1 - Introduction

1Numerous actualistic studies of bone modification resulting from predation and feeding have been undertaken on captive carnivores in zoos or free-ranging carnivores in game parks. Such investigations are critical since they provide baseline data with which to assess the taphonomy of fossil and archaeological bone assemblages, enabling researchers to identify the agent/s involved in their accumulation and or modification. For medium-sized felids, most actualistic studies have focused on leopards (e.g. Cavallo & Blumeschine, 1989; de Ruiter & Berger, 2000; Pickering et al., 2011) given their extensive association with early hominin sites in southern Africa (e.g. Brain, 1981; Pickering et al., 2004; Bountalis & Kuhn, 2014). Fewer actualistic studies have examined the taphonomy of cheetah–derived damage to carcasses (some exceptions include Brain, 1981; Phillips, 1993; Selvaggio & Wilder, 2001; Domınguez-Rodrigo & Piqueras, 2003). This probably stems from the fact that cheetahs (Acinonyx jubatus) have rarely been observed transporting carcass portions (Lewis 1997, table 2), such that their role as bone accumulators has been perceived as potentially negligible, as stated by Brain (1981, p26): “I do not intend to suggest that cheetahs would ever have contributed food remains to bone accumulations in African caves.” However, the presence of fossil cheetah remains in several early hominin sites, for example Dmanisi, Laetoli, Lukenya, Sterkfontein, Swartkrans, Makapansgat; Coopers D Kromdraai  (Werdelin & Peigné, 2010, p639; Hemmer et al., 2011; Geraads, 2014). This implies that members of this genus may have played a larger taphonomic role than previously acknowledged as a source of faunal remains in assemblages associated with early hominins. Notably, cheetah kills may serve as “carnivore hubs” that attract other scavengers (Hunter et al., 2007), including early hominins (e.g. Blumenschine, 1986; Domınguez-Rodrigo, 2000). Moreover, cheetahs lose quite a high proportion of their kills (9.5-13 %) to “kleptoparasites” (which may have included early hominins), most notably lions and spotted hyaenas (Caro, 1994; Radloff & du Toit, 2004; Hayward et al., 2006). Consequently, much can still be learnt about the potential role of this carnivore as a taphonomic agent that is of relevance to archaeozoology.

2In this study, we document on the intensity of bone damage observed on a set of mandibles belonging to different-sized prey collected from recent cheetah kills. It is hoped that this investigation will broaden our understanding of multiple-carnivore intervention and modification to cheetah prey.

2 - Material and methods

3Here we report on intensity of bone damage to 29 mandibles that were collected from 25 recent cheetah kills in the Mountain Zebra National Park (MZNP) located in the Eastern Cape Province, South Africa (fig. 1). The region is characterized by an arid climate and the vegetation of the park falls within three biomes: Grassland, Nama Karoo and Albany Thicket and one azonal vegetation type, Inland Saline Vegetation (Mucina & Rutherford, 2006). The southern portion of MZNP is mountainous with peaks of up to 1960 masl while the northern part is composed of lower lying areas ranging from 1000 m to 1500 masl. Water is available year round in dams and pans and in a perennial river the Wilgerboom which only flows during the wet season (Welch et al., 2015).

4The samples studied here derives from kills of eight radio-collared cheetahs (four adult females ranging in age from 4-8 years old; two adult males aged 4-5 years and 10 years old respectively; two young males aged 2 years old) that were monitored over a one-year period by one of the authors (CB) (March 2012-March 2013). Cheetah kills were located in MZNP using the cluster points of GPS coordinates downloaded from the satellite/GPS collars with VHF transmitters with which the cheetahs had been fitted as described by Tambling et al. (2010). Monthly fieldtrips were conducted during the sampling period to locate cheetah kill remains using the GPS cluster method (Tambling et al., 2012). During these fieldtrips the cheetahs were tracked using the telemetry receiver and if they were located on a kill the species, age and sex of the kill was recorded. Furthermore, all GPS cluster points for that month were visited to determine whether a kill was made by that particular cheetah. Each of the mandibles studied here derives from a prey of an individual rather than a group of cheetahs. The area around the GPS cluster was searched for kill remains and if the kill remains could not be identified in the field they were collected for later identification in the laboratory (van de Vyver, 2017). At the time of this study cheetahs were the apex predators in MZNP (fig. 2a-b), however meso-predators, primarily black-backed jackal and brown hyaena, were also found in the park. These meso-predators scavenged from the cheetah kills and therefore quite often only leg and jaw bones remained at the kill sites if they were visited a few weeks after the kill was made. As Brain concluded in his study of free-ranging cheetah kills in the Kruger National Park, it was “extremely difficult to find remains that had not been modified by [other] scavengers” (Brain 1981, p24). For this reason, and since researchers have noted that generally cheetah feeding results in very little damage to the skeleton of their prey, including the cranium (e.g. Blumenschine, 1986; Brain, 1981; Phillips 1993; Caro, 1994; Charlene Bissett, pers. comm. April 2017), we have assumed that the mandibles examined here exhibit an amalgam of damage potentially caused by three carnivores: minimally cheetah and to a greater extent, black-backed jackal and brown hyaena. Indeed, composite carnivore damage may perhaps be considered a characteristic of cheetah kills.

