VAN VALKENBURGH AND JENKINSHISTORY OF SYNAPSID PREDATORS

EVOLUTIONARY PATTERNS IN THE HISTORY OF PERMO-TRIASSIC AND CENOZOIC SYNAPSID PREDATORS

BLAIRE VAN VALKENBURGH1 AND IAN JENKINS2
1

Department of Organismic Biology, Ecology and Evolution, University of California, Los Angeles, California 90095-1606, USA 2 Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queens Road, Bristol, BS8 1RJ, England

ABSTRACTSynapsids include modern mammals and their fossil ancestors, the non-mammalian synapsids, or mammal-like reptiles of old classifications. The synapsid fossil record extends from the Late Carboniferous to the present, a span of nearly 300 million years. However, it can be broken into two distinct phases of diversification, separated by about 150 million years. The first phase extends from the Late Carboniferous to the mid-Triassic, includes the first large land predators on Earth, and is almost entirely non-mammalian. The second phase begins about 65 million years ago after the demise of the dinosaurs, includes only mammals, and extends to the present. In this overview of synapsid predators, we emphasize terrestrial species of large size, and their adaptations for killing and feeding, rather than locomotion. Despite fundamental differences in jaw mechanics and tooth morphology, there are significant parallels in the non-mammalian and mammalian radiations of synapsid predators. Both groups evolve sabertooth forms more than once, and both evolve short-snouted, powerful biting forms. In addition, both the Late CarboniferousTriassic and Cenozoic phases are characterized by repeated patterns of clade replacement, in which one or a few clades evolve large size and seem to dominate the carnivore guild for several million years, but then decline and are replaced by new taxa. Moreover, within both ancient and Cenozoic predator clades, there are parallel trends over time toward increased body size and hypercarnivory that likely result from a combination of interspecific competition and energetic constraints.

INTRODUCTION
THE SYNAPSIDA IS a huge clade of amniotes that is of major evolutionary significance and includes modern mammals and their fossil ancestorsthe non-mammalian synapsids, or mammal-like reptiles of old classifications (Carroll, 1988; Benton, 1998). Synapsids possess only one temporal opening for the jaw muscles, located low on the side of the skull, as opposed to the two openings in diapsid reptiles and birds. The synapsid skull type gave rise to an astonishingly versatile jaw system, allowing side-to-side as well as fore-aft chewing movements (Romer, 1966). Synapsids are currently considered to comprise the paraphyletic pelycosaurs (known as pelycosaurgrade synapsids), the Therapsida, non-mammalian cynodonts (derived non-mammalian synapsids), and mammals (Kemp, 1988; Hopson, 1991; Laurin and

Reisz, 1995). The synapsid fossil record extends from the Late Carboniferous to the present day, a span of nearly 300 million years. However, it can be broken into two distinct phases of diversification, separated by about 150 million years. The first phase extends from the Late Carboniferous to the midTriassic, includes the first large land predators on Earth, and is almost entirely non-mammalian. The second phase begins about 65 million years ago after the demise of the dinosaurs, includes only mammals, and extends to the present. The Carboniferous to Triassic fossil record of non-mammalian synapsids includes a wide variety of carnivores. Not only are sphenacodont synapsids the first mega-carnivores on Earth, but succeeding synapsid predatorssuch as dinocephalians and Late Permian gorgonopsidsmade up the first diverse carnivore guilds on Earth and pre-date those of Cenozoic mammals by as much as 200

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million years. The 170-million-year hiatus between the last diverse synapsid carnivore community (Middle Triassic cynodonts) and the first Cenozoic predators (creodonts) was the result of dinosaur prevalence during that interval (Benton, 1998). Predatory non-mammalian synapsids were profoundly dominant in their niches throughout the Permo-Carboniferous, a pivotal period in Earth history for tetrapod evolution. At this time, the fundamental amniote groupsanapsids, diapsids, and synapsidshad their origin and first diversification. In addition, ancient amphibians chiefly temnospondylsradiated tremendously and commanded inland freshwater aquatic and semi-aquatic habitats (Carroll, 1988; Benton, 1998). Carnivores in any ecosystem apply considerable evolutionary pressure and are implicated in such adaptations among prey species as crypsis, armor and cranial adornments, tusks, increased cursorial capacity, and greater size (Gittleman, 1989, 1996). This was as true for ancient terrestrial ecosystems as it is today. Gaining insights into the structure and composition of ancient predator guilds should shed light on tetrapod evolution during the Late Paleozoic. Predators, as defined in this overview, are animals that regularly kill and eat other vertebrates (Savage, 1977). In the interest of brevity, and because the fossil record is more complete for larger than for smaller vertebrates, we will largely restrict our review to terrestrial species of large sizethat is, jackal-size (about 7 kg) and larger. Our primary focus will be on heads and teeth and hence killing and feeding behavior, rather than on limbs and locomotion. This reflects the fact that cranial and dental material is much more abundant in the fossil record than are limbs, especially in the case of the Permo-Triassic synapsids. The review begins with a look at overall similarities and differences in the anatomy and feeding mechanics of the two widely separated radiations of carnivores. This is followed by a summary of the evolutionary history within each group and then by an attempt at a synthesis, noting parallel trends in morphology and guild dynamics between the Permo-Triassic and Cenozoic synapsid predators.

NON-MAMMALIAN AND MAMMALIAN SYNAPSID CARNIVORES COMPARED

All but the latest Permo-Triassic synapsid carnivores differed from Cenozoic synapsids in jaw mechanics. Reconstructing the fine details of muscles in fossil vertebrates is problematic, but general directions of muscle forces (vectors) can be estimated. In addition, the overall morphology of the skull and jaws provides some indication of function (Parrington, 1955; Olson, 1961; Kemp, 1969, 1982). Based on their anatomy, most ancient carnivores used a predominantly Kinetic-Inertial (KI) system of jaw closure in which the jaws were rapidly slammed shut, disabling the prey by the momentum and ultimately the kinetic energy of the jaws and teeth (Olson, 1961). The major jaw closing muscles were the anterior pterygoideus and temporalis (Fig. 1). In more derived amniotes, such as modern mammals, the KI system was supplemented (and supplanted) by the StaticPressure (SP) system. In SP systems, a strong bite with nearly closed jaws serves as the killing bite (Olson, 1961). The pterygoideus musculature is reduced; instead, the muscles driving the closure are the temporalis and the masseter (Fig. 1). Modern examples of predators that use KI or SP systems offer insights into differences in jaw musculature and function that can be applied to fossil tetrapods. For example, the rapid and highly damaging jaw adduction of crocodilians is a good example of a KI system combined with a significant SP bite (Cleuren and de Vree, 2000). In crocodilians, the fast KI bite is generated by an expanded anterior pterygoideus musculature which, when the jaws are wide open, lies at 90o to the long axis of the lower jaw. This is the optimal alignment for the input of forces (muscular) to a lever (lower jaw). The temporalis musculature in crocodilians is aligned at 90o to the long axis of the lower jaws when they are almost closed and thus provides the SP component of the bite. Large felids such as lions use a more purely SP system in which the jaws are closed more slowly but with great force (Biknevicius and Van Valkenburgh,

