Publications by authors named "Robbie A McDonald"

68 Publications

Genetic, social and maternal contributions to Mycobacterium bovis infection status in European badgers (Meles meles).

J Evol Biol 2021 Feb 22. Epub 2021 Feb 22.

Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Penryn Cornwall, TR10 9FE, UK.

Within host populations, individuals can vary in their susceptibility to infections and in the severity and progression of disease once infected. Though mediated through differences in behaviour, resistance or tolerance, variation in disease outcomes ultimately stems from genetic and environmental (including social) factors. Despite obvious implications for the evolutionary, ecological and epidemiological dynamics of disease traits, the relative importance of these factors has rarely been quantified in naturally infected wild animal hosts. Here, we use a long-term capture-mark-recapture study of group-living European badgers (Meles meles) to characterise genetic and environmental sources of variation in host infection status by Mycobacterium bovis, the causative agent of bovine tuberculosis (bTB). We find that genetic factors contribute to M. bovis infection status, whether measured over a lifetime or across repeated captures. In the latter case the heritability (h ) of infection status is close to zero in cubs and yearlings but increases in adulthood. Overall, environmental influences arising from a combination of social group membership (defined in time and space) and maternal effects appear to be more important than genetic factors. Thus, while genes do contribute to among-individual variation, they play a comparatively minor role, meaning that rapid evolution of host defences under parasite-mediated selection is unlikely (especially if selection is on young animals where h is lowest). Conversely, our results lend further support to the view that social and early-life environments are important drivers of the dynamics of bTB infection in badger populations specifically, and of disease traits in wild hosts more generally.
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http://dx.doi.org/10.1111/jeb.13775DOI Listing
February 2021

Provision of High Meat Content Food and Object Play Reduce Predation of Wild Animals by Domestic Cats Felis catus.

Curr Biol 2021 Feb 5. Epub 2021 Feb 5.

Environment and Sustainability Institute, University of Exeter, Penryn, Cornwall TR10 9FE, UK. Electronic address:

Predation by domestic cats Felis catus can be a threat to biodiversity conservation, but its mitigation is controversial. Confinement and collar-mounted devices can impede cat hunting success and reduce numbers of animals killed, but some owners do not wish to inhibit what they see as natural behavior, perceive safety risks associated with collars, or are concerned about device loss and ineffectiveness. In a controlled and replicated trial, we tested novel, non-invasive interventions that aim to make positive contributions to cat husbandry, alongside existing devices that impede hunting. Households where a high meat protein, grain-free food was provided, and households where 5-10 min of daily object play was introduced, recorded decreases of 36% and 25%, respectively, in numbers of animals captured and brought home by cats, relative to controls and the pre-treatment period. Introduction of puzzle feeders increased numbers by 33%. Fitting Birdsbesafe collar covers reduced the numbers of birds captured and brought home by 42% but had no discernible effect on mammals. Cat bells had no discernible effect. Reductions in predation can be made by non-invasive, positive contributions to cat nutrition and behavior that reduce their tendency to hunt, rather than impede their hunting. These measures are likely to find support among cat owners who are concerned about the welfare implications of other interventions.
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http://dx.doi.org/10.1016/j.cub.2020.12.044DOI Listing
February 2021

Characterization of potential superspreader farms for bovine tuberculosis: A review.

Vet Med Sci 2020 Sep 16. Epub 2020 Sep 16.

Environment and Sustainability Institute, University of Exeter, Penryn, Cornwall, UK.

Background: Variation in host attributes that influence their contact rates and infectiousness can lead some individuals to make disproportionate contributions to the spread of infections. Understanding the roles of such 'superspreaders' can be crucial in deciding where to direct disease surveillance and controls to greatest effect. In the epidemiology of bovine tuberculosis (bTB) in Great Britain, it has been suggested that a minority of cattle farms or herds might make disproportionate contributions to the spread of Mycobacterium bovis, and hence might be considered 'superspreader farms'.

Objectives And Methods: We review the literature to identify the characteristics of farms that have the potential to contribute to exceptional values in the three main components of the farm reproductive number - R : contact rate, infectiousness and duration of infectiousness, and therefore might characterize potential superspreader farms for bovine tuberculosis in Great Britain.

Results: Farms exhibit marked heterogeneity in contact rates arising from between-farm trading of cattle. A minority of farms act as trading hubs that greatly augment connections within cattle trading networks. Herd infectiousness might be increased by high within-herd transmission or the presence of supershedding individuals, or infectiousness might be prolonged due to undetected infections or by repeated local transmission, via wildlife or fomites.

Conclusions: Targeting control methods on putative superspreader farms might yield disproportionate benefits in controlling endemic bovine tuberculosis in Great Britain. However, real-time identification of any such farms, and integration of controls with industry practices, present analytical, operational and policy challenges.
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http://dx.doi.org/10.1002/vms3.358DOI Listing
September 2020

Estimating wildlife vaccination coverage using genetic methods.

Prev Vet Med 2020 Oct 18;183:105096. Epub 2020 Jul 18.

National Wildlife Management Centre, Animal and Plant Health Agency, Woodchester Park, Gloucestershire, GL10 3UJ, UK.

