Troubled spots: Human impacts constrain the density of an apex predator inside protected areas.

Effective conservation requires understanding the processes that determine population outcomes. Too often, we assume that protected areas conserve wild populations despite evidence that they frequently fail to do so. Without large-scale studies, however, we cannot determine what relationships are the product of localized conditions versus general patterns that inform conservation more broadly. Leopards' (Panthera pardus) basic ecology is well studied but little research has investigated anthropogenic effects on leopard density at broad scales. We investigated the drivers of leopard density among 27 diverse protected areas in northeastern South Africa to understand what conditions facilitate abundant populations. We formulated 10 working hypotheses that considered the relative influence of bottom-up biological factors and top-down anthropogenic factors on leopard density. Using camera-trap survey data, we fit a multi-session spatial capture-recapture model with inhomogenous density for each hypothesis and evaluated support using an information theoretic approach. The four supported hypotheses indicated that leopard density is primarily limited by human impacts, but that habitat suitability and management conditions also matter. The proportion of camera stations that recorded domestic animals, a proxy for the extent of human impacts and protected area effectiveness, was the only predictor variable present in all four supported models. Protected areas are the cornerstone of large felid conservation, but only when the human-wildlife interface is well managed and protected areas shelter wildlife populations from anthropogenic impacts. To ensure the long-term abundance of large carnivore populations, reserve managers should recognize the ineffectiveness of "paper parks" and promote contiguous networks of protected areas that offer leopards and other large mammal populations greater space and reduced human impacts.

Assumptions about fence permeability influence density estimates for brown hyaenas across South Africa.

Wildlife population density estimates provide information on the number of individuals in an area and influence conservation management decisions. Thus, accuracy is vital. A dominant feature in many landscapes globally is fencing, yet the implications of fence permeability on density estimation using spatial capture-recapture modelling are seldom considered. We used camera trap data from 15 fenced reserves across South Africa to examine the density of brown hyaenas (Parahyaena brunnea). We estimated density and modelled its relationship with a suite of covariates when fenced reserve boundaries were assumed to be permeable or impermeable to hyaena movements. The best performing models were those that included only the influence of study site on both hyaena density and detection probability, regardless of assumptions of fence permeability. When fences were considered impermeable, densities ranged from 2.55 to 15.06 animals per 100 km2, but when fences were considered permeable, density estimates were on average 9.52 times lower (from 0.17 to 1.59 animals per 100 km2). Fence permeability should therefore be an essential consideration when estimating density, especially since density results can considerably influence wildlife management decisions. In the absence of strong evidence to the contrary, future studies in fenced areas should assume some degree of permeability in order to avoid overestimating population density.

Unsustainable anthropogenic mortality disrupts natal dispersal and promotes inbreeding in leopards.

Anthropogenic mortality of wildlife is typically inferred from measures of the absolute decline in population numbers. However, increasing evidence suggests that indirect demographic effects including changes to the age, sex, and social structure of populations, as well as the behavior of survivors, can profoundly impact population health and viability. Specifically, anthropogenic mortality of wildlife (especially when unsustainable) and fragmentation of the spatial distribution of individuals (home-ranges) could disrupt natal dispersal mechanisms, with long-term consequences to genetic structure, by compromising outbreeding behavior and gene flow. We investigate this threat in African leopards (Panthera pardus pardus), a polygynous felid with male-biased natal dispersal. Using a combination of spatial (home-range) and genetic (21 polymorphic microsatellites) data from 142 adult leopards, we contrast the structure of two South African populations with markedly different histories of anthropogenically linked mortality. Home-range overlap, parentage assignment, and spatio-genetic autocorrelation together show that historical exploitation of leopards in a recovering protected area has disrupted and reduced subadult male dispersal, thereby facilitating opportunistic male natal philopatry, with sons establishing territories closer to their mothers and sisters. The resultant kin-clustering in males of this historically exploited population is comparable to that of females in a well-protected reserve and has ultimately led to localized inbreeding. Our findings demonstrate novel evidence directly linking unsustainable anthropogenic mortality to inbreeding through disrupted dispersal in a large, solitary felid and expose the genetic consequences underlying this behavioral change. We therefore emphasize the importance of managing and mitigating the effects of unsustainable exploitation on local populations and increasing habitat fragmentation between contiguous protected areas by promoting in situ recovery and providing corridors of suitable habitat that maintain genetic connectivity.

Ecological opportunity drives individual dietary specialization in leopards.

