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1.  Unmanned Aircraft Systems for Studying Spatial Abundance of Ungulates: Relevance to Spatial Epidemiology 
PLoS ONE  2014;9(12):e115608.
Complex ecological and epidemiological systems require multidisciplinary and innovative research. Low cost unmanned aircraft systems (UAS) can provide information on the spatial pattern of hosts’ distribution and abundance, which is crucial as regards modelling the determinants of disease transmission and persistence on a fine spatial scale. In this context we have studied the spatial epidemiology of tuberculosis (TB) in the ungulate community of Doñana National Park (South-western Spain) by modelling species host (red deer, fallow deer and cattle) abundance at fine spatial scale. The use of UAS high-resolution images has allowed us to collect data to model the environmental determinants of host abundance, and in a further step to evaluate their relationships with the spatial risk of TB throughout the ungulate community. We discuss the ecological, epidemiological and logistic conditions under which UAS may contribute to study the wildlife/livestock sanitary interface, where the spatial aggregation of hosts becomes crucial. These findings are relevant for planning and implementing research, fundamentally when managing disease in multi-host systems, and focusing on risky areas. Therefore, managers should prioritize the implementation of control strategies to reduce disease of conservation, economic and social relevance.
doi:10.1371/journal.pone.0115608
PMCID: PMC4281124  PMID: 25551673
2.  Spatiotemporal interactions between wild boar and cattle: implications for cross-species disease transmission 
Veterinary Research  2014;45(1):122.
Controlling infectious diseases at the wildlife/livestock interface is often difficult because the ecological processes driving transmission between wildlife reservoirs and sympatric livestock populations are poorly understood. Thus, assessing how animals use their environment and how this affects interspecific interactions is an important factor in determining the local risk for disease transmission and maintenance. We used data from concurrently monitored GPS-collared domestic cattle and wild boar (Sus scrofa) to assess spatiotemporal interactions and associated implications for bovine tuberculosis (TB) transmission in a complex ecological and epidemiological system, Doñana National Park (DNP, South Spain). We found that fine-scale spatial overlap of cattle and wild boar was seasonally high in some habitats. In general, spatial interactions between the two species were highest in the marsh-shrub ecotone and at permanent water sources, whereas shrub-woodlands and seasonal grass-marshlands were areas with lower predicted relative interactions. Wild boar and cattle generally used different resources during winter and spring in DNP. Conversely, limited differences in resource selection during summer and autumn, when food and water availability were limiting, resulted in negligible spatial segregation and thus probably high encounter rates. The spatial gradient in potential overlap between the two species across DNP corresponded well with the spatial variation in the observed incidence of TB in cattle and prevalence of TB in wild boar. We suggest that the marsh-shrub ecotone and permanent water sources act as important points of TB transmission in our system, particularly during summer and autumn. Targeted management actions are suggested to reduce potential interactions between cattle and wild boar in order to prevent disease transmission and design effective control strategies.
Electronic supplementary material
The online version of this article (doi:10.1186/s13567-014-0122-7) contains supplementary material, which is available to authorized users.
doi:10.1186/s13567-014-0122-7
PMCID: PMC4264384  PMID: 25496754
3.  Long-Term Dynamics of Bluetongue Virus in Wild Ruminants: Relationship with Outbreaks in Livestock in Spain, 2006-2011 
PLoS ONE  2014;9(6):e100027.
Wild and domestic ruminants are susceptible to Bluetongue virus (BTV) infection. Three BTV serotypes (BTV-4, BTV-1 and BTV-8) have been detected in Spain in the last decade. Even though control strategies have been applied to livestock, BTV circulation has been frequently detected in wild ruminant populations in Spain. The aim of the present study is to assess the role for wild ruminants in maintaining BTV after the vaccination programs in livestock in mainland Spain. A total of 931 out 1,914 (48.6%) serum samples, collected from eight different wild ruminant species between 2006 and 2011, were BTV positive by ELISA. In order to detect specific antibodies against BTV-1, BTV-4 and BTV-8, positive sera were also tested by serumneutralisation test (SNT). From the ELISA positive samples that could be tested by SNT (687 out of 931), 292 (42.5%) showed neutralising antibodies against one or two BTV serotypes. For each BTV seroptype, the number of outbreaks in livestock (11,857 outbreaks in total) was modelled with pure autoregressive models and the resulting smoothed values, representing the predicted number of BTV outbreaks in livestock at municipality level, were positively correlated with BTV persistence in wild species. The strength of this relationship significantly decreased as red deer (Cervus elaphus) population abundance increased. In addition, BTV RNA was detected by real time RT-PCR in 32 out of 311 (10.3%) spleen samples from seropositive animals. Although BT outbreaks in livestock have decreased substantially after vaccination campaigns, our results indicated that wild ruminants have been exposed to BTV in territories where outbreaks in domestic animals occurred. The detection of BTV RNA and spatial association between BT outbreaks in livestock and BTV rates in red deer are consistent with the hypothesis of virus circulation and BTV maintenance within Iberian wild ruminant populations.
