RESUMEN
The recent emergence of chronic wasting disease (CWD) in Europe has become a new public health risk for monitoring of wild and farmed cervids. This disease, due to prions, has proliferated in North America in a contagious manner. In several mammalian species, polymorphisms in the prion protein gene (PRNP) play a crucial role in the susceptibility to prions and their spread. To obtain a reliable picture of the distribution of PRNP polymorphisms in the two most common cervid species in France, we sequenced the open reading frame (ORF) of this gene in 2114 animals, 1116 roe deer (Capreolus capreolus) and 998 red deer (Cervus elaphus). Selection criteria such as historical origin, spatial distribution and sex ratio have been integrated to establish this sample collection. Except for one heterozygous animal with a non-synonymous mutation at codon 37 (G37A), all the 1116 French roe deer were monomorphic. Red deer showed greater variation with two non-synonymous substitutions (T98A; Q226E), three synonymous substitutions (codons 21, 78 and 136) and a new 24pb deletion (Δ69-77). We found significant regional variations between French regions in the frequency of the identified substitutions. After cloning of the PRNP ORF from animals presenting multiple non-synonymous polymorphisms, we identified six haplotypes and obtained a total of twelve genotypes. As in other European countries, we highlighted the apparent homogeneity of PRNP in the French roe deer and the existence of a greater diversity in the red deer. These results were in line with European phylogeographic studies on these two species.
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Ciervos , Sistemas de Lectura Abierta , Animales , Francia , Polimorfismo Genético , Priones/genética , Enfermedad Debilitante Crónica/genética , Proteínas Priónicas/genéticaRESUMEN
Living in variable and unpredictable environments, organisms face recurrent stressful situations. The endocrine stress response, which includes the secretion of glucocorticoids, helps organisms to cope with these perturbations. Although short-term elevations of glucocorticoid levels are often associated with immediate beneficial consequences for individuals, long-term glucocorticoid elevation can compromise key physiological functions such as immunity. While laboratory works highlighted the immunosuppressive effect of long-term elevated glucocorticoids, it remains largely unknown, especially in wild animals, whether this relationship is modulated by individual and environmental characteristics. In this study, we explored the co-variation between integrated cortisol levels, assessed non-invasively using faecal cortisol metabolites (FCMs), and 12 constitutive indices of innate, inflammatory, and adaptive immune functions, in wild roe deer living in three populations with previously known contrasting environmental conditions. Using longitudinal data on 564 individuals, we further investigated whether age and spatio-temporal variations in the quantity and quality of food resources modulate the relationship between FCMs and immunity. Negative covariation with glucocorticoids was evident only for innate and inflammatory markers of immunity, while adaptive immunity appeared to be positively or not linked to glucocorticoids. In addition, the negative covariations were generally stronger in individuals facing harsh environmental constraints and in old individuals. Therefore, our results highlight the importance of measuring multiple immune markers of immunity in individuals from contrasted environments to unravel the complex relationships between glucocorticoids and immunity in wild animals. Our results also help explain conflicting results found in the literature and could improve our understanding of the link between elevated glucocorticoid levels and disease spread, and its consequences on population dynamics.
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Ciervos , Animales , Ciervos/metabolismo , Animales Salvajes/metabolismo , Glucocorticoides/metabolismo , Hidrocortisona/metabolismo , Inmunidad AdaptativaRESUMEN
The biomedical literature has consistently highlighted that long-term elevation of glucocorticoids might impair immune functions. However, patterns are less clear in wild animals. Here, we re-explored the stress-immunity relationship considering the potential effects of behavioural profiles. Thirteen captive roe deer (Capreolus capreolus) were monitored over an eight-week period encompassing two capture events. We assessed how changes in baseline faecal cortisol metabolite (FCM) concentrations following a standardized capture protocol and an immune challenge using anti-rabies vaccination affected changes in 13 immune parameters of innate and adaptive immunity, and whether these changes in baseline FCM levels and immune parameters related to behavioural profiles. We found that individuals with increased baseline FCM levels also exhibited increased immunity and were characterized by more reactive behavioural profiles (low activity levels, docility to manipulation and neophilia). Our results suggest that the immunity of large mammals may be influenced by glucocorticoids, but also behavioural profiles, as it is predicted by the pace-of-life syndrome hypothesis. Our results highlight the need to consider covariations between behaviour, immunity and glucocorticoids in order to improve our understanding of the among-individual variability in the stress-immunity relationships observed in wildlife, as they may be underpinned by different life-history strategies.