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muscles is great because it has a very long moment arm (the coronoid process). Moreover, much of the temporalis is aligned close to 90o relative to this structure, enhancing muscle force when the jaws are nearly closed (Russell and Thomason, 1993). The SP bite system may have replaced the KI system in synapsids because impact stresses on teeth and bones were lessened during the killing bite. In addition, the SP system allowed a firmer grip on prey and better control of teeth at occlusion. The masseter musculature enhanced the bite force of slicing cheek teeth and reduced the need for large internal pterygoideus musculature that could obstruct air and food pathways. In addition to jaw mechanics, Permo-Triassic mammalian predators differ from their Cenozoic equivalents in tooth morphology. With the exception of some very derived, nearly mammalian, cynodonts, Permo-Triassic synapsid predators displayed little differentiation in dental morphology along the tooth row, except in size (Figs. 1, 2). Numerous simple conical to blade-shaped teeth lined the jaws. Large caniniform teeth were often present on both upper and lower jaws, thus separating the tooth row into incisors, canines, and cheek teeth. Unlike modern carnivores, there was no tooth-totooth occlusion among the cheek teeth and no precise shearing between the upper and lower teeth. As a result, the diversity of dental types among nonmammalian synapsid carnivores was much lower than that expressed among mammalian carnivores. In mammals, the evolution of precise occlusion and side-to-side jaw movements (in association with the evolution of the masseter musculature) allowed mammals to produce more effective grinding as well as slicing actions. Cenozoic carnivores include species with teeth specialized for herbivory (e.g., Giant Panda), omnivory (e.g., Brown Bear), carnivory (e.g., felids), and bone-cracking (e.g., hyaenids). By contrast, the radiation of nonmammalian synapsid carnivores produced only species specialized for meat-eating, with little evidence of adaptation for consuming bone or nonvertebrate foods. Included among these were the first sabertooth predators, foreshadowing an ecomorph that was to appear repeatedly among mammals.

FIGURE 1Kinetic-Inertial (KI) vs. Static-Pressure (SP) bite systems as illustrated by a gorgonopsid (Arctognathus ) and a modern cat (puma, Puma concolor ), respectively. 1, In the KI system, the largest jaw adductor (P) is the anterior pterygoideus musculature. Note that it has its maximum leverage for jaw closing when the jaw is wide open, and can initiate a rapid closure; A = external adductors. 2, In the SP system, the largest jaw adductor is the temporalis musculature (T) followed by the masseter (M); the pterygoideus musculature is reduced. In the SP system the major jaw adductors have their maximum advantage when the jaws are nearly closed. (1) modified from Kemp, 1982, fig. 40.

1996). The anterior pterygoideus musculature of felids is greatly reduced so there is little KI component, but the mechanical advantage (distance from fulcrum to effort divided by distance from fulcrum to bite point) of the expanded temporalis

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THE EVOLUTIONARY HISTORY OF PERMO-TRIASSIC SYNAPSID PREDATORS

Existing knowledge of terrestrial tetrapod predators from the Late Carboniferous to the middle Late Triassic has been broadly outlined as part of stratigraphical studies on these faunas (Anderson and Cruickshank, 1977; Rubidge, 1995) and systematic analyses of amniotes (Laurin and Reisz, 1995) and of synapsids in general (Hopson, 1991; Hopson and Barghusen, 1986; Reisz, 1986; Kemp, 1988; Sidor and Hopson, 1997; Sidor,

2001). The fossil record of non-mammalian synapsids is more complete than that of any terrestrial vertebrate group except Cenozoic mammals; it allows their evolutionary history and the nature of their adaptations to be considered in great detail. The early history of synapsids produced at least two firsts in Earth history. Synapsids include the first terrestrial amniotes on earth that acted as specialized herbivores (Modesto, 1995). But, of equal significance, synapsids include the Earths first large land predators, animals capable of killing and eating other vertebrates. The first obligate carnivore to appear on land was the sphenacodont pelycosaur-grade synapsid

FIGURE 2Skulls of Permian carnivorous non-mammalian synapsids. 1, sphenacodont pelycosaur-grade synapsid Dimetrodon. 2, Anteosaur dinocephalian Titanophoneus. 3, Early therocephalian Lycosuchus. 4,gorgonopsid Leontocephalus. 5, Chiniquodontid cynodont Probelesodon. (14 modified from Kemp, 1982.)

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Dimetrodon during the Early Permian (Fig. 2.1). At that time, Dimetrodon alone had a craniodental design that was sufficiently robust to disable and consume large vertebrates; it gave rise to the anatomically progressive therapsids, which include the saber-toothed genera (Kemp, 1982). So dominant were synapsids as terrestrial apex predators that no member of any other amniote clade took this role alongside synapsid killers. The abundant, large, and formidable temnospondyl amphibian Eryops of the Permo-Carboniferous was perhaps the only possible instance of any nonsynapsid predatory competition. Other gigantic temnospondyl amphibians were comparable to synapsids in terms of their habitat dominance, but were semi- or fully aquatic (Carroll, 1988; Benton, 1998), as was Eryops. The history of nonmammalian synapsids records five ecological dynasties of predator communities. Basal therapsids form a possible sixth but are poorly known, and it is not yet feasible to reconstruct a community of these carnivores. An ecological dynasty of predators is here defined as a single clade or small number of clades (relative to all that are present) that fill the large-body-size, highly carnivorous roles within a community for millions of years. The five predator dynasties (Figs. 2, 3) of the non-mammalian Synapsida, in chronological order, are sphenacodont pelycosaurs (PermoCarboniferous), anteosaur dinocephalians (middle Late Permian), therocephalians (Late Permian), gorgonopsids (Late Permian), and non-mammalian cynodonts (Permo-Triassic). These five dynasties span a total stratigraphic range extending from the Late Carboniferous (sphenacodonts) to the Middle Triassic (chiniquodontid cynodonts). Permo-Carboniferous (approximately 300270 Ma): Pelycosaur-grade synapsids.In pelycosaurgrade synapsids of the Permo-Carboniferous, the only large terrestrial predators were Dimetrodon, Ophiacodon (Romer and Price, 1941; Reisz, 1986), and possibly Secodontosaurus (IJ, pers. obs.). Secodontosaurus (Reisz et al., 1992) was a longsnouted form superficially similar to the much larger Ophiacodon. Secodontosaurus has been considered to have been an insectivore that used its elongate rostrum to reach the invertebrate occupants of burrows (Reisz et al., 1992). However, its cranial size (280 mm in length) was comparable to that of a mature Komodo Monitor. Its cranial morphology (narrow, deep, and long) shows a more robust skull than that of Ophiacodon, a welldeveloped region for the origin of the anterior pterygoideus musculature, and stout, sharp teeth. These details reflect true carnivory, not insectivory, for which numerous simple teeth are more typical. Its rostrum was not sufficiently narrow to access invertebrate burrows but may have been able to enter those of small tetrapods. Ophiacodon had the longest skull of any pelycosaur, and some remains suggest an animal with a skull length in excess of 500 mm (Romer and Price, 1941) and a total length of more than four meters. It is usually considered to have been a semi-aquatic piscivore on the basis of its unossified ankle and wrist bones and its dental arcade of many small conical teeth (Romer and Price, 1941). Its skull size suggests that tetrapod prey was an option, but this is countered by the structurally fragile nature of its lower jaws and a rostrum that was not particularly strong in bending and torsion (IJ, pers. obs.). Hence, the only large mega-carnivore in Permo-Carboniferous terrestrial ecosystems was Dimetrodon. Dimetrodon species had very deep skulls with a strongly convex dorsal profile and well-developed temporalis and anterior pterygoideus musculature. The reflected lamina of the angular bone in the lower jaw was the largest of any pelycosaur and heralds the expansion of this structure in the therapsids, where it becomes part of the hearing complex (Kemp, 1982). In Dimetrodon it supported an enlarged anterior pterygoideus musculature which operated a powerful KI bite. Dimetrodon had a strong but not especially robust lower jaw and a characteristic dentition (Romer and Price, 1941; Reisz, 1986). The postcanine dentition included fewer but larger teeth in the upper jaw. These teeth are recurved and very sharp with serrated edges; their cross section is ovoid to subrounded, suggesting considerable structural strength (Fig. 2.1). The pterygoid flanges in the palate were huge and robustly designed; their edges