Vaccination is a useful approach for the control of disease in wildlife populations. However, its effectiveness is dependent in part on delivery to a sufficient proportion of the target population. Measuring the proportions of wild animal populations that have been vaccinated is challenging and so there is a need to develop robust approaches that can contribute to our understanding of the likely efficacy of wildlife vaccination campaigns. We used a modified capture mark recapture technique to estimate vaccine coverage in a wild population of European badgers (Meles meles) vaccinated by live-trapping and injecting with Bacillus Calmette-Guérin as part of a bovine tuberculosis control initiative in Wales, United Kingdom. Our approach used genetic matching of vaccinated animals to a sample of the wider population to estimate the percentage of badgers that had been vaccinated. Individual-specific genetic profiles were obtained using microsatellite genotyping of hair samples, which were collected directly from trapped and vaccinated badgers and non-invasively from the wider population using hair traps deployed at badger burrows (setts). With two nights of trapping at each sett in an annual campaign, an estimated 50 % (95 % confidence interval 40-60 %) of the badger population received at least one dose of vaccine in a single year. Using a simple population model this suggested that the proportion of the population that would have received at least one dose of vaccine over the course of the four year vaccination campaign was between 67 % and 83 %. This is the first attempt, outside of field trials, to quantify the level of vaccine coverage achieved by trapping and injecting badgers, which is currently the only option for delivering BCG vaccine to this species. The results therefore have specific application to bTB control policy and the novel approach may have wider value in wildlife management and research.
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http://dx.doi.org/10.1016/j.prevetmed.2020.105096DOI Listing
October 2020

Age-related variation in the trophic characteristics of a marsupial carnivore, the Tasmanian devil .

Ecol Evol 2020 Jul 7;10(14):7861-7871. Epub 2020 Jul 7.

Environment and Sustainability Institute University of Exeter Penryn UK.

Age-related changes in diet have implications for competitive interactions and for predator-prey dynamics, affecting individuals and groups at different life stages. To quantify patterns of variation and ontogenetic change in the diets of Tasmanian devils , a threatened marsupial carnivore, we analyzed variation in the stable isotope composition of whisker tissue samples taken from 91 individual devils from Wilmot, Tasmania from December 2014 to February 2017. Both δC and δN decreased with increasing age in weaned Tasmanian devils, indicating that as they age devils rely less on small mammals and birds, and more on large herbivores. Devils <12 months old had broader group isotopic niches, as estimated by Bayesian standard ellipses (SEA mode = 1.042) than devils from 12 to 23 months old (mode = 0.541) and devils ≥24 months old (mode = 0.532). Devils <24 months old had broader individual isotopic niches (SEA mode range 0.492-1.083) than devils ≥24 months old (mode range 0.092-0.240). A decrease in δN from the older whisker sections to the more recently grown sections in devils <24 months old likely reflects the period of weaning in this species, as this pattern was not observed in devils ≥24 months old. Our data reveal changes in the isotopic composition of devil whiskers with increasing age, accompanied by a reduction in isotopic variation both among population age classes and within individuals, reflecting the effect of weaning in early life, and a likely shift from an initially diverse diet of small mammals, birds, and invertebrates towards increasing consumption of larger herbivores in adulthood.
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http://dx.doi.org/10.1002/ece3.6513DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7391331PMC
July 2020

A pond-side test for Guinea worm: Development of a loop-mediated isothermal amplification (LAMP) assay for detection of Dracunculus medinensis.

Exp Parasitol 2020 Oct 2;217:107960. Epub 2020 Aug 2.

Environment and Sustainability Institute, University of Exeter, Penryn, TR10 9FE, UK.

Guinea worm Dracunculus medinensis causes debilitating disease in people and is subject to an ongoing global eradication programme. Research and controls are constrained by a lack of diagnostic tools. We developed a specific and sensitive LAMP method for detecting D. medinensis larval DNA in copepod vectors. We were able to detect a single larva in a background of field-collected copepods. This method could form the basis of a "pond-side test" for detecting potential sources of Guinea worm infection in the environment, in copepods, including in the guts of fish as potential transport hosts, enabling research, surveillance and targeting of control measures. The key constraint on the utility of this assay as a field diagnostic, is a lack of knowledge of variation in the temporal and spatial distribution of D. medinensis larvae in copepods in water bodies in the affected areas and how best to sample copepods to obtain a reliable diagnostic sample. These fundamental knowledge gaps could readily be addressed with field collections of samples across areas experiencing a range of worm infection frequencies, coupled with field and laboratory analyses using LAMP and PCR.
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http://dx.doi.org/10.1016/j.exppara.2020.107960DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7526612PMC
October 2020

Ecology of domestic dogs (Canis familiaris) as a host for Guinea worm (Dracunculus medinensis) infection in Ethiopia.

Transbound Emerg Dis 2020 Jul 2. Epub 2020 Jul 2.

Environment and Sustainability Institute, University of Exeter, Penryn, UK.

The global programme for the eradication of Guinea worm disease, caused by the parasitic nematode Dracunculus medinensis, has been successful in driving down human cases, but infections in non-human animals, particularly domestic dogs (Canis familiaris), now present a major obstacle to further progress. Dog infections have mainly been found in Chad and, to a lesser extent, in Mali and Ethiopia. While humans classically acquire infection by drinking water containing infected copepods, it has been hypothesized that dogs might additionally or alternatively acquire infection via a novel pathway, such as consumption of fish or frogs as possible transport or paratenic hosts. We characterized the ecology of free-ranging dogs living in three villages in Gog woreda, Gambella region, Ethiopia, in April-May 2018. We analysed their exposure to potential sources of Guinea worm infection and investigated risk factors associated with infection histories. The home ranges of 125 dogs and their activity around water sources were described using GPS tracking, and the diets of 119 dogs were described using stable isotope analysis. Unlike in Chad, where Guinea worm infection is most frequent, we found no ecological or behavioural correlates of infection history in dogs in Ethiopia. Unlike in Chad, there was no effect of variation among dogs in their consumption of aquatic vertebrates (fish or frogs) on their infection history, and we found no evidence to support hypotheses for this novel transmission pathway in Ethiopia. Dog owners had apparently increased the frequency of clean water provision to dogs in response to previous infections. Variations in dog ranging behaviour, owner behaviour and the characteristics of natural water bodies all influenced the exposure of dogs to potential sources of infection. This initial study suggests that the classical transmission pathway should be a focus of attention for Guinea worm control in non-human animals in Ethiopia.
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http://dx.doi.org/10.1111/tbed.13711DOI Listing
July 2020

Postrelease movement and habitat selection of translocated pine martens .

