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.     

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.     

Distemper-like disease and encephalitozoonosis in wild dogs (Lycaon pictus)

Clinical signs of a fatal disease resembling those of canine distemper were observed in two groups of captive wild dog (Lycaon pictus) pups 13 days after vaccination with a commercially available combination vaccine for dogs which contained a live attenuated strain of canine distemper virus. Histopathological examination of tissues revealed the presence of intranuclear inclusion bodies in neurons and lesions resembling canine distemper as well as colonies of an Encephalitozoon sp. in the central nervous system and kidneys. Lesions were observed in both organs which resembled those described in other species infected with Encephalitozoon cuniculi.     

Inbreeding avoidance influences the viability of reintroduced populations of African wild dogs (Lycaon pictus)

The conservation of many fragmented and small populations of endangered African wild dogs (Lycaon pictus) relies on understanding the natural processes affecting genetic diversity, demographics, and future viability. We used extensive behavioural, life-history, and genetic data from reintroduced African wild dogs in South Africa to (1) test for inbreeding avoidance via mate selection and (2) model the potential consequences of avoidance on population persistence. Results suggested that wild dogs avoided mating with kin. Inbreeding was rare in natal packs, after reproductive vacancies, and between sibling cohorts (observed on 0.8%, 12.5%, and 3.8% of occasions, respectively). Only one of the six (16.7%) breeding pairs confirmed as third-order (or closer) kin consisted of animals that were familiar with each other, while no other paired individuals had any prior association. Computer-simulated populations allowed to experience inbreeding had only a 1.6% probability of extinction within 100 years, whereas all populations avoiding incestuous matings became extinct due to the absence of unrelated mates. Populations that avoided mating with first-order relatives became extinct after 63 years compared with persistence of 37 and 19 years for those also prevented from second-order and third-order matings, respectively. Although stronger inbreeding avoidance maintains significantly more genetic variation, our results demonstrate the potentially severe demographic impacts of reduced numbers of suitable mates on the future viability of small, isolated wild dog populations. The rapid rate of population decline suggests that extinction may occur before inbreeding depression is observed.     

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.     

A baiting system for delivery of an oral plague vaccine to black-tailed prairie dogs

Laboratory and field studies were conducted between July and October 1999 to identify bait preference, biomarker efficacy, and bait acceptance rates for delivering an oral plague vaccine to black-tailed prairie dogs (Cynomys ludovicianus). Twenty juvenile captive prairie dogs were offered alfalfa baits containing either alfalfa, alfalfa and 5% molasses, or alfalfa, 5% molasses and 4% salt. Based on the results of these trials we selected a bait containing alfalfa, 7% molasses, and 1% salt for field trials to determine bait acceptance rates by free-ranging animals. The biomarkers DuPont Blue dye, iophenoxic acid, and tetracycline hydrochloride were orally administered to captive prairie dogs to determine their efficacy. Only tetracycline proved effective as a biomarker. Two field trials were conducted at separate prairie dog colonies located at the Buffalo Gap National Grassland (Pennington County, South Dakota, USA). In Trial 1, three baits containing tetracycline were distributed around each active burrow entrance and an additional bait was placed inside the burrow (1,276 baits total). In Trial 2, baits were distributed at the same density per burrow as Trial 1, but along transects spaced 10 m apart (1,744 baits total). Trapping began 3 days after bait distribution, and 30 prairie dogs then were captured at each site to determine the percentage of animals marked. In Trial 1, 67% of the prairie dogs captured had tetracycline deposits indicative of bait consumption. In Trial 2, 83% of the prairie dogs had ingested a bait. Approximately 15% of the animals in both trials ate more than one bait. Fleas (Opisocrostis hirsutus) were found on 64 of 70 (91%) of the prairie dogs captured during this study.     

Prerequisites for oral immunization of free-ranging raccoons (Procyon lotor) with a recombinant rabies virus vaccine: study site ecology and bait system development.

