Publications by year
Robertson A, Palphramand KL, McDonald RA, Middleton S, Chambers MA, Delahay RJ, Carter SP
(2022). Uptake of baits by wild badgers: Influences of deployment method, badger age and activity patterns on potential delivery of an oral vaccine. Prev Vet Med
Uptake of baits by wild badgers: Influences of deployment method, badger age and activity patterns on potential delivery of an oral vaccine.
In parts of the United Kingdom and Ireland, the European badger is a wildlife host for Mycobacterium bovis (the causative agent of bovine tuberculosis). Badger vaccination is one management option for reducing disease spread. Vaccination is currently achieved by parenteral vaccination of captured badgers, but an oral vaccine delivered in a bait may provide an additional approach in the future. We conducted two field experiments in wild badger populations to identify factors that influence uptake (% of individuals with evidence of bait consumption) of candidate oral vaccine baits. In both instances, baits containing the biomarker iophenoxic acid (as a proxy for the vaccine) were fed at burrows (setts) associated with badger social groups (study A = 48 groups, study B = 40 groups). Badgers were captured following a period of bait deployment to quantify uptake in relation to age, sex and social group. In addition, groups were allocated different treatments and the bait deployment protocol was varied to identify effects on uptake. Study a tested the effects of season, bait type, bait placement and packaging, while study B investigated the effects of bait quantity and badger activity levels. Overall bait uptake was low (Study A = 24 %, Study B = 37 %) but this varied among treatment groups (range 0-58 %). In both studies, bait uptake was significantly higher in cubs than in adults. Uptake was substantially higher where baits were placed directly into sett entrances (rather than under tiles near setts), and by badgers caught at main setts rather than at outlier setts. Season, bait type and packaging did not influence uptake, while increasing the quantity of bait available increased uptake by cubs but not by adults. Levels of badger activity at setts varied over time (suggesting potential disturbance), but were positively associated with levels of bait uptake. Abstract
. Author URL
Carter SP, Robertson A, Palphramand KL, Chambers MA, McDonald RA, Delahay RJ
(2018). Bait uptake by wild badgers and its implications for oral vaccination against tuberculosis. PLoS One
Bait uptake by wild badgers and its implications for oral vaccination against tuberculosis.
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. Abstract
. Author URL
Benton CH, Delahay RJ, Smith FAP, Robertson A, McDonald RA, Young AJ, Burke TA, Hodgson D
(2018). Inbreeding intensifies sex- and age-dependent disease in a wild mammal. J Anim Ecol
Inbreeding intensifies sex- and age-dependent disease in a wild mammal.
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. Abstract
. Author URL
McDonald JL, Robertson A, Silk MJ
(2018). Wildlife disease ecology from the individual to the population: Insights from a long-term study of a naturally infected European badger population. J Anim Ecol
Wildlife disease ecology from the individual to the population: Insights from a long-term study of a naturally infected European badger population.
Long-term individual-based datasets on host-pathogen systems are a rare and valuable resource for understanding the infectious disease dynamics in wildlife. A study of European badgers (Meles meles) naturally infected with bovine tuberculosis (bTB) at Woodchester Park in Gloucestershire (UK) has produced a unique dataset, facilitating investigation of a diverse range of epidemiological and ecological questions with implications for disease management. Since the 1970s, this badger population has been monitored with a systematic mark-recapture regime yielding a dataset of >15,000 captures of >3,000 individuals, providing detailed individual life-history, morphometric, genetic, reproductive and disease data. The annual prevalence of bTB in the Woodchester Park badger population exhibits no straightforward relationship with population density, and both the incidence and prevalence of Mycobacterium bovis show marked variation in space. The study has revealed phenotypic traits that are critical for understanding the social structure of badger populations along with mechanisms vital for understanding disease spread at different spatial resolutions. Woodchester-based studies have provided key insights into how host ecology can influence infection at different spatial and temporal scales. Specifically, it has revealed heterogeneity in epidemiological parameters; intrinsic and extrinsic factors affecting population dynamics; provided insights into senescence and individual life histories; and revealed consistent individual variation in foraging patterns, refuge use and social interactions. An improved understanding of ecological and epidemiological processes is imperative for effective disease management. Woodchester Park research has provided information of direct relevance to bTB management, and a better appreciation of the role of individual heterogeneity in disease transmission can contribute further in this regard. The Woodchester Park study system now offers a rare opportunity to seek a dynamic understanding of how individual-, group- and population-level processes interact. The wealth of existing data makes it possible to take a more integrative approach to examining how the consequences of individual heterogeneity scale to determine population-level pathogen dynamics and help advance our understanding of the ecological drivers of host-pathogen systems. Abstract
. Author URL
Palphramand K, Delahay R, Robertson A, Gowtage S, Williams GA, McDonald RA, Chambers M, Carter SP
(2017). Field evaluation of candidate baits for oral delivery of BCG vaccine to European badgers, Meles meles. Vaccine
Field evaluation of candidate baits for oral delivery of BCG vaccine to European badgers, Meles meles
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. Abstract
Robertson A, Delahay RJ, Wilson GJ, Vernon IJ, McDonald RA, Judge J
(2017). How well do farmers know their badgers? Relating farmer knowledge to ecological survey data. Vet Rec
How well do farmers know their badgers? Relating farmer knowledge to ecological survey data.
