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- Materials and methods
The risk of predation or interference competition can significantly alter animal behaviour and species’ spatial distribution (Ripple & Beschta 2004; Fortin et al. 2005; Berger & Gese 2007). However, the probability of costly encounters can be minimised as risk is not homogenously distributed in space and time, but rather varies with the distribution, density, habitat use and activity of predators and competitors (Brown, Laundre & Gurung 1999). This heterogeneity allows animals to use ‘refuges’, that is, areas of low risk (Durant 1998; Chesson 2000) or adjust their behaviour, for example, habitat use or anti-predator behaviours such as vigilance, in response to changing levels of risk (Laundré, Hernández & Altendorf 2001; Creel et al. 2005).
Such a response to risk can either be reactive or predictive. A reactive response to risk is based on an animals' knowledge of actual, real-time risk. Elk (Cervus elaphus, Linnaeus), for example, used coniferous woodland, rather than grassland, when wolves (Canis lupus, Linnaeus) were in the immediate vicinity (Creel et al. 2005). Similarly, African buffalo (Syncerus caffer, Sparrman) visited waterholes during the hot, midday hours, rather than at dawn and dusk, when lions (Panthera leo, Linnaeus) were nearby (Valeix et al. 2009a). A predictive response, on the other hand, is based on a pre-emptive response to a potential for risk, derived from previous knowledge of the competitors or predators' whereabouts or the habitat types intensively used by them. For instance, browsers such as kudu (Tragelaphus strepsiceros, Pallas), giraffe (Giraffa camelopardalis, Linnaeus) and impala (Aepyceros melampus, Lichtenstein) were less likely to select areas where there was a long-term risk of predation by lions (Valeix et al. 2009b). These behavioural responses to risk are, however, by no means limited to predator–prey interactions, and numerous studies have observed similar responses between predators and humans (e.g. Woodroffe 2011; Valeix et al. 2012) and between competing carnivores (e.g. Creel, Spong & Creel 2001; Berger & Gese 2007). Whilst several studies have investigated reactive and predictive avoidance between carnivores independently (e.g. Durant 1998, 2000), these two types of avoidance in African carnivores have not yet been investigated simultaneously using the same set of data. Here, we investigate the reactive and predictive response of cheetahs (Acinonyx jubatus, Schreber) to the actual (i.e. short-term) and the prospective (i.e. long-term) risk of encountering lions and spotted hyaenas (Crocuta crocuta, Erxleben).
Due to their smaller body size and solitary nature, cheetahs are competitively subordinate to the larger and more social lions and spotted hyaenas (Caro 1994; Durant 1998, 2000). These larger predators are a potential threat to cheetahs: in the Serengeti National Park, Tanzania, for example, lions and spotted hyaenas were reported to be responsible for 73% of cheetah cub mortality and the kleptoparasitism of 12·9% of cheetah kills (Laurenson 1995; Hunter, Durant & Caro 2007b). Hence, cheetahs have been described as a ‘refugial species’, and spatial avoidance is believed to be one of the main mechanisms by which these competitively subordinate carnivores can minimise interactions with more dominant ones (e.g. Durant 1998).
To determine whether spatial avoidance of larger carnivores by cheetahs is reactive or predictive, we investigated both the effects of the short-term risk of encountering lions and spotted hyaenas (assessed by the distance to the nearest lion and spotted hyaena) and the long-term risk of encountering these predators (based on habitat use and a landscape of risk representing the likelihood of lion and spotted hyaena presence calculated over 6 months) on the spatial distribution of cheetahs.
More specifically we expected that:
- Cheetahs avoided areas that are intensively used by lions and spotted hyaenas (long-term risk),
- Cheetahs avoided immediate, short-term encounters with lions and spotted hyaenas (short-term risk),
- Cheetah habitat use was negatively influenced by the habitat used by lions and spotted hyaenas,
- The response to short- and long-term risks changed depending on the structural characteristics of the habitat.
To test these predictions, we used simultaneous Global Positioning System (GPS) radiocollar data from cheetahs, lions and spotted hyaenas in northern Botswana.
- Top of page
- Materials and methods
Our results show that the response of cheetahs to the risks posed by the larger and competitively stronger lions and spotted hyaenas is predator-specific, habitat-specific and dependent on the immediacy of the risk. More specifically, we show that cheetahs' response to risk is reactive rather than predictive. In other words, cheetahs did not consistently avoid habitats and areas with a high likelihood of encountering lions or spotted hyaenas (predictive response) but instead, adjusted their behaviour to short-term presence of lion risk (reactive response).
