The giant hyena Pachycrocuta brevirostris: Modelling the bone-cracking behavior of an extinct carnivore
Introduction
Pachycrocuta brevirostris (Aymard) (Mammalia, Carnivora, Hyaenidae) was the largest hyaenid that ever existed, with a body size 20% larger than that of the modern spotted hyena (Crocuta crocuta) and was well adapted for dismembering carcasses and consuming bone (Fig. 1) (Werdelin and Solounias, 1991, Turner and Antón, 1996, Arribas and Palmqvist, 1998, Saunders and Dawson, 1998, Werdelin, 1999, Palmqvist and Arribas, 2001). The basal lengths of the skull of the Sainzelles type specimen (322 mm; Turner and Antón, 1996) and the skull from Zhoukoudian (315 mm; estimated from Pei, 1934) provide an appropriate picture of the enormous size of this extinct carnivore, as they parallel those of the largest southern African male lions (range: 241–328 mm; Turner and Antón, 1996).
The Pachycrocuta lineage evolved from the late Miocene Hyaenictitherium (Howell and Petter, 1980) and is first recorded in Africa during late Pliocene times (Hadar, ∼3.0 Ma; Turner, 1990). Later, close to the Plio-Pleistocene boundary (recently redefined at 2.588 Ma; Gibbard et al., 2010) and coincident with the appearance in the archaeological record of the first stone tools and evidence of human activity on large mammal bones (de Heinzelin et al., 1999, Semaw et al., 2003), Pachycrocuta was extinct in East Africa but dispersed into southern Africa (e.g., Makapansgat Member 3) (Toerien, 1952, Randall, 1981, Werdelin, 1999), where it is represented by Pachycrocuta bellax. By these times, two hyaenid species, the large bone destroying Pliocrocuta perrieri and the gracile pack-hunting Chasmaporthetes lunensis, reached Eurasia within the “Elephant-Equus” dispersal event (Azzaroli et al., 1988). During the Early Pleistocene, both species were replaced by the giant form P. brevirostris, although P. perrieri re-appeared in Europe in the Middle Pleistocene (Turner and Antón, 1996, Turner et al., 2008). Pachycrocuta inhabited Asia from the end of the Pliocene to middle Pleistocene times (Nihowan, ∼3 Ma; Upper Siwaliks, 1.8–1.2 Ma; Dmanisi, ∼1.8 Ma; Zhoukoudian Locality I, ∼0.4 Ma; Turner and Antón, 1996, Boaz et al., 2000, Boaz et al., 2004, Dennell et al., 2008). In Western Europe, P. brevirostris is first recorded in Early Pleistocene deposits of Italy (Olivola Faunal unit, ∼1.99 Ma; Napoleone et al., 2003; Pirro Nord, 1.7–1.3 Ma; Arzarello et al., 2007) and its latest appearances are in the late-Early Pleistocene (1.0–0.8 Ma) (Süssenborn, Stranska Skala, Untermassfeld, Vallonnet, Cueva Victoria, Slivia, Incarcal) (Turner and Antón, 1996, Arribas and Palmqvist, 1999, Turner et al., 2008). The dispersal of P. brevirostris in Europe would in all probability be from Asia, as this species was extinct in East Africa by late Pliocene time (Werdelin, 1999).
The disappearance of the giant hyena in Europe was probably linked to the decline and subsequent extinction of saber-tooth cats, particularly Megantereon whitei (Martínez-Navarro and Palmqvist, 1996, Palmqvist, 2002a), which implied the loss of an important source of partly consumed carcasses and thus a change in the interactions between flesh-eating and bone-cracking species of the carnivore guild. During the early middle Pleistocene transition (∼0.8 Ma), P. brevirostris was replaced by the spotted hyena, as recorded at the Gran Dolina of Atapuerca deposits in Spain (García, 2003).
Apart from its enormous size, P. brevirostris differed from the modern hyenas in the shortening of the radius and the tibia relative to the humerus and the femur, respectively. As a result, the overall height of the giant hyenas (shoulder height between 90 and 100 cm) was not much greater than that of a large spotted hyena (85 cm), as the skull size alone would suggest (Turner and Antón, 1996). The shortening of the distal limb segments indicates a less cursorial life style for P. brevirostris compared to the living hyenas, although it certainly provided greater power and more stability to dismember and carry large pieces of ungulate carcasses to the denning sites (Palmqvist and Arribas, 2001). This agrees with the scavenging behavior deduced from taphonomic analysis of bone assemblages collected by this extinct hyena (Arribas and Palmqvist, 1998, Palmqvist, 2002b).