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Ciervos , Glucocorticoides , Inmunidad Adaptativa , Animales , Animales Salvajes , HidrocortisonaRESUMEN
Toll-like receptors (TLR) play a central role in recognition and host frontline defence against a wide range of pathogens. A number of recent studies have shown that TLR genes (Tlrs) often exhibit large polymorphism in natural populations. Yet, there is little knowledge on how this polymorphism is maintained and how it influences disease susceptibility in the wild. In previous work, we showed that some Tlrs exhibit similarly high levels of genetic diversity as genes of the Major Histocompatibility Complex (MHC), and signatures of contemporary balancing selection in roe deer (Capreolus capreolus), the most abundant cervid species in Europe. Here, we investigated the evolutionary mechanisms by which pathogen-mediated selection could shape this innate immunity genetic diversity by examining the relationships between Tlr (Tlr2, Tlr4 and Tlr5) genotypes (heterozygosity status and presence of specific alleles) and infections with Toxoplasma and Chlamydia, two widespread intracellular pathogens known to cause reproductive failure in ungulates. We showed that Toxoplasma and Chlamydia exposures vary significantly across years and landscape features with few co-infection events detected and that the two pathogens exert antagonistic selection on Tlr2 polymorphism. By contrast, we found limited support for Tlr heterozygote advantage. Our study confirmed the importance of looking beyond Mhc genes in wildlife immunogenetic studies. It also emphasized the necessity to consider multiple pathogen challenges and their spatiotemporal variation to improve our understanding of vertebrate defence evolution against pathogens.
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Ciervos , Selección Genética , Animales , Ciervos/genética , Inmunidad Innata/genética , Polimorfismo Genético , Receptores Toll-Like/genéticaRESUMEN
While evidence that telomere length is associated with health and mortality in humans and birds is accumulating, a large body of research is currently seeking to identify factors that modulate telomere dynamics. We tested the hypothesis that high levels of glucocorticoids in individuals under environmental stress should accelerate telomere shortening in two wild populations of roe deer (Capreolus capreolus) living in different ecological contexts. From two consecutive annual sampling sessions, we found that individuals with faster rates of telomere shortening had higher concentrations of fecal glucocorticoid metabolites, suggesting a functional link between glucocorticoid levels and telomere attrition rate. This relationship was consistent for both sexes and populations. This finding paves the way for further studies of the fitness consequences of exposure to environmental stressors in wild vertebrates.
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Ciervos/metabolismo , Glucocorticoides/metabolismo , Telómero , Animales , Femenino , MasculinoRESUMEN
Molecular epidemiology represents a powerful approach to elucidate the complex epidemiological cycles of multi-host pathogens, such as Anaplasma phagocytophilum. A. phagocytophilum is a tick-borne bacterium that affects a wide range of wild and domesticated animals. Here, we characterized its genetic diversity in populations of French cattle; we then compared the observed genotypes with those found in horses, dogs, and roe deer to determine whether genotypes of A. phagocytophilum are shared among different hosts. We sampled 120 domesticated animals (104 cattle, 13 horses, and 3 dogs) and 40 wild animals (roe deer) and used multilocus sequence analysis on nine loci (ankA, msp4, groESL, typA, pled, gyrA, recG, polA, and an intergenic region) to characterize the genotypes of A. phagocytophilum present. Phylogenic analysis revealed three genetic clusters of bacterial variants in domesticated animals. The two principal clusters included 98% of the bacterial genotypes found in cattle, which were only distantly related to those in roe deer. One cluster comprised only cattle genotypes, while the second contained genotypes from cattle, horses, and dogs. The third contained all roe deer genotypes and three cattle genotypes. Geographical factors could not explain this clustering pattern. These results suggest that roe deer do not contribute to the spread of A. phagocytophilum in cattle in France. Further studies should explore if these different clusters are associated with differing disease severity in domesticated hosts. Additionally, it remains to be seen if the three clusters of A. phagocytophilum genotypes in cattle correspond to distinct epidemiological cycles, potentially involving different reservoir hosts.
