Free-ranging Wild Mammals Research Articles

Seroprevalence to Rabies Virus in Wildlife in Brazil.

Serum samples of 638 free-ranging wild mammals from São Paulo state, Brazil, were tested for neutralizing antibodies against rabies virus by the rapid fluorescent focus inhibition test. Overall seroprevalence was 1.7% among 24 species surveyed, with individuals of six species having positive results indicating exposure to rabies virus.

Noninvasively measured immune responses reflect current parasite infections in a wild carnivore and are linked to longevity.

Host immune defenses are important components of host–parasite interactions that affect the outcome of infection and may have fitness consequences for hosts when increased allocation of resources to immune responses undermines other essential life processes. Research on host–parasite interactions in large free‐ranging wild mammals is currently hampered by a lack of verified noninvasive assays. We successfully adapted existing assays to measure innate and adaptive immune responses produced by the gastrointestinal mucosa in spotted hyena (Crocuta crocuta) feces, including enzyme‐linked immunosorbent assays (ELISAs), to quantify fecal immunoglobulins (total IgA, total IgG) and total fecal O‐linked oligosaccharides (mucin). We investigated the effect of infection load by an energetically costly hookworm (Ancylostoma), parasite richness, host age, sex, year of sampling, and clan membership on immune responses and asked whether high investment in immune responses during early life affects longevity in individually known spotted hyenas in the Serengeti National Park, Tanzania. Fecal concentrations of IgA, IgG, and mucin increased with Ancylostoma egg load and were higher in juveniles than in adults. Females had higher mucin concentrations than males. Juvenile females had higher IgG concentrations than juvenile males, whereas adult females had lower IgG concentrations than adult males. High IgA concentrations during the first year of life were linked to reduced longevity after controlling for age at sampling and Ancylostoma egg load. Our study demonstrates that the use of noninvasive methods can increase knowledge on the complex relationship between gastrointestinal parasites and host local immune responses in wild large mammals and reveal fitness‐relevant effects of these responses.

Genetic diversity of the Nubian ibex in Oman as revealed by mitochondrial DNA.

The Nubian ibex (Capra nubiana) is patchily distributed across parts of Africa and Arabia. In Oman, it is one of the few free-ranging wild mammals found in the central and southern regions. Its population is declining due to habitat degradation, human expansion, poaching and fragmentation. Here, we investigated the population's genetic diversity using mitochondrial DNA (D-loop 186 bp and cytochrome b 487 bp). We found that the Nubian ibex in the southern region of Oman was more diverse (D-loop HD; 0.838) compared with the central region (0.511) and gene flow between them was restricted. We compared the genetic profiles of wild Nubian ibex from Oman with captive ibex. A Bayesian phylogenetic tree showed that wild Nubian ibex form a distinct clade independent from captive animals. This divergence was supported by high mean distances (D-loop 0.126, cytochrome b 0.0528) and high FST statistics (D-loop 0.725, cytochrome b 0.968). These results indicate that captive ibex are highly unlikely to have originated from the wild population in Oman and the considerable divergence suggests that the wild population in Oman should be treated as a distinct taxonomic unit. Further nuclear genetic work will be required to fully elucidate the degree of global taxonomic divergence of Nubian ibex populations.

Zoonotic Bartonella species in Eurasian wolves and other free-ranging wild mammals from Italy.

Bartonellae are emerging vector‐borne pathogens infecting humans, domestic mammals and wildlife. Ninety‐seven red foxes (Vulpes vulpes), 8 European badgers (Meles meles), 6 Eurasian wolves (Canis lupus), 6 European hedgehogs (Erinaceus europaeus), 3 beech martens (Martes foina) and 2 roe deer (Capreolus capreolus) from Italian Nature Conservatory Parks were investigated for Bartonella infection. Several Bartonella species (9.84%; 95% CI: 4.55–15.12), including zoonotic ones, were molecularly detected among wolves (83.3%; 95% CI: 51–100.00), foxes (4.12%; 95% CI: 0.17–8.08), hedgehogs (33.33%; 95% CI: 0.00–71.05) and a roe deer. Bartonella rochalimae was the most common Bartonella species (i.e. in 4 foxes and 2 wolves) detected. Candidatus B. merieuxii and B. vinsonii subsp. berkhoffii were identified for the first time in wolves. Furthermore, Bartonella schoenbuchensis was identified in a roe deer and a new clone with phylogenetic proximity to B. clarridgeiae was detected in European hedgehogs. Zoonotic and other Bartonella species were significantly more frequent in Eurasian wolves (p < .0001), than in other free‐ranging wild mammals, representing a potential reservoir for infection in humans and domestic animals.

