Inbreeding depression increases susceptibility to bovine tuberculosis in lions: an experimental test using an inbred-outbred contrast through translocation

Disease can dramatically influence the dynamics of endangered wildlife populations, especially when they are small and isolated, with increased risk of inbreeding. In Hluhluwe-iMfolozi Park (HiP), a small, enclosed reserve in South Africa, a large lion (Panthera leo) population arose from a small founder group in the 1960s and started showing conspicuous signs of inbreeding. To restore the health status of the HiP lion population, outbred lions were translocated into the existing population. In this study, we determined the susceptibility to bovine tuberculosis (bTB), and the prevalence of antibody to feline viruses of native lions, and compared the findings with those from translocated outbred lions and their offspring. Antibodies to feline herpesvirus, feline calicivirus, feline parvovirus, and feline coronavirus were present in the lion population, but there was no significant difference in antibody prevalence between native and translocated lions and their offspring, and these feline viruses did not appear to have an effect on the clinical health of HiP lions. However, feline immunodeficiency virus (FIV), which was previously absent from HiP, appears to have been introduced into the lion population through translocation. Within 7 yr, the prevalence of antibody to FIV increased up to 42%. Bovine tuberculosis posed a major threat to the inbred native lion population, but not to translocated lions and their offspring. More than 30% of the native lion population died from bTB or malnutrition compared with <2% of the translocated lions and their offspring. We have demonstrated that management of population genetics through supplementation can successfully combat a disease that threatens population persistence. However, great care must be taken not to introduce new diseases into populations through translocation.     

Opportunistic feeding by lions: non-preferred prey comprise an important part of lion diets in a habitat where preferred prey are abundant

Optimal foraging theory predicts less diverse predator diets with a greater availability of preferred prey. This narrow diet niche should then be dominated by preferred prey, with implications for predator–prey dynamics and prey population ecology. We investigated lion (Panthera leo) diets in Hluhluwe–iMfolozi Park (HiP), South Africa, to assess whether lions in a site with a high density of preferred prey (prey species weighing 92–632 kg as estimated from a published meta-analysis) have a narrow diet, consisting primarily of preferred prey. HiP is a useful study site to investigate this prediction because it is a productive landscape (with a high density of prey) where lion-preferred prey constitutes up to 33% of the prey available to lions. Furthermore, to investigate whether lions in HiP exhibit sex-specific diets as documented in other southern African populations, we estimated male and female lion diets separately. We were specifically interested in testing whether traditional approaches of estimating lion diets at the population level mask sex-specific predation patterns, with possible implications for management of lions in small to medium-sized fenced reserves. Lions in HiP preferred larger prey species (63–684 kg) and had diets with a larger proportion of preferred prey than reported in an African-wide meta-analysis. However, despite the high density of preferred prey species, 36% of lion diets still consisted of typically non-preferred species such as nyala (Tragelaphus angasii). This finding suggests that lions in HiP maintain a degree of opportunism even when preferred prey are abundant. Therefore, abundant, non-preferred prey are likely to be an important resource for lion populations. Sex-specific differences in lion diets were evident in HiP, suggesting that estimation of lion resource use and carrying capacity should consider opportunistic hunting and sex-specific differences in lion diets.     

Threat of rapid extermination of the lion (Panthera leo leo) in Waza National Park,Northern Cameroon

Lion populations in West and Central Africa are small and fragmented. In areas where park management is weak, threats will likely facilitate the extinction of the lion. Wildlife management requires knowledge of the population estimate. The population of lions in Waza National Park (Waza NP) was assessed by individual identification of members in the population. The population was assessed to comprise of 14–21 adult individual lions. The age structure was skewed towards adults; cubs comprised 22% of all lions identified while the sex ratio was 1 : 3. Two out of four collared lions were lost to illegal, retaliatory killings within 1 year; and probably two more males and one more female were also killed during this period. The lion population appears to have declined during the last 5 years with six lions dying per year, which is at a much higher rate than observed in the previous decades. Human‐livestock pressure has increased tremendously in this period, resulting to frequent human‐lion conflicts. To ensure the survival of the lion in Waza NP and in the entire region, management needs to intensify efforts to mitigate the pressure from humans and their livestock.     