doi:10.1371/journal.pone.0100027
PMCID: PMC4062458  PMID: 24940879
4.  Tuberculosis Epidemiology in Islands: Insularity, Hosts and Trade 
PLoS ONE  2013;8(7):e71074.
Because of their relative simplicity and the barriers to gene flow, islands are ideal systems to study the distribution of biodiversity. However, the knowledge that can be extracted from this peculiar ecosystem regarding epidemiology of economically relevant diseases has not been widely addressed. We used information available in the scientific literature for 10 old world islands or archipelagos and original data on Sicily to gain new insights into the epidemiology of the Mycobacterium tuberculosis complex (MTC). We explored three nonexclusive working hypotheses on the processes modulating bovine tuberculosis (bTB) herd prevalence in cattle and MTC strain diversity: insularity, hosts and trade. Results suggest that bTB herd prevalence was positively correlated with island size, the presence of wild hosts, and the number of imported cattle, but neither with isolation nor with cattle density. MTC strain diversity was positively related with cattle bTB prevalence, presence of wild hosts and the number of imported cattle, but not with island size, isolation, and cattle density. The three most common spoligotype patterns coincided between Sicily and mainland Italy. However in Sicily, these common patterns showed a clearer dominance than on the Italian mainland, and seven of 19 patterns (37%) found in Sicily had not been reported from continental Italy. Strain patterns were not spatially clustered in Sicily. We were able to infer several aspects of MTC epidemiology and control in islands and thus in fragmented host and pathogen populations. Our results point out the relevance of the intensity of the cattle commercial networks in the epidemiology of MTC, and suggest that eradication will prove more difficult with increasing size of the island and its environmental complexity, mainly in terms of the diversity of suitable domestic and wild MTC hosts.
doi:10.1371/journal.pone.0071074
PMCID: PMC3726611  PMID: 23923053
5.  Sex-biased differences in the effects of host individual, host population and environmental traits driving tick parasitism in red deer 
The interactions between host individual, host population, and environmental factors modulate parasite abundance in a given host population. Since adult exophilic ticks are highly aggregated in red deer (Cervus elaphus) and this ungulate exhibits significant sexual size dimorphism, life history traits and segregation, we hypothesized that tick parasitism on males and hinds would be differentially influenced by each of these factors. To test the hypothesis, ticks from 306 red deer—182 males and 124 females—were collected during 7 years in a red deer population in south-central Spain. By using generalized linear models, with a negative binomial error distribution and a logarithmic link function, we modeled tick abundance on deer with 20 potential predictors. Three models were developed: one for red deer males, another for hinds, and one combining data for males and females and including “sex” as factor. Our rationale was that if tick burdens on males and hinds relate to the explanatory factors in a differential way, it is not possible to precisely and accurately predict the tick burden on one sex using the model fitted on the other sex, or with the model that combines data from both sexes. Our results showed that deer males were the primary target for ticks, the weight of each factor differed between sexes, and each sex specific model was not able to accurately predict burdens on the animals of the other sex. That is, results support for sex-biased differences. The higher weight of host individual and population factors in the model for males show that intrinsic deer factors more strongly explain tick burden than environmental host-seeking tick abundance. In contrast, environmental variables predominated in the models explaining tick burdens in hinds.
doi:10.3389/fcimb.2013.00023
PMCID: PMC3694362  PMID: 23819112
host-parasite; polygynous; cervidae; tick; sexual segregation
6.  Past, Present and Future Distributions of an Iberian Endemic, Lepus granatensis: Ecological and Evolutionary Clues from Species Distribution Models 
PLoS ONE  2012;7(12):e51529.
