Joaquín Vicente

Diseases shared between wildlife and livestock: a European perspective

Wildlife diseases are in fashion. This is creating an explosion of related knowledge. Despite this, the dynamics of both wildlife and diseases and the changes in livestock and wildlife management make it increasingly difficult to overview the current situation of wildlife diseases in Europe. This paper aims to discuss the available management possibilities and to highlight current research priorities. One area that causes severe concern to authorities is diseases largely under control in domestic populations but still existing as a reservoir in wildlife. Multihost situations are also of concern for wildlife management and conservation, as diseases can affect the productivity and density of wildlife populations with an economic or recreational value. Concern about emerging diseases is rising in recent years, and these may well occur at the fertile livestock–wildlife interface. Wildlife-related zoonoses are a diverse and complex issue that requires a close collaboration between wildlife ecologists, veterinarians and public health professionals. A few risk factors can be identified in most of the relevant wildlife diseases. Among them are (1) the introduction of diseases through movements or translocations of wild or domestic animals, (2) the consequences of wildlife overabundance, (3) the risks of open air livestock breeding, (4) vector expansion and (5) the expansion or introduction of hosts. Wildlife disease control requires the integration of veterinary, ecology and wildlife management expertise. In addition to surveillance, attempts to control wildlife diseases or to avoid disease transmission between wildlife and livestock have been based on setting up barriers, culling, hygienic measures, habitat management, vector control, treatments and vaccination. Surveillance and descriptive studies are still valuable in regions, species or diseases that have received less attention or are (at least apparently) emerging. Nonetheless, limiting the research effort to the mere reporting of wildlife disease outbreaks is of limited value if management recommendations are not given at the same time. Thus, more experimental approaches are needed to produce substantial knowledge that enables authorities to make targeted management recommendations. This requires policy makers to be more aware of the value of science and to provide extra-funding for the establishment of multidisciplinary scientific teams.

Disease risks and overabundance of game species

Different studies have evidenced the relationship between host abundance and health status of wildlife populations. Diseases that benefit from wildlife overabundance can affect not only the fitness and trophy quality of game species, but also public health, livestock health, and the conservation of endangered species. This paper reviews a number of European examples to highlight the relationship between overabundance and disease in game species, and discusses the possibilities of limiting the associated risks. Management tools to estimate overabundance are needed for legislative purposes and for the monitoring of wildlife populations, but artificial feeding interferes in the objective measurement of overabundance. Therefore, we propose a multidisciplinary approach to diagnose if a given wildlife population is overabundant. This includes not only signs such as adverse effects on the soil, vegetation or fauna (first group), poor body condition scores, low trophy scores or low reproductive performance (second group), or increased parasite burdens (third group), but also the measurement of infectious disease prevalences (the fourth group of overabundance signs). This combined assessment of overabundance ideally requires the cooperation of wildlife managers, botanists, and veterinarians. Once a given wildlife population is defined as overabundant, it is difficult to establish palliative management actions. These can consist in banning certain management tools (e.g. feeding) or increasing the hunting harvest, but both of them are difficult to implement in practice. A close monitoring of both wildlife densities and wildlife diseases, the establishment of reference values for all signs of overabundance, and the mapping of the disease and density hotspots will be needed to design adequate risk-control measures for each particular situation.

Estimation of European wild boar relative abundance and aggregation: a novel method in epidemiological risk assessment

Wild boars are important disease reservoirs. It is well known that abundance estimates are needed in wildlife epidemiology, but the expense and effort required to obtain them is prohibitive. We evaluated a simple method based on the frequency of faecal droppings found on transects (FBII), and developed a spatial aggregation index, based on the runs test statistic. Estimates were compared with hunting data, and with porcine circovirus and Aujeszkys disease virus seroprevalences and Mycobacterium tuberculosis complex and Metastrongylus spp. prevalence. The FBII and the aggregation index were correlated with the hunting index, but both of the former estimates correlated better than the latter with the disease prevalences. Hence, at least in habitats with high wild boar densities, the FBII combined with the aggregation index constitutes a cheap and reliable alternative for wild boar abundance estimation that can be used for epidemiological risk assessment, even outside the hunting season and in areas with no available data on hunting activities.