Social factors influencing reproduction in wild lions

The paper summarizes seven years of records of the reproductive history of two wild prides of lions ( Panthera leo L.) in the Serengeti National Park, Tanzania. These records are analyzed to demonstrate ways in which lion reproduction is influenced by their social group and by changes in that group.
Females gave birth at any time of year; they did so sooner if their previous litter died. Females synchronized births with other pride members. Takeover of the pride by new males resulted in a drop in the birth rate. Most cubs died, before two years old. Birth synchrony resulted in better cub survival. The arrival of new males resulted in an increase in cub mortality. Females came into oestrus synchronously with other pride members. Males had a much longer effective reproductive life if they had male companions.
The proximate causes of these features of lion reproduction are considered, and the evolution of aspects of the organization of reproduction in lions is discussed.     

Home Range Utilisation and Territorial Behaviour of Lions (Panthera leo) on Karongwe Game Reserve,South Africa

Interventionist conservation management of territorial large carnivores has increased in recent years, especially in South Africa. Understanding of spatial ecology is an important component of predator conservation and management. Spatial patterns are influenced by many, often interacting, factors making elucidation of key drivers difficult. We had the opportunity to study a simplified system, a single pride of lions (Panthera leo) after reintroduction onto the 85 km² Karongwe Game Reserve, from 1999–2005, using radio-telemetry. In 2002 one male was removed from the paired coalition which had been present for the first three years. A second pride and male were in a fenced reserve adjacent of them to the east. This made it possible to separate social and resource factors in both a coalition and single male scenario, and the driving factors these seem to have on spatial ecology. Male ranging behaviour was not affected by coalition size, being driven more by resource rather than social factors. The females responded to the lions on the adjacent reserve by avoiding the area closest to them, therefore females may be more driven by social factors. Home range size and the resource response to water are important factors to consider when reintroducing lions to a small reserve, and it is hoped that these findings lead to other similar studies which will contribute to sound decisions regarding the management of lions on small reserves.     

Estimating past and future male loss in three Zambian lion populations

African lions (Panthera leo) are declining continent-wide, with protected area populations subject to a variety of anthropogenic effects. Zambia contains viable lion populations of considerable importance for photographic and hunting tourism, but long-term lion demographic data do not exist to guide recent management directives and population projections under different strategies. We described population size, as well as age and sex structure of lions in 3 Zambian national park populations bordering hunting areas, and found them to be male-depleted relative to other systems. We then estimated rates of adult male loss leading to male depletion in these populations and the effect of different future hunting management options on population characteristics. Predictions from matrix population models constructed within a Bayesian framework confirmed that the observed population structure was likely due to high rates of adult male loss and that instituting age limits on male harvests with quota reductions would reduce male depletion, improve tourism by providing older and more abundant males, and slightly increase population size. Reducing male mortality from wire snare poaching would also result in similar demographic impacts, and in concert with changes in hunting regulations would substantially improve the quality and quantity of adult male lions. However, model results varied depending on whether we assumed historical population stability. Predictions assuming negative historical growth rate indicated that substantially more conservative lion harvest management is warranted. We discuss the relevance of these findings for maintaining viable lion populations in and around protected areas in Zambia. © 2012 The Wildlife Society.     

A genetically distinct lion (Panthera leo) population from Ethiopia

Lion (Panthera leo) numbers are in serious decline and two of only a handful of evolutionary significant units have already become extinct in the wild. However, there is continued debate about the genetic distinctiveness of different lion populations, a discussion delaying the initiation of conservation actions for endangered populations. Some lions from Ethiopia are phenotypically distinct from other extant lions in that the males possess an extensive dark mane. In this study, we investigated the microsatellite variation over ten loci in 15 lions from Addis Ababa Zoo in Ethiopia. A comparison with six wild lion populations identifies the Addis Ababa lions as being not only phenotypically but also genetically distinct from other lions. In addition, a comparison of the mitochondrial cytochrome b (CytB) gene sequence of these lions to sequences of wild lions of different origins supports the notion of their genetic uniqueness. Our examination of the genetic diversity of this captive lion population shows little effect of inbreeding. Immediate conservation actions, including a captive breeding programme designed to conserve genetic diversity and maintain the lineage, are urgently needed to preserve this unique lion population.     