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FIGURE 3Stratigraphic ranges and time duration of the carnivorous groups of non-mammalian synapsids (modified from Kemp, 1982, fig. 115). A star indicates the presence of a saber-toothed form within the lineage.

lay at 90o to each other and were equipped with well-developed pterygoid teeth. These structures may have functioned as intraoral guillotine blades (IJ, pers. obs.) and allowed the enhanced trituration of ingested food. The canines are very large and extremely robust, but the huge, caniniform incisors are similar in size to the canines (Romer and Price, 1941). There is a pronounced step at the maxilla premaxilla junction of the upper jaw. The canines and incisors are situated on opposite sides of this step, allowing the equally large lower canines to interpose between the upper canines and incisors, creating a tight grip on prey. Sphenacodonts were highly successful predators as shown by a long fossil record (about 40 million years) that extends from the Late Carboniferous to the Guadalupian (early Late Permian) (Benton, 1993). The skull design remained unchanged throughout this long period. Mid-Late Permian (approximately 275260 Ma): Dinocephalians.The first of three therapsid dynasties belongs to the dinocephalianslarge, often gigantic, synapsids from the early Late

Permian of South Africa and Russia (Fig. 2.2). Over their evolutionary history, they increased in size; their skull bones thickened; the adductor (temporalis) chamber became more vertical in orientation; and they developed reniform (kidneyshaped) palatal tooth bosses of considerable size, robust canines, and very large, procumbent incisors that interlaced in a precise manner (Kemp, 1982). Dinocephalians were the largest of all synapsids and rivaled some dinosaurs in size. The carnivorous members belong to the anteosaur clade (Hopson, 1991; Hopson and Barghusen, 1986) and include the South African form Anteosaurus, and the somewhat smaller Russian forms Titanophoneus (Fig. 2.2), Syodon, Archaeosyodon, Doliosaurus, and Doliosauriscus. Anteosaurus from South Africa had a high, deep skull almost a meter long (Kemp, 1982) equipped with mighty canine teeth, as did the Russian forms Archaeosyodon, Doliosaurus, and Doliosauriscus (Orlov, 1958; Tatarinov, 1974; Chudinov, 1983; Battail and Surkov, 2000). The

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body length of Anteosaurus is estimated at more than 5 meters (Boonstra, 1954). Large pterygoid flanges indicate a well-developed KI system in anteosaurs, and increased vertical alignment of the temporalis muscles suggests an expanded SP component of the bite cycle. Unlike later therapsids, in which the postcanine dentition was reduced, anteosaurs retained the three elements of their dental arcade as fully functional units. Anteosaurs possessed the heaviest canines, incisors, and skulls of all carnivorous synapsids. The postcanine teeth are large, trenchant, ovoid in cross section, and hence very strong. In many anteosaur genera, the canines are recurved, in contrast with the straighter canines of all other carnivorous synapsid genera. This pronounced recurvature is best seen in Syodon from Russia. In addition to the complete functional complement of marginal dental units, anteosaurs also possessed very prominent palatal tooth bosses. These reniform structures are more conspicuous than in any other predatory synapsid and augmented the marginal dentition considerably. Anteosaur head skeletons thus show a trend toward a remarkably expanded dental complement, comprising incisors, canines, postcanines, and palatal teeth, all of which were large. In concert with huge size, a powerful SP bite, and exceptionally heavy, thick-boned skulls, anteosaur dinocephalians were designed to prey on particularly large animals and were among the most highly predaceous of all synapsids (Sennikov, 1996). Potential prey included the bull-sized armored pareiasaurs (Lee, 1997) and enormous tapinocephalid dinocephalians (Rubidge, 1995). The latter are typified by dome-headed Moschops; it and related genera such as Tapinocephalus were the heaviest of all synapsids (Kemp, 1982). Despite their remarkable craniodental weaponry, dinocephalians do not have a fossil record as long as that of sphenacodonts and are replaced in the early part of the Late Permian by early therocephalians and gorgonopsids (Anderson and Cruickshank, 1977; Kemp, 1982; Rubidge, 1995; Battail and Surkov, 2000). Late Permian (approximately 260250 Ma): Gorgonopsids.A number of gorgonopsid ecomorphs or ecotypes can be defined, based on skull construction and jaw biomechanics (Fig. 4). Cyonosaurids such as Cyonosaurus (Fig. 4.1) were small (skull length about 140 mm) gorgonopsids with very long snouts, small canine sabers, slim lower jaws, and gracile skulls. These forms may be immature or juvenile forms of other genera (IJ, pers. obs.). Cyonosaurids have a long fossil record (relative to other gorgonopsids) and seem to have

FIGURE 4Gorgonopsid skull morphotypes that probably represented different predatory habits and niche occupation. See text for more information. 1, Cyonosaurus; 2, Gorgonops; 3, Arctops; 4, Arctognathus; 5, Rubidgea; 6, Broomicephalus. Scale bar = 100 mm. Skulls not to scale.