Ecol Evol 2020 Jun 14;10(11):5106-5118. Epub 2020 May 14.

Environment and Sustainability Institute University of Exeter Penryn UK.

Monitoring postrelease establishment and movement of animals is important in evaluating conservation translocations. We translocated 39 wild pine martens (19 females, 20 males) from Scotland to Wales. We released them into forested areas with no conspecifics in 2015, followed by a second release in 2016, alongside the previously released animals. We used radio-tracking to describe postrelease movement and habitat selection. Six martens (15%) were not re-encountered during the tracking period, of which four undertook long-distance dispersal. For the remaining individuals, we characterized two phases of movement, "exploration" followed by "settlement," that differed between releases. In the first release, martens remained in exploration phase for a mean of 14.5 days ( = 3.9 days) and settled at a mean distance of 8.7 km ( = 1.8 km) from release sites, whereas martens released in year two, alongside resident conspecifics, traveled away from release sites at a faster rate, settling sooner, at a mean of 6.6 days ( = 1.8 days), but further, at a mean distance of 14.0 km ( = 1.7 km) from release sites. Animals released in year one did not exhibit habitat preferences overall but within forests they favored recently felled areas, whereas animals released in year two showed strong selection for forested habitat but did not discriminate between forest types. The presence of conspecifics appeared influential for settlement and site fidelity of translocated martens and was associated with more rapid but more distant dispersal of the later cohort. Releases of animals in close proximity appeared to promote site fidelity and rapid establishment of ranges in the recipient environment.
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http://dx.doi.org/10.1002/ece3.6265DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7297779PMC
June 2020

Genetic evidence further elucidates the history and extent of badger introductions from Great Britain into Ireland.

R Soc Open Sci 2020 Apr 1;7(4):200288. Epub 2020 Apr 1.

Environment and Sustainability Institute, University of Exeter, Penryn, UK.

The colonization of Ireland by mammals has been the subject of extensive study using genetic methods and forms a central problem in understanding the phylogeography of European mammals after the Last Glacial Maximum. Ireland exhibits a depauperate mammal fauna relative to Great Britain and continental Europe, and a range of natural and anthropogenic processes have given rise to its modern fauna. Previous Europe-wide surveys of the European badger () have found conflicting microsatellite and mitochondrial DNA evidence in Irish populations, suggesting Irish badgers have arisen from admixture between human imported British and Scandinavian animals. The extent and history of contact between British and Irish badger populations remains unclear. We use comprehensive genetic data from Great Britain and Ireland to demonstrate that badgers in Ireland's northeastern and southeastern counties are genetically similar to contemporary British populations. Simulation analyses suggest this admixed population arose in Ireland 600-700 (CI 100-2600) years before present most likely through introduction of British badgers by people. These findings add to our knowledge of the complex colonization history of Ireland by mammals and the central role of humans in facilitating it.
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http://dx.doi.org/10.1098/rsos.200288DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7211870PMC
April 2020

Effects of trading networks on the risk of bovine tuberculosis incidents on cattle farms in Great Britain.

R Soc Open Sci 2020 Apr 22;7(4):191806. Epub 2020 Apr 22.

Environment and Sustainability Institute, Mathematics and Physical Sciences, University of Exeter, Penryn Campus, Penryn TR10 9FE, UK.

Trading animals between farms and via markets can provide a conduit for spread of infections. By studying trading networks, we might better understand the dynamics of livestock diseases. We constructed ingoing contact chains of cattle farms in Great Britain that were linked by trading, to elucidate potential pathways for the transmission of infection and to evaluate their effect on the risk of a farm experiencing a bovine tuberculosis (bTB) incident. Our findings are consistent with variation in bTB risk associated with region, herd size, disease risk area and history of previous bTB incidents on the root farm and nearby farms. However, we also identified effects of both direct and indirect trading patterns, such that connections to more farms in the England High-Risk Area up to three movements away from the root farm increased the odds of a bTB incident, while connections with more farms in the England Low-Risk Area up to eight movements away decreased the odds. Relative to other risk factors for bTB, trading behaviours are arguably more amenable to change, and consideration of risks associated with indirect trading, as well direct trading, might therefore offer an additional approach to bTB control in Great Britain.
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http://dx.doi.org/10.1098/rsos.191806DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7211880PMC
April 2020

Our Wild Companions: Domestic cats in the Anthropocene.

Trends Ecol Evol 2020 06 22;35(6):477-483. Epub 2020 Feb 22.

Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn, TR10 9FE, UK. Electronic address:

Cats share a long history with humans but are remarkable among domesticated species in largely retaining behavioural and reproductive independence from people. In many societies, the cat maintains liminal status as both a domestic and a wild animal. An adaptive push-and-pull between wild and domestic traits corresponds with dual roles as companions and pest controllers, and with conflicted treatment in husbandry, management, law, and public discourse. To move forward, we must proceed by understanding that cats are not exclusively pets or pests, but both a central component of human societies and an important, often adverse, influence on ecosystems. Developing a collaborative 'companion animal ecology', in which human-animal domestic relations link to ecological processes, will enable sustainable management of this wild companionship.
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http://dx.doi.org/10.1016/j.tree.2020.01.008DOI Listing
June 2020

Ecology of domestic dogs Canis familiaris as an emerging reservoir of Guinea worm Dracunculus medinensis infection.