However, Turner and Antón, 1996, Galobart et al., 2003 and Dennell et al. (2008) have argued that the large size of P. brevirostris could have been advantageous for the capture and subduing of medium-to-large-sized ungulate prey under concerted action within a pack, as well as in any contest with other predators in defence of a kill or during aggressive scavenging (i.e., kleptoparasitism). While acknowledging that the giant hyenas may have operated as less of a hunter than modern spotted hyenas, Turner and Antón (1996) point to several aspects of the morphology of spotted hyenas that in their opinion only make sense in relation to their hunting ability when viewed within the context of group activity. These features include their body and limbs more heavily built and massive than in both the extant brown hyena (Parahyaena brunnea) and striped hyena (Hyaena hyaena), species that need to cover longer distances searching for scavengeable carcasses.
Scavenging and hunting are simply part of a continuous spectrum (Turner et al., 2008), which means that the behavior of many extant carnivores cannot be extrapolated directly from the study of a single living population (e.g., there are marked differences between the predatory habits of spotted hyenas in Serengeti and Ngorongoro National Parks; Kruuk, 1972). This situation is even worse in the case of extinct carnivores, because the fossil record usually does not provide clear evidence on which particular predator made a kill. At best, researchers can only make inferences on which carnivore consumed the carcass and at what stage it might have gained access to it (Dennell et al., 2008). For these reasons, the question of whether an extinct predator habitually killed its own prey or scavenged the prey captured by others will be always a difficult one to address.
This paper tries to decipher the paleobiology of P. brevirostris using a combined biomechanical and taphonomic approach. The biomechanical study focuses on features of the craniodental and postcranial morphology of this extinct hyena related to feeding preferences and locomotive performance, including new body mass estimates. The taphonomic analysis concentrates on the preservational bias introduced by the bone-cracking behavior of P. brevirostris in the large mammal assemblage of Venta Micena, a locality currently interpreted as an early Pleistocene denning site of this giant hyena (Palmqvist et al., 1996, Arribas and Palmqvist, 1998, Palmqvist and Arribas, 2001).
Section snippets
The early Pleistocene large mammal fauna from Venta Micena
Venta Micena is located near the village of Orce in the Guadix-Baza intramountane basin (Granada, southeast Spain). This sedimentary basin was endorheic (i.e., characterized by interior drainage) from the end of the Miocene to late Pleistocene times, which facilitated an exceptional record of Plio-Quaternary taphocoenoses of large mammals in swampy and lacustrine sediments (Arribas and Palmqvist, 1999). The large mammal assemblage from Venta Micena shows close affinities to the one preserved at
Materials and methods
The original abundance of skeletal remains of each ungulate species in the assemblage transported by the hyenas (i.e., the bone frequencies prior to destruction of skeletal elements within the maternity dens) was estimated using the minimal number of individuals (MNI) calculated from teeth counts and cranial elements (mandibles, maxillae and cranial vaults), as well as from minimal number of elements (MNE) estimated for each major limb bone (i.e., complete elements and those represented by
Results
Table 1 shows the abundance of the main skeletal elements in equids (E. altidens), bovids (Bison sp., C. alba and S. minor) and cervids (P. verticornis and M. rhenanus). This table includes MNE estimates for these bone specimens and percentages of surviving bones and bone portions.
Table 2 shows MNI estimates for the three ungulate families, obtained from minimal number of heads (based on teeth counts and abundance of cranial elements) and estimates of minimal numbers of forelimbs and hind limbs
Discussion
What does the craniodental and postcranial anatomy of the giant hyena indicate? Apart from its large size, P. brevirostris differed from other hyaenids in the relative shortening of its distal limb segments (Table 5), with a brachial index (radius length to humerus length) of 0.91 (range for modern hyenas: 1.00–1.08) and a crural index (tibia length to femur length) of only 0.74 (range: 0.82–0.88). Although such shortening may be explained in part as a consequence of the enormous size of this
Acknowledgments
L. Spencer, A. Turner, B. Van Valkenburgh and L. Werdelin provided insightful comments on earlier versions of this manuscript. This study was developed within the framework of Research Groups RNM-146 and HUM-607 (Junta de Andalucía) and funded by projects CGL2008-04896, CGL2009-08827, CGL2010-15326, and HAR2008-04577 (Spanish Ministry of Sciences). B. Figueirido and V. Torregrosa enjoyed FPU grants and J.M. Jiménez-Arenas has a Return Contract in the University of Granada (Spain). And, last but
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