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filled roles analogous to those of modern small, long-snouted canids such as jackals and foxes that prey on both arthropods and small vertebrates. Larger gorgonopsids such as Leontocephalus, Scylacops, Aelurognathus, and Gorgonops (Fig. 4.2) display fairly long rostra and skulls with a flat dorsal profile, large canine teeth, and up to four postcanine teeth (Kemp, 1969; Sigogneau, 1970; Sigogneau-Russell, 1989). In these genera, the adductor chamber shows the characteristic flaring to produce expanded areas of origin for the temporalis musculature. The pterygoid flanges are situated far anteriorly, allowing for long anterior pterygoideus fibers that powered a strong KI bite (Jenkins, 1998). A number of even larger gorgonopsid genera, such as Arctops (Fig. 4.3), display shorter skulls with a very strongly convex dorsal profile that is reminiscent of the sphenacodont Dimetrodon. The convex profile is especially efficient for accommodating the stresses imposed during powerful canine biting (Jenkins, 1998). In especially large (skull length about 300 mm), convex-skulled genera such as Arctops, the reflected lamina of the angular bone is expanded and hence provided an increased insertion area for a correspondingly enlarged anterior pterygoideus musculature. This indicates a very powerful KI bite and the capacity to accelerate the jaws shut from a very wide gape. The saber teeth in some specimens are exceptionally long, and would have necessitated a wide gape to clear the tips of the huge teeth (Jenkins, 1998). Another gorgonopsid ecotype is defined by the short-snouted genus Arctognathus (Fig. 4.4). This small to medium-sized gorgonopsid has a box-like robust skull with a deep rostrum and a rather flat dorsal profile; the canines are large, areas of bone associated with the anterior pterygoideus musculature are expanded, and the symphysis of the lower jaw is enlarged. These details suggest a rostrum that was strong in bending and torsion, powerful KI and SP constituents of the bite cycle, and a stable lower jaw (Jenkins, 1998, 2001a, 2002b; Jenkins et al., 2002). Gorgonopsids attain their most impressive manifestation in their most derived members, the Rubidgeinae. These were the latest-surviving gorgonopsids and are found solely (so far) in South Africa just below the horizon beds of the endPermian extinction event (Rubidge, 1995). Rubidgeine gorgonopsids are characterized by a suite of cranial features that evolved for an exceedingly predaceous way of life. The skulls are often huge, exceeding 400 mm in length. Skull buttressing is extremely pronounced. The rostrum is broad, pterygoid flanges are situated far anteriorly, the lower jaw is massive, and the symphysis is expanded more than in other gorgonopsid genera. The incisors are very large, postcanine teeth are absent, and the saber canines are hugethose of Rubidgea atrox (Fig. 4.5) are longer than the teeth of the theropod dinosaur Tyrannosaurus rex (Jenkins, 1998). Rubidgeine gorgonopsids are defined taxonomically by a posterior ventral flange on the zygomatic arch (Sigogneau-Russell, 1989), which appears to reflect an enlarged zygomaticomandibularis muscle (Kemp, 1969) that stabilized the lower jaw and jaw joint during use of the large saber teeth (Jenkins, 1998). Within the Rubidgeinae, distinct ecotypes are defined by the huge buttressskulled Rubidgea, the very wide-snouted Clelandina, and the convex-skulled, long-sabertoothed Dinogorgon and Prorubidgea (figured in Sigogneau, 1970; Sigogneau-Russell, 1989). A final gorgonopsid ecomorph is represented by one of the rarest rubidgeines, Broomicephalus (Fig.4.6). Broomicephalus is the only known gorgonopsid in which maximum skull width exceeds total skull length (Sigogneau, 1970; Sigogneau-Russell, 1989; Jenkins, 1998; Jenkins and Dyke, in press). It has an unusually broad rostrum, short skull, especially flat blade-like sabers, and the largest jaw symphyseal mass of any gorgonopsid. The wide rostrum includes an expanded origin area for the anterior pterygoideus musculature, indicating more of an emphasis on the KI component of its bite cycle than in some other rubidgeines. Associated with this are rather small adductor chambers, suggesting a reduced SP constituent. Wide jaws are very stable and robust (Covey and Greaves, 1994); large jaw symphyses increase the penetration potential of the sabers and allow both sides of the jaw adductor muscle force to be

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utilized. Broomicephalus probably preyed upon unusually large animals (Jenkins, 1998), and its unusually flat sabers foreshadow the canines of scimitar-toothed cats such as Homotherium. Despite the complexity and diversity in Late Permian carnivore guilds, all gorgonopsids became extinct during the end-Permian event. To some extent, gorgonopsid ecological supremacy came at the expense of saber-toothed carnivorous therocephalians, which died out before the last gorgonopsids and were to a large extent replaced by them as top predators (Jenkins, 1998, 2001a; Jenkins et al., in press). Late Permian (approximately 265250 Ma): Therocephalians.Therocephalians overlap the tenmillion-year span of the gorgonopsids and extend slightly further into the basal Triassic (Fig. 3). Early therocephalians include the families Lycosuchidae and Scylacosauridae, and both were saber-toothed. Their saber canines are modest compared with those of large gorgonopsids, although in bigger scylacosaurid genera and in Lycosuchus they are very pronounced (Fig. 2.3). The therocephalian SP bite is larger than that of gorgonopsids due to enlarged adductor chambers for the temporalis musculature (Kemp, 1982). The anterior pterygoideus muscle fibers inserted relatively close to the jaw joint, thus reducing the mechanical advantage of the KI system relative to that of gorgonopsids but increasing the speed of closure (Jenkins, 1998). The palates of early therocephalians have a large number of discretely located and welldeveloped scarf joints that reduce biting stresses (Jenkins, 1998; Jenkins et al., 2002). Lycosuchus has a shorter snout than most scylacosaurids such as Glanosuchus, Scymnosaurus, and Ptomalestes, and its sub-rounded shape suggests strength in torsion in association with proportionally large sabers (Jenkins, 1998). The short snout also gives a greater mechanical advantage for bites at the canines. The therocephalian group Euchambersiidae (Hopson and Barghusen, 1986) contains the highly distinctive genera Euchambersia and Moschorhinus. Both these forms are characterized by very short, robust rostra and canines that are rounded in crosssection. Euchambersia is known from only two partial skulls; Moschorhinus is much better known. Moschorhinus skull dimensions range from those of a large monitor lizard to those of a lion. It is a most unusual therocephalian and shows a large temporal fenestra, convex palate, and laterally compressed incisors set in a shallowly curving arcade, in addition to the short, strong snout (Fig. 5.2). The lower jaw has remarkable canines and a symphysis that is expanded more than in any other therocephalian (Jenkins, 2001b). The canines are as long as the sabers of all except the most derived gorgonopsids (Fig. 5.1), but are round in cross-section, resembling the spikes used to secure some railway cross-ties. There is no modern analog for these teeth, the closest perhaps being the hyperelongate canines of the Clouded Leopard (Neofelis nebulosa) (Fig. 8.2). The combination of long, robust canines and flattened incisors in a shallow arcade suggests a felid-like mode of attack (sensu Biknevicius et al., 1996), in which the strong canines would have sustained a long period embedded in prey (Jenkins, 2001b). This is the earliest known instance of this design. Moschorhinus went extinct after gorgonopsids and was a therocephalian occupying a gorgonopsid-like ecological niche (Jenkins, 2001b). The powerful symphysis, robust snout, and extraordinary canines show Moschorhinus to have been a truly formidable predator; why it should have survived when equally powerful and similarly designed gorgonopsids went extinct is probably due to some as-yet-unknown feature of its physiology. Once Moschorhinus had disappeared, the roles of top predators were taken up by cynodonts (Fig. 3). Permo-Triassic (approximately 255225 Ma): Cynodonts.Small cynodonts in the basal-most Triassic (Lystrosaurus Zone) are represented by Galesaurus and Thrinaxodon (Broom, 1932). They show expanded temporalis musculature and the first signs of the masseteric musculature characteristic of modern mammals (Kemp, 1982; Hopson, 1991; Hopson and Barghusen, 1986). The snout is short and the canines dog-like; the postcanine teeth are numerous and form a series of curving blades (Kemp, 1982), similar to those of the Komodo Monitor (Varanus komodoensis). In general skull proportions and size, they most

