Does body growth impair immune function in a large herbivore?

According to the principle of allocation, trade-offs are inevitable when resources allocated to one biological function are no longer available for other functions. Growth, and to a lesser extent, immunity are energetically costly functions that may compete with allocation to reproductive success and survival. However, whether high allocation to growth impairs immune system development during the growing period or immune system performance during adulthood is currently unknown in wild mammals. Using three roe deer (Capreolus capreolus) populations experiencing contrasting environmental conditions, we tested for potential costs of growth on immune phenotype over both the short-term (during growth), and the long-term (during adulthood) over the course of an individuals' life. We investigated potential costs on a set of 12 immune traits that reflect both innate and adaptive responses, and compared them between sexes and populations. Although fast growth tended to be associated with low levels of some humoral traits (globulins) during the growing period and some cellular immune traits (i.e. eosinophil and neutrophil counts) during adulthood, evidence for a trade-off between growth and other immune components was limited. Unexpectedly, no detectable growth costs on immunity were found in females from the population experiencing the least favourable environment. We discuss our findings in the light of the complex interplay between resource allocation strategies among reproduction, maintenance and immunity, in relation to local environmental conditions experienced by roe deer.

Immunosenescence patterns differ between populations but not between sexes in a long-lived mammal.

In animals, physiological mechanisms underlying reproductive and actuarial senescence remain poorly understood. Immunosenescence, the decline in the ability to display an efficient immune response with increasing age, is likely to influence both reproductive and actuarial senescence through increased risk of disease. Evidence for such a link has been reported from laboratory animal models but has been poorly investigated in the wild, where variation in resource acquisitions usually drives life-history trade-offs. We investigated immunosenescence patterns over 7 years in both sexes of two contrasting roe deer populations (Capreolus capreolus). We first measured twelve immune markers to obtain a thorough identification of innate and adaptive components of immunity and assessed, from the same individuals, the age-dependent variation observed in parasitic infections. Although the level of innate traits was maintained at old age, the functional innate immune traits declined with increasing age in one of two populations. In both populations, the production of inflammatory markers increased with advancing age. Finally, the adaptive response declined in late adulthood. The increasing parasite burden with age we reported suggests the effective existence of immunosenescence. Age-specific patterns differed between populations but not between sexes, which indicate that habitat quality could shape age-dependent immune phenotype in the wild.

Exposure of Wildlife to the Schmallenberg Virus in France (2011-2014): Higher, Faster, Stronger (than Bluetongue)!

The Schmallenberg virus (SBV) has recently emerged in Europe, causing losses to the domestic livestock. A retrospective analysis of serodata was conducted in France for estimating seroprevalence of SBV among six wildlife species from 2011-2012 to 2013-2014, that is during the three vector seasons after the emergence of the SBV in France. Our objective was to quantify the exposure of wildlife to SBV and the potential protective effect of elevation such as previously observed for bluetongue. We also compared the spatiotemporal trends between domestic and wild animals at the level of the departments. We tested 2050 sera using competitive ELISA tests. Individual and population risk factors were further tested using general linear models among 1934 individuals. All populations but one exhibited positive results, seroprevalence up to 30% being observed for all species. The average seroprevalence did not differ between species but ranged from 0 to 90% according to the area and period, due to the dynamic pattern of infection. Seroprevalence was on average higher in the lowlands compared to areas located up to 800 m. Nevertheless, seroprevalence above 50% occurred in areas located up to 1500 m. Thus, contrary to what had been observed for bluetongue during the late 2000s in the same areas, SBV could spread to high altitudes and infect all the studied species. The spatial spread of SBV in wildlife did not fully match with SBV outbreaks reported in the domestic livestock. The mismatch was most obvious in mountainous areas where outbreaks in wildlife occurred on average one year after the peak of congenital cases in livestock. These results suggest a much larger spread and vector capacity for SBV than for bluetongue virus in natural areas. Potential consequences for wildlife dynamics are discussed.

Haematological parameters do senesce in the wild: evidence from different populations of a long-lived mammal.

