Spatiotemporal Genetic Diversity of Lions Reveals the Influence of Habitat Fragmentation across Africa.

Direct comparisons between historical and contemporary populations allow for detecting changes in genetic diversity through time and assessment of the impact of habitat fragmentation. Here, we determined the genetic architecture of both historical and modern lions to document changes in genetic diversity over the last century. We surveyed microsatellite and mitochondrial genome variation from 143 high-quality museum specimens of known provenance, allowing us to directly compare this information with data from several recently published nuclear and mitochondrial studies. Our results provide evidence for male-mediated gene flow and recent isolation of local subpopulations, likely due to habitat fragmentation. Nuclear markers showed a significant decrease in genetic diversity from the historical (HE = 0.833) to the modern (HE = 0.796) populations, whereas mitochondrial genetic diversity was maintained (Hd = 0.98 for both). Although the historical population appears to have been panmictic based on nDNA data, hierarchical structure analysis identified four tiers of genetic structure in modern populations and was able to detect most sampling locations. Mitogenome analyses identified four clusters: Southern, Mixed, Eastern, and Western and were consistent between modern and historically sampled haplotypes. Within the last century, habitat fragmentation caused lion subpopulations to become more geographically isolated as human expansion changed the African landscape. This resulted in an increase in fine-scale nuclear genetic structure and loss of genetic diversity as lion subpopulations became more differentiated, whereas mitochondrial structure and diversity were maintained over time.

Human procurement of meat from lion (Panthera leo) kills: Costs of disturbance and implications for carnivore conservation.

In Africa, humans and large carnivores compete over access to resources, including prey. Disturbance by humans to kills made by carnivores, often for purposes of obtaining all or portions of the carcass, constitutes a form of human-wildlife conflict. However the occurrence of this practice, known as human kleptoparasitism, and its impact on carnivores has received little scientific attention. We obtained expert opinions from African lion researchers and stakeholders via a standardized questionnaire to characterize the geographic extent and frequency of human kleptoparasitism as it occurs in modern times. Our survey found modern human kleptoparasitism on kills made by lions, and possibly other large carnivores in Africa, to be geographically more widespread than previously reported. Meat lost to humans requires carnivores to hunt and kill additional prey thereby causing stress, increasing their energetic costs and risks of natural injury, and exposing them to risk of direct injury or death from human usurpers. Because of their conspicuous behaviors and tendency towards killing large-bodied prey, lions are particularly susceptible to humans detecting their kills. While human kleptoparasitism was geographically widespread, socio-economic factors influenced the frequency of occurrence. Prey type (wild game or domestic livestock) influenced human attitudes towards meat theft; ownership allows for legal recovery of livestock carcasses, while possessing wild game meat is mostly illegal and may incur penalties. Meat theft was associated with other illegal activities (i.e., illegal mining) and most prevalent among people of low income, including underpaid game scouts. Despite quantifiable costs to carnivores of human disturbance to their kills, the majority of experts surveyed reported a lack of knowledge on this practice. We propose that human disturbance at kills, especially loss of prey through human kleptoparasitism, constitutes an important anthropogenic threat that may seriously impact energy budgets of individual lions and other scavengers when meat and carcasses are removed from the ecosystem, and that the costs incurred by carnivores warrants further investigation.

Naturally-occurring tooth wear, tooth fracture, and cranial injuries in large carnivores from Zambia.

Determining the incidence and causes of craniodental damage in wild carnivores is often constrained by limited access to specimens with associated ecological data, such as prey type and abundance. We assessed dental condition and cranial injuries in lion, leopard, and spotted hyena in relation to prey and predator populations in Zambia's Luangwa Valley, where large prey are more abundant and lion and leopard more numerous, and the Greater Kafue Ecosystem, where smaller prey species are more prevalent and lion and leopard less common. In Luangwa, lions had significantly higher rates of tooth fracture, and blunt trauma injuries attributable to prey-handling, compared to Kafue lions. In contrast, leopards in both regions had similar rates of tooth wear and breakage. Overall, lions showed a significantly higher tooth fracture rate than leopards on a per tooth basis. Spotted hyenas had the highest rates of tooth wear and fracture among all three carnivores, and greatly exceeded previously recorded rates based on historical samples. Despite larger numbers of lion and leopard in Luangwa, there was no difference in incidence of intraspecific injuries between regions. These results are consistent with a greater abundance of large prey species, especially buffalo, in the diets of Luangwa lions, and previous work showing a reliance on smaller prey species in Kafue throughout the large carnivore guild.

