Ecological niches are partitioned both in space and time [54, 55], and sympatric guild members have been documented to utilize spatiotemporal separation to facilitate co-existence in the same space [2, 56–61]. Within Africa’s large carnivore guild, carnivores mitigate the risk of dangerous interactions with dominant predators through spatial or temporal avoidance [10, 13, 62–64]. Our results demonstrate that lions and spotted hyenas behaviourally mediate the potential for interference competition by adjusting their space-use and activity patterns, and movement behaviours in different ways that have implications for co-existence.
Our findings indicate that lions and spotted hyenas utilize either minimal overlaps among core areas, or a large lag time of 12–24 and > 24 hr within shared space-use, as a spatiotemporal strategy to allow the two species to co-exist within the same areas without encountering one another. However, spatially fixed resources such as permanent water points or large carcasses that cannot be carried away by the predator (e.g. elephants Loxodonta africana and giraffes Giraffa camelopardalis), requires that carnivores use a different mechanism to avoid directly encountering one another at these locations. Similar to Atwood et al. [65] who recorded dominant carnivore species at nearly all of the artificial water points, lions and spotted hyenas were observed at all of the permanent water points in Etosha, providing limited opportunity for spatial resource partitioning to occur. Thus, the degree of partitioning may be associated with the differences in the densities of spatially fixed resources. Edwards et al. [63] found higher levels of temporal partitioning between free-ranging carnivores, including brown hyenas (Hyaena brunnea) and leopards (Panthera pardus) on farms with lower densities of water points.
Notwithstanding the spatiotemporal partitioning strategies observed in this study, lions and spotted hyenas persisted in tracking one another, and sometimes for extended periods. Although the type of interaction (whether remaining closer together or further apart than random) differed among pairs, the results of this study provides empirical evidence for the presence and occurrence of important interactions among lions and spotted hyenas. Other studies have documented competitive interactions between lions and spotted hyenas [6, 22, 66–68], including induced changes in one species’ behaviour according to the density and distribution of the other [20, 69–72]; however, data, such as we present, on direct interactions between lions and hyenas are rare. In a review of lion-hyena interactions, Périquet et al. [33] identified costs and benefits to both species through exploitation and interference competition, scavenging opportunities, and differences in prey selection, while acknowledging a lack of studies using telemetry data on both species simultaneously to examine spatiotemporal avoidance. A recent study in the Serengeti which deployed tracking collars simultaneously on both lions and spotted hyenas, found lions to be strongly positively associated with areas of high hyena utilization [35]. To our knowledge, our study is the first of its kind to use fine scale GPS relocation data on the two species simultaneously to allow for an analysis of the direct effects of individuals from the two species on one another.
In addition to interspecific interactions, our results indicated a prevalence of intraspecific interactions among lions. Lion prides in both Etosha and Chobe exhibited a fission-fusion social system in which different lion groups would frequently join together for short periods of time (i.e., a few hours or days) before disbanding again into their respective smaller groups [73, 74]. Although Etosha lion pairs were at closer distances more frequently than Chobe lions [75], some of our collared lions demonstrated concurrent movements in the same direction for extended periods, which corresponds with Benhamou et al. [76] who found a high degree of joint movement between lion dyads. Lions derive benefits from associating with conspecifics to attain access to high quality habitats and for territorial defense [77, 78], cooperative group hunting [79], and to defend kills against kleptoparasitism from spotted hyenas [66]. Our analysis revealed coordinated movements between conspecific pairs, and, while both individuals of the pair tended to move towards each other, we were able to determine which individual of the pair was tracking the other. This may prove advantageous in studies where social dynamics among members of the group are important to discern in determining hierarchical ranks, or in competitive systems in which we need to determine whether certain species are dependent on other species (i.e., tracking them) in search of resources. In addition to knowing who was tracking whom, our analysis was also able to illustrate the movement behaviours synonymous with mating between lion pairs, which may provide researchers with a means of confirming the occurrence of mating bouts among species of economic or conservation interest.