Hookworm infection,anaemia and genetic variability of the New Zealand sea lion

Hookworms are intestinal blood-feeding nematodes that parasitize and cause high levels of mortality in a wide range of mammals, including otariid pinnipeds. Recently, an empirical study showed that inbreeding (assessed by individual measures of multi-locus heterozygosity) is associated with hookworm-related mortality of California sea lions. If inbreeding increases susceptibility to hookworms, effects would expectedly be stronger in small, fragmented populations. We tested this assumption in the New Zealand sea lion, a threatened otariid that has low levels of genetic variability and high hookworm infection rates. Using a panel of 22 microsatellites, we found that average allelic diversity (5.9) and mean heterozygosity (0.72) were higher than expected for a small population with restricted breeding, and we found no evidence of an association between genetic variability and hookworm resistance. However, similar to what was observed for the California sea lion, homozygosity at a single locus explained the occurrence of anaemia and thrombocytopenia in hookworm-infected pups (generalized linear model, F = 11.81, p < 0.001) and the effect was apparently driven by a particular allele (odds ratio = 34.95%; CI: 7.12–162.41; p < 0.00001). Our study offers further evidence that these haematophagus parasites exert selective pressure on otariid blood-clotting processes.     

A molecular analysis of African lion (Panthera leo) mating structure and extra‐group paternity in Etosha National Park

The recent incorporation of molecular methods into analyses of social and mating systems has provided evidence that mating patterns often differ from those predicted by group social organization. Based on field studies and paternity analyses at a limited number of sites, African lions are predicted to exhibit a strict within‐pride mating system. Extra‐group paternity has not been previously reported in African lions; however, observations of extra‐group associations among lions inhabiting Etosha National Park in Namibia suggest deviation from the predicted within‐pride mating pattern. We analysed variation in 14 microsatellite loci in a population of 164 African lions in Etosha National Park. Genetic analysis was coupled with demographic and observational data to examine pride structure, relatedness and extra‐group paternity (EGP). EGP was found to occur in 57% of prides where paternity was analysed (n = 7), and the overall rate of EGP in this population was 41% (n = 34). Group sex ratio had a significant effect on the occurrence of EGP (P < 0.05), indicating that variation in pride‐level social structure may explain intergroup variation in EGP. Prides with a lower male‐to‐female ratio were significantly more likely to experience EGP in this population. The results of this study challenge the current models of African lion mating systems and provide evidence that social structure may not reflect breeding structure in some social mammals.     

Top-down population regulation of a top predator: lions in the Ngorongoro Crater

Efforts to determine whether bottom-up or top-down processes regulate populations have been hampered by difficulties in accurately estimating the population's carrying capacity and in directly measuring food intake rate, the impacts of interspecific competition and exposure to natural enemies. We report on 40 years of data on the lion population in Ngorongoro Crater, Tanzania, which showed strong evidence of density-dependent regulation at 100-120 individuals but has remained below 60 individuals for the past decade despite consistently high prey abundance. The lions enjoy a higher per capita food-intake rate and higher cub recruitment at low population density, and interspecific competition has not increased in recent years. These animals have suffered from a number of severe disease outbreaks over the past 40 years, but, whereas the population recovered exponentially from a severe epizootic in 1963, three outbreaks between 1994 and 2001 have occurred in such rapid succession that the population has been unable to return to the carrying capacity. The Crater population may have become unusually vulnerable to infectious disease in recent years owing to its close proximity to a growing human population and a history of close inbreeding. The Crater lions may therefore provide important insights into the future of many endangered populations.     

Population size of lions in Yankari Game Reserve as revealed by faecal DNA sampling

Studies have shown that lion (Panthera leo) populations in West Africa are small, isolated and fragmented. In Nigeria, lions have disappeared from unprotected areas and are nowadays found only in parks and reserves where these populations may still decline. It is therefore urgent to obtain reliable estimates of population sizes at different localities. Direct observational surveys may either fail to count all individuals or count some individuals repeatedly and are therefore associated with unknown levels of estimation errors. More accurate estimates can be obtained if direct counting is combined with DNA‐based individual identification. As lions are difficult to identify individually, presented here is a method that can be a valuable addition to the existing census methods.     

