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.

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.

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.

High temperatures and human pressures interact to influence mortality in an African carnivore.

The impacts of high ambient temperatures on mortality in humans and domestic animals are well-understood. However much less is known about how hot weather affects mortality in wild animals. High ambient temperatures have been associated with African wild dog Lycaon pictus pup mortality, suggesting that high temperatures might also be linked to high adult mortality.We analyzed mortality patterns in African wild dogs radio-collared in Kenya (0°N), Botswana (20°S), and Zimbabwe (20°S), to examine whether ambient temperature was associated with adult mortality.We found that high ambient temperatures were associated with increased adult wild dog mortality at the Kenya site, and there was some evidence for temperature associations with mortality at the Botswana and Zimbabwe sites.At the Kenya study site, which had the highest human impact, high ambient temperatures were associated with increased risks of wild dogs being killed by people, and by domestic dog diseases. In contrast, temperature was not associated with the risk of snare-related mortality at the Zimbabwe site, which had the second-highest human impact. Causes of death varied markedly between sites.Pack size was positively associated with survival at all three sites.These findings suggest that while climate change may not lead to new causes of mortality, rising temperatures may exacerbate existing anthropogenic threats to this endangered species, with implications for conservation. This evidence suggests that temperature-related mortality, including interactions between temperature and other anthropogenic threats, should be investigated in a greater number of species to understand and mitigate likely impacts of climate change. ​.

Modelling the influence of naturally acquired immunity from subclinical infection on outbreak dynamics and persistence of rabies in domestic dogs.

A number of mathematical models have been developed for canine rabies to explore dynamics and inform control strategies. A common assumption of these models is that naturally acquired immunity plays no role in rabies dynamics. However, empirical studies have detected rabies-specific antibodies in healthy, unvaccinated domestic dogs, potentially due to immunizing, non-lethal exposure. We developed a stochastic model for canine rabies, parameterised for Laikipia County, Kenya, to explore the implications of different scenarios for naturally acquired immunity to rabies in domestic dogs. Simulating these scenarios using a non-spatial model indicated that low levels of immunity can act to limit rabies incidence and prevent depletion of the domestic dog population, increasing the probability of disease persistence. However, incorporating spatial structure and human response to high rabies incidence allowed the virus to persist in the absence of immunity. While low levels of immunity therefore had limited influence under a more realistic approximation of rabies dynamics, high rates of exposure leading to immunizing non-lethal exposure were required to produce population-level seroprevalences comparable with those reported in empirical studies. False positives and/or spatial variation may contribute to high empirical seroprevalences. However, if high seroprevalences are related to high exposure rates, these findings support the need for high vaccination coverage to effectively control this disease.

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.

Volunteer based approach to dog vaccination campaigns to eliminate human rabies: Lessons from Laikipia County, Kenya.

BACKGROUND: An estimated 59,000 people die from rabies annually, with 99% of those deaths attributable to bites from domestic dogs (Canis lupus familiaris). This preventable Neglected Tropical Disease has a large impact across continental Africa, especially for rural populations living in close contact with livestock and wildlife. Mass vaccinations of domestic dogs are effective at eliminating rabies but require large amounts of resources, planning, and political will to implement. Grassroots campaigns provide an alternative method to successful implementation of rabies control but remain understudied in their effectiveness to eliminate the disease from larger regions. METHODOLOGY/PRINCIPAL FINDINGS: We report on the development, implementation, and effectiveness of a grassroots mass dog rabies vaccination campaign in Kenya, the Laikipia Rabies Vaccination Campaign. During 2015-2017, a total of 13,155 domestic dogs were vaccinated against rabies in 17 communities covering approximately 1500 km2. Based on an estimated population size of 34,275 domestic dogs, percent coverages increased across years, from 2% in 2015 to 24% in 2017, with only 3 of 38 community-years of vaccination exceeding the 70% target. The average cost of vaccinating an animal was $3.44 USD with in-kind contributions and $7.44 USD without in-kind contributions. CONCLUSIONS/SIGNIFICANCE: The evolution of the Laikipia Rabies Vaccination Campaign from a localized volunteer-effort to a large-scale program attempting to eliminate rabies at the landscape scale provides a unique opportunity to examine successes, failures, and challenges facing grassroots campaigns. Success, in the form of vaccinating more dogs across the study area, was relatively straightforward to achieve. However, lack of effective post-vaccination monitoring and education programs, limited funding, and working in diverse community types appeared to hinder achievement of 70% coverage levels. These results indicate that grassroots campaigns will inevitably be faced with a philosophical question regarding the value of local impacts versus their contributions to a larger effort to eliminate rabies at the regional, country, or global scale.

