Climate change is predicted to cause population collapse in a cooperative breeder.

It has been suggested that animals may have evolved cooperative breeding strategies in response to extreme climatic conditions. Climate change, however, may push species beyond their ability to cope with extreme climates, and reduce the group sizes in cooperatively breeding species to a point where populations are no longer viable. Predicting the impact of future climates on these species is challenging as modelling the impact of climate change on their population dynamics requires information on both group- and individual-level responses to climatic conditions. Using a single-sex individual-based model incorporating demographic responses to ambient temperature in an endangered species, the African wild dog Lycaon pictus, we show that there is a threshold temperature above which populations of the species are predicted to collapse. For simulated populations with carrying capacities equivalent to the median size of real-world populations (nine packs), extinction risk increases once temperatures exceed those predicted in the best-case climate warming scenario (Representative Concentration Pathway [RCP] 2.6). The threshold is higher (between RCP 4.5 and RCP 6.0) for larger simulated populations (30 packs), but 84% of real-world populations number <30 packs. Simulated populations collapsed because, at high ambient temperatures, juvenile survival was so low that packs were no longer recruiting enough individuals to persist, leading them to die out. This work highlights the importance of social dynamics in determining impacts of climatic variables on social species, and the critical role that recruitment can play in driving population-level impacts of climate change. Population models parameterised on long-term data are essential for predicting future population viability under climate change.

MODIFIED LIVE DISTEMPER VACCINES CARRY LOW MORTALITY RISK FOR CAPTIVE AFRICAN WILD DOGS, LYCAON PICTUS.

Recently, canine distemper virus (CDV) has been linked to population declines in the endangered African wild dog (Lycaon pictus). As CDV appears able to persist in wildlife, threats to free-ranging wild dogs cannot be eliminated by vaccinating domestic dogs. Conservation managers may therefore consider CDV vaccination of wild dogs in highly threatened populations. For use in field conservation, the ideal CDV vaccine would be safe, immunogenic, and readily available in Africa. The CDV vaccine type most commonly used for domestic dogs (modified live vaccine) is available in Africa, and apparently immunogenic in wild dogs, but has been linked to fatal vaccine-induced distemper in captive wild dogs. However, alternatives are either ineffective (inactivated vaccine) or difficult to obtain in Africa (recombinant vaccine). Data from a questionnaire survey of zoo vaccination practices were therefore combined with studbook tracing to assess the safety of modified live CDV vaccine in captive African wild dogs. Among 135 wild dog pups given modified live CDV vaccine for the first time, there was a single, unconfirmed, case of potential vaccine-induced distemper. Pups given modified live vaccine survived better than those given inactivated vaccine or no vaccine. Although studbook tracing revealed higher overall pup survival at zoos which responded to the questionnaire than at zoos which did not, tracing of all pups born during a 20-yr period that lived long enough to be vaccinated (n = 698 pups in 155 litters) revealed no mortality events consistent with vaccine-induced distemper. Modified live CDV vaccine thus appears to carry low mortality risks for African wild dog pups in captivity, and may warrant trials in free-ranging populations.

Within- and between-group dynamics in an obligate cooperative breeder.

Cooperative behaviour can have profound effects on demography. In many cooperative species, components of fitness (e.g. survival, reproductive success) are diminished in smaller social groups. These effects (termed group-level component Allee effects) may lead smaller groups to grow relatively slowly or fail to persist (termed group-level demographic Allee effects). If these group-level effects were to propagate to the population level, small populations would grow slowly or decline to extinction (termed population-level demographic Allee effects). However, empirical studies have revealed little evidence of such population-level effects. Theoretical studies suggest that dispersal behaviour could either cause or prevent the propagation of group-level Allee effects to the population level. We therefore characterized within- and between-pack dynamics in a population of African wild dogs (Lycaon pictus) to test these contrasting model predictions. Larger wild dog packs produced more pups, and their members experienced higher survival than those in smaller packs. Nevertheless, larger packs grew more slowly than smaller packs, because natal adults dispersed away from them. Most packs either died out in whole-pack death events or broke up when their founders died, irrespective of pack size. Overall, packs showed negative density dependence rather than group-level demographic Allee effects. Larger packs produced more, but not larger, dispersal groups and hence generated more, but not larger, new packs. Larger packs thus contributed more than smaller packs to the number of packs in the population, but their large size did not propagate to their daughter packs. This pattern helps to explain the absence of population-level Allee effects in this species. Dispersal behaviour, itself driven by natural selection on individual reproductive strategies, played a pivotal role in population dynamics, leading to the formation of new packs and limiting the size of established packs. Understanding dispersal processes is likely to be important to understanding the population dynamics of other cooperatively breeding species.