The size of savannah Africa: a lion’s (Panthera leo) view

We define African savannahs as being those areas that receive between 300 and 1,500 mm of rain annually. This broad definition encompasses a variety of habitats. Thus defined, savannahs comprise 13.5 million km² and encompass most of the present range of the African lion (Panthera leo). Dense human populations and extensive conversion of land to human use preclude use by lions. Using high-resolution satellite imagery and human population density data we define lion areas, places that likely have resident lion populations. In 1960, 11.9 million km² of these savannahs had fewer than 25 people per km². The comparable area shrank to 9.7 million km² by 2000. Areas of savannah Africa with few people have shrunk considerably in the last 50 years and human population projections suggest they will likely shrink significantly in the next 40. The current extent of free-ranging lion populations is 3.4 million km² or about 25 % of savannah area. Habitats across this area are fragmented; all available data indicate that between 32,000 and 35,000 free-ranging lions live in 67 lion areas. Although these numbers are similar to previous estimates, they are geographically more comprehensive. There is abundant evidence of widespread declines and local extinctions. Under the criteria we outline, ten lion areas qualify as lion strongholds: four in East Africa and six in Southern Africa. Approximately 24,000 lions are in strongholds, with an additional 4,000 in potential ones. However, over 6,000 lions are in populations of doubtful long-term viability. Lion populations in West and Central Africa are acutely threatened with many recent, local extinctions even in nominally protected areas.     

Individual Identification and Genetic Variation of Lions (Panthera leo) from Two Protected Areas in Nigeria

This survey was conducted in two protected areas in Nigeria to genetically identify individual lions and to determine the genetic variation within and between the populations. We used faecal sample DNA, a non-invasive alternative to the risky and laborious task of taking samples directly from the animals, often preceded by catching and immobilization. Data collection in Yankari Game Reserve (YGR) spanned through a period of five years (2008 –2012), whereas data in Kainji Lake National Park (KLNP) was gathered for a period of three years (2009, 2010 and 2012). We identified a minimum of eight individuals (2 males, 3 females, 3 unknown) from YGR and a minimum of ten individuals (7 males, 3 females) from KLNP. The two populations were found to be genetically distinct as shown by the relatively high fixation index (F_ST  = 0.17) with each population exhibiting signs of inbreeding (YGR F_IS  = 0.49, KLNP F_IS  = 0.38). The genetic differentiation between the Yankari and Kainji lions is assumed to result from large spatial geographic distance and physical barriers reducing gene flow between these two remaining wild lion populations in Nigeria. To mitigate the probable inbreeding depression in the lion populations within Nigeria it might be important to transfer lions between parks or reserves or to reintroduce lions from the zoos back to the wild.     

The evolutionary dynamics of the lion Panthera leo revealed by host and viral population genomics

The lion Panthera leo is one of the world's most charismatic carnivores and is one of Africa's key predators. Here, we used a large dataset from 357 lions comprehending 1.13 megabases of sequence data and genotypes from 22 microsatellite loci to characterize its recent evolutionary history. Patterns of molecular genetic variation in multiple maternal (mtDNA), paternal (Y-chromosome), and biparental nuclear (nDNA) genetic markers were compared with patterns of sequence and subtype variation of the lion feline immunodeficiency virus (FIV(Ple)), a lentivirus analogous to human immunodeficiency virus (HIV). In spite of the ability of lions to disperse long distances, patterns of lion genetic diversity suggest substantial population subdivision (mtDNA Phi(ST) = 0.92; nDNA F(ST) = 0.18), and reduced gene flow, which, along with large differences in sero-prevalence of six distinct FIV(Ple) subtypes among lion populations, refute the hypothesis that African lions consist of a single panmictic population. Our results suggest that extant lion populations derive from several Pleistocene refugia in East and Southern Africa ( approximately 324,000-169,000 years ago), which expanded during the Late Pleistocene ( approximately 100,000 years ago) into Central and North Africa and into Asia. During the Pleistocene/Holocene transition ( approximately 14,000-7,000 years), another expansion occurred from southern refugia northwards towards East Africa, causing population interbreeding. In particular, lion and FIV(Ple) variation affirms that the large, well-studied lion population occupying the greater Serengeti Ecosystem is derived from three distinct populations that admixed recently.     