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Anaplasma phagocytophilum/genética , Anaplasmosis/microbiología , Ciervos , Enfermedades de los Perros/microbiología , Variación Genética , Enfermedades de los Caballos/microbiología , Anaplasma phagocytophilum/clasificación , Anaplasmosis/epidemiología , Animales , Proteínas Bacterianas/genética , Proteínas Bacterianas/metabolismo , Bovinos , Enfermedades de los Bovinos , Enfermedades de los Perros/epidemiología , Perros , Francia , Enfermedades de los Caballos/epidemiología , Caballos , Datos de Secuencia Molecular , Tipificación de Secuencias Multilocus/veterinaria , Filogenia , Análisis de Secuencia de ADN/veterinariaRESUMEN
The use of fecal corticosteroid metabolites (FCMs) has proven to be well suited to evaluate adrenocortical activity, a major component of the stress response, particularly in wildlife. As with any tools, confounding factors and drawbacks must be carefully considered. Among them, sample preservation and storage are of particular importance, as they can affect stability of FCMs and lead to biased results and interpretations. Arguably, immediate freezing of fecal samples upon collection is the best practice to preserve FCM integrity, however, for logistical reasons, this condition is rarely feasible in the field. It is generally argued that temporary storage of samples at low above-zero temperature is an acceptable way of preserving samples in the field before freezing them for long-term storage. However, to our knowledge, there is no empirical study that demonstrates the stability of fecal metabolites in samples stored at +4°C. In this study, we collected a fresh fecal sample from 20 captive roe deer, each of which was homogenized and split into three subsamples (60 subsamples in total) to investigate the effects on FCMs levels of temporary storage at +4°C for 24 h and 48 h before freezing versus immediate freezing at -20°C after feces collection. Compared to immediate freezing, mean FCMs levels decreased by 25% every 24 h when feces were stored at +4°C before freezing. The variance of FCMs levels followed the same pattern, leading to a clear reduction in the ability to detect biological effects. Minimizing the storage time at +4°C before freezing should therefore be seriously considered when establishing sampling and storage protocols for feces in the field for adequate hormonal profiling.
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Ciervos , Glucocorticoides , Animales , Glucocorticoides/metabolismo , Congelación , Heces , Animales Salvajes/metabolismoRESUMEN
BACKGROUND: Trypanosomes are protozoan parasites of vertebrates that are of medical and veterinary concern. A variety of blood-feeding invertebrates have been identified as vectors, but the role of ticks in trypanosome transmission remains unclear. METHODS: In this study, we undertook extensive molecular screening for the presence and genetic diversity of trypanosomes in field ticks. RESULTS: Examination of 1089 specimens belonging to 28 tick species from Europe and South America led to the identification of two new trypanosome strains. The prevalence may be as high as 4% in tick species such as the castor bean tick Ixodes ricinus, but we found no evidence of transovarial transmission. Further phylogenetic analyses based on 18S rRNA, EF1-α, hsp60 and hsp85 gene sequences revealed that different tick species, originating from different continents, often harbour phylogenetically related trypanosome strains and species. Most tick-associated trypanosomes cluster in a monophyletic clade, the Trypanosoma pestanai clade, distinct from clades of trypanosomes associated with transmission by other blood-feeding invertebrates. CONCLUSIONS: These observations suggest that ticks may be specific arthropod hosts for trypanosomes of the T. pestanai clade. Phylogenetic analyses provide further evidence that ticks may transmit these trypanosomes to a diversity of mammal species (including placental and marsupial species) on most continents.