The application of species distribution models (SDMs) in ecology and conservation biology is increasing and assuming an important role, mainly because they can be used to hindcast past and predict current and future species distributions. However, the accuracy of SDMs depends on the quality of the data and on appropriate theoretical frameworks. In this study, comprehensive data on the current distribution of the Iberian hare (Lepus granatensis) were used to i) determine the species’ ecogeographical constraints, ii) hindcast a climatic model for the last glacial maximum (LGM), relating it to inferences derived from molecular studies, and iii) calibrate a model to assess the species future distribution trends (up to 2080). Our results showed that the climatic factor (in its pure effect and when it is combined with the land-cover factor) is the most important descriptor of the current distribution of the Iberian hare. In addition, the model’s output was a reliable index of the local probability of species occurrence, which is a valuable tool to guide species management decisions and conservation planning. Climatic potential obtained for the LGM was combined with molecular data and the results suggest that several glacial refugia may have existed for the species within the major Iberian refugium. Finally, a high probability of occurrence of the Iberian hare in the current species range and a northward expansion were predicted for future. Given its current environmental envelope and evolutionary history, we discuss the macroecology of the Iberian hare and its sensitivity to climate change.
doi:10.1371/journal.pone.0051529
PMCID: PMC3521729  PMID: 23272115
7.  Ecological Factors Driving Avian Influenza Virus Dynamics in Spanish Wetland Ecosystems 
PLoS ONE  2012;7(11):e46418.
Studies exploring the ecological interactions between avian influenza viruses (AIV), natural hosts and the environment are scarce. Most work has focused on viral survival and transmission under laboratory conditions and through mathematical modelling. However, more integrated studies performed under field conditions are required to validate these results. In this study, we combined information on bird community, environmental factors and viral epidemiology to assess the contribution of biotic and abiotic factors in the occurrence of low pathogenic AIV in Spanish wetlands. For that purpose, seven locations in five different wetlands were studied during two years (2007–2009), including seven sampling visits by location. In each survey, fresh faeces (n = 4578) of wild birds and water samples were collected for viral detection. Also, the vegetation structure, water physical properties of wetlands, climatic conditions and wild bird community composition were determined. An overall AIV prevalence of 1.7%±0.4 was detected in faecal samples with important fluctuations among seasons and locations. Twenty-six AIV were isolated from the 78 RRT-PCR positive samples and eight different haemagglutinines and five neuraminidases were identified, being the combination H3N8 the most frequent. Variation partitioning procedures identified the combination of space and time variables as the most important pure factor – independently to other factors – explaining the variation in AIV prevalence (36.8%), followed by meteorological factor (21.5%) and wild bird community composition/vegetation structure (21.1%). These results contribute to the understanding of AIV ecological drivers in Spanish ecosystems and provide useful guidelines for AIV risk assessment identifying potential hotspots of AIV activity.
doi:10.1371/journal.pone.0046418
PMCID: PMC3495955  PMID: 23152749
8.  Factors Driving the Abundance of Ixodes ricinus Ticks and the Prevalence of Zoonotic I. ricinus-Borne Pathogens in Natural Foci 
Environmental factors may drive tick ecology and therefore tick-borne pathogen (TBP) epidemiology, which determines the risk to animals and humans of becoming infected by TBPs. For this reason, the aim of this study was to analyze the influence of environmental factors on the abundance of immature-stage Ixodes ricinus ticks and on the prevalence of two zoonotic I. ricinus-borne pathogens in natural foci of endemicity. I. ricinus abundance was measured at nine sites in the northern Iberian Peninsula by dragging the vegetation with a cotton flannelette, and ungulate abundance was measured by means of dung counts. In addition to ungulate abundance, data on variables related to spatial location, climate, and soil were gathered from the study sites. I. ricinus adults, nymphs, and larvae were collected from the vegetation, and a representative subsample of I. ricinus nymphs from each study site was analyzed by PCR for the detection of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum DNA. Mean prevalences of these pathogens were 4.0% ± 1.8% and 20.5% ± 3.7%, respectively. Statistical analyses confirmed the influence of spatial factors, climate, and ungulate abundance on I. ricinus larva abundance, while nymph abundance was related only to climate. Interestingly, cattle abundance rather than deer abundance was the main driver of B. burgdorferi sensu lato and A. phagocytophilum prevalence in I. ricinus nymphs in the study sites, where both domestic and wild ungulates coexist. The increasing abundance of cattle seems to increase the risk of other hosts becoming infected by A. phagocytophilum, while reducing the risk of being infected by B. burgdorferi sensu lato. Controlling ticks in cattle in areas where they coexist with wild ungulates would be more effective for TBP control than reducing ungulate abundance.
