Movement-driven modelling reveals new patterns in disease transmission networks.

Interspecific interactions are highly relevant in the potential transmission of shared pathogens in multi-host systems. In recent decades, several technologies have been developed to study pathogen transmission, such as proximity loggers, GPS tracking devices and/or camera traps. Despite the diversity of methods aimed at detecting contacts, the analysis of transmission risk is often reduced to contact rates and the probability of transmission given the contact. However, the latter process is continuous over time and unique for each contact, and is influenced by the characteristics of the contact and the pathogen's relationship with both the host and the environment. Our objective was to assess whether a more comprehensive approach, using a movement-based model which assigns a unique transmission risk to each contact by decomposing transmission into contact formation, contact duration and host characteristics, could reveal disease transmission dynamics that are not detected with more traditional approaches. The model was built from GPS-collar data from two management systems in Spain where animal tuberculosis (TB) circulates: a national park with extensively reared endemic cattle, and an area with extensive free-range pigs and cattle farms. In addition, we evaluated the effect of the GPS device fix rate on the performance of the model. Different transmission dynamics were identified between both management systems. Considering the specific conditions under which each contact occurs (i.e. whether the contact is direct or indirect, its duration, the hosts characteristics, the environmental conditions, etc.) resulted in the identification of different transmission dynamics compared to using only contact rates. We found that fix intervals greater than 30 min in the GPS tracking data resulted in missed interactions, and intervals greater than 2 h may be insufficient for epidemiological purposes. Our study shows that neglecting the conditions under which each contact occurs may result in a misidentification of the real role of each species in disease transmission. This study describes a clear and repeatable framework to study pathogen transmission from GPS data and provides further insights to understand how TB is maintained in multi-host systems in Mediterranean environments.

The method matters. A comparative study of biologging and camera traps as data sources with which to describe wildlife habitat selection.

Habitat use is a virtually universal activity among animals and is highly relevant as regards designing wildlife management and conservation actions. This has led to the development of a great variety of methods to study it, of which resource selection functions combined with biologging-derived data (RSF) is the most widely used for this purpose. However this approach has some constraints, such as its invasiveness and high costs. Analytical approaches taking into consideration imperfect detection coupled with camera trap data (IDM) have, therefore, emerged as a non-invasive cost-effective alternative. However, despite the fact that both approaches (RSF and IDM) have been used in habitat selection studies, they should also be comparatively assessed. The objective of this work is consequently to assess them from two perspectives: explanatory and predictive. This has been done by analyzing data obtained from camera traps (60 sampling sites) and biologging (17 animals monitored: 7 red deer Cervus elaphus, 6 fallow deer Dama dama and 4 wild boar Sus scrofa) in the same periods using IDM and RSF, respectively, in Doñana National Park (southern Spain) in order to explain and predict habitat use patterns for three studied species. Our results showed discrepancies between the two approaches, as they identified different predictors as being the most relevant to determine species intensity of use, and they predicted spatial patterns of habitat use with a contrasted level of concordance, depending on species and scale. Given these results and the characteristics of each approach, we suggested that although partly comparable interpretations can be obtained with both approaches, they are not equivalent but rather complementary. The combination of data from biologging and camera traps would, therefore, appear to be suitable for the development of an analytical framework with which to describe and characterise the habitat use processes of wildlife.

Environmental factors driving fine-scale ixodid tick abundance patterns.