5The mandibles (representing a small sub-set of skeletal elements collected from the kills) were examined at the Florisbad Quaternary Research Department (National Museum, Bloemfontein). They were sided and identified to species based on morphological features and comparison with a modern osteological collection. The age of the animals was determined using tooth eruption and dental wear where necessary. Carcasses could not be sexed as pelves were not collected systematically as often only the mandibles were left at the kill site due to the other skeletal elements being dispersed by scavengers.

6Intensity of damage for selected features on each mandible was scored using a simple three-part system: 1 = intact/undamaged; 2 = slight to moderate gnaw damage; 3 = heavy/extensive gnaw damage with parts, or all, of that feature missing. Mandible features scored were: incisor area and diastema (grouped as ‘anterior mandible’); premolar and molar corpus (grouped as ‘mandible corpus’); coronoid process, ramus, gonion, mandible condyle (grouped as ‘posterior mandible’). The individual scores (1 through 3) for each feature were summed to obtain an intensity value for that entire portion of the mandible e.g. individual scores of 2 for the coronoid process, 1 for the ramus, 3 for gonion and 1 for the mandible condyle would give an overall damage intensity value of 7 for the ‘posterior mandible’.

7Surface modifications were identified using a magnifying glass and defined following Delaney-Rivera et al. (2009): tooth scores - striae with length measuring three or more times their breadth; tooth punctures - circular to oval depressions in which the entire thickness of compact bone has been penetrated; tooth pits - circular, oval or triangular superficial depressions often resembling the shape of a tooth crown or cusp. The greatest length and breadth of each mark was measured under magnification directly on the bone using a vernier caliper.

8The most common weight range for successful cheetah kills is 23-56 kg (Hayward et al., 2006). Given that we do not know the sex of the prey or the precise body weight of the juvenile animals, we calculated a “hypothetical” juvenile weight (tab. 1) following the method outlined in Radloff and du Toit (2004). We used adult weights given in Stuart and Stuart (2001). For prey taxa, the small size class and lower weights for the medium size class are well within the range of typical cheetah prey, but the large size class (juvenile elands) may have weighed a minimum of 102 kg which is far heavier than typical cheetah kills, though male cheetahs take larger prey than females (e.g. Radloff & du Toit, 2004; Bissett & Bernard, 2007).

3 - Results

9Data for the individual specimens studied are listed in table 1, with adult and juvenile body weights and mandible damage intensity scores. The following species fall within the diet of the MZNP cheetahs: blesbok, grey rhebok, klipspringer, mountain reedbuck, springbok, black wildebeest, duiker, eland, red hartebeest, gemsbok, kudu and steenbok. The first five species are medium-sized and fully grown adults are preyed upon. The latter seven species are larger size and generally juveniles and sub-adults are targeted, although in some instances adults are also taken.

10In MZNP, juvenile kudu (Tragelaphus strepsiceros) were the preferred cheetah prey, a species found in thickets and scrub and rarely seen in open areas. Welch et al. (2015) suggested that ecological factors might be responsible since kudu hide their calves in secluded areas for the first three months before rejoining the herd, making them easy prey. Springbok (Antidorcas marsupialis) was the second most common species taken by cheetahs and together with kudu comprised 85 % of all cheetah prey. Animals taken less commonly by the cheetahs in MZNP were those inhabiting rocky areas - mountain reedbuck, grey rhebok - and those inhabiting the open mountain plateau areas of the park - red hartebeest, eland (Welch et al., 2015).