Clinical leishmaniosis in a captive Eurasian otter (Lutra lutra) in Spain: a case report

BackgroundCaptive and free-ranging wild mammals have been recognized as potential reservoirs of Leishmania infantum infection. The aim of this study was to describe the first clinical case of leishmaniosis in the Eurasian otter.Case presentationA case of clinical leishmaniosis is reported in a 4-year-old male Eurasian otter housed at a wildlife park (Murcia, South Eastern Spain). The Eurasian otter showed bilateral epistaxis, anorexia, apathy, and weight loss. A complete blood cell count and biochemical analyses revealed hyperproteinemia, hyperglobulinemia, decreases of paraoxonase-1, increases of haptoglobin and ferritin, and proteinuria. Bilateral nephropathy with hydronephrosis, mesenteric lymphadenomegaly, and ascites were also observed. L. infantum infection was confirmed by microscopy (amastigotes were detected in macrophages from spleen aspirate), molecular diagnosis (L. infantum DNA was detected by real-time polymerase chain reaction), and serology (anti-Leishmania IgG2 antibodies were detected by time-resolved immunofluorometry). The animal was treated with allopurinol for 3 months and gained weight, the epistaxis disappeared, and the ferritin concentration decreased.ConclusionsThis is the first report of clinical leishmaniosis in the Eurasian otter. Our results suggest that Eurasian otters are susceptible to infection with L. infantum and can develop clinical leishmaniosis in endemic areas.

Long-Term Safety of Intraperitoneal Radio Transmitter Implants in Brown Bears (Ursus arctos).

Intraperitoneal radio transmitters have been widely used in free-ranging wild mammals, but there are no long-term studies on their biocompatibility or technical stability within the abdominal cavity of animals. Possible negative health effects may bias results from ecological studies on instrumented animals and raise concerns over animal welfare issues. The aim of this study was to evaluate the long-term technical stability and pathological effects of Telonics intraperitoneal very high frequency (VHF) radio transmitters in brown bears (Ursus arctos). We instrumented 305 individual bears with intraperitoneal VHF radio transmitters during a 19-year period. We surgically removed devices that had been in bears for 1–9 years and collected transmitters from animals that died 1–13 years after implantation. We took biopsies for histopathology from tissue encapsulating implants in live bears. Retrieved transmitters underwent a technical inspection. Of the 125 transmitters removed from live bears, 66 were free-floating in the peritoneal cavity [a mean (SD) of 3.8 (1.5) years after implantation], whereas 59 were encapsulated in the greater omentum [4.0 (1.8) years after implantation]. Histopathology of biopsies of the 1–15 mm thick capsules in 33 individuals showed that it consisted of organized layers of connective tissue. In one third of the bears, the inner part of the capsule was characterized by a foreign body reaction. We inspected 68 implants that had been in bears for 3.9 (2.4) years. The batteries had short-circuited four (5.9%) of these devices. This resulted in the death of two animals 10 and 13 years after implantation. In two other bears that underwent surgery, we found the short-circuited devices to be fully encapsulated within the peritoneal cavity 5 and 6 years after implantation. A significant proportion of the other 64 inspected implants showed serious technical problems, such as corrosion of metal parts or the batteries (50%), detachment of the end cap (11.8%), and erosion (7.4%) or melting (5.9%) of the wax coating. We conclude that the wax coating of the transmitters was not biocompatible, that the technical quality of the devices was poor, and that these implants should not be used in brown bears.