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Ixodes , Trypanosoma , Animales , Ixodes/parasitología , Filogenia , Trypanosoma/genéticaRESUMEN
Changes in the risk of exposure to infectious disease agents can be tracked through variations in antibody prevalence in vertebrate host populations. However, information on the temporal dynamics of the immune status of individuals is critical. If antibody levels persist a long time after exposure to an infectious agent, they could enable the efficient detection of the past circulation of the agent; if they persist only a short time, they could provide snap shots of recent exposure of sampled hosts. Here, we explored the temporal dynamics of seropositivity against Lyme disease agent Borrelia burgdorferi sensu lato (Bbsl) in individuals of a widespread medium-sized mammal species, the roe deer (Capreolus capreolus), in France. Using a modified commercially available immunoassay we tested 1554 blood samples obtained in two wild deer populations monitored from 2010 to 2020. Using multi-event capture-mark-recapture models, we estimated yearly population-, age-, and sex-specific rates of seroconversion and seroreversion after accounting for imperfect detection. The yearly seroconversion rates indicated a higher level of exposure in early (2010-2013) than in late years (2014-2019) to infected tick bites in both populations, without any detectable influence of sex or age. The relatively high rates of seroreversion indicated a short-term persistence of antibody levels against Bbsl in roe deer. This was confirmed by the analysis of samples collected on a set of captive individuals that were resampled several times a few weeks apart. Our findings show the potential usefulness of deer as a sentinel for tracking the risk of exposure to Lyme disease Bbsl, although further investigation on the details of the antibody response to Bbsl in this incompetent host would be useful. Our study also highlights the value of combining long-term capture-mark-recapture sampling and short-time analyses of serological data for wildlife populations exposed to infectious agents of relevance to wildlife epidemiology and human health.
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The growth of livestock farming and the recent expansion of wild ungulate populations in Europe favor opportunities for direct and/or indirect cross-transmission of pathogens. Comparatively few studies have investigated the epidemiology of gastro-intestinal nematode parasites, an ubiquitous and important community of parasites of ungulates, at the wildlife/livestock interface. In this study, we aimed to assess the influence of livestock proximity on the gastrointestinal nematode community of roe deer in a rural landscape located in southern France. Using ITS-2 rDNA nemabiome metabarcoding on fecal larvae, we analysed the gastrointestinal nematode communities of roe deer and sheep. In addition, we investigated Haemonchus contortus nad4 mtDNA diversity to specifically test parasite circulation among domestic and wild host populations. The dominant gastrointestinal nematode species found in both the roe deer and sheep were generalist species commonly found in small ruminant livestock (e.g. H. contortus), whereas the more specialised wild cervid nematode species (e.g. Ostertagia leptospicularis) were only present at low frequencies. This is in marked contrast with previous studies that found the nemabiomes of wild cervid populations to be dominated by cervid specialist nematode species. In addition, the lack of genetic structure of the nad4 mtDNA of H. contortus populations between host species suggests circulation of gastrointestinal nematodes between roe deer and sheep. The risk of contact with livestock only has a small influence on the nemabiome of roe deer, suggesting the parasite population of roe deer has been displaced by generalist livestock parasites due to many decades of sheep farming, not only for deer grazing close to pastures, but also at a larger regional scale. We also observed some seasonal variation in the nemabiome composition of roe deer. Overall, our results demonstrate significant exchange of gastrointestinal nematodes between domestic and wild ungulates, with generalist species spilling over from domestic ungulates dominating wild cervid parasite communities.
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Ciervos , Parasitosis Intestinales , Nematodos , Animales , Ovinos , Ciervos/parasitología , Simpatría , Nematodos/genética , Rumiantes/parasitología , Ganado , ADN Mitocondrial/genéticaRESUMEN
Ixodes ricinus ticks (Acari: Ixodidae) are the most important vector for Lyme borreliosis in Europe. As climate change might affect their distributions and activities, this study aimed to determine the effects of environmental factors, i.e., meteorological, bioclimatic, and habitat characteristics on host-seeking (questing) activity of I. ricinus nymphs, an important stage in disease transmissions, across diverse climatic types in France over 8 years. Questing activity was observed using a repeated removal sampling with a cloth-dragging technique in 11 sampling sites from 7 tick observatories from 2014 to 2021 at approximately 1-month intervals, involving 631 sampling campaigns. Three phenological patterns were observed, potentially following a climatic gradient. The mixed-effects negative binomial regression revealed that observed nymph counts were driven by different interval-average meteorological variables, including 1-month moving average temperature, previous 3-to-6-month moving average temperature, and 6-month moving average minimum relative humidity. The interaction effects indicated that the phenology in colder climates peaked differently from that of warmer climates. Also, land cover characteristics that support the highest baseline abundance were moderate forest fragmentation with transition borders with agricultural areas. Finally, our model could potentially be used to predict seasonal human-tick exposure risks in France that could contribute to mitigating Lyme borreliosis risk.