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resemble modern-day mustelids (weasels) and viverrids (civets), and probably behaved more like modern hypocarnivorous/omnivorous viverrids than specialized hypercarnivorous mustelids. The largest carnivorous cynodont, Cynognathus, defines the Cynognathus Zone of the Lower-Middle Triassic (succeeding the Lystrosaurus Zone), and has a disproportionately large, robust skull (Broom, 1932; Kemp, 1982). More than 400 mm long, its proportions are similar to those of extant canids, characterized by a long rostrum. The dentition is broadly similar to that of Galesaurus and Thrinaxodon, with pointed incisors, welldeveloped canines, and a long row of sharp, recurved postcanine teeth. There are two striking features of the Cynognathus skullboth the lower jaw and zygomatic arch are extraordinarily deep vertically (Fig. 5.3). The zygomatic arch is so deep that the orbit appears as a simple hole punched through the plate formed by the zygomatic arch (Kemp, 1982). Application of lever mechanics to the Cynognathus skull reveals a very powerful temporalis musculature and an expanded masseteric component. There is little KI component to the bite, but the SP constituent must have been extremely powerful. This and the overall robustness of the skull suggest a hyena- or bear-like design. However, Cynognathus did not have the bone-cracking premolars or carnassial blades of modern hyaenids. Its trenchant, recurved postcanine teeth, in concert with this strong SP bite and huge lower jaw, indicate that Cynognathus used its postcanine teeth to a much greater extent than perhaps all previous synapsid predators (IJ, pers. obs.). Later cynodont predators are the chiniquodontids of the Middle and Late Triassic. Their skull dimensions (Romer, 1969a, 1969b) range from those of a modern coyote (Probelesodon, Fig. 2.4) to those of a large hyena (Chiniquodon and Belesodon). Analysis of jaw muscle biomechanics indicates that the horizontal component of the jaw muscle vectors in cynodonts increased throughout the lineage and served to reduce reaction forces at the jaw joint (Crompton, 1963, 1972; Bramble, 1978). At this stage, the jaws of carnivorous chiniquodontids were functioning in an almost identical manner to those of modern carnivores.

FIGURE 5Diagram illustrating the geometric differences in skull, jaw and tooth morphology among: 1, a very derived gorgonopsid, Dinogorgon; 2, the unusual therocephalian Moschorhinus, which represents a convergence with the gorgonopsid cranial design; and 3, the large Triassic cynodont Cynognathus . This illustration charts the change from a largely KI bite (with some SP component)Dinogorgonto an SP bite with very little KI component Cynognathus. Ventral views of the anterior palates are shown to the right. Note the parabolic incisor arcade of gorgonopsids, and the peculiarly felid-like straight incisor arcade of Moschorhinus along with its palatal fenestrae (for muscular attachments). In Cynognathus an almost complete osseous secondary palate has formed. The flat sabers of the gorgonopsid can be contrasted with the round elongate spikes of Moschorhinus. See text for details. Scale bar = 100 mm. Skulls not to scale.

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NON-MAMMALIAN SYNAPSID PREDATORS: LONG-TERM TRENDS

The long-term evolutionary trends seen in the crania of carnivorous non-mammalian synapsid predators are essentially those documented for the whole of the Permo-Triassic Synapsida (Romer, 1966; Kemp, 1982; Hopson and Barghusen, 1986). They include an increase in solidification of the braincase wall, reduction in the number of skull bones, expansion of the temporalis musculature and development of the masseteric musculature, reduction of the pterygoideus component, increased heterodonty, formation of an osseous secondary palate, increased brain size, and reduction of the postdentary bones, which evolve into bones of the mammalian middle ear (Kemp, 1982; Sidor, 2001). In terms of skull mechanisms relating to a carnivorous habit, the KI bite system is replaced by the SP bite system, and the saber-toothed adaptation prevalent in the Late Permian is not seen after gorgonopsids until the advent of Cenozoic creodonts. In temporal sequence, convex-skulled, step-jawed sphenacodonts were followed by pachyostotic (thick-boned) skulls and gigantism among anteosaurs. These in turn were succeeded by a variety of saber-toothed forms, both early therocephalians and gorgonopsids, which dominated Late Permian ecosystems. Smaller, rather mammallike carnivores of the Triassic cynodont clade supersede the Late Permian saber-toothed predator community. These animals were close to mammal ancestry and very similar to modern mammals in their skull design (Kemp, 1982).

THE EVOLUTIONARY HISTORY OF CENOZOIC SYNAPSID PREDATORS

Synapsids relinquished the role of dominant terrestrial predator to theropod dinosaurs for the remainder of the Mesozoic. Then, following the demise of the dinosaurs about 65 Ma, about ten million years passed before the first appearance of a large, specialized meat-eater (e.g., Oxyaena;

Gunnell, 1998). Thus, the period to be covered in this part of the review, the last 55 million years, is much shorter than that spanned by the abovedescribed non-mammalian synapsids (80100 million years). Nevertheless, because of its relative recency, the fossil record of carnivorous mammals is much richer in detail and diversity than that of the ancient synapsids. Here we can provide only a brief summary, but there are several recent reviews of carnivore history that offer more information (e.g., Martin, 1989; Hunt, 1996; Werdelin, 1996; Van Valkenburgh, 1999). Our emphasis will be on notable morphological innovations and repeated patterns in the history of carnivorous mammals, including convergence on similar ecotypes and dynasty replacement (as was described for PermoTriassic synapsids). Most of the discussion relies on examples from the excellent North American and Eurasian fossil records. Today, the large, terrestrial predators of the world all belong to a single placental order, the Carnivora. Until very recently, there was one marsupial predator of reasonable size, the Australian thylacine (Thylacinus cynocephalus), but its extinction has left the carnivorans (members of the order Carnivora) as sole occupants of this adaptive zone. In the early part of the Cenozoic, two nowextinct orders, Mesonychia and Creodonta, dominated predator guilds. The mesonychids were perhaps the first Cenozoic predators, although their dentition is not highly specialized for meat-eating, and they may have been quite omnivorous. Mesonychids, such as the 62 Ma coyote-sized Dissacus, looked somewhat dog-like externally, but their teeth differed markedly from those of canids. The lower tooth row of Dissacus includes a series of premolar-like teeth with blunt cusps and weakly developed cutting blades (Fig. 6.1) that seem less specialized for carnivory than those of the Triassic cynodont Cynognathus (Fig. 5.3). The first unquestionable Cenozoic hypercarnivores (specialists on vertebrate prey) were among the creodonts. Unlike mesonychids, creodonts evolved specialized slicing molar teeth, in which upper and lower molars occluded like scissors and created large shear facets on opposing teeth (Fig. 6.2).