Seroprevalence of Mycobacterium avium Complex in Wild Mammals in the Iberian Peninsula

A retrospective serologic survey was conducted for antibodies against MAC in a random sample of 623 free-ranging wild mammals killed on roads and by hunters, or found dead in east-central Portugal. Animals were tested for antibodies to Mycobacterium avium complex with a commercial enzyme linked assay. The seroprevalence of Mycobacterium avium complex infection was 4.7% (n=29; CI 95%: 25.4 - 32.7%). Antibodies against MAC were detected in 4 out of 11 animal species included in this study, consisted of 1/42 red fox (Vulpes vulpes) (2.4%; CI 95%: 0.0-4.0%), 1/6 Eurasian otter (Lutra lutra) (16.7%), 1/3 European badger (Meles meles) (33.3%), and 26/109 wild boar (Sus scrofa) (23.9%; CI 95%: 17.8-34.2%). Infection was found in three taxonomic families: 2.4% (CI 95%: 0.0-4.0%) in Canidae, 16.7% (CI 95%: 0.0-37.8%) in Mustelidae, and 23.9% (CI 95%: 17.8-34.2%) in Suidae. No positive sera were found in the common genet, Egyptian mongoose, beech marten, hedgehog, wild rabbit, red deer or fallow deer. Results of the present study indicate that antibodies against MAC were present in wild carnivores and wild boars in Iberian Peninsula. According to the test sensitivity and specificity claimed by the manufacturer, the true prevalence Mycobacterium avium complex infection among wild mammals in the Iberian Peninsula was calculated to be between 10.7% and 13.6%.

Bartonella species pathogenic for humans infect pets, free-ranging wild mammals and their ectoparasites in the Caatinga biome, Northeastern Brazil: a serological and molecular study

This study verified the occurrence of Bartonella spp. in dogs, cats, wild mammals and their ectoparasites in Petrolina and Lagoa Grande Counties, Pernambuco, located in a semi-arid region in Northeastern Brazil. Anti-Bartonella spp. antibodies were detected by indirect immunofluorescence assay (IFA) in 24.8% of dogs (27/109) and in 15% of cats (6/40). Bartonella sp. DNA was identified by PCR performed on DNA extracted from blood and ectoparasites using primers targeting Bartonella sp. gltA and ribC genes in 100% (9/9) of Pulex irritans from Cerdocyon thous, 57.4% (35/61) of P. irritans from dogs, 2.3% (1/43) of Ctenocephalides felis felis from dogs, 53.3% (24/45) of C. felis felis from cats, and 10% (1/10) of Polyplax spp. from Thrichomys apereoides. DNA sequencing identified Bartonella clarridgeiae and Bartonella henselae in C. felis felis from cats, Bartonella rochalimae in P. irritans from dog and C. thous, and Bartonella vinsoni berkhofii in P. irritans from dog.

Isolation of Escherichia coli and Salmonella spp. from free-ranging wild animals.

Increasing interactions between humans, domestic animals and wildlife may result in inter-species transmission of infectious agents. To evaluate the presence of pathogenic E. coli and Salmonella spp. and to test the antimicrobial susceptibility of isolates, rectal swabs from 36 different free-ranging wild mammals were taken from two distinct natural sites in Brazil: Cantareira State Park (CSP, state of São Paulo) and Santa Isabel do Rio Negro Region (SIRNR, state of Amazonas). The swabs were randomly collected and processed for bacterial isolation, identification, characterization and antimicrobial resistance. Eighteen E. coli strains from CSP and 20 from SIRNR were recovered from 14 and 22 individuals, respectively. Strains from animals captured in CSP, the site with the greatest anthropization, exhibited a higher range and percentage of virulence genes, including an eae+/bfpA+ strain. Antimicrobial resistance was verified in strains originating from both sites; however, in strains from SIRNR, aminopenicillins were almost the exclusive antimicrobial class to which strains exhibited resistance, whereas in CSP there were strains resistant to cephalosporins, sulfonamide, aminoglycoside, tetracycline and fluoroquinolone, in addition to strains exhibiting multidrug resistance. Two strains of Salmonella enterica that are known to be associated with reptiles, serotypes Belem and 60:r:e,n,z15, were recovered only from Amazonian animals and showed susceptibility to all classes of antimicrobials that were tested. Although the potential impact of these pathogens on wildlife remains unknown, bacteria isolated from free-ranging wild animals may provide relevant information about environmental health and should therefore be more deeply studied.

Serological Evidence of Infection by Leishmania (Leishmania) infantum (Synonym: Leishmania (Leishmania) chagasi) in Free-Ranging Wild Mammals in a Nonendemic Region of the State of São Paulo, Brazil.