Knowledge of badger distribution is important for the management of bovine tuberculosis. At the farm level, typically the only information on badger activity available is from the farmers themselves. This study compares how well farmer perceptions of badger activity match data obtained from ecological surveys. Farmer estimates of numbers of badger setts (burrows) surrounding their farms were generally correlated with field survey results, but tended to be underestimates. Farmers correctly recorded 50 per cent of setts recorded in surveys, with larger setts and active setts more likely to be correctly recorded. Badger visits to farm buildings and yards were also monitored using surveillance cameras. The majority of farmers were aware of badger visits to their farm buildings, but in 22 per cent of cases farmers were not aware of badger visits. At the farm level, knowledge of badger activity will be useful in informing vets and animal health professionals of the potential risks of disease transmission, and hence directing management interventions. However, the tendency to underestimate activity, combined with a lack of detailed knowledge of sett locations, means that farmer estimates of badger activity should be interpreted with caution and in isolation may not be sufficient to inform management interventions. Abstract
. Author URL
Gowtage S, Williams GA, Henderson R, Aylett P, MacMorran D, Palmer S, Robertson A, Lesellier S, Carter SP, Chambers MA, et al
(2017). Testing of a palatable bait and compatible vaccine carrier for the oral vaccination of European badgers (Meles meles) against tuberculosis. Vaccine
Testing of a palatable bait and compatible vaccine carrier for the oral vaccination of European badgers (Meles meles) against tuberculosis.
The oral vaccination of wild badgers (Meles meles) with live Bacillus Calmette-Guérin (BCG) is one of the tools being considered for the control of bovine tuberculosis (caused by Mycobacterium bovis) in the UK. The design of a product for oral vaccination requires that numerous, and often competing, conditions are met. These include the need for a highly palatable, but physically stable bait that will meet regulatory requirements, and one which is also compatible with the vaccine formulation; in this case live BCG. In collaboration with two commercial bait companies we have developed a highly attractive and palatable bait recipe designed specifically for European badgers (Meles meles) that meets these requirements. The palatability of different batches of bait was evaluated against a standardised palatable control bait using captive badgers. The physical properties of the bait are described e.g. firmness and colour. The microbial load in the bait was assessed against European and US Pharmacopoeias. The bait was combined with an edible vaccine carrier made of hydrogenated peanut oil in which BCG vaccine was stable during bait manufacture and cold storage, demonstrating Abstract
. Author URL
Robertson A, Delahay RJ, McDonald RA, Aylett P, Henderson R, Gowtage S, Chambers MA, Carter SP
(2016). Behaviour of European badgers and non-target species towards candidate baits for oral delivery of a tuberculosis vaccine. Preventive Veterinary Medicine
Behaviour of European badgers and non-target species towards candidate baits for oral delivery of a tuberculosis vaccine
In the UK and the Republic of Ireland, the European badger (Meles meles) is a maintenance host for Mycobacterium bovis, and may transmit the infection to cattle causing bovine tuberculosis (TB). Vaccination of badgers using an injectable Bacillus Calmette-Guerin (BCG) vaccine is undertaken in some areas of the UK with the intention of interrupting this transmission, and vaccination research is underway in Ireland. An oral badger TB vaccine is also under development. We investigated the behaviour of badgers and non-target wildlife species towards three candidate baits being considered for delivering BCG to badgers orally. Bait preference was investigated by recording removal rates of baits and through the use of video surveillance at 16 badger setts. We found high variation in rates of bait removal by badgers among setts but no significant differences in removal rates among bait types or in preference behaviour from video footage. Variation in bait removal among setts correlated with the number of nights on which badgers were seen at the sett, with most baits being removed where badgers were seen on >50% of nights during the ten-day study period. Relatively few baits were removed at setts with low levels of recorded badger activity. Monitoring badger activity prior to bait deployment may therefore be useful in increasing bait uptake and vaccine coverage. Bait removal by badgers increased over the ten-day study period, suggesting initial neophobic behaviour at some setts and that a period of ‘pre-feeding’ may be required prior to vaccine deployment. Our results indicate that all three candidate baits are attractive to badgers. Removal of baits by non-target wildlife species was generally low, but varied among bait types, with smaller baits in packaging less likely to be removed. Enclosing baits in packaging is likely to deter non-target species, although in some cases non-target species did remove up to 13% of packaged baits. Abstract