Tick abundance is an essential demographic parameter to infer tick-borne pathogen transmission risks. Spatiotemporal patterns of tick abundance are heterogeneous, so its determinants at small spatial scales need to be understood to reduce their negative effects on hosts. Current knowledge of these determinants is scarce, especially in Mediterranean environments, limiting the possibilities for designing efficient tick control strategies. With the goal of unravelling tick abundance determinants and informing new tick management strategies, we estimated tick burdens on 1965 wild ungulates in Doñana National Park, Spain, annually between 2010 and 2020. Under the hypothesis of a predominant host influence on tick abundance, we modelled the burdens of Rhipicephalus annulatus, Hyalomma lusitanicum, and Ixodes ricinus with relevant predictors grouped into four factors: i) environment; ii) host population; iii) host individual; and iv) land-use. Generalized linear mixed models with a zero-inflated negative binomial distribution were built. Additionally, we analysed the differential contribution to abundance of each factor by deviance partitioning. We finally estimated the similarity in the environmental space of tick species by analysing their niche overlap with the environmental principal component analysis method. Our work hypothesis was confirmed for R. annulatus and H. lusitanicum, but we found that tick abundance at a fine spatial scale is jointly driven by multiple drivers, including all four factors considered in this study. This result points out that understanding the demography of ticks is a complex multifactorial issue, even at small spatial scales. We found no niche differences between the three tick species at the study spatial scale, thus showing similar host and environmental dependencies. Overall results identify that host aggregation areas displaying environmentally favourable traits for ticks are relevant tick and vector-borne pathogen transmission hotspots. Our findings will facilitate the design of new strategies to reduce the negative effects of tick parasitism.

A survey of shared pathogens at the domestic-wild ruminants' interface in Doñana National Park (Spain).

A cross-sectional study was carried out to evaluate shared pathogens that can be transmitted by close or non-close contact at the domestic-wild ruminants' interface. During summer-autumn 2015, a total of 138 cattle and 203 wild ruminants (red deer, Cervus elaphus, and fallow deer, Dama dama) were sampled in Doñana National Park (DNP, south-western Spain), a Mediterranean ecosystem well known for the interaction network occurring in the ungulate host community. Pestiviruses, bovine respiratory syncytial virus (BRSV; Bovine orthopneumovirus), bovine herpesvirus 1 (BoHV-1; Bovine alphaherpesvirus 1) and Mycobacterium tuberculosis complex (MTC) were assessed using serological, microbiological and molecular techniques. The overall seroprevalence against viruses in cattle was 2.2% for pestiviruses, 11.6% for BRSV and 27.5% for BoHV-1. No virus-specific antibodies were found in wildlife. MTC incidence in cattle was 15.9%, and MTC seroprevalence in wild ruminants was 14.3%. The same Mycobacterium bovis spoligotypes (SB1232, SB1230 and SB1610) were identified in cattle, red deer and fallow deer. The serological results for the selected respiratory viruses suggest epidemiological cycles only in cattle. Surveillance efforts in multi-host epidemiological scenarios are needed to better drive and prioritize control strategies for shared pathogens.

The spatial ecology of red deer under different land use and management scenarios: Protected areas, mixed farms and fenced hunting estates.

The knowledge regarding the spatial ecology of red deer (Cervus elaphus) in different environments is crucial if effective management actions are to be designed. However, this knowledge continues to be scarce in the complex contexts of mixed land use and management circumstances. This study describes the spatial ecology of red deer monitored using GPS collars in Mediterranean ecosystems of South-Central Spain, considering the effect of individual and seasonal (food shortage period, rut, hunting season and food abundance period) factors on different land use and management scenarios, namely protected areas, mixed farms and fenced hunting estates. Our results showed less activity (ACT), a shorter daily range (DR) and a smaller home range (HR) during the food shortage period: ACT: 0.38 ± (SD) 0.12; DR: 3010.9 ± 727.3 m; and weekly HR: 122.2 ± 59.6 ha. With regard to land use, individuals were less ACT and had a smaller DR on fenced hunting estates (ACT: 0.24 ± 0.12; DR: 1946.3 ± 706.7 m) than in protected areas (ACT: 0.59 ± 0.12; DR: 4071.4 ± 1068.2 m) or on mixed farms (ACT: 0.57 ± 0.29; DR: 5431.1 ± 1939.5 m) in all the periods studied. Red deer selected land cover with forage and shelter when foraging and resting, respectively. When drive hunt events occurred (mixed farms and fenced hunting estates), the deer were more prone to select safer habitats (scrublands) and avoid open areas (crops or grasslands) than were their counterparts in protected areas. The patterns observed can be explained by sexual and seasonal differences as regards requirements, the response to disturbances and, interestingly, population management. Our results provide useful information with which to design scientifically-based species adaptive management in response to relevant and timely situations in Europe, such as the potential transmission of shared infections, vehicle collisions, and damage to crops and ecosystems.