The global decline of cheetah Acinonyx jubatus and what it means for conservation.

Establishing and maintaining protected areas (PAs) are key tools for biodiversity conservation. However, this approach is insufficient for many species, particularly those that are wide-ranging and sparse. The cheetah Acinonyx jubatus exemplifies such a species and faces extreme challenges to its survival. Here, we show that the global population is estimated at ∼7,100 individuals and confined to 9% of its historical distributional range. However, the majority of current range (77%) occurs outside of PAs, where the species faces multiple threats. Scenario modeling shows that, where growth rates are suppressed outside PAs, extinction rates increase rapidly as the proportion of population protected declines. Sensitivity analysis shows that growth rates within PAs have to be high if they are to compensate for declines outside. Susceptibility of cheetah to rapid decline is evidenced by recent rapid contraction in range, supporting an uplisting of the International Union for the Conservation of Nature (IUCN) Red List threat assessment to endangered. Our results are applicable to other protection-reliant species, which may be subject to systematic underestimation of threat when there is insufficient information outside PAs. Ultimately, conserving many of these species necessitates a paradigm shift in conservation toward a holistic approach that incentivizes protection and promotes sustainable human-wildlife coexistence across large multiple-use landscapes.

Coping with climate change: limited behavioral responses to hot weather in a tropical carnivore.

Climate change is widely accepted to be one of the greatest threats to species globally. Identifying the species most at risk is, therefore, a conservation priority. Some species have the capacity to adapt to rising temperatures through changing their phenology, behavior, distribution, or physiology, and, therefore, may be more likely to persist under rising temperatures. Recent findings suggest that the African wild dog Lycaon pictus may be impacted by climate change, since reproductive success is consistently lower when pup-rearing coincides with periods of high ambient temperature. We used GPS collars, combined with generalized linear mixed-effects models, to assess wild dogs' potential to adapt to high ambient temperatures through flexible timing of hunting behavior. On days with higher maximum temperatures, wild dogs showed lower daytime activity and greater nocturnal activity, although nocturnal activity did not fully balance the decrease in daytime activity, particularly during the denning period. Increases in nocturnal activity were confined mainly to moonlit nights, and were seldom observed when packs were raising pups. Our findings suggest that nocturnal activity helps this cursorial hunter to cope with high daytime temperatures. However, wild dogs appear not to use this coping strategy when they are raising pups, suggesting that their resource needs may not be fulfilled during the pup-rearing period. Given that moonlight availability-which will not change as the climate changes-constrains wild dogs' nocturnal activity, the species may have insufficient behavioral plasticity to mitigate increasing diurnal temperatures. These findings raise concerns about climate change impacts on this endangered species, and highlight the need for behavior to be considered when assessing species' vulnerability to climate change.

Hot dogs: High ambient temperatures impact reproductive success in a tropical carnivore.