Infanticide by Male Lions Hypothesis: A Fallacy Influencing Research into Human Behavior

Recently, familial abuse and killing of children have been correlated with infanticidal behavior by nonhuman male animals which is postulated to be genetic. However, infanticide by males as an evolutionary mechanism is unlikely to occur in primates, and is equally unlikely in lions. To investigate the sexual selection hypothesis of infanticide for lions, four questions should be considered: (1) because they all mate freely with lionesses, are male pride lions closely related? (often they are not), (2) do males kill the young cubs when they join a pride? (few such cases have been observed), (3) do the females then mate with the new males to produce offspring? (yes), and (4) do the males remain with the pride for over two years to protect this new generation? (often not). Field data indicate that in NO instance do we know that male lions killed cubs in a new pride, mated with their mother, and then remained with the pride to protect their own young. Rather, female lions may kill more cubs than males and certainly cause many more cub deaths by allowing them to starve, [ infanticide by male lions, infanticide hypothesis, faulty science]     

Phylogeography of lions (Panthera leo ssp.) reveals three distinct taxa and a late Pleistocene reduction in genetic diversity

Lions were the most widespread carnivores in the late Pleistocene, ranging from southern Africa to the southern USA, but little is known about the evolutionary relationships among these Pleistocene populations or the dynamics that led to their extinction. Using ancient DNA techniques, we obtained mitochondrial sequences from 52 individuals sampled across the present and former range of lions. Phylogenetic analysis revealed three distinct clusters: (i) modern lions, Panthera leo ; (ii) extinct Pleistocene cave lions, which formed a homogeneous population extending from Europe across Beringia (Siberia, Alaska and western Canada); and (iii) extinct American lions, which formed a separate population south of the Pleistocene ice sheets. The American lion appears to have become genetically isolated around 340 000 years ago, despite the apparent lack of significant barriers to gene flow with Beringian populations through much of the late Pleistocene. We found potential evidence of a severe population bottleneck in the cave lion during the previous interstadial, sometime after 48 000 years, adding to evidence from bison, mammoths, horses and brown bears that megafaunal populations underwent major genetic alterations throughout the last interstadial, potentially presaging the processes involved in the subsequent end-Pleistocene mass extinctions.     

Habitat selection and feeding ecology of the cheetah (Acinonyx jubatus) in thicket vegetation: is the cheetah a savanna specialist?

Habitat selection and feeding ecology of a reintroduced population of cheetahs Acinonyx jubatus were studied in a 16 000 ha game reserve in the Eastern Cape Province (South Africa). Seventy per cent of the reserve is characterized by very dense thicket vegetation (valley bushveld) and the remainder is open and savanna-like. The results illustrated a strong effect of sex and group size on the behaviour of cheetahs. The coalition (three adult males) killed significantly larger animals (55% of kills weighed more than 65 kg) than single female cheetahs (less than 2% of kills weighed more than 65 kg). Female cheetahs showed temporal and spatial avoidance of lions by hunting at dawn and dusk and positioning their home ranges [95% utilization distribution (UDs)] significantly farther from the pride of lions than did the coalition. The coalition hunted earlier and later than female cheetahs, and 46% of their kills were made in darkness. In addition, their home range overlapped that of the lions and they showed neither temporal nor spatial avoidance of the lions. The rates of kleptoparasitism were lower and the kill retention times were longer than those reported elsewhere in Africa, and it is suggested that this is a consequence of the cover provided by the thicket vegetation and prey size. The home ranges (95% UDs) of female cheetahs incorporated more thicket vegetation than that of the coalition, indicating that the coalition is less susceptible to predation than single females. These data suggest that cheetahs possess greater behavioural flexibility than previously reported, that they can hunt successfully in thicket vegetation, sometimes in darkness, that they are not restricted to killing small to medium-sized prey, and that they may not be savanna specialists.     