In contrast, collared hyenas in Chobe were observed to exhibit tolerant behaviours towards one another when they came together, more so than was seen with the collared hyenas in Etosha [75]. Hyenas from different clans in Chobe were sometimes observed to share large carcasses, at times feeding together or within minutes of each other. Etosha clans occupied nearly exclusive territories that fluctuated seasonally with the migratory movements of prey species, and encounters among members of neighbouring clans were rare. These findings coincide with previous studies in Etosha [80, 81], and are similar to hyena clan territories in the Serengeti, which remain largely exclusive with frequent foraging trips outside territories to feed on migratory herbivores [82]. On the rare occasions during our study when two individuals of different clans encountered one another, we observed a sudden halt in movement, increased vigilance and acute sniffing of the air in the direction of the other. Additionally, either one or both individuals were then seen to actively change direction to avoid each other, or retreat in the direction they had just come. During night follows in Chobe, hyenas were sometimes observed to be startled by the unexpected appearance of a conspecific (noted by the sudden jerk backwards and the rapidly departing speed of both individuals in opposite directions). It is potentially likely that hyenas exhibiting similar foraging strategies may unknowingly come close together in dense, riparian habitats, which would account for the retreating behaviours between hyenas that we observed in Chobe, unlike Etosha which lacks extensive dense riparian habitat.
The increased proportion of overlaps among home ranges observed in Chobe hyenas coincides with the “uninterrupted mosaic” of hyena territories from the Maasai Mara in Kenya [41], and in the Savuti region of the Chobe National Park [83]. Hyenas were found to scavenge more food from lions, and had higher food intake in areas of low lion densities relative to areas of higher lion densities [69], and adjusted their grouping patterns in response to feeding competition [43]. In contrast to a previous study in Etosha which never saw hyenas steal food from lions [68], the hyenas in this study were observed to successfully appropriate food from female lions in both ecosystems. Thus, hyenas presumably derive benefits from conspecifics to both appropriate resources and for protection from lions.
Coexistence among species is possible when a trade-off occurs between exploitation and interference [84]. Carnivore species that employ costly interference mechanisms (i.e. territoriality or resource guarding) are able to coexist with competitors provided that they also engage in interference mechanisms that confer a benefit to themselves (i.e., predation or kleptoparastism) [84]. Our analysis of interspecific pair movements demonstrates that a majority of hyenas exhibit retreat behaviours away from lions, while a third of lions exhibited approach behaviours towards hyenas. This is in line with Vanak et al. [13], who demonstrated that lions consistently move towards other carnivore species that turn away from the lions, although their study lacked data on spotted hyenas. Similarly, cheetahs (Acinonyx jubatus) have been observed to avoid immediate risk by positioning themselves at further distances from lions and hyenas than lions and hyenas do towards cheetahs [9], despite this behaviour not being emulated by the hyenas in response to the lions in that study. Furthermore, lions and hyenas were found to actively track each other [28], and hyenas appeared to lose more of their kills to lions, although not in terms of biomass [33]. As lions are significantly larger and stronger than hyenas, and the success of acquiring food from hyenas is largely dependent on the ratio of lions to hyenas [66, 67], it follows that lions would likely approach hyenas at the prospect of encountering a feeding opportunity.
In our data, we observed that the retreat behaviour of hyenas in the presence of lions persisted even at large distances of 1–10 km. This suggests that the strength of pairwise interactions is not associated with the distance between the paired individuals. Kittle et al. [35] suggested that the observed positive association between lions and spotted hyenas in his study resulted from one species tracking the other. Our results support this hypothesis, with long periods of interaction occurring between the two species (upwards of 300 consecutive minutes). Despite considerable variation among individual animals, more than half of the hyena individuals consistently show retreat behaviours away from lions. Similarly, cheetahs were observed to exhibit localized reactive avoidance to lions in the Serengeti [28]. However, lions rarely retreated and, instead, demonstrated mainly movements towards hyenas, as hyenas simultaneously moved away.
Alternatively, if both species interfere less with each other than they do among themselves with regard to the acquisition of resources, then the higher intensity of intraspecific competition relative to interspecific competition enables species coexistence [85, 86]. We also applied our analyses to intraspecific interactions between conspecific pairs. Our results indicated that both species differed in the utilization of approach and retreat movements towards conspecifics, with lions utilizing approach movements in nearly three quarters of cases, and hyenas retreating in more than half of the cases. However, lions were found to spend considerably more time together than hyenas did. Lions have been documented in other studies to have fission-fusion societies in which pride members form subgroups of various sizes [73]. Larger prides were found to have a competitive advantage in intergroup competition for territory [87], and better able to defend against kleptoparasitism from other predators [66]. Prides with more adult females were more likely to gain access to higher quality habitats and had increased reproductive success [78], and were able to better defend cubs against predation and infanticidal males [88]. Similarly, intraspecific interactions in a reintroduced population of lions resulted in shifts in the habitat selection among lion groups, relegating subordinate members to suboptimal habitats [77]. Thus, for the lions in our study, it is likely that the direct effect of intraspecific interactions exerted a stronger influence on lion movement behaviour than the indirect effect of interspecific interactions.