Genetic analysis of African lions (Panthera leo) in Zambia support movement across anthropogenic and geographical barriers.

The Luangwa Valley in eastern Zambia is a transverse offshoot of the Great Rift Valley system. This region appears to have an isolating effect as evidenced by suspected endemic subspecies, such as the Cookson's wildebeest and Thornicroft's giraffe. Recent mitochondrial DNA studies demonstrated that African lions in Zambia consist of two highly diverse eastern and western sub-populations. Herein, we report nuclear and mitochondrial DNA results from 409 lions that support this population substructure across Zambia but proposes only partial isolation of the Luangwa Valley with more movement between the populations than previously thought. Population assignment analysis identifies two populations with little evidence of admixture assigning lions to either the eastern or western sub-populations. A high occurrence of private alleles and clear evidence for a Wahlund effect further justify the presence of a highly structured population. But, while mitochondrial DNA analysis still shows little to no matrilineal gene flow (FST = 0.53) between sub-populations, microsatellite analysis suggests there is gene flow (FST = 0.04) with low but significant isolation-by-distance and an average of 6 migrants per generation. Evidence of isolation-by-distance is also found in factorial correspondence analysis with the Lower Zambezi National Park and eastern corridor clusters overlapping isolated clusters of the Luangwa Valley and western sub-population. From this evidence, the Luangwa Valley appears separated from the western sub-population with some dispersal through the southern regions of the eastern sub-population. Both the eastern and western sub-populations have high heterozygosity (0.68 and 0.69, respectively) and genetic diversity (0.47 and 0.50, respectively) values, indicative of genetically healthy populations.

Correction: Age Estimation of African Lions Panthera leo by Ratio of Tooth Areas.

[This corrects the article DOI: 10.1371/journal.pone.0153648.].

Age Estimation of African Lions Panthera leo by Ratio of Tooth Areas.

Improved age estimation of African lions Panthera leo is needed to address a number of pressing conservation issues. Here we present a formula for estimating lion age to within six months of known age based on measuring the extent of pulp closure from X-rays, or Ratio Of tooth AReas (ROAR). Derived from measurements taken from lions aged 3-13 years for which exact ages were known, the formula explains 92% of the total variance. The method of calculating the pulp/tooth area ratio, which has been used extensively in forensic science, is novel in the study of lion aging. As a quantifiable measure, ROAR offers improved lion age estimates for population modeling and investigations of age-related mortality, and may assist national and international wildlife authorities in judging compliance with regulatory measures involving age.

Provisioning of game meat to rural communities as a benefit of sport hunting in Zambia.

Sport hunting has reportedly multiple benefits to economies and local communities; however, few of these benefits have been quantified. As part of their lease agreements with the Zambia Wildlife Authority, sport hunting operators in Zambia are required to provide annually to local communities free of charge i.e., provision a percentage of the meat obtained through sport hunting. We characterized provisioning of game meat to rural communities by the sport hunting industry in Zambia for three game management areas (GMAs) during 2004-2011. Rural communities located within GMAs where sport hunting occurred received on average > 6,000 kgs per GMA of fresh game meat annually from hunting operators. To assess hunting industry compliance, we also compared the amount of meat expected as per the lease agreements versus observed amounts of meat provisioned from three GMAs during 2007-2009. In seven of eight annual comparisons of these GMAs, provisioning of meat exceeded what was required in the lease agreements. Provisioning occurred throughout the hunting season and peaked during the end of the dry season (September-October) coincident with when rural Zambians are most likely to encounter food shortages. We extrapolated our results across all GMAs and estimated 129,771 kgs of fresh game meat provisioned annually by the sport hunting industry to rural communities in Zambia at an approximate value for the meat alone of >US$600,000 exclusive of distribution costs. During the hunting moratorium (2013-2014), this supply of meat has halted, likely adversely affecting rural communities previously reliant on this food source. Proposed alternatives to sport hunting should consider protein provisioning in addition to other benefits (e.g., employment, community pledges, anti-poaching funds) that rural Zambian communities receive from the sport hunting industry.