PLoS Negl Trop Dis 2020 04 20;14(4):e0008170. Epub 2020 Apr 20.

The Carter Center, Atlanta, GA, United States of America.

Global eradication of human Guinea worm disease (dracunculiasis) has been set back by the emergence of infections in animals, particularly domestic dogs Canis familiaris. The ecology and epidemiology of this reservoir is unknown. We tracked dogs using GPS, inferred diets using stable isotope analysis and analysed correlates of infection in Chad, where numbers of Guinea worm infections are greatest. Dogs had small ranges that varied markedly among villages. Diets consisted largely of human staples and human faeces. A minority of ponds, mostly <200 m from dog-owning households, accounted for most dog exposure to potentially unsafe water. The risk of a dog having had Guinea worm was reduced in dogs living in households providing water for animals but increased with increasing fish consumption by dogs. Provision of safe water might reduce dog exposure to unsafe water, while prioritisation of proactive temephos (Abate) application to the small number of ponds to which dogs have most access is recommended. Fish might have an additional role as transport hosts for Guinea worm, by concentrating copepods infected with worm larvae.
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http://dx.doi.org/10.1371/journal.pntd.0008170DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7170223PMC
April 2020

Humanity's Best Friend: A Dog-Centric Approach to Addressing Global Challenges.

Animals (Basel) 2020 Mar 17;10(3). Epub 2020 Mar 17.

Palaeogenomics & Bio-Archaeology Research Network, School of Archaeology, 1 South Parks Road, Oxford OX1 3TG, UK.

No other animal has a closer mutualistic relationship with humans than the dog (). Domesticated from the Eurasian grey wolf (), dogs have evolved alongside humans over millennia in a relationship that has transformed dogs and the environments in which humans and dogs have co-inhabited. The story of the dog is the story of recent humanity, in all its biological and cultural complexity. By exploring human-dog-environment interactions throughout time and space, it is possible not only to understand vital elements of global history, but also to critically assess our present-day relationship with the natural world, and to begin to mitigate future global challenges. In this paper, co-authored by researchers from across the natural and social sciences, arts and humanities, we argue that a dog-centric approach provides a new model for future academic enquiry and engagement with both the public and the global environmental agenda.
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http://dx.doi.org/10.3390/ani10030502DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7142965PMC
March 2020

Stable isotopes are quantitative indicators of trophic niche.

Ecol Lett 2019 Nov 28;22(11):1990-1992. Epub 2019 Aug 28.

Centre for Ecology and Conservation, University of Exeter, Penryn, UK.

Hette-Tronquart (2019, Ecol. Lett.) raises three concerns about our interpretation of stable isotope data in Sheppard et al. (2018, Ecol. Lett., 21, 665). We feel that these concerns are based on comparisons that are unreasonable or ignore the ecological context from which the data were collected. Stable isotope ratios provide a quantitative indication of, rather than being exactly equivalent to, trophic niche.
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http://dx.doi.org/10.1111/ele.13374DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6851704PMC
November 2019

Integrating social behaviour, demography and disease dynamics in network models: applications to disease management in declining wildlife populations.

Philos Trans R Soc Lond B Biol Sci 2019 09 29;374(1781):20180211. Epub 2019 Jul 29.

Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn, UK.

The emergence and spread of infections can contribute to the decline and extinction of populations, particularly in conjunction with anthropogenic environmental change. The importance of heterogeneity in processes of transmission, resistance and tolerance is increasingly well understood in theory, but empirical studies that consider both the demographic and behavioural implications of infection are scarce. Non-random mixing of host individuals can impact the demographic thresholds that determine the amplification or attenuation of disease prevalence. Risk assessment and management of disease in threatened wildlife populations must therefore consider not just host density, but also the social structure of host populations. Here we integrate the most recent developments in epidemiological research from a demographic and social network perspective, and synthesize the latest developments in social network modelling for wildlife disease, to explore their applications to disease management in populations in decline and at risk of extinction. We use simulated examples to support our key points and reveal how disease-management strategies can and should exploit both behavioural and demographic information to prevent or control the spread of disease. Our synthesis highlights the importance of considering the combined impacts of demographic and behavioural processes in epidemics to successful disease management in a conservation context. This article is part of the theme issue 'Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation'.
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http://dx.doi.org/10.1098/rstb.2018.0211DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6710568PMC
September 2019

High-resolution contact networks of free-ranging domestic dogs Canis familiaris and implications for transmission of infection.

PLoS Negl Trop Dis 2019 07 15;13(7):e0007565. Epub 2019 Jul 15.

Environment and Sustainability Institute, University of Exeter, Cornwall, United Kingdom.