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Carnivorans also evolved specialized slicing teeth, but unlike creodonts, they have only a single pair, the upper fourth premolar and lower first molar (Fig. 6.3). This single carnassial pair is a key diagnostic character of the order Carnivora. In a typical canid, the carnassials lie about midway along the tooth row, separating somewhat conical premolars from more flattened rear molars. This variety of tooth form has allowed great evolutionary versatility within the order. By enhancing one set of teeth over another, species can evolve toward omnivory (larger rear molars for grinding; e.g., bears), carnivory (larger carnassials; e.g., cats), or bone-cracking (larger, bulbous premolars; e.g., hyenas) (Ewer, 1973). In both Eurasia and North America, the Cenozoic history of mammalian carnivores comprises a series of five dynasties (Van Valkenburgh, 1999). Each dynasty is defined by the prevalence in body size and diversity of one or more groups. The taxa are not identical on both continents, but there is considerable overlap reflecting the fact that the two have been connected several times over the last 65 million years. In North America, the sequence of large predator dynasties was: 1) creodonts; 2) creodonts and nimravids; 3) canids, amphicyonids, hemicyonine ursids; 4) borophagine canids and felids; and 5) canine canids and felids. In Eurasia, the pattern is very similar, except that hyenas fulfill many of the same roles filled by canids up until the Pliocene (Werdelin and Solounias, 1991, 1996). We next review each of these dynasties, highlighting significant morphological advances. Early to middle Eocene (approximately 5540 Ma): Creodonts.Creodonts appear in the late Paleocene (about 57 Ma) and reach their maximum diversity in North America in the early to middle Eocene (4854 Ma). Early forms were civet-like, preying on relatively small mammals, birds, and perhaps arthropods (Gunnell, 1998). Over time, creodonts expanded into more hypercarnivorous forms, including the first sabertooth predator since the Permian. This early sabertooth, Macheroides, is poorly represented but appears to have been about the size of a bobcat (Lynx rufus), which is much smaller than typical sabercats, though comparable to some Late Permian gorgonopsids (Dawson et al., 1986). There were also a few very short-faced creodonts in the Eocene, with deep jaws and robust premolars, that may have been bone-crackers, such as Patriofelis and Paleonictis. This diverse array of creodonts ranged in body size from that of foxes to that of leopards and they were the dominant carnivores of the Eocene. They coexisted with smaller species, feliforms and caniforms that represent the earliest members of the order Carnivora (Flynn, 1998), as well as a few omnivorous mesonychids.

FIGURE 6Lateral view of the lower jaws of 1, Dissacus, a mesonychid; 2, Hyaenodon crucians, a creodont; and 3, Hesperocyon gregarius, a canid carnivoran. Arrows indicate molar teeth specialized for cutting. Dissacus is modified from Fig. 1 of OLeary and Rose (1995b); the others are from color transparencies.

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The creodonts included ambulatory, stoutlimbed species (oxyaenids) as well as more slenderlimbed, cursorial forms (hyaenodontids), although nothing was as cursorial as a modern canid (Gunnell, 1998). This ecological diversity of forms declined to a single subfamily, the Hyaenodontinae, in the late Eocene of North America. Hyaenodontines were fairly cursorial hypercarnivores with well-developed shearing dentition set into long jaws. They were capable of large gapes and may have emphasized KI biting as well as SP biting, as their masseter muscles were reduced relative to their internal pterygoid muscles (Mellett, 1969). Hyaenodontines persisted in North America for about 12 million years, sharing the role of dominant carnivore with the cat-like Nimravidae. Late Eocene to Oligocene (approximately 40 28 Ma): Creodonts and Nimravids.The second Cenozoic dynasty was made up of hyaenodontine creodonts and sabertooth nimravids (Fig. 7). Coexisting with them at somewhat smaller sizes were more omnivorous species within the families Canidae and Amphicyonidae. The family Nimravidae includes the first truly cat-like predators bearing grappling forelimbs armed with retractile claws, enlarged canines, and foreshortened skulls with no postcarnassial crushing molars. The convergence in form between nimravid and some felid carnivorans is so marked (Emerson and Radinsky, 1980) that nimravids were considered to be felids until relatively recently (Hunt, 1987; Bryant, 1991). Almost all nimravids had enlarged, laterally flattened saber-like canines that slid into a sheath on the lower jaw (Fig. 8.3). A single, poorly known early Miocene genus, Dinaeleurus, displays conical, more peg-like

FIGURE 7Stratigraphic ranges and time duration of the carnivorous groups of large North American mammals. Data are from Janis et al. (1998).

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FIGURE 8Lateral views of extinct sabertooth (1, 3, 4) and extant conical-tooth (2) cats. 1, Smilodon fatalis; 2, Neofelis nebulosa (Clouded Leopard); 3, Barbourofelis fricki; and 4 , Thylacosmilus atrox. (1) and (2) are members of the family Felidae, (3) is a member of the extinct family Nimravidae, and (4) is a South American marsupial.

canines as is typical of extant cats (Martin, 1998a). The first nimravids appear about 37 Ma in North America as two sabertooth genera, Dinictis and Hoplophoneus, each of which has a distinct canine morphology. Dinictis is scimitar-toothed with moderately elongate canines that are broader from

front to back than those of Hoplophoneus. Hoplophoneus is a dirk-toothed form with very elongate, narrow canines. These two saber-like canine forms appear again in felids in the later Cenozoic alongside species with conical canines (Martin, 1980). Thus, the Oligocene sees the first

