The effects of anthrax on endangered African wild dogs (Lycaon pictus)

African wild dogs ( Lycaon pictus ) are large, social canids formerly found throughout sub-Saharan Africa. Wild dogs are now endangered; only six nations hold populations larger than 100 individuals. Considerable evidence suggests that disease plays a central role in the regulation of some wild dog populations. In particular, it has been suggested that epizootics of rabies, canine distemper and anthrax can have strong local effects on wild dog numbers. Resolution of the regulatory importance of these diseases has been hampered by lack of data from wild populations. Here we report on an outbreak of anthrax among wild dogs in the Selous Game Reserve in southern Tanzania, describing clinical signs and diagnosis, measuring mortality, and testing for effects on hunting success and movements. Only one of five packs under study was affected. Immediate mortality was mild, with none of 18 adults (0%) and four of 24 pups (17%) dying. Mortality was significantly higher among puppies (<1 year old) than among adults. Mortality of individuals that showed signs of disease but did not die immediately was not significantly elevated over the following six months. The hunting success and movement patterns of the pack were not affected by the outbreak. Collectively, these data suggest that African wild dogs possess a degree of resistance to anthrax.     

Consequences of non-intervention for infectious disease in African great apes

Infectious disease has recently joined poaching and habitat loss as a major threat to African apes. Both "naturally" occurring pathogens, such as Ebola and Simian Immunodeficiency Virus (SIV), and respiratory pathogens transmitted from humans, have been confirmed as important sources of mortality in wild gorillas and chimpanzees. While awareness of the threat has increased, interventions such as vaccination and treatment remain controversial. Here we explore both the risk of disease to African apes, and the status of potential responses. Through synthesis of published data, we summarize prior disease impact on African apes. We then use a simple demographic model to illustrate the resilience of a well-known gorilla population to disease, modeled on prior documented outbreaks. We found that the predicted recovery time for this specific gorilla population from a single outbreak ranged from 5 years for a low mortality (4%) respiratory outbreak, to 131 years for an Ebola outbreak that killed 96% of the population. This shows that mortality rates comparable to those recently reported for disease outbreaks in wild populations are not sustainable. This is particularly troubling given the rising pathogen risk created by increasing habituation of wild apes for tourism, and the growth of human populations surrounding protected areas. We assess potential future disease spillover risk in terms of vaccination rates amongst humans that may come into contact with wild apes, and the availability of vaccines against potentially threatening diseases. We discuss and evaluate non-interventionist responses such as limiting tourist access to apes, community health programs, and safety, logistic, and cost issues that constrain the potential of vaccination.     

Development of a bait and baiting system for delivery of oral rabies vaccine to free-ranging African wild dogs (Lycaon pictus)

The objective of the study was to develop a bait and baiting system capable of delivering one effective dose of oral rabies vaccine to each member of a free-ranging African wild dog (Lycaon pictus) pack. Trials were conducted between June and October 2000. The results of cafeteria-style bait preference trials testing seven candidate baits in captive wild dogs revealed a significant preference for chicken heads (June trials: P = 0.023, September trials: P = 0.021). Trials using a topical biomarker (rhodamine B) showed that chicken head baits were sufficiently chewed on most occasions to rupture the vaccine container. Free-ranging wild dogs and young pups ingested chicken head baits. Significant dominance of bait intake by a single individual was seen in four of six study packs and in the three packs in which an alpha pair could be distinguished, the dominant feeder was an alpha animal. Pattern of bait distribution and degree of satiation had no effect on pack coverage (proportion of pack ingesting at least one bait). Pack coverage was significantly related to trial number (r = 0.71, P < 0.001), with pack coverage increasing with increased exposure of the pack to the baits. During 46 hr of diurnal observations of free-ranging wild dogs only two baits were lost to non-target species. A baiting system for the oral vaccination of captive and free-ranging wild dogs is proposed.     

Contact with domestic dogs increases pathogen exposure in endangered African wild dogs (Lycaon pictus)

Background

Infectious diseases have contributed to the decline and local extinction of several wildlife species, including African wild dogs (Lycaon pictus). Mitigating such disease threats is challenging, partly because uncertainty about disease dynamics makes it difficult to identify the best management approaches. Serious impacts on susceptible populations most frequently occur when generalist pathogens are maintained within populations of abundant (often domestic) “reservoir” hosts, and spill over into less abundant host species. If this is the case, disease control directed at the reservoir host might be most appropriate. However, pathogen transmission within threatened host populations may also be important, and may not be controllable by managing another host species.