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Ixodes , Enfermedad de Lyme , Animales , Ecosistema , Bosques , Humanos , Enfermedad de Lyme/epidemiología , Ninfa , Estaciones del AñoRESUMEN
Forest fragmentation may benefit generalist herbivores by increasing access to various substitutable food resources, with potential consequences for their population dynamics. We studied a European roe deer (Capreolus capreolus) population living in an agricultural mosaic of forest, woodlots, meadows and cultivated crops. We tested whether diet composition and quality varied spatially across the landscape using botanical analyses of rumen contents and chemical analyses of the plants consumed in relation to landscape metrics. In summer and non-mast winters, roe deer ate more cultivated seeds and less native forest browse with increasing availability of crops in the local landscape. This spatial variation resulted in contrasting diet quality, with more cell content and lower lignin and hemicellulose content (high quality) for individuals living in more open habitats. The pattern was less marked in the other seasons when diet composition, but not diet quality, was only weakly related to landscape structure. In mast autumns and winters, the consumption of acorns across the entire landscape resulted in a low level of differentiation in diet composition and quality. Our results reflect the ability of generalist species, such as roe deer, to adapt to the fragmentation of their forest habitat by exhibiting a plastic feeding behavior, enabling them to use supplementary resources available in the agricultural matrix. This flexibility confers nutritional advantages to individuals with access to cultivated fields when their native food resources are depleted or decline in quality (e.g. during non-mast years) and may explain local heterogeneities in individual phenotypic quality.
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Ciervos/fisiología , Contenido Digestivo/química , Herbivoria , Plantas/química , Animales , Dieta , Ambiente , Femenino , Francia , Masculino , Estaciones del AñoRESUMEN
Tick-borne diseases have a complex epidemiology that depends on different ecological communities, associating several species of vertebrate hosts, vectors and pathogens. While most studies in Europe are focused on Ixodes ricinus, other Ixodes species may also be involved in the transmission or maintenance of pathogens. This is the case of Ixodes frontalis, a poorly known species associated with different bird species such as blackbirds, thrushes and robins, with a wide distribution covering most European countries. In a previous study, high densities of questing I. frontalis larvae were found during autumn-winter at a site close to Nantes (western France) where a long-term survey focused on I. ricinus was conducted. These I. frontalis were mostly observed under bamboo bushes. In the present study, we investigated the presence of I. frontalis under bamboo bushes at various locations. With that aim in mind, a systematic search for questing I. frontalis was undertaken by the flagging method in public urban parks and private gardens presenting bamboo bushes (32 sites). This survey was carried out during autumn-winter to maximize the probability of finding the most abundant stage, i.e. larvae. We searched for I. frontalis first in the area of Nantes (10 sites), then in other regions of France (21 sites) and at one site in northern Italy. A single visit to each site revealed the presence of I. frontalis at 29 out of 32 sites: larvae were always present, nymphs were frequent (59 % of the positive sites), while adults were found at only 14 % of the sites. Questing stages of this understudied species are thus easy to find, by dragging or flagging under bamboo bushes in autumn or winter. We make the assumption that bamboo offers a favourable place for birds to roost overnight outside their breeding period (i.e. spring), sheltered from both predators and wind. This would explain higher densities of I. frontalis under bamboo, relative to other biotopes. As I. frontalis is known to harbour zoonotic pathogens, the consequences of this discovery on the epidemiology of tick-borne diseases are discussed.