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appearance of ambush predators with retractile claws and all three canine tooth types: scimitar, dirk, and conical. The nimravids persisted in North America until about 23 Ma, filling the ecological roles held now by bobcat- to jaguar-sized felids, while the hyaenodontids filled more canid-like roles. Between 23 Ma and 17 Ma, specialized cat-like predators were absent from North America for about 5 million years until felids arrived from the Old World (Fig. 7). Notably, nimravids eventually reappeared in North America in the late Miocene (circa 11 Ma) in the form of the most bizarre and last of all nimravids, Barbourofelis. Barbourofelis (Fig. 8.3) had enormously elongate dirk-shaped upper canines and highly reduced cheek teeth. The coronoid process on the lower jaw was very small in order to allow the jaws to open wide enough to provide space between upper and lower canine tips. Late Oligocene to mid-Miocene (approximately 2815 Ma): Canids, Amphicyonids, Hemicyonine Ursids.In the latter half of the Oligocene, the formerly dominant nimravids and creodonts declined in diversity for reasons that are unclear. They were replaced by species that evolved in North America (canids, amphicyonids) as well as by new immigrant taxa (ursids, amphicyonids, mustelids) from the Old World. The elimination of cat-like nimravids around 23 Ma seems to have promoted the evolution of hypercarnivory in several taxa. Among the canids, short-snouted forms such as Enhydrocyon appeared before the nimravids disappeared but were smaller in body size than the sabertooths. During the cat gap in the record, a large, leopard-sized mustelid (Megalictis), as well as several wolf-like ursids (e.g., Phoberocyon) and amphicyonids (e.g., Daphoenodon), filled the hypercarnivorous niche (Van Valkenburgh, 1991). With the exception of the large mustelid, all these hypercarnivores appear to have been more cursorial than either Hyaenodon or any of the Oligocene canids (Hunt, 1998a, 1998b). Although several of these species converged on the cat pattern in having shorter snouts and reduced postcarnassial molars, a sabertooth ecomorph did not evolve among them. One additional group outside the order Carnivora should be mentioned as possible predators and scavengers of this period: the entelodonts, non-ruminant artiodactyls of large size (150170 kg) with formidable canines, incisors and crushing premolars (Joeckel, 1990). These large, somewhat boar-like ungulates exhibit heavily worn teeth suggestive of bone-cracking behavior, and they may have played a somewhat hyena-like role in the late Oligoceneearly Miocene. MidLate Miocene (approximately 155 Ma): Borophagine Canids and Felids.Cat-like carnivorans reappeared in the New World about 18 Ma with the immigration of the Old World felid Pseudaeleurus (Martin, 1998b). Pseudaeleurus had conical canines but was joined by the scimitartoothed and larger felid Nimravides and the dirktoothed nimravid Barbourofelis around 11 Ma. The generic diversity of felids reaches a maximum of six in North America in the latest Miocene (about 6 Ma) at which time there were dirk-toothed (tribe Homotheriini) and scimitar-toothed (tribe Smilodontini) sabercats as well as at least one conical-toothed genus. Alongside the rise in felid diversity, there were declines in diversity in all other large hypercarnivorous taxa, including hemicyonine ursids, amphicyonids, and borophagine canids (Van Valkenburgh, 1999). Of these three, the borophagine canids declined slowest and persisted into the Pliocene. The borophagine canids of the middle and late Miocene were of two typeslarge cursorial wolf-like predators (e.g., Epicyon) and less cursorial specialized hyena-like bone-crackers (e.g., Osteoborus) (Munthe, 1998). Both types are likely to have hunted in packs, taking down prey as large as or larger than themselves (Van Valkenburgh et al., in press). The bone-cracking borophagines are very similar to living hyaenids in cranial morphology, with dome-like skulls that provide extensive areas for jaw adductor musculature, as well as short snouts to increase bite force at the canines (Fig. 9). However, whereas hyenas use their robust premolars to crack bones, borophagines used both their carnassials and premolars (Werdelin, 1989). This activity blunted their carnassials and likely inhibited their ability to use them as many species do today, to slice through tough skin to access muscle and viscera (Van Valkenburgh, 1996).

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The last of the Borophaginae, Borophagus, was extinct by the start of the Pleistocene (1.8 Ma), and a bone-cracking ecomorph did not reappear in North America, despite the fact that a hyaenid did immigrate from the Old World about 3.5 Ma. This species, Chasmoporthetes ossifraga, did not have the enlarged bone-cracking premolars of extant hyenas. Instead, it was more wolf-like in its dentition, except that unlike wolves and like hyenas, Chasmoporthetes had no postcarnassial molars (Berta, 1981). This hypercarnivore is relatively rare in the North American record, vanishing about 750,000 years ago. Pliocene to Recent (approximately 5 Ma to present): Felids and Canine Canids.This final turnover event within the carnivore guild is associated with a major extinction event among terrestrial mammals that occurred near the MiocenePliocene boundary (85 Ma). In both the Old and New Worlds, more than 60 percent of the genera went extinct (Webb, 1983, 1984; Savage and Russell, 1983) at a time when there was significant climatic shift towards increased aridification. Associated with this was a decline in mesic woodlands and expansion of seasonally arid grasslands (Janis, 1993). In North America, the losers among the predators were the wolf-like hypercarnivorous borophagine canids. In Eurasia, this was paralleled by a significant decline in the diversity of wolf-like hyaenids as well as sabertooth cats. In both the Old and New Worlds, the bonecracking canids and hyaenids were less affected by the extinction event, suggesting that their ability to more fully exploit carcasses was advantageous. In North America, wolf-like borophagine canids were replaced by members of the extant subfamily Caninae. Canines dispersed from North America to Asia about 78 Ma and there replaced the wolf-like hyaenids of the Old World. In both regions, the canines coexisted with sabertooth and conicaltoothed felids. Over the past 5 million years, sabertooth cats decreased in diversity as conicaltoothed big cats increased. Although sabertooth nimravids and felids were never very diversemost paleocommunities included two speciesthey were present in both the Old and New Worlds throughout most of the past 40 million years, and it is not clear why this widespread ecomorph declined to extinction in the Pleistocene. They disappeared first from Africa (circa 1 Ma), then Eurasia (circa 0.5 Ma), and finally North America (circa 0.01 Ma), which hints that humans may have played some role in their demise, but the mechanism is as yet unclear. Because we dont understand fully the functional significance of having elongate flattened canines as opposed to shorter, stouter canines, it is difficult to determine what factors, such as extinction of a particular size or type of prey, might have had a negative impact on sabertooths. It does seem probable that sabertooth cats, almost all of which

FIGURE 9Lateral view of the skulls of two Cenozoic bone-crackers drawn to the same size. 1, the extant Spotted Hyena, Crocuta crocuta, and 2, the Pliocene borophagine canid, Borophagus secundus (drawn from Matthew and Stirton, 1930).

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were leopard-sized and larger, killed relatively large prey, and their knife-like canines may have made it easier for a solitary individual to succeed. The last five million years witnessed the evolution of a number of highly cursorial carnivorans among a variety of families. For example, most of the Caninae are characterized by slender, relatively inflexible limbs, compact feet, and the ability to run tirelessly. Within the felids, long-legged genera arose in both Eurasia (the cheetah Acinonyx) and North America (the cheetahlike puma Miracinonyx) (Van Valkenburgh et al., 1990). Running hyenas, such as Chasmoporthetes, were present in both the Old and New Worlds, and there was even a long-legged running bear, Arctodus, in North America. This burst of large cursorial predators in the Plio-Pleistocene is not associated with a similar trend among their ungulate prey. Instead, the ungulates evolved their cursorial adaptations some 20 million years earlier (Janis and Wilhelm, 1993). Consequently, it seems likely that the predators were responding to a global change in vegetation structure that favored longdistance pursuit over ambush, such as a dramatic reduction in vegetative cover. In any case, the PlioPleistocene guilds of large carnivorans display a greater diversity of locomotor types than any previous guild. coyotes. These fundamental carnivorous feeding types evolved multiple times over the last 55 million years. The absence of secular trends in the dentition and feeding mechanics of the Cenozoic predators suggests that the synapsid craniodental architecture that evolved in the Mesozoic was very successful and required little or no tinkering to produce capable meat-eaters. In addition, the lack of a trend reflects the fact that the material properties of the food (prey) probably changed little over the Cenozoic; skin, muscle, and bone are assumed to have been much the same in the Paleocene as the present. By contrast, Cenozoic herbivorous mammals do exhibit long-term trends in dental morphology that reflect an environmental shift toward cooler, more arid habitats and associated tougher vegetation (e.g., grass) (cf. Janis, 1993). However, the Cenozoic cooling trend did have an impact on predators. It produced more open habitats and favored the evolution of cursoriality in both predator and prey. Thus, over the course of the past 55 million years, there are repeated trends towards longer limbs and more compact joints in carnivores. However, it is not a steady progression; instead, it occurred in steps, with the most obvious anatomical advances made in the early Miocene, and then in the Plio-Pleistocene (Janis and Wilhelm, 1993). Whether these anatomical changes actually corresponded to improvements in running ability is not known. It is very difficult to ascertain either top speed or endurance ability from mammalian skeletons, in part because species with very different builds, such as spotted hyenas and wolves, display similar locomotor capabilities (Bakker, 1983; Janis and Wilhelm, 1993). Nevertheless, in general, extant predators are more gracile in form than their Eocene and Oligocene counterparts and this probably reflects a shift toward speed over brawn.