Individual specialization, when individuals exploit only a subset of resources utilized by the population, is a widespread phenomenon. It provides the basis for evolutionary diversification and can impact population and community dynamics. Both phenotypic traits and environmental conditions are predicted to influence individual specialization; however, its adaptive consequences are poorly understood, particularly among large mammalian carnivores that play an important role in shaping ecosystems. We used observations of 2,960 kills made by 49 leopards Panthera pardus in the Sabi Sand Game Reserve, South Africa, to quantify the magnitude of individual dietary specialization in a solitary large carnivore, and to examine the proximate and ultimate drivers of this behaviour. We found evidence of individual specialization in leopard diet, with respect to both the species and size of prey killed. Males tended to be more specialized than females, likely because they could access a wider range of prey due to larger body size. Similarly, individuals that encountered a greater diversity of prey tended to be more specialized. Our results confirmed that ecological opportunity was a key determinant of individual specialization; however, contrary to predictions, per capita resource availability (and by extension, intraspecific competition) did not affect the degree of specialization exhibited by individuals. Surprisingly, dietary specialization appeared to disadvantage male leopards. Specialist males overlapped with fewer resident females, had fewer cubs born on their home ranges and had fewer cubs survive to independence on their home ranges than generalist males. This may have resulted from the high degree of environmental stochasticity experienced during our study, as dietary specialization is expected to advantage individuals more during periods of resource predictability. In summary, we showed that a species usually considered to be a dietary generalist was in fact a heterogeneous collection of specialist and generalist individuals. Individual specialization is typically assumed to be maintained by disruptive and/or fluctuating selection; hence, the somewhat paradoxical coexistence of both in the same population might be explained by a dynamic evolutionary equilibrium that exists between specialists and generalists, in which each benefit under different conditions.

Lions and leopards coexist without spatial, temporal or demographic effects of interspecific competition.

Although interspecific competition plays a principal role in shaping species behaviour and demography, little is known about the population-level outcomes of competition between large carnivores, and the mechanisms that facilitate coexistence. We conducted a multilandscape analysis of two widely distributed, threatened large carnivore competitors to offer insight into coexistence strategies and assist with species-level conservation. We evaluated how interference competition affects occupancy, temporal activity and population density of a dominant competitor, the lion (Panthera leo), and its subordinate competitor, the leopard (Panthera pardus). We collected camera-trap data over 3 years in 10 study sites covering 5,070 km2 . We used multispecies occupancy modelling to assess spatial responses in varying environmental and prey conditions and competitor presence, and examined temporal overlap and the relationship between lion and leopard densities across sites and years. Results showed that both lion and leopard occupancy was independent of-rather than conditional on-their competitor's presence across all environmental covariates. Marginal occupancy probability for leopard was higher in areas with more bushy, "hideable" habitat, human (tourist) activity and topographic ruggedness, whereas lion occupancy decreased with increasing hideable habitat and increased with higher abundance of very large prey. Temporal overlap was high between carnivores, and there was no detectable relationship between species densities. Lions pose a threat to the survival of individual leopards, but they exerted no tractable influence on leopard spatial or temporal dynamics. Furthermore, lions did not appear to suppress leopard populations, suggesting that intraguild competitors can coexist in the same areas without population decline. Aligned conservation strategies that promote functioning ecosystems, rather than target individual species, are therefore advised to achieve cost- and space-effective conservation.

Flexibility in the duration of parental care: Female leopards prioritise cub survival over reproductive output.

Deciding when to terminate care of offspring is a key consideration for parents. Prolonging care may increase fitness of current offspring, but it can also reduce opportunities for future reproduction. Despite its evolutionary importance, few studies have explored the optimal duration of parental care, particularly among large carnivores. We used a 40-year dataset to assess the trade-offs associated with the length of maternal care in leopards in the Sabi Sand Game Reserve, South Africa. We compared the costs imposed by care on the survival and residual reproductive value of leopard mothers against the benefits derived from maternal care in terms of increased offspring survival, recruitment and reproduction. We also examined the demographic and ecological factors affecting the duration of care in the light of five explanatory hypotheses: litter size, sex allocation, resource limitation, timing of independence and terminal investment. Duration of care exhibited by female leopards varied markedly, from 9 to 35 months. Mothers did not appear to suffer any short- or long-term survival costs from caring for cubs, but extending care reduced the number of litters that mothers could produce during their lifetimes. Interestingly, the duration of care did not appear to affect the post-independence survival or reproductive success of offspring (although it may have indirectly affected offspring survival by influencing dispersal distance). However, results from generalised linear mixed models showed that mothers prolonged care during periods of prey scarcity, supporting the resource limitation hypothesis. Female leopards also cared for sons longer than daughters, in line with the sex-allocation hypothesis. Cub survival is an important determinant of the lifetime reproductive success in leopards. By buffering offspring against environmental perturbation without jeopardising their own survivorship, female leopards apparently "hedge their bets" with current offspring rather than gamble on future offspring which have a small probability of surviving. In many species, parents put their own needs before that of their offspring. Leopard mothers appear sensitive to their offspring's demands, and adjust levels of care accordingly.