Increasing evidence of senescence has been reported from long-term studies of wild populations. However, most studies have focused on life-history traits like survival, reproduction or body mass, generally from a single intensively monitored population. However, variation in the intensity of senescence across populations, and to a lesser extent between sexes, is still poorly understood. In addition, the pattern of age-specific changes in haematological parameters remains virtually unknown to date for any population of vertebrate living in the wild. Using repeated blood samples collected from known-aged (2-15 years of age) roe deer (Capreolus capreolus) from two populations facing highly different environmental conditions, we filled the gap. In particular, we investigated age-specific changes in haematocrit, albumin and creatinine. We reported clear evidence of senescence in all haematological parameters. Moreover, senescence patterns differed between sexes and populations. The rate of senescence was higher in males than in females for haematocrit with no site difference. On the other hand, the rate of senescence in creatinine was higher at Trois Fontaines than at Chizé with no sex difference. Our findings provide a first demonstration of age-specific declines in haematological parameters in wild populations of large herbivores and show that the process of senescence in vertebrates is not restricted to body mass or fitness components. We also demonstrate that the senescence pattern of haematological parameters is context dependent and varies both between sexes and according to environmental conditions.

A comparison of the physiological status in parasitized roe deer (Capreolus capreolus) from two different populations.

Studies of the impact of parasites on host performance have mainly focused on body mass, a phenotypic trait that responds relatively slowly to the presence of parasites, and the expectedly faster response of physiological parameters has been mostly overlooked. We filled the gap by measuring the impact of endoparasites on four hematological/biochemical parameters (hematocrit, albumin, creatinine and fructosamine) in two contrasting free-living populations of roe deer. We generally found negative relationships between parasites and physiological parameters. Our findings also indicate little role of host sex on parasite impact and strongest parasite effects on young and senescent hosts.

Sustainable control of zoonotic pathogens in wildlife: how to be fair to wild animals?

Wildlife may harbour infectious pathogens that are of zoonotic concern. However, culling such reservoir populations to mitigate or control the transmission of these pathogens to humans has proved disappointingly inefficient. Alternatives are still in an experimental stage of development. They include vaccination, medication, contraception and environmental manipulation, including fencing and biosecurity measures. This review examines the general concepts involved in the control of wildlife diseases and presents relevant case studies. Since wildlife disease control inevitably involves interfering with wildlife ecology, this is a complex goal whose attempts at realisation should be supervised by a scientific organisation. Most approaches within natural ecosystems should first be carefully tested in trials that are progressively extended to a larger scale. Finally, all measures that aim to prevent infection in humans (such as personal hygiene or vaccination) or that encourage us to avoid infectious contacts with wildlife should be recommended.

Transmission dynamics of Toxoplasma gondii along an urban-rural gradient.

Recently, several authors have proposed that the availability of intermediate hosts (IHs) for definitive hosts (DHs) may contribute to determining the dynamics and evolutionary ecology of parasites with facultative complex life cycles. The protozoa Toxoplasma gondii may be transmitted to DHs either via predation of infected IHs through a complex life cycle (CLC) or directly from a contaminated environment through a simple life cycle (SLC). This parasite is also present in contrasting host density environments. We tested the hypothesis that the relative contributions of the CLC and SLC along an urban-rural gradient depend on the IH supply. We built and analysed a deterministic model of the T. gondii transmission cycle. The SLC relative contribution is important only in urban-type environments, i.e., with low predation rate on IHs. In contrast, the parasite is predominantly transmitted through a CLC in suburban and rural environments. The association of the two cycles enables the parasite to spread in situations of low IH availability and low DH population size for which each cycle alone is insufficient.

Epidemiological survey of trichinellosis in wild boar (Sus scrofa) and fox (Vulpes vulpes) in a French insular region, Corsica.

The Mediterranean island of Corsica was considered Trichinella-free until 2004, when T. britovi larvae were discovered in domestic pigs at meat inspection. One red fox was also found infected the same year and in the same area than the infected pigs. This last finding highlighted the presence of trichinellosis in Corsican wildlife. A Trichinella survey was thus performed in wild boar (Sus scrofa) and fox (Vulpes vulpes), the two large wild species present on the island, to determine prevalence of muscle larvae and antibodies. Diaphragm muscles of 1881 wild boars and 74 forelegs of foxes were tested by artificial digestion. No Trichinella larva was identified. The highly sensitive ELISA was used to test muscle fluid samples of 1492 wild boars. The apparent serological prevalence of Trichinella infections in wild boar was 2.01% (95% CI: 1.36-2.86). The present results suggest that wildlife is currently exposed to Trichinella in Corsica. In this context, adequate cooking and veterinary controls of meat offer the only complete sanitary warranties to consumers.