Contact patterns strongly influence the dynamics of disease transmission in both human and non-human animal populations. Domestic dogs Canis familiaris are a social species and are a reservoir for several zoonotic infections, yet few studies have empirically determined contact patterns within dog populations. Using high-resolution proximity logging technology, we characterised the contact networks of free-ranging domestic dogs from two settlements (n = 108 dogs, covering >80% of the population in each settlement) in rural Chad. We used these data to simulate the transmission of an infection comparable to rabies and investigated the effects of including observed contact heterogeneities on epidemic outcomes. We found that dog contact networks displayed considerable heterogeneity, particularly in the duration of contacts and that the network had communities that were highly correlated with household membership. Simulations using observed contact networks had smaller epidemic sizes than those that assumed random mixing, demonstrating the unsuitability of homogenous mixing models in predicting epidemic outcomes. When contact heterogeneities were included in simulations, the network position of the individual initially infected had an important effect on epidemic outcomes. The risk of an epidemic occurring was best predicted by the initially infected individual's ranked degree, while epidemic size was best predicted by the individual's ranked eigenvector centrality. For dogs in one settlement, we found that ranked eigenvector centrality was correlated with range size. Our results demonstrate that observed heterogeneities in contacts are important for the prediction of epidemiological outcomes in free-ranging domestic dogs. We show that individuals presenting a higher risk for disease transmission can be identified by their network position and provide evidence that observable traits hold potential for informing targeted disease management strategies.
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http://dx.doi.org/10.1371/journal.pntd.0007565DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6658143PMC
July 2019

Elevated aggression is associated with uncertainty in a network of dog dominance interactions.

Proc Biol Sci 2019 07 3;286(1906):20190536. Epub 2019 Jul 3.

1 Environment and Sustainability Institute, University of Exeter , Penryn TR10 9FE, Cornwall , UK.

Dominance hierarchies are widespread in animal societies and reduce the costs of within-group conflict over resources and reproduction. Variation in stability across a social hierarchy may result in asymmetries in the benefits obtained from hierarchy formation. However, variation in the stability and behavioural costs of dominance interactions with rank remain poorly understood. Previous theoretical models have predicted that the intensity of dominance interactions and aggression should increase with rank, but these models typically assume high reproductive skew, and so their generality remains untested. Here we show in a pack of free-living dogs with a sex-age-graded hierarchy that the central region of the hierarchy was dominated by more unstable social relationships and associated with elevated aggression. Our results reveal unavoidable costs of ascending a dominance hierarchy, run contrary to theoretical predictions for the relationship between aggression and social rank in high-skew societies, and widen our understanding of how heterogeneous benefits of hierarchy formation arise in animal societies.
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http://dx.doi.org/10.1098/rspb.2019.0536DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6650704PMC
July 2019

Predicting badger visits to farm yards and making predictions available to farmers.

PLoS One 2019 24;14(5):e0216953. Epub 2019 May 24.

Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn United Kingdom.

The use of agricultural resources or environments by wildlife may result in opportunities for transmission of infections amongst wild animals, livestock and humans. Targeted use of biosecurity measures may therefore reduce disease risks, although this requires practical knowledge of where such measures would be most effective, and effective means of communicating risks so that stakeholders can make informed decisions about such investment. In parts of Europe, the European badger Meles meles may act as a wildlife reservoir for Mycobacterium bovis, the causative agent of bovine tuberculosis, and badger visits to farmyards may provide potential opportunities for transmission of M. bovis to cattle. Biosecurity measures are effective in reducing badger activity in farmyards, although it is unclear which farms should be targeted with such measures. We used cameras to monitor badger activity in 155 farmyards in south west England and Wales, and related variations in the presence and frequency of badger visits to farm characteristics. Badgers were recorded on camera in 40% of farmyards monitored. However, the frequency of visits was highly variable, with badgers recorded on >50% of nights in only 10% of farms. The presence of badgers in farmyards was positively associated with the density of badger setts, the number of feed stores and the number of cattle sheds, and negatively associated with the distance to the nearest active badger sett, the presence of a house/dwelling and the number of cattle housed on the farm. The frequency of visits was negatively associated with the distance to the nearest active badger sett and the number of cattle housed. Models predicted the presence/absence of badgers in farmyards with 73% accuracy (62% sensitivity, 81% specificity, using a cut off value of 0.265). Models could not distinguish between farms with low/high frequency of visits, although farms predicted as having badgers present typically had a higher frequency of visits than those that were not. We developed and present an interactive web based application: the Badger Farm Assessment Tool (BFAT), to allow users to enter the characteristics of a farm and generate a relative risk score describing the likelihood of badger visits.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0216953PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6534311PMC
January 2020

Individual variation and the source-sink group dynamics of extra-group paternity in a social mammal.

Behav Ecol 2019 Mar-Apr;30(2):301-312. Epub 2019 Jan 14.

Centre for Ecology and Conservation, University of Exeter, Penryn, Cornwall, UK.

Movement of individuals, or their genes, can influence eco-evolutionary processes in structured populations. We have limited understanding of the extent to which spatial behavior varies among groups and individuals within populations. Here, we use genetic pedigree reconstruction in a long-term study of European badgers () to characterize the extent of extra-group paternity, occurring as a consequence of breeding excursions, and to test hypothesized drivers of variation at multiple levels. We jointly estimate parentage and paternity distance (PD; distance between a cub's natal and its father's social group), and test whether population density and sex ratio influence mean annual PD. We also model cub-level PD and extra-group paternity (EGP) to test for variation among social groups and parental individuals. Mean PD varied among years but was not explained by population density or sex ratio. However, cub-level analysis shows strong effects of social group, and parental identities, with some parental individuals being consistently more likely to produce cubs with extra-group partners. Group effects were partially explained by local sex ratio. There was also a strong negative correlation between maternal and paternal social group effects on cub paternity distance, indicating source-sink dynamics. Our analyses of paternity distance and EGP indicate variation in extra-group mating at multiple levels-among years, social groups and individuals. The latter in particular is a phenomenon seldom documented and suggests that gene flow among groups may be disproportionately mediated by a nonrandom subset of adults, emphasizing the importance of the individual in driving eco-evolutionary dynamics.
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http://dx.doi.org/10.1093/beheco/ary164DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6450204PMC
January 2019

Contact chains of cattle farms in Great Britain.