11Welch et al. (2015) reported a link between cheetah prey density and habitat. Of the twelve different vegetation types identified in MZNP, those with the highest prey density were the degraded shrubland, riverine woodland and the plateau grassland. Cheetahs were observed in all three habitats and the kills described here derive from these locations; kudu, the most common prey, is found in intermediately dense vegetation (riverine woodland and degraded shrubland), while the springbok, the second most common prey, inhabits the open plateau grassland areas. These data demonstrate that cheetah hunting success is equal in open or dense cover (see discussion in Bissett & Bernard, 2007; Welch et al., 2015).

12All animals represented in the mandible sample were either adult with fully erupted permanent dentition, or juvenile defined as having a deciduous dp4 in advanced wear and/or with M1 erupting or erupted (as illustrated in fig. 1). Clearly prey size is a critical factor; all medium and large-sized ungulates taken at MZNP (≥ 100 kg), were juveniles weighing less than half adult weight, while adult prey weighed ≤ 41 kg. This complements data reported by Mills et al. (2004) for cheetah prey in the Kruger National Park (South Africa), where for large prey species (zebra, waterbuck, kudu), 69 % were juveniles and only 39 % adults.

13Given the small and unequal sample sizes, the non-parametric Mann-Whitney test was used to examine differences in damage intensity between different sized prey (data given in tab. 1). Significance was set at < 0.05. Statistically significant differences were found in the posterior portion of the jaws between small and large-sized prey (P = 0.01) and medium and large-sized prey (P = 0.03) but not between small and medium-sized prey, suggesting that damage intensity to the posterior mandible in large-sized prey is the driver, and differs significantly from the others. Similar results were obtained for the mandible corpus, with significant differences found between small and large-sized prey (P = 0.04), again signifying that the intensity of damage in large-sized prey differs from the others. No statistically significant differences were found between small and medium-sized prey, or between medium and large-sized prey. Similarly, no meaningful differences were found between taxa in the intensity of damage to the anterior portion of the jaw. Damage to juvenile and adult mountain reedbuck mandibles were also compared, but no significant age-related differences were found between them in the extent of damage. This result is surprising given the smaller size and softer bones of juvenile reedbuck and may perhaps be attributed to the small number of jaws examined (N = 6 juveniles and 2 adults).

14It should also be noted that on all mandibles surface micro-damage was observed. The gnawed edges usually had jagged, crenulated outlines (fig. 3). Tooth punctures were the most frequent type of damage followed by small pits and lastly tooth scores; all were commonly located adjacent to a gnawed edge (fig. 3). Tooth mark dimensions taken here may have been affected by having been measured directly on the bone. Moreover, the dimensions of micro-damage tends to be larger on cancellous bone tissue than on dense cortical surfaces (Domınguez-Rodrigo & Piqueras, 2003; Delaney-Rivera et al., 2009). Since our mandibles are composed of cancellous bone, their surface damage should more closely resemble dimensions of epiphyses than diaphysis. The vast majority of pits and tooth scores on the studied mandibles have small dimensions (tab. 2) and conform to the size ranges (e.g. pit length of ≤ 4 mm and width of ≤ 2 mm or less) of epiphyses given in Domınguez-Rodrigo and Piqueras (2003) and Delaney-Rivera et al. (2009) for small-sized canids such as jackals, and medium-sized felids such as cheetahs or leopards. There are a few larger puncture marks (but none of the pits) with a length dimension of ≥ 5 mm, and these conform to marks made by large carnivores, such as hyaena.

4 - Discussion

15Several researchers (e.g. Brain, 1981, p24; Pobiner, 2008; Geraads 2014), have noted that cheetahs have short canines, a reduced or absent second premolar, well developed third and fourth premolars and carnassials, which makes them specialized for slicing meat, but with a reduced bone-crushing component compared to other felids. Phillips (1993) noted that when consuming bone such as ribs, cheetahs adopt a typical gnawing position by rotating the head and crushing the bone with their carnassial teeth. Field observations by one of the authors (CB) on cheetah kills at MZNP and other reserves in South Africa confirm that cheetahs typically consume only the meat of their prey and maybe the tips of the ribs. On adult animals they do not even touch the head. Phillips (1993) noted that when adult springbok were killed by cheetahs, only parts of the ribcage, the dorsal spines of the vertebral column, and the scapular spines were partially consumed, with the width of the consumed bones always ˂ 15 mm. Brain‘s research (1981) on both free-living and captive cheetahs, confirms this observation as does research by Blumenschine (1986) and others. Moreover, as noted by Houston (1979), cheetahs seldom consume an entire carcass and tend to leave their kills quickly. These data imply that carcasses at cheetah kills will be relatively undamaged, and certainly the skull and jaws will be untouched.