Molecular and biological characteristics of Toxoplasma gondii isolates from wildlife in France.

Toxoplasma gondii isolates have been classified into 3 genetic types. Little is known about genotypes of T. gondii isolates in wild animals in Europe. In this report, genotypes of T. gondii isolates from wildlife in France are described. Sera from wildlife were tested for antibodies to T. gondii with the modified agglutination test, and the hearts from animals with titers superior or equal to 1:6 were bioassayed individually in mice. T.gondii was isolated from 9 of 14 seropositive red foxes (Vulpes vulpes), 12 of 33 roe deer (Capreolus capreolus), 1 of 4 deer (Cervus elaphus), 1 of 7 mouflons (Ovis gmelini musimon) and 1 of 2 common mallards (Anas platyrhynchos). No isolate was obtained by bioassay in mice of 1 fallow deer (Dama dama) and of 3 European brown hares (Lepus europaeus). Genotyping of the 24 isolates using PCR-RFLP and microsatellite markers indicated that all were type II and none of these Toxoplasma isolates was virulent for mice.

Seroprevalence and factors associated with Toxoplasma gondii infection in wild boar ( Sus scrofa) in a Mediterranean island.

Knowledge of the factors affecting the presence of Toxoplasma gondii in wildlife is limited. Here we analyse which local landscape characteristics are associated with the presence of toxoplasmosis in wild boar, Sus scrofa, on the island of Corsica, France. Meat juice samples from 1399 wild boars collected during two hunting seasons were tested for T. gondii antibodies using the modified agglutination test (titre 1:4). The overall seroprevalence was 0.55 (95% CI 0.50-0.59) for the first year and 0.33 (95% CI 0.29-0.35) for the second year. Seroprevalence varied according to age and county. At the county level, seropositivity in adults was related to farm density during year 1, and to habitat fragmentation, farm density and altitude during year 2. The exposure of wild boar to T. gondii is thus variable according to landscape characteristics and probably results in a variable risk of transmission of toxoplasmosis to humans.

Flock management and histomoniasis in free-range turkeys in France: description and search for potential risk factors.

The relationship between flock management and histomoniasis, a re-emergent infection in poultry, was investigated by statistical techniques used in veterinary epidemiology to deal with various problems including: multicollinearity, confounding, interaction or sample size. Associations between the variables describing flock management were examined by multivariate descriptive analysis to reduce the number of independent variables, prior to investigating associations with the disease. No homogenous groups of farms were found in the 44 free-range turkey flocks sampled in France. Histomonas meleagridis was identified in 26/38 flocks and histomoniasis was confirmed in 19 flocks. Cleanliness of the building, wet litter and diarrhoea were linked with H. meleagridis and severity of histomoniasis. Sharing outdoor fields simultaneously with chickens was related to serious macroscopic lesions determined by post-mortem examinations. Contrary to general belief, acidification of drinking water with organic acid had consistent association with the presence of H. meleagridis in turkey caeca. These results confirm previous findings and provide several new hypotheses on the effects of hygiene and water management on H. meleagridis and histomoniasis.

Local meteorological conditions, dynamics of seroconversion to Toxoplasma gondii in cats (Felis catus) and oocyst burden in a rural environment.

The aim of this study was to analyse the spatio-temporal dynamics of Toxoplasma gondii infection in long-term monitoring of domestic cats (8-15 years) in three populations living in rural France. Overall seroprevalence was 52.7% (modified agglutination test > or =1:40). Incidence was 0.26-0.39 seroconversions/cat per year, and the estimated rate of soil contamination by T. gondii oocysts ranged between 31 and 3600 oocysts/m2 per year, depending on the population. Incidence risk in cats was related to mean precipitation, explaining both the spatial and temporal variability in risk: local conditions explained differences between the three study sites and incidence risk increased during rainy years. This study brings rare quantitative information on the level of contamination of the environment by T. gondii oocysts, and suggests that the spatio-temporal distribution of incidence risk in cats may reflect both the influence of rain on prey populations and infectivity of T. gondii oocysts.