R Soc Open Sci 2019 Feb 27;6(2):180719. Epub 2019 Feb 27.

Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn TR10 9FE, UK.

Network analyses can assist in predicting the course of epidemics. Time-directed paths or 'contact chains' provide a measure of host-connectedness across specified timeframes, and so represent potential pathways for spread of infections with different epidemiological characteristics. We analysed networks and contact chains of cattle farms in Great Britain using Cattle Tracing System data from 2001 to 2015. We focused on the potential for between-farm transmission of bovine tuberculosis, a chronic infection with potential for hidden spread through the network. Networks were characterized by scale-free type properties, where individual farms were found to be influential 'hubs' in the network. We found a markedly bimodal distribution of farms with either small or very large ingoing and outgoing contact chains (ICCs and OCCs). As a result of their cattle purchases within 12-month periods, 47% of British farms were connected by ICCs to more than 1000 other farms and 16% were connected to more than 10 000 other farms. As a result of their cattle sales within 12-month periods, 66% of farms had OCCs that reached more than 1000 other farms and 15% reached more than 10 000 other farms. Over 19 000 farms had both ICCs and OCCs reaching more than 10 000 farms for two or more years. While farms with more contacts in their ICCs OCCs might play an important role in disease spread, farms with extensive ICCs OCCs might be particularly important by being at higher risk of both acquiring and disseminating infections.
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http://dx.doi.org/10.1098/rsos.180719DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6408381PMC
February 2019

Social structure contains epidemics and regulates individual roles in disease transmission in a group-living mammal.

Ecol Evol 2018 Dec 11;8(23):12044-12055. Epub 2018 Nov 11.

Department of Integrative Biology University of California, Berkeley Berkeley California.

Population structure is critical to infectious disease transmission. As a result, theoretical and empirical contact network models of infectious disease spread are increasingly providing valuable insights into wildlife epidemiology. Analyzing an exceptionally detailed dataset on contact structure within a high-density population of European badgers we show that a modular contact network produced by spatially structured stable social groups, lead to smaller epidemics, particularly for infections with intermediate transmissibility. The key advance is that we identify considerable variation among individuals in their role in disease spread, with these new insights made possible by the detail in the badger dataset. Furthermore, the important impacts on epidemiology are found even though the modularity of the Badger network is much lower than the threshold that previous work suggested was necessary. These findings reveal the importance of stable social group structure for disease dynamics with important management implications for socially structured populations.
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http://dx.doi.org/10.1002/ece3.4664DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6303749PMC
December 2018

Bait uptake by wild badgers and its implications for oral vaccination against tuberculosis.

PLoS One 2018 9;13(11):e0206136. Epub 2018 Nov 9.

National Wildlife Management Centre, Animal and Plant Health Agency, Woodchester Park, Gloucestershire, United Kingdom.

The deployment of baits containing vaccines or toxins has been used successfully in the management of wildlife populations, including for disease control. Optimisation of deployment strategies seeks to maximise uptake by the targeted population whilst ensuring cost-effectiveness. Tuberculosis (TB) caused by infection with Mycobacterium bovis affects a broad range of mammalian hosts across the globe, including cattle, wildlife and humans. The control of TB in cattle in the UK and Republic of Ireland is hampered by persistent infection in European badgers (Meles meles). The present study aimed to determine the best strategy for maximising uptake of an oral vaccine by wild badgers, using a surrogate novel bait deployed at 40 badger social groups. Baits contained a blood-borne biomarker (Iophenoxic Acid, IPA) in order to measure consumption in badgers subsequently cage trapped at targeted setts. Evidence for the consumption of bait was found in 83% (199/240) of captured badgers. The probability that badgers had consumed at least one bait (IPA >10 μg ml-1) was significantly higher following deployment in spring than in summer. Lower uptake amongst social groups where more badgers were captured, suggested competition for baits. The probability of bait consumption was significantly higher at groups where main and outlier setts were provided with baits than at those where outliers were present but not baited. Badgers captured 10-14 days post bait feeding had significantly higher levels of bait uptake compared to those caught 24-28 days later. Uptake rates did not vary significantly in relation to badger age and whether bait was placed above ground or down setts. This study suggests that high levels of bait uptake can be achieved in wild badger populations and identifies factors influencing the potential success of different deployment strategies. The implications for the development of an oral badger vaccine are discussed.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0206136PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6226152PMC
April 2019

Inbreeding intensifies sex- and age-dependent disease in a wild mammal.

J Anim Ecol 2018 11 20;87(6):1500-1511. Epub 2018 Jul 20.

Centre for Ecology and Conservation, University of Exeter, Penryn, UK.

The mutation accumulation theory of senescence predicts that age-related deterioration of fitness can be exaggerated when inbreeding causes homozygosity for deleterious alleles. A vital component of fitness, in natural populations, is the incidence and progression of disease. Evidence is growing for natural links between inbreeding and ageing; between inbreeding and disease; between sex and ageing; and between sex and disease. However, there is scant evidence, to date, for links among age, disease, inbreeding and sex in a single natural population. Using ecological and epidemiological data from a long-term longitudinal field study, we show that in wild European badgers (Meles meles) exposed naturally to bovine tuberculosis (bTB), inbreeding (measured as multilocus homozygosity) intensifies a positive correlation between age and evidence of progressed infection (measured as an antibody response to bTB), but only among females. Male badgers suffer a steeper relationship between age and progressed infection than females, with no influence of inbred status. We found no link between inbreeding and the incidence of progressed infection during early life in either sex. Our findings highlight an age-related increase in the impact of inbreeding on a fitness-relevant trait (disease state) among females. This relationship is consistent with the predictions of the mutation accumulation theory of senescence, but other mechanisms could also play a role. For example, late-life declines in condition, arising through mechanisms other than mutation accumulation might have increased the magnitude of inbreeding depression in late life. Whichever mechanism causes the observed patterns, we have shown that inbreeding can influence age-dependent patterns of disease and, by extension, is likely to affect the magnitude and timing of the late-life declines in components of fitness that characterise senescence. Better understanding of sex-specific links between inbreeding, disease and ageing provides insights into population-level pathogen dynamics and could influence management strategies for wildlife reservoirs of zoonotic disease.
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http://dx.doi.org/10.1111/1365-2656.12878DOI Listing
November 2018