A model baiting system suitable for the delivery of an oral rabies vaccine to free-ranging raccoons (Procyon lotor) was developed and tested on barrier islands in South Carolina (USA). Features of barrier island physiography and ecology were studied relative to selective bait deployment and site biosecurity. Capture-mark-recapture data were obtained from 228 raccoons. Raccoon density estimates, using a modified census assessment technique, were one raccoon per 1.8 to 2.7 ha. Mean (+/- SE) and range home area estimates of radio-collared raccoons were 84 (+/- 15.6) ha (27 to 176 ha) by a minimum convex polygon method and 138 (+/- 22.8) ha (43 to 241 ha), by a harmonic mean transformation method. Habitat utilization determinations of radio-collared raccoons were conducted to identify study areas to potentially maximize selectivity of bait towards raccoons and to reduce the absolute number of baits deployed. Island raccoons showed a habitat preference for maritime forest, maritime shrub and marsh areas. Additionally, there was no evidence of inter-island or mainland exchange of ear-tagged or radio-collared raccoons. A disease and mortality survey was conducted to identify baseline pathology and incidental lesions in the target raccoon population, prior to actual vaccination initiation. Thirty-eight percent of 30 clinically suspect raccoons sampled had intracytoplasmic eosinophilic inclusions diagnostic of canine distemper; no other lesions suggestive of viral etiologies were found. Serological surveys for raccoon poxvirus and rabies virus antibodies were negative. Antibody titers to canine adenovirus 1 and 2 indicated a moderate level of exposure (approximately 10 to 16%) in the raccoon population. Overall, 93 to 100% of placebo baits were consistently disturbed by 7 days post-bait deployment, and bait acceptance rates by raccoons ranged from 49 to 85%, by using a modular systems approach to select the optimum combination of bait attractant, biomarker, matrix, density, and distribution. These results suggest that a large proportion (up to 85%) of a free-ranging island raccoon population can be selectively and safely targeted, marked and monitored utilizing a proposed oral bait delivery system for recombinant or other rabies vaccines.     

Evolutionary ecology meets wildlife management: artificial group augmentation in the re-introduction of endangered African wild dogs (Lycaon pictus)

As an alternative to kin selection, group augmentation theory provides a framework for evolutionary mechanisms maintaining cooperative breeding when individual fitness is positively related to group size. It is expected that a cooperator group would accept or adopt unrelated foreigners when it is below a critical threshold size and group members could thus benefit from recruiting additional helpers. In re-introduction attempts, this would allow for a group to be augmented artificially before release, which would enhance its chance to establish itself successfully in the release area. This possibility was tested using endangered African wild dogs Lycaon pictus studied in Hluhluwe-iMfolozi Park, South Africa. Here, we report on the first successful artificial integration of an unrelated adult female with her three male pups into an existing pack. In addition, post-release monitoring data are presented, including how a yearling male displaced the dominant male that adopted him as a pup, adding to the controversy over the evolutionary stability of group augmentation as a route to cooperative breeding. This study thus demonstrates how theory from evolutionary ecology can be applied to practical wildlife management, and vice versa.     

Steroid metabolism and validation of noninvasive endocrine monitoring in the African wild dog (Lycaon pictus)

The purpose of this study was to validate noninvasive endocrine monitoring techniques for African wild dogs (Lycaon pictus) and to establish physiological validity of these methods by evaluating longitudinal reproductive-endocrine profiles in captive individuals. To determine the primary excretory by-products of ovarian steroid metabolism, [¹⁴C]-progesterone and [³H]-estradiol were co-administered to a female and all excreta were collected for 80 hr postinjection. Radiolabel excretion peaked ≤ 18 hr postinfusion, and progesterone and estradiol metabolites were excreted in almost equivalent proportions in urine (39.7 and 41.1%, respectively) and feces (60.3 and 58.9%, respectively). Most of the urinary metabolites were conjugated (estradiol, 94.3 ± 0.3%; progesterone, 90.4 ± 0.5%), so that immunoassays for pregnanediol-3α-glucuronide (PdG) and estrogen conjugates (EC) were effective for assessing steroid metabolites. Two immunoreactive estrogens (estradiol and estrone) and at least one immunoreactive progesterone metabolite (3α-hydroxy-5α, pregnan-20-one) were detected in feces. Urine and fecal samples were collected (1–3 times per week) for 1.5 yr from one adult female and two adult males to assess longitudinal steroid metabolite excretion. Overall correlation of urinary PdG to matched, same-day fecal progesterone metabolites immunoreactivity was 0.38 (n = 71, P < 0.05). Similarly, urinary EC was correlated (P < 0.05) with same-day fecal estrogen immunoreactivity (r = 0.49, n = 71). During pregnancy and nonpregnant cycles, copulation occurred at the time of peak (or declining) estrogen metabolites and increasing progesterone metabolites concentrations. Estrus duration was 6–9 days and gestation lasted 69 days with parturition occurring coincident with a drop in progesterone metabolites. Males exhibited seasonal trends in fecal testosterone excretion with maximal concentrations from July to September coincident with peak mating activity. Although these limited longitudinal hormone profiles should be interpreted cautiously, noninvasive gonadal steroid monitoring suggests that: (1) both female and male wild dogs may exhibit reproductive seasonality in North America, (2) females are monoestrous, and (3) peak testicular activity occurs between August and October coincident with mating behavior. From a conservation perspective, noninvasive endocrine monitoring techniques should be useful for augmenting captive breeding programs, as well as for developing an improved understanding of the physiological mechanisms underlying reproductive suppression in response to social and ecological pressures. Zoo Biol 16:533–548, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Bait delivery for oral rabies vaccine to gray foxes