Climate change imposes an urgent need to recognise and conserve the species likely to be worst affected. However, while ecologists have mostly explored indirect effects of rising ambient temperatures on temperate and polar species, physiologists have predicted direct impacts on tropical species. The African wild dog (Lycaon pictus), a tropical species, exhibits few of the traits typically used to predict climate change vulnerability. Nevertheless, we predicted that wild dog populations might be sensitive to weather conditions, because the species shows strongly seasonal reproduction across most of its geographical range. We explored associations between weather conditions, reproductive costs, and reproductive success, drawing on long-term wild dog monitoring data from sites in Botswana (20°S, 24 years), Kenya (0°N, 12 years), and Zimbabwe (20°S, 6 years). High ambient temperatures were associated with reduced foraging time, especially during the energetically costly pup-rearing period. Across all three sites, packs which reared pups at high ambient temperatures produced fewer recruits than did those rearing pups in cooler weather; at the non-seasonal Kenya site such packs also had longer inter-birth intervals. Over time, rising ambient temperatures at the (longest-monitored) Botswana site coincided with falling wild dog recruitment. Our findings suggest a direct impact of high ambient temperatures on African wild dog demography, indicating that this species, which is already globally endangered, may be highly vulnerable to climate change. This vulnerability would have been missed by simplistic trait-based assessments, highlighting the limitations of such assessments. Seasonal reproduction, which is less common at low latitudes than at higher latitudes, might be a useful indicator of climate change vulnerability among tropical species.

Badger responses to small-scale culling may compromise targeted control of bovine tuberculosis.

Where wildlife disease requires management, culling is frequently considered but not always effective. In the British Isles, control of cattle tuberculosis (TB) is hindered by infection in wild badger (Meles meles) populations. Large-scale badger culling can reduce the incidence of confirmed cattle TB, but these benefits are undermined by culling-induced changes in badger behavior (termed perturbation), which can increase transmission among badgers and from badgers to cattle. Test-vaccinate/remove (TVR) is a novel approach that entails testing individual badgers for infection, vaccinating test-negative animals, and killing test-positive animals. Imperfect capture success, diagnostic sensitivity, and vaccine effectiveness mean that TVR would be expected to leave some infected and some susceptible badgers in the population. Existing simulation models predict that TVR could reduce cattle TB if such small-scale culling causes no perturbation, but could increase cattle TB if considerable perturbation occurs. Using data from a long-term study, we show that past small-scale culling was significantly associated with four metrics of perturbation in badgers: expanded ranging, more frequent immigration, lower genetic relatedness, and elevated prevalence of Mycobacterium bovis, the causative agent of TB. Though we could not reject the hypothesis that culling up to three badgers per social group might avoid perturbation, we also could not reject the hypothesis that killing a single badger prompted detectable perturbation. When considered alongside existing model predictions, our findings suggest that implementation of TVR, scheduled for 2014, risks exacerbating the TB problem rather than controlling it. Ongoing illegal badger culling is likewise expected to increase cattle TB risks.

Genome sequence, population history, and pelage genetics of the endangered African wild dog (Lycaon pictus).

BACKGROUND: The African wild dog (Lycaon pictus) is an endangered African canid threatened by severe habitat fragmentation, human-wildlife conflict, and infectious disease. A highly specialized carnivore, it is distinguished by its social structure, dental morphology, absence of dewclaws, and colorful pelage. RESULTS: We sequenced the genomes of two individuals from populations representing two distinct ecological histories (Laikipia County, Kenya and KwaZulu-Natal Province, South Africa). We reconstructed population demographic histories for the two individuals and scanned the genomes for evidence of selection. CONCLUSIONS: We show that the African wild dog has undergone at least two effective population size reductions in the last 1,000,000 years. We found evidence of Lycaon individual-specific regions of low diversity, suggestive of inbreeding or population-specific selection. Further research is needed to clarify whether these population reductions and low diversity regions are characteristic of the species as a whole. We documented positive selection on the Lycaon mitochondrial genome. Finally, we identified several candidate genes (ASIP, MITF, MLPH, PMEL) that may play a role in the characteristic Lycaon pelage.

Badgers prefer cattle pasture but avoid cattle: implications for bovine tuberculosis control.