Methodology/Principal Findings

We investigated interspecific and intraspecific transmission routes, by comparing African wild dogs'' exposure to six canine pathogens with behavioural measures of their opportunities for contact with domestic dogs and with other wild dogs. Domestic dog contact was associated with exposure to canine parvovirus, Ehrlichia canis, Neospora caninum and perhaps rabies virus, but not with exposure to canine distemper virus or canine coronavirus. Contact with other wild dogs appeared not to increase the risk of exposure to any of the pathogens.

Conclusions/Significance

These findings, combined with other data, suggest that management directed at domestic dogs might help to protect wild dog populations from rabies virus, but not from canine distemper virus. However, further analyses are needed to determine the management approaches – including no intervention – which are most appropriate for each pathogen.     

Documenting Freedom From Disease and Re-Establishing a Free Status After a Breakdown Rabies

Rabies reappeared in Finland in the spring of 1988 after a 29-year absence. This time rabies occurred in sylvatic form and the major species involved was the raccoon dog. During the outbreak 1988–89 66 animals were diagnosed rabid. Vaccination of cats, cattle and horses was strongly recommended and vaccination of dogs was compulsory in the outbreak area. A field trial was started on oral immunisation of raccoon dogs and foxes against rabies using baits containing rabies vaccine strain. The outbreak area and a wide buffer zone were baited three times. Finland was declared free of rabies again in 1991. Oral vaccination campaign with vaccine baits has been organised along the southeastern border once a year since the beginning of 90s. Continuous surveillance and epidemiological screening is necessary to detect any new outbreaks of rabies at an early stage.     

Fence management and time since pack formation influence African wild dog escapes from protected areas in South Africa

In human-dominated and highly fragmented landscapes, keeping wildlife within reserve boundaries is vital for conservation success. In South Africa, fences are a widely employed conservation management tool for protected areas and are successful in mitigating human-wildlife conflict. However, fences are permeable, and predators are able to cross through reserve fences. African wild dogs (Lycaon pictus) often leave fenced boundaries, resulting in high capture and translocation costs. Moreover, when wild dog packs (up to 30 individuals) leave fenced reserves they enter human-dominated landscapes where they face strong persecution and livestock predation incurs high costs. The factors driving packs to leave managed reserves are poorly understood, thus, to effectively manage wild dogs in fenced systems, it is important to understand why they leave reserve boundaries. There are several hypotheses as to why wild dogs cross through reserve fences, including inter- and intra-specific competition, social behaviour, management, prey density and environmental variability. Using a long-term dataset comprising 32 resident packs across five reserves, we investigated the relative strength of these hypotheses on the probability of wild dogs exiting a fenced reserve. During the 14-year study period, we recorded 154 exit events. We found that the interaction of fence integrity and time since pack formation were the primary factors affecting the probability of a pack leaving a reserve. When fence integrity was poor, escape probability decreased with pack age likely due to the exploratory behaviour of new packs. When fence integrity was average, escape probability increased with pack age likely due to the fitness benefits of holding larger and more exclusive territories as packs age. When fence integrity was good, the probability of a pack escaping was very low (only 1% occurrence). The implications of this research suggest that the primary management consideration for reducing wild dog escapes from fenced reserves should be maintaining adequate reserve-wide fence integrity, rather than focusing on social structure or drivers of inter- and intra-specific competition.     

Presence of rabies neutralizing antibodies in wild carnivores following an outbreak of bovine rabies.

In an outbreak of bovine rabies in Argentina, a study was made of vampire bats (Desmodus rotundus) and wild carnivores. Rabies antibody rates of high prevalence were found in the bats, foxes (Dusicyon gymnocercus) and skunks (Conepatus chinga). The outbreak was part of an extensive continuing epizootic of vampire transmitted bovine rabies which may have also involved other vectors in the area of this study. Consumption of dead and dying bats by the carnivores is the suggested means of passage of rabies virus from vampire bats to foxes and skunks. Given optimum conditions it is conceivable that some outbreaks in carnivores may begin in this way.     