The wildlife-livestock interface on extensive free-ranging pig farms in central Spain during the "montanera" period.

The effective management of shared pathogens between wild ungulates and livestock requires the understanding of the processes of interaction between them. In this work, we studied the interspecific frequency of interaction (ifreq) and its spatiotemporal pattern between wild and domestic ungulates that coexist in free-ranging farms. For this purpose, 6 red deer, 6 wild boar, 8 Iberian pigs and 3 cattle were monitored using GPS devices during the "montanera" period (the period in which Iberian pigs are maintained in extensive conditions to feed on acorn). The ifreq was quantified for two spatiotemporal windows: 30 m - 10 min, for inferring potential direct interactions (short window), and 30 m - 12 days for indirect interactions (large window). Secondly, the variation in the ifreq was modelled with regard to 2 temporal (time of the day and week of the year) and 4 environmental factors (distance to water, distance to vegetation cover, Quercus density and distance to feeding points). The interactions at the short window were scarce (N = 13); however, they were very frequent at the large one (N = 37,429), with the red deer as the species with the greatest involvement in the interactions. Models showed that the time of the day and distance to water were the variables that best predicted the ifreq and they were conditioned by differences in the activity pattern of the targeted species. Food resource availability also predicted the ifreq, especially at the short window and between wild species. The results presented here highlight the role that wild ungulates may play in the transmission of pathogens to extensive livestock in general and pigs in particular and show the epidemiological risk of certain areas, periods of time and management practices (for wildlife and livestock) as well as providing useful information in the prevention of the transmission of shared pathogens.

Dynamic Network of Interactions in the Wildlife-Livestock Interface in Mediterranean Spain: An Epidemiological Point of View.

The correct management of diseases that are transmitted between wildlife and livestock requires a reliable estimate of the pathogen transmission rate. The calculation of this parameter is a challenge for epidemiologists, since transmission can occur through multiple pathways. The social network analysis is a widely used tool in epidemiology due to its capacity to identify individuals and communities with relevant roles for pathogen transmission. In the present work, we studied the dynamic network of interactions in a complex epidemiological scenario using information from different methodologies. In 2015, nine red deer, seven fallow deer, six wild boar and nine cattle were simultaneously monitored using GPS-GSM-Proximity collars in Doñana National Park. In addition, 16 proximity loggers were set in aggregation points. Using the social network analysis, we studied the dynamic network of interactions, including direct and indirect interactions, between individuals of different species and the potential transmission of pathogens within this network. The results show a high connection between species through indirect interactions, with a marked seasonality in the conformation of new interactions. Within the network, we differentiated four communities that included individuals of all the species. Regarding the transmission of pathogens, we observed the important role that fallow deer could be playing in the maintenance and transmission of pathogens to livestock. The present work shows the need to consider different types of methodologies in order to understand the complete functioning of the network of interactions at the wildlife/livestock interface. It also provides a methodological approach applicable to the management of shared diseases.

Tuberculosis Epidemiology and Badger (Meles meles) Spatial Ecology in a Hot-Spot Area in Atlantic Spain.