Caching reduces kleptoparasitism in a solitary, large felid.

Food caching is a common strategy used by a diversity of animals, including carnivores, to store and/or secure food. Despite its prevalence, the drivers of caching behaviour, and its impacts on individuals, remain poorly understood, particularly for short-term food cachers. Leopards Panthera pardus exhibit a unique form of short-term food caching, regularly hoisting, storing and consuming prey in trees. We explored the factors motivating such behaviour among leopards in the Sabi Sand Game Reserve, South Africa, associated with four not mutually exclusive hypotheses: food-perishability, consumption-time, resource-pulse and kleptoparasitism-avoidance. Using data from 2032 prey items killed by 104 leopards from 2013 to 2015, we built generalized linear mixed models to examine how hoisting behaviour, feeding time and the likelihood of a kill being kleptoparasitized varied with leopard sex and age, prey size and vulnerability, vegetation, elevation, climate, and the immediate and long-term risk posed by dominant competitors. Leopards hoisted 51% of kills. They were more likely to hoist kills of an intermediate size, outside of a resource pulse and in response to the presence of some competitors. Hoisted kills were also fed on for longer than non-hoisted kills. At least 21% of kills were kleptoparasitized, mainly by spotted hyaenas Crocuta crocuta. Kills were more likely to be kleptoparasitized at lower temperatures and if prey were larger, not hoisted, and in areas where the risk of encountering hyaenas was greatest. Female leopards that suffered higher rates of kleptoparasitism exhibited lower annual reproductive success than females that lost fewer kills. Our results strongly support the kleptoparasitism-avoidance hypothesis and suggest hoisting is a key adaptation that enables leopards to coexist sympatrically with high densities of competitors. We further argue that leopards may select smaller-sized prey than predicted by optimal foraging theory, to balance trade-offs between kleptoparasitic losses and the energetic gains derived from killing larger prey. Although caching may provide the added benefits of delaying food perishability and enabling consumption over an extended period, the behaviour primarily appears to be a strategy for leopards, and possibly other short-term cachers, to reduce the risks of kleptoparasitism.

Data-poor management of African lion hunting using a relative index of abundance.

Sustainable management of terrestrial hunting requires managers to set quotas restricting offtake. This often takes place in the absence of reliable information on the population size, and as a consequence, quotas are set in an arbitrary fashion, leading to population decline and revenue loss. In this investigation, we show how an indirect measure of abundance can be used to set quotas in a sustainable manner, even in the absence of information on population size. Focusing on lion hunting in Africa, we developed a simple algorithm to convert changes in the number of safari days required to kill a lion into a quota for the following year. This was tested against a simulation model of population dynamics, accounting for uncertainties in demography, observation, and implementation. Results showed it to reliably set sustainable quotas despite these uncertainties, providing a robust foundation for the conservation of hunted species.

Creating larger and better connected protected areas enhances the persistence of big game species in the maputaland-pondoland-albany biodiversity hotspot.

The ideal conservation planning approach would enable decision-makers to use population viability analysis to assess the effects of management strategies and threats on all species at the landscape level. However, the lack of high-quality data derived from long-term studies, and uncertainty in model parameters and/or structure, often limit the use of population models to only a few species of conservation concern. We used spatially explicit metapopulation models in conjunction with multi-criteria decision analysis to assess how species-specific threats and management interventions would affect the persistence of African wild dog, black rhino, cheetah, elephant, leopard and lion, under six reserve scenarios, thereby providing the basis for deciding on a best course of conservation action in the South African province of KwaZulu-Natal, which forms the central component of the Maputaland-Pondoland-Albany biodiversity hotspot. Overall, the results suggest that current strategies of managing populations within individual, small, fenced reserves are unlikely to enhance metapopulation persistence should catastrophic events affect populations in the future. Creating larger and better-connected protected areas would ensure that threats can be better mitigated in the future for both African wild dog and leopard, which can disperse naturally, and black rhino, cheetah, elephant, and lion, which are constrained by electric fences but can be managed using translocation. The importance of both size and connectivity should inform endangered megafauna conservation and management, especially in the context of restoration efforts in increasingly human-dominated landscapes.