G. G. 1945. The principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist. 85: 350. Teilhard de Chardin, P. 1915. Les carnassiers des phosphorites du Quercy. Ann. Paléontol. 9(3,4): 1-90. Wayne, R. K., R. E. Benveniste, D. N. Janczews- ki, and S. J. O’Brien 1989. Molecular and biochemical evolution of the Carnivora. In J. Gittleman (ed.), Carnivore behavior, ecology, and evo- lution 2: 465—494. Ithaca, NY: Cornell Univ. Press. Wurster, D. H., and K. Benirschke 1968. Comparative cytogenetic studies in the Order Carnivora. Chromosoma 24: 336-382. Wurster-Hill, D. H., and C. W. Gray 1975. The interrelationships of chromosome banding patterns in procyonids, viver- rids, and felids. Cytogenet. Cell Genet. 15: 306-331. Wyss, A. R., and J. J. Flynn 1993. A phylogenetic analysis and definition of the Carnivora. Jn FE S. Szalay, M. J. Novacek, M. C. McKenna (eds.), Mammal phylogeny (placentals) 32— 52. New York: Springer.

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