Rabies is a widespread zoonotic disease that has reached epizootic proportions in gray foxes (Urocyon cinereoargenteus) in central Texas. Because each species of carnivore has different food preferences and foraging strategies, it is essential that the efficacy of a bait delivery program be examined for gray foxes prior to an oral vaccination program being attempted. Field trials were conducted to determine bait preferences of free-ranging gray foxes to selected baits and odor attractants. Baits consisted of polymer cubes made of either dog food meal or fish meal, and a wax-lard cake that was enhanced with marshmallow flavoring. Attractants added to baits exuded sulfurous, fatty, cheesy, or sweet odors and flavors. During 3,589 operable bait station nights, gray fox visitation and bait uptake rates were 9.2% and 8.3%, respectively. Gray foxes exhibited no preference in bait uptake rates between bait and odor attractant combinations. Gray foxes exhibited no difference in cumulative bait uptake rates between onroad and offroad sites; however, the uptake rate by raccoons was significantly greater for baits placed on roads than for baits randomly placed. Raccoons were the major non-target species competing for baits, being attributed with 73% of the total uptake. Visitation and bait uptake rates by raccoons significantly increased after a 7-day lethal removal of raccoons (n = 37) from the study area. Random distribution of baits is recommended; it reduced bait uptake by non-target species without adversely affecting uptake by gray foxes.     

A new flavor-coated sachet bait for delivering oral rabies vaccine to raccoons and coyotes

Research was conducted during 1996-2000 to develop baits for delivering an oral rabies vaccine to raccoons (Procyon lotor) and coyotes (Canis latrans). A bait was sought that: (1) was attractive to the target species, (2) could be distributed by aircraft, (3) was as effective (or more so) than the currently used fish meal polymer bait, and (4) could be produced in large numbers by automated procedures and could be purchased by user groups at substantially lower cost. Ten field trials were conducted to document raccoons' bait flavor preferences, evaluate a new vaccine sachet bait coated with various attractants, and determine if the sachet bait would effectively deliver Raboral V-RG oral rabies vaccine (Merial Limited, Athens, Georgia, USA) to this species. Raccoons preferred fish and crustacean-based flavors over those derived from plant materials. Raccoon visits to tracking stations, frequency of bait removals, and percent of sachets discarded by this species that were emptied of placebo vaccine indicated efficacy of the new bait was equal or superior to the currently used fish meal polymer bait. A field trial conducted in fall 1998 compared aerially distributed vaccine-laden sachet and polymer baits and showed there was no difference between the percent of raccoons from the test and reference areas subsequently found positive for rabies antibody. Four bait trials to determine coyote response to sachet baits were conducted in 1997-98. The propensity for canids to gulp or bolt smaller food items is well known. Thus, a first trial involved offering fish-flavored sachet baits of different sizes to 30 captive coyotes to determine if smaller size baits were more frequently swallowed intact. Two field trials were also conducted in fall 1997 to determine if free-ranging coyotes discriminated among sachet baits coated with different attractants. Finally, Raboral V-RG-laden poultry-flavored sachet baits were aerially dropped and the percent of seropositive coyotes was compared with coyotes from surrounding areas where fish meal polymer vaccine baits had been distributed. Captive coyotes did not swallow sachet baits intact, regardless of size. Bait preference field trials indicated that coyotes preferred poultry, cheese/beef tallow, and fish-flavored sachet baits and that such baits were taken at the same rate as polymer baits. A sample of coyotes from the area baited with vaccine-laden sachet baits had a markedly higher (P = 0.01) seropositivity rate than coyotes from areas where vaccine was distributed in polymer baits. Sachet bait production could be facilitated by automated technology and sachet baits used either as an alternative vaccine delivery device or in combination with the fish meal polymer bait.