Effective management of infectious disease relies upon understanding mechanisms of pathogen transmission. In particular, while models of disease dynamics usually assume transmission through direct contact, transmission through environmental contamination can cause different dynamics. We used Global Positioning System (GPS) collars and proximity-sensing contact-collars to explore opportunities for transmission of Mycobacterium bovis [causal agent of bovine tuberculosis] between cattle and badgers (Meles meles). Cattle pasture was badgers' most preferred habitat. Nevertheless, although collared cattle spent 2914 collar-nights in the home ranges of contact-collared badgers, and 5380 collar-nights in the home ranges of GPS-collared badgers, we detected no direct contacts between the two species. Simultaneous GPS-tracking revealed that badgers preferred land > 50 m from cattle. Very infrequent direct contact indicates that badger-to-cattle and cattle-to-badger M. bovis transmission may typically occur through contamination of the two species' shared environment. This information should help to inform tuberculosis control by guiding both modelling and farm management.

Recovery of African wild dogs suppresses prey but does not trigger a trophic cascade.

Increasingly, the restoration of large carnivores is proposed as a means through which to restore community structure and ecosystem function via trophic cascades. After a decades-long absence, African wild dogs (Lycaon pictus) recolonized the Laikipia Plateau in central Kenya, which we hypothesized would trigger a trophic cascade via suppression of their primary prey (dik-dik, Madoqua guentheri) and the subsequent relaxation of browsing pressure on trees. We tested the trophic-cascade hypothesis using (1) a 14-year time series of wild dog abundance; (2) surveys of dik-dik population densities conducted before and after wild dog recovery; and (3) two separate, replicated, herbivore-exclusion experiments initiated before and after wild dog recovery. The dik-dik population declined by 33% following wild dog recovery, which is best explained by wild dog predation. Dik-dik browsing suppressed tree abundance, but the strength of suppression did not differ between before and after wild dog recovery. Despite strong, top-down limitation between adjacent trophic levels (carnivore-herbivore and herbivore-plant), a trophic cascade did not occur, possibly because of a time lag in indirect effects, variation in rainfall, and foraging by herbivores other than dik-dik. Our ability to reject the trophic-cascade hypothesis required two important approaches: (1) temporally replicated herbivore exclusions, separately established before and after wild dog recovery; and (2) evaluating multiple drivers of variation in the abundance of dik-dik and trees. While the restoration of large carnivores is often a conservation priority, our results suggest that indirect effects are mediated by ecological context, and that trophic cascades are not a foregone conclusion of such recoveries.

SINGLE- VERSUS DOUBLE-DOSE RABIES VACCINATION IN CAPTIVE AFRICAN WILD DOGS (LYCAON PICTUS).

The immune responses of 35 captive African wild dogs (Lycaon pictus) to an inactivated rabies virus vaccine were evaluated. Seventeen animals received one 1-ml dose of inactivated rabies vaccine administered intramuscularly, while 18 received two 1-ml doses given simultaneously but at different injection sites. Sera were collected from all animals prior to vaccination and intermittently from a subset of animals between 3 and 49 mo postvaccination. Rabies neutralizing serum antibody titers were measured by rapid fluorescent focus inhibition testing. Within 3 mo postvaccination, all 28 animals that were tested within that time period had seroconverted. Overall, titers were significantly higher among animals given two doses of vaccine than among those given a single dose, although this difference was no longer significant by 15 mo postvaccination. Regardless of initial dose, a single administration of inactivated rabies virus vaccine resulted in long-term elevation of titers in the African wild dogs in this study. In the two individuals followed for greater than 36 mo, both (one from each group) maintained detectable titers.

Effect of Rabies Booster Vaccination on Antibody Levels in African Wild Dogs (Lycaon pictus).