MAMMALIAN PREDATORS: LONG-TERM TRENDS

The long-term trends in morphological change observed among the Cenozoic synapsids are not nearly as profound or dramatic as those of the Permo-Triassic. As noted above, the evolutionary history of these ancient synapsids documents the transition from a reptilian type of craniodental and jaw muscle architecture to that of mammals. No such major advances were made by Cenozoic synapsids. Instead, the history is more one of early diversification into a variety of feeding morphologies followed by repeated iterations of these types by different groups over time. For example, among Eocene creodonts, there were species similar to cats (both sabertooth and conicaltoothed), bone-cracking hyaenids, wolves, and

PATTERNS IN THE EVOLUTIONARY HISTORY OF SYNAPSID PREDATORS

Despite the striking differences in anatomy between Permo-Triassic and Cenozoic synapsid

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predators, there are a number of parallels. Both radiations produced saber-toothed forms multiple timesgorgonopsids and therocephalians in the Permo-Triassic, and creodonts, nimravids, felids, and even marsupials (Thylacosmilus (Fig. 8.4) of South America) in the Cenozoic. Without a doubt, saber-like canines are advantageous, but their absence today frustrates our ability to explain their obvious success. As noted above, it might enhance the ability to take relatively large, thick-skinned prey. Both radiations also produced short-snouted, powerful, biting predators (e.g., the ancient Moschorhinus and Arctognathus), although this form is much more common among Cenozoic predators, where it appears across a wide array of families, including oxyaenids, felids, nimravids, canids, ursids, and mustelids. The lower diversity of short-snouted species in the Permo-Triassic is understandable given that most species relied on a KI jaw system for killing and feeding. Both radiations of predators show a pattern of dynasty replacement. That is, one or a few clades evolve large size and seem to dominate the carnivore guild for several million years, but then decline and are replaced by new taxa. In the Cenozoic, most of the dynasties appear to be made up of a more diverse collection of taxa than those of the Permo-Triassic. That is, the Cenozoic dynasties include two to three families whereas the Permo-Triassic dynasties include a single suborder or infraorder (e.g., gorgonopsids). In some cases, such as the gorgonopsids (Fig. 4), a fairly diverse array of ecomorphs is included within the group, rivaling that seen in the Cenozoic. However, in most cases there does seem to have been less ecological diversity in feeding types within PermoTriassic predator guilds, based on their similarities in tooth form and jaw mechanics. In both the Permo-Triassic and Cenozoic, dynasty replacement is associated with considerable evolutionary convergence, as declining clades seem to leave ecological vacuums that are subsequently filled by new taxa. This is especially apparent in the Cenozoic record. For example, during the North American cat gap (2317 Ma), several families (e.g., canids, ursids, mustelids) produced relatively short-snouted species with large canines and reduced post-carnassial teeth. A similar trend toward hypercarnivory is apparent in South American Pleistocene canids and also occurred under conditions of very low felid diversity (Van Valkenburgh, 1991). In this instance, the near absence of cat-like species was a result of a prior extinction of the sabertooth marsupial Thylacosmilus, and an apparently slower immigration of felids than canids into South America. Convergence among Permo-Triassic synapsids is less common, but is evident between therocephalian sabertooths and the gorgonopsids that replace them, as well as between derived gorgonopsids, which went extinct at the end of the Permian, and moschorhinid therocephalians, which did not. Another example is that of the convex dorsal profile that is seen in the sphenacodont pelycosaur-grade synapsid Dimetrodon and some gorgonopsids such as Arctops. Functional convergence may also underlie the broadly similar skull proportions of the sphenacodont Secodontosaurus and some dolichorostral therocephalians such as Lycideops. Within both ancient and Cenozoic predator clades, there is frequently a tendency toward increasing body size and hypercarnivory over time. For example, therocephalians, gorgonopsids, and dinocephalians all tend to get larger in body size, enlarge their canine teeth, and strengthen their jaws and snouts over their history. Among Cenozoic mammals, the tendency toward large size is usually accompanied by a reduction in snout length and postcarnassial molars. This trend is apparent among all three subfamilies of canids (Van Valkenburgh et al., in press), oxyaenids (Gunnell, 1998), hyaenodontids (Mellet, 1977), amphicyonids (Viranta, 1996; Hunt, 1998b), and hyaenids (Werdelin and Solounias, 1996). The prevalence of this pattern suggests that it is driven by aspects of the large carnivore niche. Levels of interspecific competition for food are relatively high within guilds of extant carnivorous mammals (Eaton, 1979; Palomares and Caro, 1999; Van Valkenburgh, 1985, 2000). Because larger individuals tend to dominate inter- and intraspecific conflicts, such as occur over carcasses,

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selection favors the evolution of larger body size. However, large size brings with it a costthe need to feed on prey as large as or larger than oneself. As shown by Carbone et al. (1999), almost all living carnivoran species larger than about 21 kg take prey as large as or larger than themselves, whereas smaller species feed mostly on prey that is 45% or less of their body weight. Using an energetic model, they argued that because of limitations on intake rate and foraging time, it becomes increasingly difficult to subsist on small prey items as predator body mass grows. Consequently, the evolution of large body size (>20 kg) in a carnivore must be associated with craniodental adaptations for killing and feeding on large prey. These include shortened snouts to enhance bite force at the canines, as well as robust canines and large carnassials. Nonmammalian synapsids seem to have been subject to these same evolutionary forces, and modified their skulls to improve the KI bite system as well as to add the SP bite system. Van Valkenburgh (1999) argued that this tendency toward specialization within carnivore clades might explain their inevitable declines. Large, hypercarnivorous species may do well in the short run, but their specialization results in a loss of evolutionary versatility that inhibits their ability to adapt rapidly to changing environmental conditions. Moreover, families or subfamilies of large-sized carnivores tend to be less species-rich than those of smaller carnivores, and consequently more vulnerable to extinction. Thus, as clades of carnivores evolve toward large size and hypercarnivory, they dwindle in species richness leading to their decline and ultimate extinction. Thus, the cycle of rising and falling dynasties that so typifies the fossil record of carnivores seems better explained by the dynamics of competition among predators themselves than by changes in prey diversity or adaptations.

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