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Interacciones Huésped-Parásitos , Ixodes/fisiología , Poaceae , Animales , Conducta Alimentaria , Femenino , Francia , Humanos , Italia , Ixodes/crecimiento & desarrollo , Larva/crecimiento & desarrollo , Larva/fisiología , Masculino , Ninfa/crecimiento & desarrollo , Ninfa/fisiología , Poaceae/crecimiento & desarrolloRESUMEN
Wildlife populations are increasingly exposed to human-induced modifications of their habitats. To cope with anthropogenic stressors, animals can adjust their behaviour-for example, by shifting their activity to more sheltered habitats, or becoming more nocturnal. However, whether use of spatial and temporal adjustments in behaviour may regulate the endocrine response is poorly documented. Here, we analyzed faecal cortisol metabolites (FCMs) of wild roe deer (Capreolus capreolus) living in a human-dominated agro-ecosystem. Using Global Positioning System monitoring of 116 individuals, we assessed their spatial behaviour and tested whether proximity to anthropogenic structures (linear distance to built-up areas) and the use of refuge habitats (woodland and hedges) influenced FCM levels. In accordance with our predictions, individuals ranging closer to anthropogenic structures during daytime had higher FCM levels, but this relationship was buffered as use of refuge habitat increased. In addition, this link between proximity to anthropogenic structures and FCM levels disappeared when we analyzed spatial behaviour at night. Finally, FCM levels were higher when the ambient temperature was lower, and during years of low resource availability. Our results demonstrate that the stress levels of large mammals may be strongly influenced by their proximity to anthropogenic activities, but that these effects may be buffered by behavioural adjustments in terms of space use and circadian rhythm. Whereas most studies have focused on the influence of environmental heterogeneity, our analysis highlights the need to also consider the fine-scale spatial response of individuals when studying the hormonal response of wild animals to human disturbance. We emphasize the potential to mitigate this hormonal stress response, and its potential negative consequences on population dynamics, through the preservation or restoration of patches of refuge habitat in close proximity to human infrastructure.
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BACKGROUND: In Europe, ticks are major vectors of both human and livestock pathogens (e.g. Lyme disease, granulocytic anaplasmosis, bovine babesiosis). Agricultural landscapes, where animal breeding is a major activity, constitute a mosaic of habitat types of various quality for tick survival and are used at different frequencies by wild and domestic hosts across seasons. This habitat heterogeneity, in time and space, conditions the dynamics of these host-vector-pathogen systems and thus drives acarological risk (defined as the density of infected ticks). The principal objective of the OSCAR project (2011-2016) was to examine the links between this heterogeneity and acarological risk for humans and their domestic animals. Here, we present the data associated with this project. NEW INFORMATION: This paper reports a database on the distribution and densities of I. ricinus ticks - the most common tick species in French agricultural landscapes - and the prevalence of three tick-borne pathogens (Anaplasma phagocytophilum, Borrelia spp. and Babesia spp.) in two sites in north-western ("Zone Atelier Armorique": ZA site) and south-western ("Vallées et Coteaux de Gascogne": VG site) France. The distribution and density of ticks along a gradient of wooded habitats, as well as biotic variables, such as the presence and abundance of their principal domestic (livestock) and wild hosts (small mammals), were measured from forest cores and edges to more or less isolated hedges, all bordering meadows. Ticks, small mammals and information on local environmental conditions were collected along 90 transects in each of the two sites in spring and autumn 2012 and 2013 and in spring 2014, corresponding to the main periods of tick activity. Local environmental conditions were recorded along each tick and small mammal transect: habitat type, vegetation type and characteristics, slope and traces of livestock presence. Samples consisted of questing ticks collected on the vegetation (mainly I. ricinus nymphs), biopsies of captured small mammals and ticks fixed on small mammals. In the VG site, livestock occurrence and abundance were recorded each week along each tick transect.A total of 29004 questing ticks and 1230 small mammals were captured during the study across the two sites and over the five field campaigns. All questing nymphs (N = 12287) and questing adults (N = 646) were identified to species. Ticks from small mammals (N = 1359) were also identified to life stage. Questing nymphs (N = 4518 I. ricinus) and trapped small mammals (N = 908) were analysed for three pathogenic agents: A. phagocytophilum, Borrelia spp. and Babesia spp.In the VG site, the average prevalence in I. ricinus nymphs for A. phagocytophilum, Borrelia spp. and Babesia spp. were, respectively 1.9% [95% CI: 1.2-2.5], 2.5% [95% CI: 1.8-3.2] and 2.7% [95% CI: 2.0-3.4]. In small mammals, no A. phagocytophilum was detected, but the prevalence for Borrelia spp. was 4.2% [95% CI: 0.9-7.5]. On this site, there was no screening of small mammals for Babesia spp. In ZA site, the average prevalence in nymphs for A. phagocytophilum, Borrelia spp. and Babesia were, respectively 2.2% [95% CI: 1.6-2.7], 3.0% [95% CI: 2.3-3.6] and 3.1% [95% CI: 2.5-3.8]. In small mammals, the prevalence of A. phagocytophilum and Borrelia spp. were, respectively 6.9% [95% CI: 4.9-8.9] and 4.1% [95% CI: 2.7-5.9]. A single animal was found positive for Babesia microti at this site amongst the 597 tested.