Rabies is a highly virulent viral disease that has been associated with large-scale population declines of the endangered African wild dog (Lycaon pictus). Rabies vaccination may be a valuable conservation tool in this species, but studies indicate that a single dose does not always confer protective immunity. We examined 47 serum samples from 22 captive African wild dogs (sampled opportunistically for other purposes) to assess whether serum antibody levels after vaccination correlated with the number of doses received and whether other factors affected outcomes. Results of the fluorescent antibody virus neutralization test showed that median antibody titers were 0.085 IU/mL prevaccination, 0.660 IU/mL after a single vaccination, and 22.150 IU/mL after a booster vaccination. Antibody titers above 0.5 IU/mL, internationally accepted as the threshold for seroconversion, were found in none of the samples taken prevaccination, 66.67% of samples taken after primary vaccination, and 90.90% of samples collected after booster vaccination. This study illustrates the probable protective benefit a rabies booster vaccination may provide in African wild dogs and serves as a basis for future research to improve vaccination protocols contributing to the conservation of this endangered species.

A restatement of the natural science evidence base relevant to the control of bovine tuberculosis in Great Britain.

Bovine tuberculosis (bTB) is a very important disease of cattle in Great Britain, where it has been increasing in incidence and geographical distribution. In addition to cattle, it infects other species of domestic and wild animals, in particular the European badger (Meles meles). Policy to control bTB is vigorously debated and contentious because of its implications for the livestock industry and because some policy options involve culling badgers, the most important wildlife reservoir. This paper describes a project to provide a succinct summary of the natural science evidence base relevant to the control of bTB, couched in terms that are as policy-neutral as possible. Each evidence statement is placed into one of four categories describing the nature of the underlying information. The evidence summary forms the appendix to this paper and an annotated bibliography is provided in the electronic supplementary material.

Comparison of oral and intramuscular recombinant canine distemper vaccination in African wild dogs (Lycaon pictus).

A series of three doses of recombinant canary-pox-vectored canine distemper virus vaccine was administered at 1-mo intervals, orally (n = 8) or intramuscularly (n = 13), to 21 previously unvaccinated juvenile African wild dogs (Lycaon pictus) at the Wildlife Conservation Society's Bronx Zoo. Titers were measured by serum neutralization at each vaccination and at intervals over a period of 3.5-21.5 mo after the initial vaccination. All postvaccination titers were negative for orally vaccinated animals at all sampling time points. Of the animals that received intramuscular vaccinations, 100% had presumed protective titers by the end of the course of vaccination, but only 50% of those sampled at 6.5 mo postvaccination had positive titers. None of the three animals sampled at 21.5 mo postvaccination had positive titers.

Optimizing the automated recognition of individual animals to support population monitoring.

Reliable estimates of population size and demographic rates are central to assessing the status of threatened species. However, obtaining individual-based demographic rates requires long-term data, which is often costly and difficult to collect. Photographic data offer an inexpensive, noninvasive method for individual-based monitoring of species with unique markings, and could therefore increase available demographic data for many species. However, selecting suitable images and identifying individuals from photographic catalogs is prohibitively time-consuming. Automated identification software can significantly speed up this process. Nevertheless, automated methods for selecting suitable images are lacking, as are studies comparing the performance of the most prominent identification software packages. In this study, we develop a framework that automatically selects images suitable for individual identification, and compare the performance of three commonly used identification software packages; Hotspotter, I3S-Pattern, and WildID. As a case study, we consider the African wild dog, Lycaon pictus, a species whose conservation is limited by a lack of cost-effective large-scale monitoring. To evaluate intraspecific variation in the performance of software packages, we compare identification accuracy between two populations (in Kenya and Zimbabwe) that have markedly different coat coloration patterns. The process of selecting suitable images was automated using convolutional neural networks that crop individuals from images, filter out unsuitable images, separate left and right flanks, and remove image backgrounds. Hotspotter had the highest image-matching accuracy for both populations. However, the accuracy was significantly lower for the Kenyan population (62%), compared to the Zimbabwean population (88%). Our automated image preprocessing has immediate application for expanding monitoring based on image matching. However, the difference in accuracy between populations highlights that population-specific detection rates are likely and may influence certainty in derived statistics. For species such as the African wild dog, where monitoring is both challenging and expensive, automated individual recognition could greatly expand and expedite conservation efforts.