Bovine Tuberculosis in Doñana Biosphere Reserve: The Role of Wild Ungulates as Disease Reservoirs in the Last Iberian Lynx Strongholds

Doñana National Park (DNP) in southern Spain is a UNESCO Biosphere Reserve where commercial hunting and wildlife artificial feeding do not take place and traditional cattle husbandry still exists. Herein, we hypothesized that Mycobacterium bovis infection prevalence in wild ungulates will depend on host ecology and that variation in prevalence will reflect variation in the interaction between hosts and environmental risk factors. Cattle bTB reactor rates increased in DNP despite compulsory testing and culling of infected animals. In this study, 124 European wild boar, 95 red deer, and 97 fallow deer were sampled from April 2006 to April 2007 and analyzed for M. bovis infection. Modelling and GIS were used to identify risk factors and intra and inter-species relationships. Infection with M. bovis was confirmed in 65 (52.4%) wild boar, 26 (27.4%) red deer and 18 (18.5%) fallow deer. In the absence of cattle, wild boar M. bovis prevalence reached 92.3% in the northern third of DNP. Wild boar showed more than twice prevalence than that in deer (p<0.001). Modelling revealed that M. bovis prevalence decreased from North to South in wild boar (p<0.001) and red deer (p<0.01), whereas no spatial pattern was evidenced for fallow deer. Infection risk in wild boar was dependent on wild boar M. bovis prevalence in the buffer area containing interacting individuals (p<0.01). The prevalence recorded in this study is among the highest reported in wildlife. Remarkably, this high prevalence occurs in the absence of wildlife artificial feeding, suggesting that a feeding ban alone would have a limited effect on wildlife M. bovis prevalence. In DNP, M. bovis transmission may occur predominantly at the intra-species level due to ecological, behavioural and epidemiological factors. The results of this study allow inferring conclusions on epidemiological bTB risk factors in Mediterranean habitats that are not managed for hunting purposes. Our results support the need to consider wildlife species for the control of bTB in cattle and strongly suggest that bTB may affect animal welfare and conservation.

Genetic resistance to bovine tuberculosis in the Iberian wild boar

Bovine tuberculosis (bTB) is an important re‐emerging zoonotic disease, causing major economic losses and constraining international trade of animals and their products. Despite eradication programmes, some countries continue to encounter outbreaks, mainly due to wildlife acting as primary hosts or reservoirs. While the genetic component of tuberculosis in humans and cattle is well documented, the role of genetic factors as modulators of bTB resistance remains unclear for natural populations. To address this issue, we investigated the relative contribution of host genetic variability to susceptibility to bTB infection and disease progression in wild boars from southern Spain. We found that genetic heterozygosity is an important predictor of bTB, not only modulating resistance to infection but also influencing containment of disease progression in infected individuals. Our results provide further evidence that host genetic variability plays a central role in natural populations. Testing each marker separately reveals evidence of both general and single‐locus associative effects on bTB and several loci reveal high homology to regions of the genome with known immune function. Our results may prove to be crucial for understanding outbreaks of bTB in wildlife that could potentially affect domestic livestock and humans.

Animal-side serologic assay for rapid detection of Mycobacterium bovis infection in multiple species of free-ranging wildlife

Numerous species of mammals are susceptible to Mycobacterium bovis, the causative agent of bovine tuberculosis (TB). Several wildlife hosts have emerged as reservoirs of M. bovis infection for domestic livestock in different countries. In the present study, blood samples were collected from Eurasian badgers (n=1532), white-tailed deer (n=463), brushtail possums (n=129), and wild boar (n=177) for evaluation of antibody responses to M. bovis infection by a lateral-flow rapid test (RT) and multiantigen print immunoassay (MAPIA). Magnitude of the antibody responses and antigen recognition patterns varied among the animals as determined by MAPIA; however, MPB83 was the most commonly recognized antigen for each host studied. Other seroreactive antigens included ESAT-6, CFP10, and MPB70. The agreement of the RT with culture results varied from 74% for possums to 81% for badgers to 90% for wild boar to 97% for white-tailed deer. Small numbers of wild boar and deer exposed to M. avium infection or paratuberculosis, respectively, did not cross-react in the RT, supporting the high specificity of the assay. In deer, whole blood samples reacted similarly to corresponding serum specimens (97% concordance), demonstrating the potential for field application. As previously demonstrated for badgers and deer, antibody responses to M. bovis infection in wild boar were positively associated with advanced disease. Together, these findings suggest that a rapid TB assay such as the RT may provide a useful screening tool for certain wildlife species that may be implicated in the maintenance and transmission of M. bovis infection to domestic livestock.

Antibodies to Selected Viral and Bacterial Pathogens in European Wild Boars from Southcentral Spain

Serum samples from 78 European wild boars (Sus scrofa) harvested during the 1999–2000 hunting season were tested for antibodies to Brucella spp., classical swine fever virus, Erysipelothrix rhusiopathiae, Haemophilus parasuis, Leptospira interrogans serovar pomona, Mycoplasma hyopneumoniae, pseudorabies virus (PRV), porcine parvovirus (PPV), porcine reproductive and respiratory syndrome virus, Salmonella serogroups B, C, and D, Streptococcus suis, and swine influenza virus (SIV) serotypes H1N1 and H3N2. Samples were collected from Sierra Morena and Montes de Toledo in southcentral Spain. Antibodies were detected to PRV (36%), L. interrogans serovar pomona (12%), PPV (10%), E. rhusiopathiae (5%), SIV serotype H1N1 (4%), Salmonella serogroup B (4%), and Salmonella serogroup C (3%). Our results suggest that more research is needed to describe the epidemiology of infectious diseases of Spanish wild boars.