doi:10.1128/AEM.06564-11
PMCID: PMC3318823  PMID: 22286986
9.  A Bayesian approach to study the risk variables for tuberculosis occurrence in domestic and wild ungulates in South Central Spain 
Background
Bovine tuberculosis (bTB) is a chronic infectious disease mainly caused by Mycobacterium bovis. Although eradication is a priority for the European authorities, bTB remains active or even increasing in many countries, causing significant economic losses. The integral consideration of epidemiological factors is crucial to more cost-effectively allocate control measures. The aim of this study was to identify the nature and extent of the association between TB distribution and a list of potential risk factors regarding cattle, wild ungulates and environmental aspects in Ciudad Real, a Spanish province with one of the highest TB herd prevalences.
Results
We used a Bayesian mixed effects multivariable logistic regression model to predict TB occurrence in either domestic or wild mammals per municipality in 2007 by using information from the previous year. The municipal TB distribution and endemicity was clustered in the western part of the region and clearly overlapped with the explanatory variables identified in the final model: (1) incident cattle farms, (2) number of years of veterinary inspection of big game hunting events, (3) prevalence in wild boar, (4) number of sampled cattle, (5) persistent bTB-infected cattle farms, (6) prevalence in red deer, (7) proportion of beef farms, and (8) farms devoted to bullfighting cattle.
Conclusions
The combination of these eight variables in the final model highlights the importance of the persistence of the infection in the hosts, surveillance efforts and some cattle management choices in the circulation of M. bovis in the region. The spatial distribution of these variables, together with particular Mediterranean features that favour the wildlife-livestock interface may explain the M. bovis persistence in this region. Sanitary authorities should allocate efforts towards specific areas and epidemiological situations where the wildlife-livestock interface seems to critically hamper the definitive bTB eradication success.
doi:10.1186/1746-6148-8-148
PMCID: PMC3483254  PMID: 22931852
10.  Fine-tuning the space, time, and host distribution of mycobacteria in wildlife 
BMC Microbiology  2011;11:27.
Background
We describe the diversity of two kinds of mycobacteria isolates, environmental mycobacteria and Mycobacterium bovis collected from wild boar, fallow deer, red deer and cattle in Doñana National Park (DNP, Spain), analyzing their association with temporal, spatial and environmental factors.
Results
High diversity of environmental mycobacteria species and M. bovis typing patterns (TPs) were found. When assessing the factors underlying the presence of the most common types of both environmental mycobacteria and M. bovis TPs in DNP, we evidenced (i) host species differences in the occurrence, (ii) spatial structuration and (iii) differences in the degree of spatial association of specific types between host species. Co-infection of a single host by two M. bovis TPs occurred in all three wild ungulate species. In wild boar and red deer, isolation of one group of mycobacteria occurred more frequently in individuals not infected by the other group. While only three TPs were detected in wildlife between 1998 and 2003, up to 8 different ones were found during 2006-2007. The opposite was observed in cattle. Belonging to an M. bovis-infected social group was a significant risk factor for mycobacterial infection in red deer and wild boar, but not for fallow deer. M. bovis TPs were usually found closer to water marshland than MOTT.
Conclusions
The diversity of mycobacteria described herein is indicative of multiple introduction events and a complex multi-host and multi-pathogen epidemiology in DNP. Significant changes in the mycobacterial isolate community may have taken place, even in a short time period (1998 to 2007). Aspects of host social organization should be taken into account in wildlife epidemiology. Wildlife in DNP is frequently exposed to different species of non-tuberculous, environmental mycobacteria, which could interact with the immune response to pathogenic mycobacteria, although the effects are unknown. This research highlights the suitability of molecular typing for surveys at small spatial and temporal scales.
doi:10.1186/1471-2180-11-27
PMCID: PMC3040691  PMID: 21288321
11.  A Broad Assessment of Factors Determining Culicoides imicola Abundance: Modelling the Present and Forecasting Its Future in Climate Change Scenarios 
PLoS ONE  2010;5(12):e14236.