The opposite, however, is true for spotted hyenas. Our findings effectively demonstrated that, despite variation among individuals, lions actively tracked spotted hyenas across much of their shared ranges, while hyenas utilized local reactive avoidance behaviours in response to being in close proximity to lions. The active behavioural avoidance of lions by spotted hyenas demonstrated in this study is similar to the behaviours exhibited by cheetahs and wild dogs (Lycaon pictus) from other studies which have actively avoided lions [9, 13, 28, 89]. In studies that examined the behavioural response of hyenas to lion calls, hyenas were found to vary their level of vigilance and responses to lion calls based on individual characteristics of risk-taking temperaments [70, 90]. In the Hwange National Park, spotted hyenas selected den sites and altered their patterns of den attendance, and shifted their foraging strategy from active predation to scavenging in response to the potential of competitive interactions with lions [71, 72]. Therefore, and as observed in this study, spotted hyenas have the capacity to behaviourally mediate their responses to a dynamic environment, including whether they choose to track, or to retreat from lions.
Measures of dynamic interactions have been proposed to allow researchers to quantify the type of interactions between dyads based on movement data (see [91, 92] for a complete review). The majority of these approaches focuses on proximity which reflects the proportion of time the two individuals spent together [76, 93–95], and is generally given as a range of 0 to 1 [93, 96–99], or reflects the movement coordination within a range of -1 to 1 [95, 100, 101]. Some of these metrics are either difficult to interpret [95, 100], require a reference area [96, 98], or depend on a parameter with its underlying assumptions [93, 95, 97, 99, 100]. Benhamou et al. [76] uses successive distances between lion individuals while moving to determine joint movements of a dyad. To our knowledge, previous measures of dynamic interaction do not illustrate following/leadership behaviour, or whether individuals exhibit approach/retreat behaviours. Here, we have used a reliable inferential framework for analyzing the movement interactions of paired individuals, to understand the dynamics of asymmetrical movement interactions.
The relative-motion method we used allows us to analyze approach and retreat behaviours as a means of identifying the type of interaction occurring between individuals. The application of this method also allows us to ascertain specific nuances of the animal’s behaviour in relation to the other, so that we could test hypotheses related to how movement interactions are dictated by species that compete for the same resources, and how they are influenced by sex and social bonds within conspecifics. In addition, if analyses are performed on relatively high frequency relocation data (e.g., 5 min sampling intervals) then movement interactions are able to clearly reveal approach and avoidance behaviours when competing individuals encounter each other as they move across shared space-use areas. Animals that segregate their shared space use, or visit the same areas at different times, never meet. Our findings indicate that this is not the case for lions and spotted hyenas, which not only have shared space-use areas, but also often encounter one another within these jointly used areas. Consequently, knowledge of the nuances with which individuals utilize approach or retreat behaviours is essential for understanding the dynamic interactions between pairs.
Furthermore, with respect to large-scale spatiotemporal partitioning exhibited by sympatric lions and spotted hyenas occupying the same area at different times, we conclude that fine scale temporal partitioning of activity periods, and reactive local avoidance employed by hyenas, acts as the main mechanisms for facilitating the co-existence of the two species. Specifically, spotted hyenas minimize the potential for interference competition by behaviourally adjusting their movements to effectively avoid encountering lions. Understanding the space-use patterns and movement characteristics of sympatric predators on a fine-scale provides insight into the dynamic interactions between co-existing species [76, 91, 92, 102–105]. Such dynamic interactions between individuals can reveal how behaviour choices are made by predators and scavengers of a guild, and has profound implications for the management strategies for both species [32, 86, 106]. For instance, conservation managers may consider incorporating landscape features at artificial water sources to provide competing species with opportunities for spatial partitioning, or to supplement alternative water sources in areas with low densities of water points where species demonstrate high levels of temporal partitioning behaviours. In light of a changing global climate and increasing land-use pressures, factors influencing the spatial and temporal constraints imposed by predator movements can inform future area and configuration requirements of co-existing large predators [107–111], which ultimately may prove vital towards the conservation of multi-trophic communities and the maintenance of ecosystem function.