Two Different Epidemiological Scenarios of Border Disease in the Populations of Pyrenean chamois (Rupicapra p. pyrenaica) after the First Disease Outbreaks

Since 2001 several outbreaks of a new disease associated with Border disease virus (BDV) infection have caused important declines in Pyrenean chamois (Rupicapra pyrenaica) populations in the Pyrenees. The goal of this study was to analyze the post-outbreak BDV epidemiology in the first two areas affected by disease with the aim to establish if the infection has become endemic. We also investigated if BDV infected wild and domestic ruminants sharing habitat with chamois. Unexpectedly, we found different epidemiological scenarios in each population. Since the disease outbreaks, some chamois populations recuperated quickly, while others did not recover as expected. In chamois from the first areas, prevalence was high (73.47%) and constant throughout the whole study period and did not differ between chamois born before and after the BDV outbreak; in all, BDV was detected by RT-PCR in six chamois. In the other areas, prevalence was lower (52.79%) and decreased during the study period; as well, prevalence was significantly lower in chamois born after the disease outbreak. No BDV were detected in this population. A comparative virus neutralisation test performed with four BDV strains and one Bovine viral diarrhoea virus (BVDV) strain showed that all the chamois had BDV-specific antibodies. Pestivirus antibodies were detected in all the rest of analyzed species, with low prevalence values in wild ruminants and moderate values in domestic ruminants. No viruses were detected in these species. These results confirm the hypothesis that outbreaks of BDV infection only affect the Pyrenean chamois, although other wild ruminants can occasionally be infected. In conclusion, two different scenarios have appeared since the first border disease outbreaks in Pyrenean chamois: on the one hand frequent BDV circulation with possible negative impact on population dynamics in some areas and on the other, lack of virus circulation and quick recovery of the chamois population.     

Inbreeding, heterozygosity and fitness in a reintroduced population of endangered African wild dogs (Lycaon pictus)

It is crucial to understand the genetic health and implications of inbreeding in wildlife populations, especially of vulnerable species. Using extensive demographic and genetic data, we investigated the relationships among pedigree inbreeding coefficients, metrics of molecular heterozygosity and fitness for a large population of endangered African wild dogs (Lycaon pictus) in South Africa. Molecular metrics based on 19 microsatellite loci were significantly, but modestly correlated to inbreeding coefficients in this population. Inbred wild dogs with inbreeding coefficients of ??0.25 and subordinate individuals had shorter lifespans than outbred and dominant contemporaries, suggesting some deleterious effects of inbreeding. However, this trend was confounded by pack-specific effects as many inbred individuals originated from a single large pack. Despite wild dogs being endangered and existing in small populations, findings within our sample population indicated that molecular metrics were not robust predictors in models of fitness based on breeding pack formation, dominance, reproductive success or lifespan of individuals. Nonetheless, our approach has generated a vital database for future comparative studies to examine these relationships over longer periods of time. Such detailed assessments are essential given knowledge that wild canids can be highly vulnerable to inbreeding effects over a few short generations.     

Codetection of Respiratory Syncytial Virus in Habituated Wild Western Lowland Gorillas and Humans During a Respiratory Disease Outbreak

Pneumoviruses have been identified as causative agents in several respiratory disease outbreaks in habituated wild great apes. Based on phylogenetic evidence, transmission from humans is likely. However, the pathogens have never been detected in the local human population prior to or at the same time as an outbreak. Here, we report the first simultaneous detection of a human respiratory syncytial virus (HRSV) infection in western lowland gorillas (Gorilla gorilla gorilla) and in the local human population at a field program in the Central African Republic. A total of 15 gorilla and 15 human fecal samples and 80 human throat swabs were tested for HRSV, human metapneumovirus, and other respiratory viruses. We were able to obtain identical sequences for HRSV A from four gorillas and four humans. In contrast, we did not detect HRSV or any other classic human respiratory virus in gorilla fecal samples in two other outbreaks in the same field program. Enterovirus sequences were detected but the implication of these viruses in the etiology of these outbreaks remains speculative. Our findings of HRSV in wild but human-habituated gorillas underline, once again, the risk of interspecies transmission from humans to endangered great apes.     