Benton CH, Delahay RJ, Robertson A, McDonald RA, Wilson AJ, Burke TA, Hodgson D
(2016). Blood thicker than water: kinship, disease prevalence and group size drive divergent patterns of infection risk in a social mammal. Proc Biol Sci
Blood thicker than water: kinship, disease prevalence and group size drive divergent patterns of infection risk in a social mammal.
The importance of social- and kin-structuring of populations for the transmission of wildlife disease is widely assumed but poorly described. Social structure can help dilute risks of transmission for group members, and is relatively easy to measure, but kin-association represents a further level of population sub-structure that is harder to measure, particularly when association behaviours happen underground. Here, using epidemiological and molecular genetic data from a wild, high-density population of the European badger (Meles meles), we quantify the risks of infection with Mycobacterium bovis (the causative agent of tuberculosis) in cubs. The risk declines with increasing size of its social group, but this net dilution effect conceals divergent patterns of infection risk. Cubs only enjoy reduced risk when social groups have a higher proportion of test-negative individuals. Cubs suffer higher infection risk in social groups containing resident infectious adults, and these risks are exaggerated when cubs and infectious adults are closely related. We further identify key differences in infection risk associated with resident infectious males and females. We link our results to parent-offspring interactions and other kin-biased association, but also consider the possibility that susceptibility to infection is heritable. These patterns of infection risk help to explain the observation of a herd immunity effect in badgers following low-intensity vaccination campaigns. They also reveal kinship and kin-association to be important, and often hidden, drivers of disease transmission in social mammals. Abstract
. Author URL
Robertson A, Chambers MA, Delahay RJ, McDonald RA, Palphramand KL, Rogers F, Carter SP (2015). Exposure of nontarget wildlife to candidate TB vaccine baits deployed for European badgers. European Journal of Wildlife Research
Robertson A, Palphramand KL, Carter SP, Delahay RJ
(2015). Group size correlates with territory size in European badgers: Implications for the resource dispersion hypothesis?. Oikos
Group size correlates with territory size in European badgers: Implications for the resource dispersion hypothesis?
The resource dispersion hypothesis (RDH) predicts that resource heterogeneity can act as a passive cause of group-living in social carnivores and potentially many other species. One central prediction of the RDH is that territory size and group size are not related, as they are determined by resource dispersion and quality, respectively. In this study we investigated the relationship between territory size, group size and group composition in the European badger, a non-cooperative social mustelid whose behavioural ecology was central to the development of the RDH. Using data from a long-term study in the UK, we found that territory size and group size were positively related, contradicting a core prediction of the RDH. Furthermore, territory size was more strongly correlated with the number of adult males in the group than to the number of females or total group size. This result suggests that male badgers may have a more important role in territoriality and receive greater benefits from territory enlargement. These findings are consistent with the predictions of the anti-kleptogamy hypothesis, and suggest that badger territorial and social behaviour is not purely driven by resource dispersion, but may also be associated with breeding behaviour, as in other mustelids. Abstract
Ideozu EJ, Whiteoak AM, Tomlinson AJ, Robertson A, Delahay RJ, Hide G
(2015). High prevalence of trypanosomes in European badgers detected using ITS-PCR. Parasit Vectors
High prevalence of trypanosomes in European badgers detected using ITS-PCR.