Concerns about the interface between wildlife, domestic animals, and humans in the transmission of visceral leishmaniasis (VL) have been growing due to natural or anthropogenic environmental changes. In this context, investigations of the infection in wild mammals are important to assess their exposure to the vector and the parasite. A study of anti-Leishmania (Leishmania) infantum antibodies was carried out using the direct agglutination test (DAT) on 528 free-ranging wild mammals of 38 species from the region of Botucatu, state of São Paulo, Brazil, a municipality that has no records of the vector or of human or canine autochthony. Antibodies were detected, with a cutoff of 1:320, in 9/528 (1.7%; 95% confidence interval [CI] 0.6-2.8%) mammals of the species Callithrix jacchus, Lepus europaeus, Sphiggurus villosus, Nasua nasua, Eira barbara, and Galictis cuja, with high titers (≥1280) for the last three. These three are little-studied species, and previous records of the detection of anti-Leishmania spp. antibodies in Brazil exist only for coatis (N. nasua), whereas worldwide, infection by L. (L.) infantum has been confirmed only in hares (Le. europaeus). On the other hand, opossums and canids, the species most commonly reported to be naturally infected by L. (L.) infantum, were not seropositive. Fifty-eight (58/528; 10.9%) mammals were found to have antibody titers ranging from 20 to 160 and were not included among the seropositive animals due to the adopted cutoff. However, the possibility of infection in these animals should not be discarded, because there is no standard cutoff point for the different wild species. Our findings indicate the need for investigations into the exact role of the seropositive species in the epidemiology of VL and for effective epidemiological surveillance to prevent its expansion, because even in regions where there are no records of canine or human autochthonous cases, there may be parasite circulation among wild mammals.

Ticks on free-living wild mammals in Emas National Park, Goias State, central Brazil

This paper reports the occurrence of ticks on different species of free-ranging wild mammals in Emas National Park, Goias State, Brazil. Between November 1999 and July 2008, ticks were collected from free-ranging wild mammals during 330 capture events. The tick species Amblyomma cajennense (Fabricius, 1787), Amblyomma coelebs Neumann, 1899, Amblyomma naponense (Packard, 1869), Amblyomma ovale Koch, 1844, Amblyomma parvum Aragao, 1908, Amblyomma tigrinum Koch, 1844, Amblyomma triste Koch, 1844, and Rhipicephalus microplus (Canestrini, 1888) were identified on hosts of the order Carnivora. Among other host orders (Xenarthra, Artiodactyla, Perissodactyla, Rodentia, Didelphimorphia, Primates), specimens of A. cajennense, A. coelebs, A. ovale, A. triste, Amblyomma pseudoconcolor Aragao, 1908, A. naponense and Amblyomma nodosum Neumann, 1899 were identified. Although most of the tick-host associations found in this study have been previously reported, this is the first report of adults of A. tigrinum parasitizing a pampas cat, Leopardus colocolo (Molina, 1782), nymphs of Amblyomma parvum and Amblyomma ovale on Cerdocyon thous (Linnaeus, 1766), nymphs of Amblyomma naponense on C. thous and Tayassu tajacu (Linnaeus, 1758), nymphs of Amblyomma triste on C. thous and L. colocolo, nymphs of Amblyomma coelebs on Puma yagouaroundi (Geoffroy, 1803) and Dasyprocta azarae Lichtenstein, 1823, and nymphs of Amblyomma cajennense on L. colocolo, Conepatus semistriatus (Boddaert, 1785), Galictis cuja (Molina, 1782) and Nasua nasua (Linnaeus, 1766). This study is therefore a significant contribution to our knowledge of the ectoparasites associated with free-ranging Brazilian wild mammals.

Acute toxic hazard evaluations of glyphosate herbicide on terrestrial vertebrates of the oregon coast range