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Midichloria mitochondrii is a tick-borne intracellular bacterium of the order Rickettsiales, found with high prevalence in the sheep tick ( Ixodes ricinus). Midichloria mitochondrii is capable of vertical transmission in the tick, but recently evidence of potential horizontal transmission to the tick hosts through the blood meal has been reported. We investigated the presence of the bacterium in the blood of roe deer ( Capreolus capreolus) collected from an area known to be highly infested with I. ricinus ticks. We collected blood and sera samples for 3 yr in Gardouch (Haute Garonne, France) and subjected them to molecular screening through PCR and to serological investigation using enzyme-linked immunosorbent assay and western blot. Bacterial DNA was detected in the blood of four of seven animals, but only at one or two points in time, whereas all sera were positive for M. mitochondrii antigens at all times. Our results indicated that the presence of the bacterium in the blood is transient, but the antibody response appeared to be long-lasting, possibly due to constant exposure to tick bites, and thus to repeated injection of bacteria. The role of M. mitochondrii in the mammalian host, and its interaction with other tick-borne bacteria, remains unknown.
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Alphaproteobacteria/aislamiento & purificación , Infecciones Bacterianas/veterinaria , Ciervos/microbiología , Animales , Francia/epidemiología , Ixodes/microbiología , Pruebas Serológicas/veterinaria , Enfermedades por Picaduras de Garrapatas/epidemiología , Enfermedades por Picaduras de Garrapatas/microbiología , Enfermedades por Picaduras de Garrapatas/veterinariaRESUMEN
BACKGROUND: Anaplasma phagocytophilum is a tick-transmitted Gram-negative obligate intracellular bacterium able to infect a wide variety of wild and domestic animals worldwide. Based on the genetic diversity observed with different molecular markers, several host-specific lineages have been identified. Roe deer is one of the most important reservoirs of this bacterium and hosts different genetic groups sometimes found on domestic animals. We therefore developed an ankA cluster-specific nested PCR (nPCR) to evaluate the prevalence of the three different ankA genetic groups described in roe deer (clusters II, III and IV) at three locations in France and the level of co-infections. RESULTS: The specificity of the three nPCRs was assessed by partially sequencing 35 amplicons of ankA genes obtained from the different nested PCRs. All three genetic lineages were detected in roe deer from all three geographical locations. Of the infected deer population, 60.7% were co-infected by two or three different genetic variants. Co-infections varied from 42.9 to 70.6% of the infected population depending on the local infection prevalences (from 33.3 to 73.9%). All types of mixed infections occurred, suggesting the absence of a strict variant exclusion by another variant. CONCLUSIONS: Mixed infections by two or three genetic variants of A. phagocytopilum are a common feature in roe deer. Genetic variants (cluster IV) also found in domestic ruminants (cattle and sheep) were present in all the roe deer populations analyzed, suggesting a shared epidemiological cycle.
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Anaplasma phagocytophilum/genética , Vectores Arácnidos/microbiología , Ciervos/microbiología , Ehrlichiosis/veterinaria , Variación Genética , Reacción en Cadena de la Polimerasa/métodos , Animales , Animales Domésticos , Coinfección , ADN Bacteriano/genética , Reservorios de Enfermedades , Ehrlichiosis/diagnóstico , Ehrlichiosis/epidemiología , Ehrlichiosis/microbiología , Francia/epidemiología , Ixodes/microbiología , Filogenia , Sensibilidad y EspecificidadRESUMEN
Anaplasma phagocytophilum is a bacterial pathogen mainly transmitted by Ixodes ricinus ticks in Europe. It infects wild mammals, livestock, and, occasionally, humans. Roe deer are considered to be the major reservoir, but the genotypes they carry differ from those that are found in livestock and humans. Here, we investigated whether roe deer were the main source of the A. phagocytophilum genotypes circulating in questing I. ricinus nymphs in a fragmented agricultural landscape in France. First, we assessed pathogen prevalence in 1837 I. ricinus nymphs (sampled along georeferenced transects) and 79 roe deer. Prevalence was dramatically different between ticks and roe deer: 1.9% versus 76%, respectively. Second, using high-throughput amplicon sequencing, we characterized the diversity of the A. phagocytophilum genotypes found in 22 infected ticks and 60 infected roe deer; the aim was to determine the frequency of co-infections. Only 22.7% of infected ticks carried genotypes associated with roe deer. This finding fits with others suggesting that cattle density is the major factor explaining infected tick density. To explore epidemiological scenarios capable of explaining these patterns, we constructed compartmental models that focused on how A. phagocytophilum exposure and infection dynamics affected pathogen prevalence in roe deer. At the exposure levels predicted by the results of this study and the literature, the high prevalence in roe deer was only seen in the model in which superinfections could occur during all infection phases and when the probability of infection post exposure was above 0.43. We then interpreted these results from the perspective of livestock and human health.