Decoupling of Genetic and Cultural Inheritance in a Wild Mammal.

Curr Biol 2018 06 24;28(11):1846-1850.e2. Epub 2018 May 24.

Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Penryn, Cornwall TR10 9FE, UK. Electronic address:

Cultural inheritance, the transmission of socially learned information across generations, is a non-genetic, "second inheritance system" capable of shaping phenotypic variation in humans and many non-human animals [1-3]. Studies of wild animals show that conformity [4, 5] and biases toward copying particular individuals [6, 7] can result in the rapid spread of culturally transmitted behavioral traits and a consequent increase in behavioral homogeneity within groups and populations [8, 9]. These findings support classic models of cultural evolution [10, 11], which predict that many-to-one or one-to-many transmission erodes within-group variance in culturally inherited traits. However, classic theory [10, 11] also predicts that within-group heterogeneity is preserved when offspring each learn from an exclusive role model. We tested this prediction in a wild mammal, the banded mongoose (Mungos mungo), in which offspring are reared by specific adult carers that are not their parents, providing an opportunity to disentangle genetic and cultural inheritance of behavior. We show using stable isotope analysis that young mongooses inherit their adult foraging niche from cultural role models, not from their genetic parents. As predicted by theory, one-to-one cultural transmission prevented blending inheritance and allowed the stable coexistence of distinct behavioral traditions within the same social groups. Our results confirm that cultural inheritance via role models can promote rather than erode behavioral heterogeneity in natural populations.
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http://dx.doi.org/10.1016/j.cub.2018.05.001DOI Listing
June 2018

Intragroup competition predicts individual foraging specialisation in a group-living mammal.

Ecol Lett 2018 05 14;21(5):665-673. Epub 2018 Mar 14.

Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Cornwall, TR10 9FE, UK.

Individual foraging specialisation has important ecological implications, but its causes in group-living species are unclear. One of the major consequences of group living is increased intragroup competition for resources. Foraging theory predicts that with increased competition, individuals should add new prey items to their diet, widening their foraging niche ('optimal foraging hypothesis'). However, classic competition theory suggests the opposite: that increased competition leads to niche partitioning and greater individual foraging specialisation ('niche partitioning hypothesis'). We tested these opposing predictions in wild, group-living banded mongooses (Mungos mungo), using stable isotope analysis of banded mongoose whiskers to quantify individual and group foraging niche. Individual foraging niche size declined with increasing group size, despite all groups having a similar overall niche size. Our findings support the prediction that competition promotes niche partitioning within social groups and suggest that individual foraging specialisation may play an important role in the formation of stable social groupings.
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http://dx.doi.org/10.1111/ele.12933DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5947261PMC
May 2018

Long-term increase in secondary exposure to anticoagulant rodenticides in European polecats Mustela putorius in Great Britain.

Environ Pollut 2018 May;236:689-698

Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn, Cornwall, TR10 9FE, UK. Electronic address:

As a result of legal protection and population recovery, European polecats (Mustela putorius) in Great Britain are expanding into areas associated with greater usage of second-generation anticoagulant rodenticides (SGARs). We analysed polecat livers collected from road casualties from 2013 to 2016 for residues of five SGARs. We related variation in residues to polecat traits and potential exposure pathways, by analysing stable isotopes of carbon (δC) and nitrogen (δN) in their whiskers. 54 of 68 (79%) polecats had detectable residues of at least one SGAR. Bromadiolone (71%) was the most frequently detected compound, followed by difenacoum (53%) and brodifacoum (35%). Applying historical limits of detection to allow comparison between these new data and previous assessments, we show that in the 25 years from 1992 to 2016 inclusive, the rate of detection of SGARs in polecats in Britain has increased by a factor of 1.7. The probability of SGAR detection was positively related to increasing values of δN, suggesting that polecats feeding at a higher trophic level were more likely to be exposed. Total concentrations of SGARs in polecats with detectable residues were higher in polecats collected in arable compared to pastoral habitats, and in the west compared to the east of Britain. The number of compounds detected and total concentrations of SGARs increased with polecat age. There was no evidence of regional or seasonal variation in the probability of detecting SGARs, suggesting that the current risk of exposure to SGARs does not vary seasonally and has increased (from that in the 1990s) throughout the polecat's range. We recommend quantification of current practices in rodenticide usage, particularly in the light of recent regulatory changes, to enable assessment and mitigation of the risks of secondary exposure to rodenticides in non-target wildlife.
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http://dx.doi.org/10.1016/j.envpol.2018.02.004DOI Listing
May 2018

The parakeet protectors: Understanding opposition to introduced species management.

J Environ Manage 2019 Jan 2;229:120-132. Epub 2018 Jan 2.

Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn, Cornwall, TR10 9FE, UK.