On the distinctiveness of the Cape lion (Panthera leo melanochaita Smith, 1842), and a possible new specimen from the Zoological Museum, Copenhagen

The Cape lion was a population of lions that probably inhabited the western part of the Cape Province of South Africa until their extermination by man in the mid-19th century. Only a few skeletal remains are known, making every specimen valuable. In this paper, I report on a possible new male specimen CN1570 from the Zoological Museum in Copenhagen. A multivariate discriminant analysis on 27 craniodental variables provided clear separation between four of the five lion subspecies (Panthera leo krugeri, nubica, persica, senegalensis) that were included, whereas P. l. bleyenberghi showed some overlap with P. l. senegalensis and P. l. krugeri. The only two undisputed Cape lion males grouped separately from all other lions. CN1570 also grouped separately from other lions, and towards the two Cape lions. The external morphology of the Cape lion is often cited as having been different from other sub-Saharan lions, but phenotypic plasticity argues for caution in placing emphasis on mane morphology as a distinguishing character among lion subspecies. Skull morphology, however, appears to clearly distinguish male Cape lions from other African lions.     

Evidence for African origins of founders of the asiatic lion species survival plan

The Asiatic lion (Panthera leo persica) exists in the wild as a single relict population of approximately 250 individuals in the protected Gir Forest Sanctuary in western India. In 1981, a species survival plan (SSP) for the Asiatic lion was established by the American Association of Zoological Parks and Aquariums to manage the 200 + descendants of Asiatic lions in captivity in western zoological facilities. This captive population was derived from seven founders. In order to compare the genetic structure of the Gir Forest population with that of the captive SSP population, a genetic survey of 46 electrophoretic allozyme systems resolved from extracts of lion blood was undertaken by using 29 SSP Asiatic lions and 28 wild-caught or captive-bred lions maintained at the Sakkarbaug Zoo in India but originally derived from the Gir Forest. The Gir lion population was found to be genetically monomorphic at each of 46 allozyme loci. This was in contrast to several African lion (Panthera leo leo) populations, which show moderate levels of allozyme variation at the same loci. The SSP lion population was polymorphic at three allozyme loci (IDHI, TF, and PTI) for alleles that were previously found only in African lion populations. Pedigree analysis of the genetic transmission of these three biochemical loci demonstrated that two of the five primary founder animals of the SSP Asiatic lion population (a breeding pair originally imported from the Trivandrum Zoo in southern India) were descendants of the African subspecies. Three other founder animals were pure Asian. A retrospective SSP pedigree analysis of two morphologic characters (prominent abdominal fold and pairing of infraorbital foramen) that are partially diagnostic for persica vs leo was consistent with this conclusion as well. The implications for the management of small captive populations of threatened species and of the Asiatic lion SSP population are discussed.     

Large mainland populations of South Island robins retain greater genetic diversity than offshore island refuges

For conservation purposes islands are considered safe refuges for many species, particularly in regions where introduced predators form a major threat to the native fauna, but island populations are also known to possess low levels of genetic diversity. The New Zealand archipelago provides an ideal system to compare genetic diversity of large mainland populations where introduced predators are common, to that of smaller offshore islands, which serve as predator-free refuges. We assessed microsatellite variation in South Island robins (Petroica australis australis), and compared large mainland, small mainland, natural island and translocated island populations. Large mainland populations exhibited more polymorphic loci and higher number of alleles than small mainland and natural island populations. Genetic variation did not differ between natural and translocated island populations, even though one of the translocated populations was established with five individuals. Hatching failure was recorded in a subset of the populations and found to be significantly higher in translocated populations than in a large mainland population. Significant population differentiation was largely based on heterogeneity in allele frequencies (including fixation of alleles), as few unique alleles were observed. This study shows that large mainland populations retain higher levels of genetic diversity than natural and translocated island populations. It highlights the importance of protecting these mainland populations and using them as a source for new translocations. In the future, these populations may become extremely valuable for species conservation if existing island populations become adversely affected by low levels of genetic variation and do not persist.