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Anaplasma phagocytophilum/clasificación , Anaplasma phagocytophilum/genética , Enfermedades de los Animales/microbiología , Ciervos/microbiología , Ehrlichiosis/veterinaria , Especificidad del Huésped , Ganado/microbiología , Garrapatas/microbiología , Agricultura , Enfermedades de los Animales/epidemiología , Enfermedades de los Animales/transmisión , Animales , Técnicas de Tipificación Bacteriana , Reservorios de Enfermedades , Exposición a Riesgos Ambientales , Genotipo , Humanos , Filogenia , Prevalencia , SobreinfecciónRESUMEN
Individuals differ in the manner that they cope with risk. When these behavioral differences are manifested in risky or challenging environments (i.e. stressful situations), they are generally interpreted within the "coping style" framework. As studying inter-individual variability in behavior is particularly challenging in the wild, we used a captive facility to explore consistency in the individual behavioral response to an acute stress in roe deer (Capreolus capreolus). Using behavioral and physiological parameters measured six times across a calendar year, we first quantified individual repeatability and, second, explored the correlations among these parameters that might indicate a coherent stress response. Finally, we analyzed the link between the stress response and individual body mass, a reliable indicator of phenotypic quality in roe deer. We found that the measured parameters were highly repeatable across seasons, indicating that the individual stress response is consistent over time. Furthermore, there was considerable covariation among the stress response parameters, describing a proactivity-reactivity gradient at the individual level. Finally, proactive individuals had higher body mass than reactive individuals. We suggest that consistent individual differences in energy metabolism and physiology may promote consistent individual differences in behavioral traits, providing a mechanistic link between food acquisition tactics and demographic performance.
Asunto(s)
Adaptación Psicológica/fisiología , Ciervos/fisiología , Ciervos/psicología , Herbivoria , Individualidad , Estrés Psicológico/fisiopatología , Animales , Conducta Animal , Temperatura Corporal , Peso Corporal , Femenino , Hematócrito , Recuento de Leucocitos , Masculino , Reproducibilidad de los Resultados , Estaciones del AñoRESUMEN
Investigations on fecal samples, vaginal swabs and sera from roe deer (Capreolus capreolus) in south-western France led to the detection of a non-classified Chlamydiaceae strain. A total of 85 vaginal swabs were sampled from roe deer that had been captured in 2012 (n=42) and 2013 (n=43). Using a Chlamydiaceae family-specific real-time PCR, only one vaginal swab out of the 42 samples done in 2012 tested positive and was subsequently identified as Chlamydia (C.) psittaci. In contrast, 6/43 vaginal swab samples were positive in 2013. Four of these positive samples came from a single group of roe deer, captured in the Fabas plain. Fecal samples from this group of 9 females were subsequently analyzed, with 6 of them testing positive with the Chlamydiaceae-specific PCR. All positive samples collected in 2013 were negative when re-tested with C. abortus-, C. pecorum- and C. suis-specific real-time PCR assays. Sera from this group of 9 females were analyzed with two immunoassays (recomLine and ELISA). Whereas intense positive reactions with C. pneumoniae antigens were observed for all sera when tested with the recomLine test, none was positive with the C. abortus specific ELISA test. Comparative sequence analysis of the 16S, 23S rRNA and ompA gene sequences from 3 animals, as well as the MLST analysis from 2 animals, showed that this roe deer group likely harbored the same bacterium related to members of the family Chlamydiaceae. Notably, the roe deer strain formed a separate entity different from the currently recognized chlamydial species, with C. trachomatis, C. suis and C. muridarum appearing as its closest relatives.