Whilst it has been suggested that less dominant species can minimise negative encounters with competitors or predators by selecting areas or habitat types that attract fewer predators and competitors, such as prey-poor areas (Chesson 1986; Rosenzweig 1991; Durant 1998), we did not detect any spatial segregation between cheetahs and lions or between cheetahs and spotted hyaenas both in terms of habitat use and long-term risk. The lack of predictive avoidance may result from (i) the fact that cheetahs do not directly benefit from avoiding areas of long-term risk, (ii) the inability of cheetahs to detect and infer long-term risks, or (iii) our failure to detect avoidance due to unaccountability of uncollared individuals. Whilst the latter may apply for spotted hyaenas (see below), we believe that this is not the case for lions since a significant proportion of the population was collared (for more details see the Methods section). We also believe that if it was evolutionary advantageous to discriminate between risky and nonrisky areas; cheetahs would have developed the ability to do so. It thus appears that cheetahs do not necessarily benefit from avoiding areas with a high chance of finding lions. These results are corroborated by recent findings in the Serengeti that have similarly shown that cheetahs do not avoid areas characterised by a high likelihood of encountering lions (A. Swanson, unpublished data). As in the Serengeti, the extensive overlap in space and habitat use between cheetahs and lions is likely driven by the distribution and acquisition of similar resources such as prey. In our study, cheetahs and lions selected for grassland and mixed woodland both for the 2nd and 3rd order selection and avoided mopane. In the Okavango delta, impala, which represents 75% of the diet of cheetahs (n = 92) and 17% of the diet of lions (n = 118, F. Broekhuis unpublished data), prefer mixed woodland over mopane (van Bommel et al. 2006). The observed differences in habitat use between lions and cheetahs on a finer spatial scale can be attributed to differences in behavioural traits, such as hunting strategies, rather than active avoidance. For instance, being high-speed hunters, cheetahs prefer more open habitats, while lions, being ambush hunters, are more successful in vegetated areas (Mills, Broomhall & du Toit 2004; Hopcraft, Sinclair & Packer 2005).
The immediate risk of encountering lions, however, appeared to be an important factor influencing the spatial distribution of cheetahs as the latter were generally further away from lions than would be expected under a random distribution. This suggests that lions pose a threat to cheetahs and that cheetahs can detect lion presence, assess the level of risk and adjust their behaviour accordingly, probably responding to more immediately and spatially reliable cues such as visual or auditory detection (Durant 2000). Interestingly, in mixed woodland, cheetahs were found to be closer to lions than expected. Since it is unlikely that cheetahs would actively move towards lions, this suggests that when cheetahs are in denser vegetated habitats they either cannot detect lions or do not feel the need to avoid them. Either way, denser habitats, such as mixed woodland, may be a relatively safe refuge for cheetahs as the reduced visibility is likely to reduce detection (Janssen et al. 2007), decreasing the likelihood of encounters with lions. This interpretation is supported by previous studies, which showed that vegetation cover minimised cheetah interactions with lions and spotted hyaenas (Bissett & Bernard 2007; Hunter, Durant & Caro 2007a). Similarly, elk have been shown to move into denser vegetation when wolves were nearby (Creel et al. 2005). Despite the fact that we believe there to be very little seasonal variation in the distribution and ranging behaviours of these carnivores, we acknowledge that the 6-month windows used in this study are a relatively short time span. We therefore encourage longer studies to be carried out in the future to account for seasonality and stochasticity among years.
In general, cheetah response to both the long- and short-term risk was less pronounced for spotted hyaenas than for lions. Spotted hyaenas pose less of a threat to cheetahs and are less predictable than lions, mostly because spotted hyaenas are extremely flexible in their prey preference, foraging strategies and habitat selection (Kruuk 1972; Hayward 2006). Our results are thus consistent with past studies, which showed that cheetahs exhibited a less marked response to spotted hyaenas than to lions (Laurenson 1995; Durant 1998). It is, however, important to note that quantifying spotted hyaena risk was difficult due to their social system and structure. Spotted hyaenas live in large, hierarchical, fission–fusion social groups but, unless on a large carcass, they generally occur alone or in smaller subgroups (Kruuk 1972, F. Broekhuis, pers. obs.). By collaring several individuals in a clan, however, we feel that we had a good representation of their general space and habitat use. Nonetheless, the relatively large number of uncollared individuals may have influenced our results on short-term cheetah avoidance behaviour of spotted hyaenas.
Overall, risk avoidance seems to be a reactive, rather than a predictive process – findings that are corroborate by other studies. For example, Creel et al. (2008) showed that elk did not increase their level of vigilance in areas where there was a higher risk of predation; vigilance levels were, however, higher when wolves were in the immediate vicinity compared to when they were absent. Lima & Bednekoff (1999) suggested that previous experiences of variation in the risk (i.e. long-term risk) could influence an animals' behaviour in terms of the temporal, short-term variation in risk. According to this risk allocation hypothesis (see also some empirical tests of this hypothesis; e.g. Sih & McCarthy 2002), as the overall time spent under risk increases, animals should increase their allocation of risky activities, such as foraging, during periods of high risk. Our findings could be interpreted in this framework; encounters of subordinate carnivores with larger carnivores are not uncommon in the study ecosystem, therefore if the subordinate species were to completely avoid the dominant species it could result in a costly loss of feeding opportunities. Our results thus highlight the importance of reactive responses in ecosystems where risks are widespread and recurrent.
In conclusion, we show that spatial resolution, temporal context and environmental complexity need to be taken into consideration to understand the mechanisms by which competing carnivores coexist. Whilst our results suggest that short-term space and habitat use is a hierarchical process first driven by resource acquisition and thereafter fine-tuned by predator avoidance (also see Cozzi et al. 2012), we encourage a more dynamic approach to investigate interactions between species.