Revealing the Micro-scale Signature of Endemic Zoonotic Disease Transmission in an African Urban Setting

The development of novel approaches that combine epidemiological and genomic data provides new opportunities to reveal the spatiotemporal dynamics of infectious diseases and determine the processes responsible for their spread and maintenance. Taking advantage of detailed epidemiological time series and viral sequence data from more than 20 years reported by the National Reference Centre for Rabies of Bangui, the capital city of Central African Republic, we used a combination of mathematical modeling and phylogenetic analysis to determine the spatiotemporal dynamics of rabies in domestic dogs as well as the frequency of extinction and introduction events in an African city. We show that although dog rabies virus (RABV) appears to be endemic in Bangui, its epidemiology is in fact shaped by the regular extinction of local chains of transmission coupled with the introduction of new lineages, generating successive waves of spread. Notably, the effective reproduction number during each wave was rarely above the critical value of 1, such that rabies is not self-sustaining in Bangui. In turn, this suggests that rabies at local geographic scales is driven by human-mediated dispersal of RABV among sparsely connected peri-urban and rural areas as opposed to dispersion in a relatively large homogenous urban dog population. This combined epidemiological and genomic approach enables development of a comprehensive framework for understanding disease persistence and informing control measures, indicating that control measures are probably best targeted towards areas neighbouring the city that appear as the source of frequent incursions seeding outbreaks in Bangui.     

Presence of Virus Neutralizing Antibodies in Cerebral Spinal Fluid Correlates with Non-Lethal Rabies in Dogs

Background

Rabies is traditionally considered a uniformly fatal disease after onset of clinical manifestations. However, increasing evidence indicates that non-lethal infection as well as recovery from flaccid paralysis and encephalitis occurs in laboratory animals as well as humans.

Methodology/Principal Findings

Non-lethal rabies infection in dogs experimentally infected with wild type dog rabies virus (RABV, wt DRV-Mexico) correlates with the presence of high level of virus neutralizing antibodies (VNA) in the cerebral spinal fluid (CSF) and mild immune cell accumulation in the central nervous system (CNS). By contrast, dogs that succumbed to rabies showed only little or no VNA in the serum or in the CSF and severe inflammation in the CNS. Dogs vaccinated with a rabies vaccine showed no clinical signs of rabies and survived challenge with a lethal dose of wild-type DRV. VNA was detected in the serum, but not in the CSF of immunized dogs. Thus the presence of VNA is critical for inhibiting virus spread within the CNS and eventually clearing the virus from the CNS.

Conclusions/Significance

Non-lethal infection with wt RABV correlates with the presence of VNA in the CNS. Therefore production of VNA within the CNS or invasion of VNA from the periphery into the CNS via compromised blood-brain barrier is important for clearing the virus infection from CNS, thereby preventing an otherwise lethal rabies virus infection.     

Assessing re-introductions of the African Wild dog (Lycaon pictus) in the Limpopo Valley Conservancy, South Africa, using the stochastic simulation program VORTEX

The African wild dog (Lycaon pictus) is one of Africa's most endangered species and therefore classified as endangered by IUCN. Earlier distributions included most of Africa but currently the African wild dog only has populations larger than 300 individuals in three countries (Botswana, Tanzania and South Africa). In 1998, a plan was launched in South Africa to manage sub-populations of the African wild dog in several small, geographically isolated, conservation areas. This management program involved the reintroduction of wild dogs into suitable conservation areas and periodic translocations among them. We used the stochastic population simulation model VORTEX to evaluate the Limpopo Valley Conservancy in the north of South Africa, as a possible reintroduction site for African wild dogs. The simulations showed that the size of the initial population released only had a small effect on the population dynamics. However, when individuals were supplemented and harvested over a longer period the probability of persistence increased. Number of females breeding, male mortality, and carrying capacity were key factors in the population dynamics, but according to VORTEX the severity of natural catastrophes had the greatest influence on the extinction risk and inbreeding. We suggest that the reintroduction program may be successful, if areas are properly secured, the dogs are held in a boma before release, wild animals or at least a mix of wild and captive animals are used for the release and the animals are vaccinated against rabies. It is, however, essential to continue monitoring followed by modelling efforts to re-evaluate the success of the reintroduction program.     