Genetic characterization of Toxoplasma gondii from wild boar (Sus scrofa) in France.

Toxoplasma gondii strains isolated from domestic animals and humans have been classified into three clonal lineages types I-III, with differences in terms of pathogenicity to mice. Much less is known on T. gondii genotypes in wild animals. In this report, genotypes of T. gondii isolated from wild boar (Sus scrofa) in France are described. During the hunting seasons 2002-2008, sera and tissues of individuals from two French regions, one continental and one insular, were tested for Toxoplasma infection. Antibodies to T. gondii were found in 26 (17.6%) of 148 wild boars using the modified agglutination test (MAT, positivity threshold: 1:24). Seroprevalence was 45.9% when considering a threshold of 1:6. Hearts of individuals with a positive agglutination (starting dilution 1:6) (n=60) were bioassayed in mice for isolation of viable T. gondii. In total, 21 isolates of T. gondii were obtained. Genotyping of the isolates using 3 PCR-restriction fragment length polymorphism markers (SAG1, SAG2 and GRA7) and 6 microsatellite loci analysis (TUB2, TgM-A, W35, B17, B18 and M33) revealed that all belonged to type II lineage. These results underline that wild boar may serve as an important reservoir for transmission of T. gondii, and that strains present in wildlife may not be different from strains from the domestic environment.

Landscape, herd management and within-herd seroprevalence of Toxoplasma gondii in beef cattle herds from Champagne-Ardenne, France.

Toxoplasmosis is the most common parasitic zoonosis worldwide. Its prevalence and impact on human health are highly variable geographically. Humans may be infected by ingesting oocysts from the environment, or bradyzoits contained in meat products from various domestic species, thus data on the dynamics of toxoplasmosis in domestic herds is needed. However, few information is available on the factors that determine the level of infection of cattle herds. In this study, we aimed to estimate within-herd seroprevalence of toxoplasmosis in bovine herds and analyze its variability in relation with environmental characteristics and herd management. We tested the presence of anti Toxoplasma gondii antibodies in 1329 cattle from 24 beef herds in the Champagne-Ardenne region, using the Modified Agglutination Test. Information on herds was collected using a questionnaire. After describing the relationships between explanatory variables, we built a multivariate model using logistic Generalized Linear Models (GLMs) and estimated parameters with a Generalized Estimating Equations (GEE) procedure. The crude seroprevalence at threshold 1:24 equalled 7.8%, which is low, however positive individuals were found in 21 out of 24 herds. The final multivariate model showed that within-herd seroprevalence was highest in herds that were both small and isolated. The presence of cats modified the age-prevalence relationship: maximal seroprevalence was observed in oldest cows in farms without cats, and in youngest individuals in farms with cats. Finally, using a natural water point on pastures was associated to a high within-herd seroprevalence (Odds-Ratio: 1.93). Cows are often exposed to toxoplasmosis, however landscape characteristics (water point, isolation) and herd management (herd size, cats) may affect seroprevalence. Our results may help to find ways of reducing T. gondii prevalence in cattle.

Toxoplasmosis in prey species and consequences for prevalence in feral cats: not all prey species are equal.

Toxoplasma gondii is largely transmitted to definitive felid hosts through predation. Not all prey species represent identical risks of infection for cats because of differences in prey susceptibility, exposure and/or lifespan. Previously published studies have shown that prevalence in rodent and lagomorph species is positively correlated with body mass. We tested the hypothesis that different prey species have different infection risks by comparing infection dynamics of feral cats at 4 sites in the sub-Antarctic Kerguelen archipelago which differed in prey availability. Cats were trapped from 1994 to 2004 and anti-T. gondii IgG antibodies were detected using the modified agglutination test (> or =1:40). Overall seroprevalence was 51.09%. Antibody prevalence differed between sites, depending on diet and also on sex, after taking into account the effect of age. Males were more often infected than females and the difference between the sexes tended to be more pronounced in the site where more prey species were available. A difference in predation efficiency between male and female cats may explain this result. Overall, our results suggest that the composition of prey items in cat diet influences the risk of T. gondii infection. Prey compositon should therefore be considered important in any understanding of infection dynamics of T. gondii.