Biases in the data
Marks meeting criteria for unambiguous claw marks could be reliably attributed to lions; however, lions probably inflicted some of the ambiguous marks and reported claw-mark prevalence is therefore conservative. Moreover, some marks were inevitably missed due to varying photographic conditions. Claw marks were hardest to detect on mature adult males, whose coat markings darken with age (Brand, 2007; Berry & Bercovitch, 2012), sometimes to an almost black shade (Dagg, 1968; Berry, 1973). The giraffe has very thick skin (Dimond & Montagna, 1976; Sathar, Ludo Badlangana & Manger, 2010), so some contact attacks may leave no evidence. Fine marks may fade with time. Marks on young animals may also heal differently than those on older individuals. However, all marks that were observed at the start of this 2-year study, including those on subadults, were still visible at the end.
Lion attack behavior
Factors affecting lion-hunting success include prey size, the number of lions participating in the hunt, time of day and the amount of cover (Schaller, 1972; Funston et al., 2001; Hopcraft, Sinclair & Packer, 2005). Although solitary lions can attack adult giraffes (Pienaar, 1969), groups of lions are more successful at bringing down large prey (Schaller, 1972). During this 2-year study, we observed few lion-hunting attempts on giraffes, and none that resulted in contact. Coupled with the small number of claw marks acquired during the study, this suggests that attacks with contact are infrequent.
We expected to find claw marks on giraffe hindquarters because lions regularly attack large prey from the rear, grasping with their forepaws (Schaller, 1972). Consistent with this, claw marks were predominantly located on giraffe rumps, hind legs and flanks, suggesting that most non-lethal attacks also occur from the rear. This finding also supports the hypothesis of Sathar et al. (2010) that thicker skin on the upper flank and rump of giraffes may protect against lion-inflicted wounds. Lions kill with a bite or hold to the nose or throat of their prey (Schaller, 1972) and are able to seize hold of the neck of a standing adult giraffe. Two adult females in our sample had claw marks on the upper neck region. A giraffe would be extremely vulnerable if brought to the ground, so these females presumably were not. Lions rarely attack their prey from the front (Schaller, 1972), consistent with our finding that few giraffes had claw marks on the chest, neck and forelegs. Giraffes defend themselves with front and rear kicks (Schaller, 1972; Dagg & Foster, 1982), capable of maiming or even killing a lion, and lions risk significant injury during attacks on giraffes.
Patterns of lion predation
The giraffe is not a preferred prey species of lions in Serengeti (Scheel & Packer, 1991), where smaller prey like zebras and wildebeest are abundant (Sinclair & Norton-Griffiths, 1979). Nevertheless, the giraffe's size means that it can provide a large quantity of meat. Schaller (1972) estimated that although lions killed few giraffes, giraffes made up 27.5–32.5% of the lion's annual diet in Serengeti in the late 1960s. Since then, wildebeest numbers in Serengeti have doubled (Mduma, Sinclair & Hilborn, 1999), while giraffe numbers have declined (Strauss, unpubl. data). Today, giraffes probably contribute substantially less to the lion's diet.
The lack of claw marks among giraffe calves suggests that calves are highly unlikely to survive attacks where contact is made. Carcasses of calves were found in proportion to their availability in the giraffe population (Pellew, 1983a; Strauss, unpubl. data). However, calves are quickly consumed so we expect lions kill more calves than observed. We found few claw marks on subadult giraffes, and younger subadults appear to be more vulnerable than older, larger subadults (Fig. 4).
Claw-mark prevalence increased steeply from the subadult to the adult age class. Although size appears to be an important factor in escape probability, claw-mark acquisition also depends on other variables, as suggested by our height analysis and by the fact that subadult males reach the height of adult females at 3–4 years of age yet display a lower claw-mark prevalence. Bleich (1999) proposed inexperience as a cause of higher rates of fatal coyote Canis latrans attacks on young mountain sheep Ovis canadensis. Likewise, older and more experienced adult giraffes may be most successful at surviving lion attacks. In addition, the maximum age of giraffes is c. 25 years, so adults are exposed to attacks over a substantially longer period than subadults. In support of this, the majority of adults with claw marks (92.5%) were fully mature.
The observed sex difference in claw-mark prevalence in adults but not subadults requires explanation. Male giraffes suffer higher mortality from lion predation in southern Africa (Hirst, 1969; Pienaar, 1969; Owen-Smith, 2008), so we expected a similar pattern in Serengeti. Lower claw-mark prevalence among adult males may indicate increased male vulnerability to lethal attacks as has been observed in other ungulates, including Kongoni Alcelaphus buselaphus (Rudnai, 1974) and Thompson's gazelles Gazella thomsonii (FitzGibbon, 1990). A possible explanation for this pattern in giraffes is that adult males tend to be more solitary (Foster & Dagg, 1972; Leuthold, 1979; Pratt & Anderson, 1985; van der Jeugd & Prins, 2000; Bercovitch & Berry, 2010), and solitary ungulates have been shown to be at higher risk of predation (FitzGibbon, 1990). Also, adult males habitually spend more time than females in densely vegetated areas (Foster, 1966; Foster & Dagg, 1972; Young & Isbell, 1991; Caister, Shields & Gosser, 2003) that offer good cover for lions (Hopcraft et al., 2005).