Pasteurella multocida involved in respiratory disease of wild chimpanzees

Pasteurella multocida can cause a variety of diseases in various species of mammals and birds throughout the world but nothing is known about its importance for wild great apes. In this study we isolated P. multocida from wild living, habituated chimpanzees from Taï National Park, Côte d''Ivoire. Isolates originated from two chimpanzees that died during a respiratory disease outbreak in 2004 as well as from one individual that developed chronic air-sacculitis following this outbreak. Four isolates were subjected to a full phenotypic and molecular characterisation. Two different clones were identified using pulsed field gel electrophoresis. Multi Locus Sequence Typing (MLST) enabled the identification of previous unknown alleles and two new sequence types, ST68 and ST69, were assigned. Phylogenetic analysis of the superoxide dismutase (sodA) gene and concatenated sequences from seven MLST-housekeeping genes showed close clustering within known P. multocida isolated from various hosts and geographic locations. Due to the clinical relevance of the strains described here, these results make an important contribution to our knowledge of pathogens involved in lethal disease outbreaks among endangered great apes.     

Community-Based Measures for Mitigating the 2009 H1N1 Pandemic in China

Since the emergence of influenza A/H1N1 pandemic virus in March–April 2009, very stringent interventions including Fengxiao were implemented to prevent importation of infected cases and decelerate the disease spread in mainland China. The extent to which these measures have been effective remains elusive. We sought to investigate the effectiveness of Fengxiao that may inform policy decisions on improving community-based interventions for management of on-going outbreaks in China, in particular during the Spring Festival in mid-February 2010 when nationwide traveling will be substantially increased. We obtained data on initial laboratory-confirmed cases of H1N1 in the province of Shaanxi and used Markov-chain Monte-Carlo (MCMC) simulations to estimate the reproduction number. Given the estimates for the exposed and infectious periods of the novel H1N1 virus, we estimated a mean reproduction number of 1.68 (95% CI 1.45–1.92) and other A/H1N1 epidemiological parameters. Our results based on a spatially stratified population dynamical model show that the early implementation of Fengxiao can delay the epidemic peak significantly and prevent the disease spread to the general population but may also, if not implemented appropriately, cause more severe outbreak within universities/colleges, while late implementation of Fengxiao can achieve nothing more than no implementation. Strengthening local control strategies (quarantine and hygiene precaution) is much more effective in mitigating outbreaks and inhibiting the successive waves than implementing Fengxiao. Either strong mobility or high transport-related transmission rate during the Spring Festival holiday will not reverse the ongoing outbreak, but both will result in a large new wave. The findings suggest that Fengxiao and travel precautions should not be relaxed unless strict measures of quarantine, isolation, and hygiene precaution practices are put in place. Integration and prompt implementation of these interventions can significantly reduce the overall attack rate of pandemic outbreaks.     

Update on oral Chagas disease outbreaks in Venezuela: epidemiological, clinical and diagnostic approaches

Orally transmitted Chagas disease has become a matter of concern due to outbreaks reported in four Latin American countries. Although several mechanisms for orally transmitted Chagas disease transmission have been proposed, food and beverages contaminated with whole infected triatomines or their faeces, which contain metacyclic trypomastigotes of Trypanosoma cruzi, seems to be the primary vehicle. In 2007, the first recognised outbreak of orally transmitted Chagas disease occurred in Venezuela and largest recorded outbreak at that time. Since then, 10 outbreaks (four in Caracas) with 249 cases (73.5% children) and 4% mortality have occurred. The absence of contact with the vector and of traditional cutaneous and Romana’s signs, together with a florid spectrum of clinical manifestations during the acute phase, confuse the diagnosis of orally transmitted Chagas disease with other infectious diseases. The simultaneous detection of IgG and IgM by ELISA and the search for parasites in all individuals at risk have been valuable diagnostic tools for detecting acute cases. Follow-up studies regarding the microepidemics primarily affecting children has resulted in 70% infection persistence six years after anti-parasitic treatment. Panstrongylus geniculatus has been the incriminating vector in most cases. As a food-borne disease, this entity requires epidemiological, clinical, diagnostic and therapeutic approaches that differ from those approaches used for traditional direct or cutaneous vector transmission.     