Spatial distribution and risk factors of Brucellosis in Iberian wild ungulates

BackgroundThe role of wildlife as a brucellosis reservoir for humans and domestic livestock remains to be properly established. The aim of this work was to determine the aetiology, apparent prevalence, spatial distribution and risk factors for brucellosis transmission in several Iberian wild ungulates.MethodsA multi-species indirect immunosorbent assay (iELISA) using Brucella S-LPS antigen was developed. In several regions having brucellosis in livestock, individual serum samples were taken between 1999 and 2009 from 2,579 wild bovids, 6,448 wild cervids and4,454 Eurasian wild boar (Sus scrofa), and tested to assess brucellosis apparent prevalence. Strains isolated from wild boar were characterized to identify the presence of markers shared with the strains isolated from domestic pigs.ResultsMean apparent prevalence below 0.5% was identified in chamois (Rupicapra pyrenaica), Iberian wild goat (Capra pyrenaica), and red deer (Cervus elaphus). Roe deer (Capreolus capreolus), fallow deer (Dama dama), mouflon (Ovis aries) and Barbary sheep (Ammotragus lervia) tested were seronegative. Only one red deer and one Iberian wild goat resulted positive in culture, isolating B. abortus biovar 1 and B. melitensis biovar 1, respectively. Apparent prevalence in wild boar ranged from 25% to 46% in the different regions studied, with the highest figures detected in South-Central Spain. The probability of wild boar being positive in the iELISA was also affected by age, age-by-sex interaction, sampling month, and the density of outdoor domestic pigs. A total of 104 bacterial isolates were obtained from wild boar, being all identified as B. suis biovar 2. DNA polymorphisms were similar to those found in domestic pigs.ConclusionsIn conclusion, brucellosis in wild boar is widespread in the Iberian Peninsula, thus representing an important threat for domestic pigs. By contrast, wild ruminants were not identified as a significant brucellosis reservoir for livestock.

Observed Prevalence of Tick‐borne Pathogens in Domestic Animals in Sicily, Italy during 2003–2005

The objective of this study was to characterize the observed prevalence of tick‐borne pathogens (TBP) in domestic animals in Sicily, Italy during 2003–2005. Serological (competitive ELISA and indirect immunofluorescence antibody, n = 3299) and DNA tests (polymerase chain reaction and reverse line blot, n = 2565) were conducted on horse, donkey, cattle, sheep, goat, pig and dog samples. Pathogens analysed included Anaplasma, Ehrlichia, Rickettsia, Babesia and Theileria species, and Coxiella burnetii. The most prevalent TBP were Anaplasma and Babesia species. The results reported herein suggested that cattle could serve as the major reservoir for Babesia and Theileria spp. while for Anaplasma spp. cattle, dogs, sheep and goats may be the most important reservoir species. These results expanded our knowledge about the prevalence of TBP in Sicily and provided information to understand the epidemiology of tick‐borne diseases and may help to implement measures to diagnose, treat and control transmission to humans and animals in this region.

Serologic Tests for Detecting Antibodies against Mycobacterium Bovis and Mycobacterium Avium Subspecies Paratuberculosis in Eurasian Wild Boar (Sus Scrofa Scrofa)

New tools to detect exposure of free-range Eurasian wild boar (Sus scrofa scrofa) to pathogenic mycobacteria would be valuable for improved disease surveillance and wildlife management. Two hundred sera from wild boar of known Mycobacterium bovis infection status were used to evaluate test suitability for the detection of antibodies against M. bovis and Mycobacterium avium subsp. paratuberculosis (or cross-reacting members of the M. avium complex). Two traditional enzyme-linked immunosorbent assays were evaluated using M. bovis purified protein derivative (bPPD) and paratuberculosis protoplasmatic antigen 3 (PPA3) as antigens, respectively, and a new point-of-care test format for bovine tuberculosis (bTB) that uses the innovative dual-path platform (DPP TB) test. The effect of individual factors (sex, age, lesions) on the diagnostic performance of the serologic tests was also determined. Although the DPP had a sensitivity of 89.6% and a specificity of 90.4%, for bPPD, the sensitivity was 79.2% and the specificity 100%. Both tests had a kappa agreement of 0.80. Sixty-five of 68 (95.6%) wild boar sera with antibodies against the PPA3 antigen corresponded to known M. bovis–infected wild boar. Significant differences were not observed in the bPPD and DPP readings among lesion categories or between age classes. A slight sex-related difference in sensitivity toward males in the DPP was found, but it was not detected in the bPPD enzyme-linked immunosorbent assay. The results support the use of antibody-based diagnostic tests for both large-scale and individual bTB testing of Eurasian wild boar and suggest that wild boar cannot be used as sentinels for infections caused by M. avium complex members.