Rabies virus-neutralising antibodies in healthy, unvaccinated individuals: What do they mean for rabies epidemiology?

Rabies has been a widely feared disease for thousands of years, with records of rabid dogs as early as ancient Egyptian and Mesopotamian texts. The reputation of rabies as being inevitably fatal, together with its ability to affect all mammalian species, contributes to the fear surrounding this disease. However, the widely held view that exposure to the rabies virus is always fatal has been repeatedly challenged. Although survival following clinical infection in humans has only been recorded on a handful of occasions, a number of studies have reported detection of rabies-specific antibodies in the sera of humans, domestic animals, and wildlife that are apparently healthy and unvaccinated. These 'seropositive' individuals provide possible evidence of exposure to the rabies virus that has not led to fatal disease. However, the variability in methods of detecting these antibodies and the difficulties of interpreting serology tests have contributed to an unclear picture of their importance. In this review, we consider the evidence for rabies-specific antibodies in healthy, unvaccinated individuals as indicators of nonlethal rabies exposure and the potential implications of this for rabies epidemiology. Our findings indicate that whilst there is substantial evidence that nonlethal rabies exposure does occur, serology studies that do not use appropriate controls and cutoffs are unlikely to provide an accurate estimate of the true prevalence of nonlethal rabies exposure.

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.

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.

Effect of culling on individual badger Meles meles behaviour: Potential implications for bovine tuberculosis transmission.

Culling wildlife as a form of disease management can have unexpected and sometimes counterproductive outcomes. In the UK, badgers Meles meles are culled in efforts to reduce badger-to-cattle transmission of Mycobacterium bovis, the causative agent of bovine tuberculosis (TB). However, culling has previously been associated with both increased and decreased incidence of M. bovis infection in cattle.The adverse effects of culling have been linked to cull-induced changes in badger ranging, but such changes are not well-documented at the individual level. Using GPS-collars, we characterized individual badger behaviour within an area subjected to widespread industry-led culling, comparing it with the same area before culling and with three unculled areas.Culling was associated with a 61% increase (95% CI 27%-103%) in monthly home range size, a 39% increase (95% CI 28%-51%) in nightly maximum distance from the sett, and a 17% increase (95% CI 11%-24%) in displacement between successive GPS-collar locations recorded at 20-min intervals. Despite travelling further, we found a 91.2 min (95% CI 67.1-115.3 min) reduction in the nightly activity time of individual badgers associated with culling. These changes became apparent while culls were ongoing and persisted after culling ended.Expanded ranging in culled areas was associated with individual badgers visiting 45% (95% CI 15%-80%) more fields each month, suggesting that surviving individuals had the opportunity to contact more cattle. Moreover, surviving badgers showed a 19.9-fold increase (95% CI 10.8-36.4-fold increase) in the odds of trespassing into neighbouring group territories, increasing opportunities for intergroup contact.Synthesis and applications. Badger culling was associated with behavioural changes among surviving badgers which potentially increased opportunities for both badger-to-badger and badger-to-cattle transmission of Mycobacterium bovis. Furthermore, by reducing the time badgers spent active, culling may have reduced badgers' accessibility to shooters, potentially undermining subsequent population control efforts. Our results specifically illustrate the challenges posed by badger behaviour to cull-based TB control strategies and furthermore, they highlight the negative impacts culling can have on integrated disease control strategies.

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.

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.

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.

Localised Badger Culling Increases Risk of Herd Breakdown on Nearby, Not Focal, Land.

Bovine tuberculosis is an important disease affecting the UK livestock industry. Controlling bovine tuberculosis (TB) is made more complex by the presence of a wildlife host, the Eurasian badger, Meles meles. Repeated large-scale badger culls implemented in the Randomised Badger Culling Trial (RBCT) were associated with decreased cattle risks inside the culling area, but also with increased cattle risks up to the 2km outside the culling area. Intermediate reductions in badger density, as achieved by localised reactive culling in the RBCT, significantly increased cattle TB. Using a matched-pairs case-control study design (n = 221 pairs of cattle herds), we investigated the spatial scale over which localised badger culling had its biggest impact. We found that reactive badger culling had a significant positive association with the risk of cattle TB at distances of 1-3km and 3-5km, and that no such association existed over shorter distances (<1km). These findings indicate that localised badger culls had significant negative effects, not on the land on which culling took place, but, perhaps more importantly, on adjoining lands and farms.

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.

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.

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.