Bluetongue (BT) is still present in Europe and the introduction of new serotypes from endemic areas in the African continent is a possible threat. Culicoides imicola remains one of the most relevant BT vectors in Spain and research on the environmental determinants driving its life cycle is key to preventing and controlling BT. Our aim was to improve our understanding of the biotic and abiotic determinants of C. imicola by modelling its present abundance, studying the spatial pattern of predicted abundance in relation to BT outbreaks, and investigating how the predicted current distribution and abundance patterns might change under future (2011–2040) scenarios of climate change according to the Intergovernmental Panel on Climate Change. C. imicola abundance data from the bluetongue national surveillance programme were modelled with spatial, topoclimatic, host and soil factors. The influence of these factors was further assessed by variation partitioning procedures. The predicted abundance of C. imicola was also projected to a future period. Variation partitioning demonstrated that the pure effect of host and topoclimate factors explained a high percentage (>80%) of the variation. The pure effect of soil followed in importance in explaining the abundance of C. imicola. A close link was confirmed between C. imicola abundance and BT outbreaks. To the best of our knowledge, this study is the first to consider wild and domestic hosts in predictive modelling for an arthropod vector. The main findings regarding the near future show that there is no evidence to suggest that there will be an important increase in the distribution range of C. imicola; this contrasts with an expected increase in abundance in the areas where it is already present in mainland Spain. What may be expected regarding the future scenario for orbiviruses in mainland Spain, is that higher predicted C. imicola abundance may significantly change the rate of transmission of orbiviruses.
doi:10.1371/journal.pone.0014236
PMCID: PMC2997795  PMID: 21151914
12.  Spatial distribution and risk factors of Brucellosis in Iberian wild ungulates 
Background
The 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.
Methods
A 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.
Results
Mean 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.
Conclusions
In 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.
doi:10.1186/1471-2334-10-46
PMCID: PMC2841660  PMID: 20205703
13.  Evidence of the Importance of Host Habitat Use in Predicting the Dilution Effect of Wild Boar for Deer Exposure to Anaplasma spp 
PLoS ONE  2008;3(8):e2999.
Foci of tick-borne pathogens occur at fine spatial scales, and depend upon a complex arrangement of factors involving climate, host abundance and landscape composition. It has been proposed that the presence of hosts that support tick feeding but not pathogen multiplication may dilute the transmission of the pathogen. However, models need to consider the spatial component to adequately explain how hosts, ticks and pathogens are distributed into the landscape.
In this study, a novel, lattice-derived, behavior-based, spatially-explicit model was developed to test how changes in the assumed perception of different landscape elements affect the outcome of the connectivity between patches and therefore the dilution effect. The objective of this study was to explain changes in the exposure rate (ER) of red deer to Anaplasma spp. under different configurations of suitable habitat and landscape fragmentation in the presence of variable densities of the potentially diluting host, wild boar. The model showed that the increase in habitat fragmentation had a deep impact on Habitat Sharing Ratio (HSR), a parameter describing the amount of habitat shared by red deer and wild boar, weighted by the probability of the animals to remain together in the same patch (according to movement rules), the density of ticks and the density of animals at a given vegetation patch, and decreased the dilution effect of wild boar on deer Anaplasma ER.
The model was validated with data collected on deer, wild boar and tick densities, climate, landscape composition, host vegetation preferences and deer seropositivity to Anaplasma spp. (as a measure of ER) in 10 study sites in Spain. However, although conditions were appropriate for a dilution effect, empirical results did not show a decrease in deer ER in sites with high wild boar densities. The model showed that the HSR was the most effective parameter to explain the absence of the dilution effect. These results suggest that host habitat usage may weaken the predicted dilution effect for tick-borne pathogens and emphasize the importance of the perceptual capabilities of different hosts in different landscapes and habitat fragmentation conditions for predictions of dilution effects.
doi:10.1371/journal.pone.0002999
PMCID: PMC2500193  PMID: 18714379
14.  Bovine Tuberculosis in Doñana Biosphere Reserve: The Role of Wild Ungulates as Disease Reservoirs in the Last Iberian Lynx Strongholds 
PLoS ONE  2008;3(7):e2776.
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.
doi:10.1371/journal.pone.0002776
PMCID: PMC2464716  PMID: 18648665

Results 1-14 (14)