Mitochondrial Haplotype Diversity in Zambian Lions: Bridging a Gap in the Biogeography of an Iconic Species.

Analysis of DNA sequence diversity at the 12S to 16S mitochondrial genes of 165 African lions (Panthera leo) from five main areas in Zambia has uncovered haplotypes which link Southern Africa with East Africa. Phylogenetic analysis suggests Zambia may serve as a bridge connecting the lion populations in southern Africa to eastern Africa, supporting earlier hypotheses that eastern-southern Africa may represent the evolutionary cradle for the species. Overall gene diversity throughout the Zambian lion population was 0.7319 +/- 0.0174 with eight haplotypes found; three haplotypes previously described and the remaining five novel. The addition of these five novel haplotypes, so far only found within Zambia, nearly doubles the number of haplotypes previously reported for any given geographic location of wild lions. However, based on an AMOVA analysis of these haplotypes, there is little to no matrilineal gene flow (Fst = 0.47) when the eastern and western regions of Zambia are considered as two regional sub-populations. Crossover haplotypes (H9, H11, and Z1) appear in both populations as rare in one but common in the other. This pattern is a possible result of the lion mating system in which predominately males disperse, as all individuals with crossover haplotypes were male. The determination and characterization of lion sub-populations, such as done in this study for Zambia, represent a higher-resolution of knowledge regarding both the genetic health and connectivity of lion populations, which can serve to inform conservation and management of this iconic species.

Autosomal and mtDNA Markers Affirm the Distinctiveness of Lions in West and Central Africa.

The evolutionary history of a species is key for understanding the taxonomy and for the design of effective management strategies for species conservation. The knowledge about the phylogenetic position of the lion (Panthera leo) in West/Central Africa is largely based on mitochondrial markers. Previous studies using mtDNA only have shown this region to hold a distinct evolutionary lineage. In addition, anthropogenic factors have led to a strong decline in West/Central African lion numbers, thus, the conservation value of these populations is particularly high. Here, we investigate whether autosomal markers are concordant with previously described phylogeographic patterns, and confirm the unique position of the West/Central African lion. Analysis of 20 microsatellites and 1,454 bp of the mitochondrial DNA in 16 lion populations representing the entire geographic range of the species found congruence in both types of markers, identifying four clusters: 1) West/Central Africa, 2) East Africa, 3) Southern Africa and 4) India. This is not in line with the current taxonomy, as defined by the IUCN, which only recognizes an African and an Asiatic subspecies. There are no indications that genetic diversity in West/Central Africa lions is lower than in either East or Southern Africa, however, given this genetic distinction and the recent declines of lion numbers in this region, we strongly recommend prioritization of conservation projects in West/Central Africa. As the current taxonomic nomenclature does not reflect the evolutionary history of the lion, we suggest that a taxonomic revision of the lion is warranted.

Sea ice occurrence predicts genetic isolation in the Arctic fox.

Unlike Oceanic islands, the islands of the Arctic Sea are not completely isolated from migration by terrestrial vertebrates. The pack ice connects many Arctic Sea islands to the mainland during winter months. The Arctic fox (Alopex lagopus), which has a circumpolar distribution, populates numerous islands in the Arctic Sea. In this study, we used genetic data from 20 different populations, spanning the entire distribution of the Arctic fox, to identify barriers to dispersal. Specifically, we considered geographical distance, occurrence of sea ice, winter temperature, ecotype, and the presence of red fox and polar bear as nonexclusive factors that influence the dispersal behaviour of individuals. Using distance-based redundancy analysis and the BIOENV procedure, we showed that occurrence of sea ice is the key predictor and explained 40-60% of the genetic distance among populations. In addition, our analysis identified the Commander and Pribilof Islands Arctic populations as genetically unique suggesting they deserve special attention from a conservation perspective.