Spatial and temporal patterns of neutral and adaptive genetic variation in the endangered African wild dog (Lycaon pictus).

Deciphering patterns of genetic variation within a species is essential for understanding population structure, local adaptation and differences in diversity between populations. Whilst neutrally evolving genetic markers can be used to elucidate demographic processes and genetic structure, they are not subject to selection and therefore are not informative about patterns of adaptive variation. As such, assessments of pertinent adaptive loci, such as the immunity genes of the major histocompatibility complex (MHC), are increasingly being incorporated into genetic studies. In this study, we combined neutral (microsatellite, mtDNA) and adaptive (MHC class II DLA-DRB1 locus) markers to elucidate the factors influencing patterns of genetic variation in the African wild dog (Lycaon pictus); an endangered canid that has suffered extensive declines in distribution and abundance. Our genetic analyses found all extant wild dog populations to be relatively small (N(e) < 30). Furthermore, through coalescent modelling, we detected a genetic signature of a recent and substantial demographic decline, which correlates with human expansion, but contrasts with findings in some other African mammals. We found strong structuring of wild dog populations, indicating the negative influence of extensive habitat fragmentation and loss of gene flow between habitat patches. Across populations, we found that the spatial and temporal structure of microsatellite diversity and MHC diversity were correlated and strongly influenced by demographic stability and population size, indicating the effects of genetic drift in these small populations. Despite this correlation, we detected signatures of selection at the MHC, implying that selection has not been completely overwhelmed by genetic drift.

Positive and negative effects of widespread badger culling on tuberculosis in cattle.

Human and livestock diseases can be difficult to control where infection persists in wildlife populations. For three decades, European badgers (Meles meles) have been culled by the British government in a series of attempts to limit the spread of Mycobacterium bovis, the causative agent of bovine tuberculosis (TB), to cattle. Despite these efforts, the incidence of TB in cattle has risen consistently, re-emerging as a primary concern for Britain's cattle industry. Recently, badger culling has attracted controversy because experimental studies have reached contrasting conclusions (albeit using different protocols), with culled areas showing either markedly reduced or increased incidence of TB in cattle. This has confused attempts to develop a science-based management policy. Here we use data from a large-scale, randomized field experiment to help resolve these apparent differences. We show that, as carried out in this experiment, culling reduces cattle TB incidence in the areas that are culled, but increases incidence in adjoining areas. These findings are biologically consistent with previous studies but will present challenges for policy development.

The effect of protected areas on pathogen exposure in endangered African wild dog (Lycaon pictus) populations.

Infectious diseases impact African wild dogs (Lycaon pictus), but the nature and magnitude of this threat likely varies among populations according to different factors, such as the presence and prevalence of pathogens and land-use characteristics. We systematically evaluated these factors to assist development of locally appropriate strategies to mitigate disease risk. Wild dogs from 16 sites representing five unconnected populations were examined for rabies virus, canine distemper virus (CDV), canine parvovirus, canine coronavirus, and Babesia spp. exposure. Analyses revealed widespread exposure to viral pathogens, but Babesia was never detected. Exposure to CDV was associated with unprotected and protected-unfenced areas where wild dogs likely have a high probability of domestic dog contact and, in the case of protected-unfenced areas, likely reside amongst high wildlife densities. Our findings also suggest that domestic dog contact may increase rabies and coronavirus exposure risk. Therefore, domestic dogs may be a source of CDV, rabies and coronavirus, while wildlife may also play an important role in CDV transmission dynamics. Relatively high parvovirus seroprevalence across land-use types suggests that it might persist in the absence of spillover from domestic dogs. Should intervention be needed to control pathogens in wild dogs, efforts to prevent rabies and coronavirus exposure might be directed at reducing infection in the presumed domestic dog reservoir through vaccination. If prevention of CDV and parvovirus infections were deemed a management necessity, control of disease in domestic dogs may be insufficient to reduce transmission risks, and vaccination of wild dogs themselves may be the optimal strategy.