The degree to which dose responses of model organisms (lab rodents) can adequately predict dose responses of free-ranging wild mammals or amphibians is unknown, and the relative sensitivity of such species to body loading of a toxicant such as glyphosate is seldom reported. For relative effects of dosage, we compare sensitivity of nine wild vertebrate species to effects of high doses of glyphosate in Swiss-Webster laboratory mice both by gavage and by intraperitoneal injection. We also evaluate sublethal effects of herbicide exposure on behavior and reproductive success of one mammal and one amphibian species. Comparisons of acute toxicity of glyphosate were made with intraperitoneal dosings of technical glyphosate isopropylamine salt to nine species of terrestrial vertebrates (five amphibians, four mammals) and compared with responses in Swiss-Webster laboratory mice. Animals collected from sites that had no recent herbicide application were allowed 7-14 days to equilibrate in captivity before treatment. Median lethal dose ranged from 800 to 1,340 mg kg(-1) in mammals, and 1,170 to >2,000 mg kg(-1) in amphibians, with Oregon vole being the most sensitive. White lab mice were in the middle of the mammalian range. Tailed frog, at >2,000 mg kg(-1) was the least sensitive. Calibration of IP sensitivity to oral administration by gavage indicated that roughly four times as much glyphosate must be administered to obtain a comparable estimate of lethality. Administration by gavage in highly concentrated solutions tended to cause physical injury, hence may prove less useful as a relative indicator of toxicity. When sublethal dosages were given to roughskin newts or chipmunks, mobility and use of cover appeared largely unaffected. Direct toxic effects of spraying glyphosate under normal forest management seem unlikely for the nine species examined. Nor could we detect significant indirect effects of exposure on behavior and use of cover features in two species. There may be effects on other aspects of the field biology of these animals, such as reproductive rates, which we did not investigate. Recent field data indicate that changes in habitat quality following herbicide application can result in high reproductive activity in species associated with the grasses and forbs that proliferate following field applications. When compared to field data on body burdens of wild mammals exposed after aerial application of glyphosate at maximum rates in forests, there seems to be a large margin of safety between dosages encountered and those causing either death or limitation of movement, foraging or shelter. Margins of safety for small mammals and amphibians appear to be large under any probable exposure scenarios, however our results indicate high variability in responses among species. Uncertainty introduced into field studies from unknown sources of mortality (e.g, likely predation) must be considered when interpreting our results.

Use of feces to estimate isotopic abundance in doubly labeled water studies in reindeer in summer and winter.

The reliance on samples of blood or urine to estimate isotopic abundance in studies of energy metabolism using the doubly labeled water method has restricted application of the technique to animals that are either tame or easy to catch. This is generally not the case with large, free-ranging wild mammals. The use of feces as a source of body water in which to measure the concentration of isotopic markers was investigated in four female reindeer in summer and in winter. (2)H2O and H2(18)O were injected to approximately 160 parts per million excess. Samples of plasma and feces were then collected simultaneously for up to 456 h. Both isotopes were equilibrated with body water at 8 h postdose. There were no significant differences by animal between dilution spaces, rate constants, rates of CO2 production, and total energy expenditure (TEE) calculated based on samples of plasma or feces in any trial. Mean TEE was 3.557 W/kg (SD 0.907, n = 4) in summer and 1.865 W/kg (SD 0.166, n = 4) in winter.

The efficacy of anthelmintic treatment on the parasite abundance of free-ranging snowshoe hares

We examined the efficacy of an anthelmintic agent (ivermectin, Merck–Agvet) on the parasitic nematodes of free-ranging snowshoe hares (Lepus americanus) during 27 months in southern Manitoba. Marked hares on six 25-ha sites were injected bimonthly with ivermectin (treatment, n = 134) or propylene glycol (control; n = 149) and carcasses were necropsied to determine prevalence and intensity of Obeliscoides cuniculi, Nematodirus triangularis, Trichuris leporis, Dirofilaria scapiceps, and Protostrongylus boughtoni. We supplemented the control sample with hares (n = 175) captured off the study sites and not given propylene glycol. Mean prevalence (percentage of hosts infected) and intensity (number of parasites among infected hosts) of each nematode species decreased after treatment and were 35 – 85% lower than controls after 20–40 days. Treatment significantly reduced prevalence of D. scapiceps and P. boughtoni for about 50 days and of O. cuniculi and N. triangularis for longer periods. Overall intensity of O. cuniculi, N. triangularis, and P. boughtoni was significantly lower in treated than in control hares, and intensity of D. scapiceps was marginally (P &lt; 0.10) lower for 50 days post treatment. Total reductions in nematode abundance (prevalence × intensity) ranged from 29 to 88% among the five species. Neither prevalence nor intensity of ticks (Haemaphysalis leporispalustris) was reduced following treatment. We conclude that ivermectin is effective at controlling nematodes in snowshoe hares but that its efficacy is variable among species. We use our results as a basis for discussing the applicability of anthelmintics to the conservation and management of free-ranging wild mammals.