: We provide a temporal overview (from 2012 to 2018) of the outcomes of tuberculosis (TB) in the cattle and badger populations in a hot-spot in Asturias (Atlantic Spain). We also study the badger's spatial ecology from an epidemiological perspective in order to describe hazardous behavior in relation to TB transmission between cattle and badgers. Culture and single intradermal tuberculin test (SITT) were available for cattle as part of the National Program for the Eradication of TB. A field survey was also carried out in order to determine the paddocks and buildings used by each farm, and the information obtained was stored by using geographic information systems. Moreover, eighty-three badgers were submitted for necropsy and subsequent bacteriological studies. Ten badgers were also tracked, using global positioning system (GPS) collars. The prevalence of TB in cattle herds in the hot-spot increased from 2.2% in 2012 to 20% in 2016; it then declined to 0.0% in 2018. In contrast, the TB prevalence in badgers increased notably (from 5.55% in 2012-2015 to 10.64% in 2016-2018). Both cattle and badgers shared the same strain of Mycobacterium bovis. The collared badgers preferred paddocks used by TB-positive herds in spring and summer (when they were more active). The males occupied larger home ranges than the females (Khr95: males 149.78 ± 25.84 ha and females 73.37 ± 22.91 ha; Kcr50: males 29.83 ± 5.69 ha and females 13.59 ± 5.00 ha), and the home ranges were smaller in autumn and winter than in summer. The averages of the index of daily and maximum distances traveled by badgers were 1.88 ± (SD) 1.20 km and 1.99 ± 0.71 km, respectively. One of them presented a dispersive behavior with a maximum range of 18.3 km. The most preferred habitat was apple orchards in all seasons, with the exception of winter, in which they preferred pastures. Land uses and landscape structure, which have been linked with certain livestock-management practices, provide a scenario of great potential for badger-cattle interactions, thus enhancing the importance of the badgers' ecology, which could potentially transmit TB back to cattle in the future.

A vaccinology Approach to the Identification and Characterization of Dermanyssus Gallinae Candidate Protective Antigens for the Control of Poultry Red Mite Infestations.

The poultry red mite (PRM), Dermanyssus gallinae, is a hematophagous ectoparasite considered as the major pest in the egg-laying industry. Its pesticide-based control is only partially successful and requires the development of new control interventions such as vaccines. In this study, we follow a vaccinology approach to identify PRM candidate protective antigens. Based on proteomic data from fed and unfed nymph and adult mites, we selected a novel PRM protein, calumenin (Deg-CALU), which is tested as a vaccine candidate on an on-hen trial. Rhipicephalus microplus Subolesin (Rhm-SUB) was chosen as a positive control. Deg-CALU and Rhm-SUB reduced the mite oviposition by 35 and 44%, respectively. These results support Deg-CALU and Rhm-SUB as candidate protective antigens for the PRM control.

Spatio-temporal trends in the frequency of interspecific interactions between domestic and wild ungulates from Mediterranean Spain.

Controlling infections shared by wildlife and livestock requires the understanding and quantification of interspecific interactions between the species involved. This is particularly important in extensive multi-host systems, in which controlled domestic animals interact with uncontrolled, abundant and expanding wild species, such as wild ungulates. We have, therefore, quantified the interspecific interactions between wild boar (Sus scrofa) and free-ranging cattle in Mediterranean Spain, along with their spatio-temporal variability. GPS-GSM-collars were used to monitor 12 cows and 14 wild boar in the Doñana National Park between 2011 and 2013. Interactions were defined as encounters between cattle and wild boar within a spatio-temporal window of 52 m and 1 hour. On average, each wild boar interacted with one cow 1.5 ± (SE) 0.5 times per day, while each cow interacted with one wild boar 1.3 ± 0.4 times per day. The frequency of interaction was significantly higher during crepuscular hours owing to the overlap of both species' activity, and also during spring and autumn, probably owing to a higher individual aggregation around shared resources. Finally, the frequency of interaction was higher near the most significant shared resources (e.g. water points) but was lower in areas with dense vegetation. The results presented here show the usefulness of GPS monitoring as regards quantifying interactions and helping to clarify the process of pathogen transmission at the wildlife-livestock interface in Mediterranean Spain, along with the main spatio-temporal risk factors. In a changing scenario in which European populations of wild ungulates are increasing, more efficient measures with which to control interactions are required to meet the demands of farmers and managers. Our results, therefore, provide directional hypotheses that could be used to design disease control programmes.