The surveillance and control of introduced and invasive species has become an increasingly important component of environmental management. However, initiatives targeting 'charismatic' wildlife can be controversial. Opposition to management, and the subsequent emergence of social conflict, present significant challenges for would-be managers. Understanding the substance and development of these disputes is therefore vital for improving the legitimacy and effectiveness of wildlife management. It also provides important insights into human-wildlife relations and the 'social dimensions' of wildlife management. Here, we examine how the attempted eradication of small populations of introduced monk parakeets (Myiopsitta monachus) from England has been challenged and delayed by opposition from interested and affected communities. We consider how and why the UK Government's eradication initiative was opposed, focusing on three key themes: disagreements about justifying management, the development of affective attachments between people and parakeets, and the influence of distrustful and antagonistic relationships between proponents and opponents of management. We draw connections between our UK case and previous management disputes, primarily in the USA, and suggest that the resistance encountered in the UK might readily have been foreseen. We conclude by considering how management of this and other introduced species could be made less conflict-prone, and potentially more effective, by reconfiguring management approaches to be more anticipatory, flexible, sensitive, and inclusive.
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http://dx.doi.org/10.1016/j.jenvman.2017.11.036DOI Listing
January 2019

Contact networks structured by sex underpin sex-specific epidemiology of infection.

Ecol Lett 2018 02 20;21(2):309-318. Epub 2017 Dec 20.

Environment and Sustainability Institute, University of Exeter, Penryn, TR10 9FE, UK.

Contact networks are fundamental to the transmission of infection and host sex often affects the acquisition and progression of infection. However, the epidemiological impacts of sex-related variation in animal contact networks have rarely been investigated. We test the hypothesis that sex-biases in infection are related to variation in multilayer contact networks structured by sex in a population of European badgers Meles meles naturally infected with Mycobacterium bovis. Our key results are that male-male and between-sex networks are structured at broader spatial scales than female-female networks and that in male-male and between-sex contact networks, but not female-female networks, there is a significant relationship between infection and contacts with individuals in other groups. These sex differences in social behaviour may underpin male-biased acquisition of infection and may result in males being responsible for more between-group transmission. This highlights the importance of sex-related variation in host behaviour when managing animal diseases.
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http://dx.doi.org/10.1111/ele.12898DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6849844PMC
February 2018

Seasonal variation in daily patterns of social contacts in the European badger .

Ecol Evol 2017 11 25;7(21):9006-9015. Epub 2017 Sep 25.

Environment and Sustainability Institute University of Exeter Penryn UK.

Social interactions among hosts influence the persistence and spread of infectious pathogens. Daily and seasonal variation in the frequency and type of social interactions will play an important role in disease epidemiology and, alongside other factors, may have an influence on wider disease dynamics by causing seasonal forcing of infection, especially if the seasonal variation experienced by a population is considerable. We explored temporal variation in within-group contacts in a high-density population of European badgers naturally infected with (the causative agent of bovine tuberculosis). Summer contacts were more likely and of longer duration during the daytime, while the frequency and duration of winter contacts did not differ between day and night. In spring and autumn, within-group contacts peaked at dawn and dusk, corresponding with when they were of shortest duration with reduced potential for aerosol transmission of pathogens. Summer and winter could be critical for transmission of in badgers, due to the high frequency and duration of contacts during resting periods, and we discuss the links between this result and empirical disease data. This study reveals clear seasonality in daily patterns of contact frequency and duration in species living in stable social groups, suggesting that changes in social contacts could drive seasonal forcing of infection in wildlife populations even when the number of individuals interacting remains similar.
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http://dx.doi.org/10.1002/ece3.3402DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5677474PMC
November 2017

Field evaluation of candidate baits for oral delivery of BCG vaccine to European badgers, Meles meles.

Vaccine 2017 08 6;35(34):4402-4407. Epub 2017 Jul 6.

National Wildlife Management Centre, Animal and Plant Health Agency, Woodchester Park, Gloucestershire GL10 3UJ, UK. Electronic address:

The control of tuberculosis (TB) in cattle in the UK and Ireland is compromised by transmission of Mycobacterium bovis to cattle from the European badger (Meles meles), which acts as a wildlife reservoir. Vaccination of badgers could potentially contribute to TB control but the only licensed vaccine is injectable BadgerBCG which requires the live-capture of badgers. Current research is aimed at developing an oral TB vaccine (where vaccine is contained within bait) that is intended to be more cost-effective to deploy over large areas. In order to identify a lead product, candidate baits identified from captive badger studies were evaluated in three successive bait screening studies with wild badgers. A fourth field study, using the lead candidate bait and biomarkers, investigated the effectiveness of different carriers for their potential to deliver liquid payloads (vaccine surrogate). In each field study, bait disappearance was monitored daily for ten days and remote video surveillance was used to determine preference (i.e. the order in which baits were taken). In the carrier study, biomarkers were used to determine what proportion of subsequently trapped badgers had ingested the bait and the vaccine-carrier biomarker payload. Across all four studies, 79% (3397/4330) of baits were taken by badgers although the number varied significantly by badger social group and bait type. In all studies, bait disappearance increased over time, with 75-100% of baits being taken by day ten. In the carrier study, 75% (9/12) of trapped badgers tested positive for at least one of the biomarkers and the type of carrier did not influence bait attractiveness. Together with data from complementary laboratory and captive animal studies, this study identified a highly attractive and palatable bait (peanut-based paste bait; PT) and vaccine-carrier (hydrogenated peanut oil; HPO) combination with the potential to deliver a liquid vaccine to wild badgers.
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http://dx.doi.org/10.1016/j.vaccine.2017.06.059DOI Listing
August 2017