As expected, Serengeti lions killed more giraffes in the dry season, coinciding with the decrease in preferred migratory prey. This is also a period when giraffes are nutritionally stressed (Hirst, 1969; Hall-Martin & Basson, 1975; Owen-Smith, 2008). During the Serengeti dry season, browse availability in midslope and ridgetop woodland areas declines (Pellew, 1983b) and giraffes shift habitat use to valley bottom and riverine areas (Pellew, 1984), prime ambush areas for lions (Hopcraft et al., 2005). The diet of adult male giraffes is nutritionally poorer than that of females (Pellew, 1984) and malnourished adult males may be particularly vulnerable to predation (Owen-Smith, 2008).
In contrast to adult males, adult female giraffes, especially mothers with young, are frequently observed in large herds (e.g. Foster & Dagg, 1972; van der Jeugd & Prins, 2000) and in open areas or areas with short vegetation (Foster & Dagg, 1972; Young & Isbell, 1991), a pattern consistent with our observations in Serengeti. Bercovitch & Berry (2010) suggested that in open terrain, increasing herd size does reduce predation risk for giraffes. In mountain sheep, similar behavior is observed: females and offspring occupy areas where they can detect and evade predation, while males occupy high-risk areas where they are more likely to encounter predators (Bleich, Bowyer & Wehausen, 1997). Consistent with this idea, claw marks were rarest in Kirawira, where giraffes commonly gather in large herds in open grassland areas. Although we did not find any relationship between an individual's mean herd size and claw-mark presence in Seronera, mean individual herd size may not be a useful measure if individuals are only likely to be attacked when temporarily alone.
If adult females generally behave in less risky ways, then why do they have the highest claw-mark prevalence? High claw-mark prevalence in adult females could be partially explained by marks acquired during calf defense. In a study of bottlenose dolphins Tursiops truncatus, Corkeron et al. (1987) observed fresh predation marks on a relatively high number of females with calves, and they suggested that female–calf pairs are more vulnerable to predation. Giraffe calves are an attractive target for lions. Mothers protect their calves by positioning them between their legs and by chasing or kicking at predators (Pratt & Anderson, 1979; Dagg & Foster, 1982). Lions have been observed lunging at nursing females to distract them from their calves, and this may be when they inflict superficial claw marks. In support of this hypothesis, we found a substantial jump in the prevalence of claw marks among females at age 4–5 years, coincident with the onset of first parturition (Fig. 4a). Injuries incurred during calf defense could also explain why only adult female giraffes were observed with marks on 4 or more body regions. In addition, the only observation of an individual surviving more than 1 non-lethal attack was that of an adult female. Observations of fresh claw marks on nursing females would provide additional support for this hypothesis.
Adult females may be most susceptible to lethal lion attacks in the last weeks of pregnancy and just after parturition, when females behave more like mature males: pregnant females spend more time browsing in dense vegetation to meet nutritional needs (Young & Isbell, 1991). Females also become solitary shortly before giving birth (Foster & Dagg, 1972; Strauss, pers. obs.) and keep their neonates relatively isolated from other giraffes for up to 3 weeks post-partum (Langman, 1977; Pratt & Anderson, 1979; Mejia, in Moss, 1982), thereby forgoing the vigilance benefits of additional herd members.
Index of predation risk
Studies of marine mammals suggest that predation-mark prevalence can be a useful index of predation risk (Heithaus, 2001; Bertilsson-Friedman, 2006). For example, in bottlenose dolphins Tursiops spp., predation-mark prevalence varies widely among populations, from 0 to >70% (Corkeron et al., 1987; Cockcroft et al., 1989; Bearzi, Notarbartolo-di-Sciara & Politi, 1997; Heithaus, 2001).
Likewise, lion claw-mark prevalence is 1 way to assess spatial and temporal patterns in predation risk for giraffes. We speculate that the low claw-mark prevalence observed in Kirawira is an indication of low lion-predation risk. With high densities of preferred prey available, lions probably target Kirawira giraffes infrequently. In addition, Kirawira giraffes benefit from high visibility due to low vegetation. Kirawira giraffes also aggregate in large herds, which reduces each individual's risk of predation due to increased likelihood of predator detection and a dilution effect (Hamilton, 1971; Pulliam, 1973; Bercovitch & Berry, 2010). Giraffe recumbency during the daytime was observed frequently in Kirawira but rarely in Seronera and further supports our hypothesis of low lion-predation risk in Kirawira. Further research is needed to explain large herd sizes typical of Kirawira.
The giraffe is an important food source for lions in some regions, including Kruger National Park, South Africa (Pienaar, 1969; Owen-Smith & Mills, 2008) and Hwange National Park, Zimbabwe (Loveridge et al., 2006). Where giraffes are a large component of the lion's diet, we might expect even higher claw-mark prevalence than observed in Serengeti. Alternatively, claw-mark prevalence could be lower if lions in these areas are more successful giraffe hunters or if giraffes are less adept at surviving attacks.
In summary, predation marks demonstrate that nature is indeed ‘red in tooth and claw’, even for the largest prey. Our results support prior published data on giraffe predation, suggesting that young giraffes are most vulnerable to predation and that lethal attacks increase in the dry season. We find evidence to suggest that while adult males are more vulnerable to lethal attacks, females are also likely to incur non-lethal attacks during calf defense. Our results also suggest that there is significant spatial variation in predation risk within Serengeti.
Overall, we find that in the absence of direct observation, claw marks provide an important source of data on lion predation attempts on giraffes. Unlike carcass data, claw-mark data can be collected on a large sample of individuals over a relatively short amount of time, with prompt analysis aided by continuing advances in digital camera technology and pattern-matching software. Thus, we recommend the use of claw marks to increase the sample size of lion predation attempts on giraffes. Claw-mark studies may also prove useful for other lion prey species.