16Brain (1981) does however report an exceptional instance where captive cheetahs were fed the carcass of a shot baboon: “the entire vertebral column, from atlas to first caudal, had disappeared, as had most of the ribs. The innominate bones showed damage round the edges, and both knee joints had been disarticulated and chewed“ (Brain, 1981, p26). He attributed the extensive damage to the less porous nature of the baboon trunk elements compared to those of bovids. However, it is most unlikely that in the wild cheetahs would prey on live baboons. Another exception to general cheetah feeding patterns, is the documented consumption of the entire skeleton of springbok fawns with only the digestive tract left (e.g. Phillips 1993; Charlene Bissett, pers. comm., May 2017), while for adult steenbok, a similar small-sized ungulate, most of the bones of the skeleton were consumed but the head, hooves and digestive tract remained (Phillips 1993). Thus, the extensive damage (stage 2 and 3) found on many of the mandibles, especially in the medium and large-sized prey classes, is undoubtedly the result of feeding by other carnivores on the cheetah kills i.e. black-backed jackals and brown hyaena. This is further corroborated by the dimensions of the surface micro-damage documented on the jaws (tab. 2).

17In this study, the medium and large-sized cheetah prey were all juvenile animals, with softer bone tissue that yields more easily to pressure than in adults. This and the cancellous nature of the mandible probably facilitated the intensive damage inflicted to many of the jaws. As documented for other carnivores, damage to the mandible was primarily located on bone protuberances and extremities, which are easily accessed with most damage occurring on the posterior portion of the jaws, which is the area of most masticatory muscle attachment (Sisson 1930).

18Together with bone composition, prey body mass is a critical feature influencing the intensity of damage. This is illustrated by the absence of differences in damage intensity to mandibles of adult and juvenile mountain reedbuck. Though of different ages, both are small-sized ruminants. In contrast, the most extensive damage occurred on the juvenile eland jaws. We propose that this relates to greater quantities of meat and muscle the eland provides making it a more attractive carcass. Moreover, as noted by Blumeschine (1986), large carcasses persist for a significantly longer period of time in the landscape than small carcasses and thereby tend to attract more scavengers. In turn, this would have promoted: (i) prolonged feeding and/or multiple visits by carnivores to the eland carcasses, though cheetahs are not known to return to their kills; (ii) multiple carnivore taxa attending a cheetah kill after the cheetah has left or been driven off. This seems the most likely explanation given the nature and extent of damage observed on the mandibles and the fact that cheetah kills are known feeding hubs for other carnivores. In several instances, one of the authors (CB) noted brown hyaena and black-backed jackal scats near cheetah kills, and in one instance three jackals chased a cheetah off a kill. Consequently, multiple carnivore engagement with the cheetah kill carcasses is the most parsimonious explanation for the observed damage, and appears to have involved both black-backed jackals and brown hyaenas. This is corroborated by the size of the surface micro-damage observed on the jaws, which indicates the primary activity of a small-sized canid, such as the black-backed jackal, with the secondary input of a large carnivore, such as hyaena.

5 - Conclusion

19The results presented here, together with published data on cheetah kills, provide a broader perspective on the potential damage that carcasses may experience at cheetah kills. Notably, these localities serve as feeding hubs for other carnivore species given the large quantity of meat, marrow etc. left on the bones following cheetah feeding.

20The size of the prey species - often linked to its age, as well as bone composition (i.e. cancellous or cortical bone), appear to be decisive factors in determining the extent of damage. For very small animals (and young fawns), many if not most of the skeletal elements can be totally destroyed by the cheetah (as documented by Phillips 1993). Given that the skeletons of most cheetah prey are left undamaged following their feeding, the remains recovered by us are those which were subsequently modified by other carnivores who fed on the same carcasses. Finally, larger prey with more meat (such as the juvenile eland) will be more “attractive” than smaller-sized prey (such as the reedbuck) which have less meat, resulting in differential destruction to their bones. In future investigations, we hope to expand the quantity of prey species studied and types of skeletal elements examined in order to test whether the patterns found in this pilot study hold up.