Migration of Whooper Swans and Outbreaks of Highly Pathogenic Avian Influenza H5N1 Virus in Eastern Asia

Evaluating the potential involvement of wild avifauna in the emergence of highly pathogenic avian influenza H5N1 (hereafter H5N1) requires detailed analyses of temporal and spatial relationships between wild bird movements and disease emergence. The death of wild swans (Cygnus spp.) has been the first indicator of the presence of H5N1 in various Asian and European countries; however their role in the geographic spread of the disease remains poorly understood. We marked 10 whooper swans (Cygnus cygnus) with GPS transmitters in northeastern Mongolia during autumn 2006 and tracked their migratory movements in relation to H5N1 outbreaks. The prevalence of H5N1 outbreaks among poultry in eastern Asia during 2003–2007 peaked during winter, concurrent with whooper swan movements into regions of high poultry density. However outbreaks involving poultry were detected year round, indicating disease perpetuation independent of migratory waterbird presence. In contrast, H5N1 outbreaks involving whooper swans, as well as other migratory waterbirds that succumbed to the disease in eastern Asia, tended to occur during seasons (late spring and summer) and in habitats (areas of natural vegetation) where their potential for contact with poultry is very low to nonexistent. Given what is known about the susceptibility of swans to H5N1, and on the basis of the chronology and rates of whooper swan migration movements, we conclude that although there is broad spatial overlap between whooper swan distributions and H5N1 outbreak locations in eastern Asia, the likelihood of direct transmission between these groups is extremely low. Thus, our data support the hypothesis that swans are best viewed as sentinel species, and moreover, that in eastern Asia, it is most likely that their infections occurred through contact with asymptomatic migratory hosts (e.g., wild ducks) at or near their breeding grounds.     

Lower richness of small wild mammal species and chagas disease risk

A new epidemiological scenario involving the oral transmission of Chagas disease, mainly in the Amazon basin, requires innovative control measures. Geospatial analyses of the Trypanosoma cruzi transmission cycle in the wild mammals have been scarce. We applied interpolation and map algebra methods to evaluate mammalian fauna variables related to small wild mammals and the T. cruzi infection pattern in dogs to identify hotspot areas of transmission. We also evaluated the use of dogs as sentinels of epidemiological risk of Chagas disease. Dogs (n = 649) were examined by two parasitological and three distinct serological assays. kDNA amplification was performed in patent infections, although the infection was mainly sub-patent in dogs. The distribution of T. cruzi infection in dogs was not homogeneous, ranging from 11–89% in different localities. The interpolation method and map algebra were employed to test the associations between the lower richness in mammal species and the risk of exposure of dogs to T. cruzi infection. Geospatial analysis indicated that the reduction of the mammal fauna (richness and abundance) was associated with higher parasitemia in small wild mammals and higher exposure of dogs to infection. A Generalized Linear Model (GLM) demonstrated that species richness and positive hemocultures in wild mammals were associated with T. cruzi infection in dogs. Domestic canine infection rates differed significantly between areas with and without Chagas disease outbreaks (Chi-squared test). Geospatial analysis by interpolation and map algebra methods proved to be a powerful tool in the evaluation of areas of T. cruzi transmission. Dog infection was shown to not only be an efficient indicator of reduction of wild mammalian fauna richness but to also act as a signal for the presence of small wild mammals with high parasitemia. The lower richness of small mammal species is discussed as a risk factor for the re-emergence of Chagas disease.     

Safety of lyophilized SAG2 oral rabies vaccine in collared lemmings

Fifteen collared lemmings (Dicrostonyx groenlandicus) were exposed to a lyophilized oral rabies vaccine designed to immunize wild carnivore populations. No animals contracted rabies from the vaccine as determined by the absence of clinical signs after 37 days and lack of rabies virus in brain tissue determined by the fluorescent antibody (FA) test. These results suggest that collared lemmings would not contract rabies if they ingested this lyophilized vaccine in the wild during bait vaccination programs for arctic foxes (Alopex lagopus).