BACKGROUND: Wildlife can be important sources and reservoirs for pathogens. Trypanosome infections are common in many mammalian species, and are pathogenic in some. Molecular detection tools were used to measure trypanosome prevalence in a well-studied population of wild European badgers (Meles meles). FINDINGS: a nested ITS-PCR system, that targeted the ribosomal RNA gene locus, has been widely used to detect pathogenic human and animal trypanosomes in domestic animals in Africa and some wildlife hosts. Samples from a long-term DEFRA funded capture-mark-recapture study of wild badgers at Woodchester Park (Gloucestershire, SW England) were investigated for trypanosome prevalence. A total of 82 badger blood samples were examined by nested ITS-PCR. Twenty-nine of the samples were found to be positive for trypanosomes giving a prevalence of 35.4% (25.9% - 46.2%; 95% CI). Infection was not found to be linked to badger condition, sex or age. Analysis of DNA sequence data showed the badgers to be infected with Trypanosoma (Megatrypanum) pestanai and phylogenetic analysis showed the Woodchester badger trypanosomes and T. pestanai to cluster in the Megatrypanum clade. CONCLUSIONS: the results show that the ITS Nested PCR is an effective tool for diagnosing trypanosome infection in badgers and suggests that it could be widely used in wildlife species with unknown trypanosomes or mixed infections. The relatively high prevalence observed in these badgers raises the possibility that a significant proportion of UK badgers are naturally infected with trypanosomes. Abstract
. Author URL
Robertson A, McDonald RA, Delahay RJ, Kelly SD, Bearhop S
(2015). Resource availability affects individual niche variation and its consequences in group-living European badgers Meles meles. Oecologia
Resource availability affects individual niche variation and its consequences in group-living European badgers Meles meles.
Although intra-population variation in niches is a widespread phenomenon with important implications for ecology, evolution and management of a range of animal species, the causes and consequences of this variation remain poorly understood. We used stable isotope analysis to characterise foraging niches and to investigate the causes and consequences of individual niche variation in the European badger, a mustelid mammal that lives in territorial social groups, but forages alone. We found that the degree of individual niche variation within social groups was negatively related to the availability of farmland habitats, which represent an important foraging habitat for badgers; and was positively related to territory size, supporting the idea that resource limitation and ecological opportunity lead to increased individual specialisation. We also found that the degree of individual specialisation related to an individual's body condition and that this effect varied with ecological context; such that specialisation had a stronger positive relationship with body condition in social groups with reduced availability of key farmland habitats. Body condition was also related to the utilisation of specific resources (woodland invertebrates), but again this relationship varied with the availability of farmland foraging habitats. This study supports the idea that resource availability plays an important role in determining patterns of individual niche variation, and identifies the potential adaptive consequences of specialised foraging strategies. Abstract
. Author URL
Trewby ID, Young R, McDonald RA, Wilson GJ, Davison J, Walker N, Robertson A, Doncaster CP, Delahay RJ
(2014). Impacts of removing badgers on localised counts of hedgehogs. PLoS One
Impacts of removing badgers on localised counts of hedgehogs.
Experimental evidence of the interactions among mammalian predators that eat or compete with one another is rare, due to the ethical and logistical challenges of managing wild populations in a controlled and replicated way. Here, we report on the opportunistic use of a replicated and controlled culling experiment (the Randomised Badger Culling Trial) to investigate the relationship between two sympatric predators: European badgers Meles meles and western European hedgehogs Erinaceus europaeus. In areas of preferred habitat (amenity grassland), counts of hedgehogs more than doubled over a 5-year period from the start of badger culling (from 0.9 ha-1 pre-cull to 2.4 ha-1 post-cull), whereas hedgehog counts did not change where there was no badger culling (0.3-0.3 hedgehogs ha-1). This trial provides experimental evidence for mesopredator release as an outcome of management of a top predator. Abstract
. Author URL
Robertson A, McDonald RA, Delahay RJ, Kelly SD, Bearhop S
(2014). Individual foraging specialisation in a social mammal: the European badger (Meles meles). Oecologia
Individual foraging specialisation in a social mammal: the European badger (Meles meles).
Individual specialisation has been identified in an increasing number of animal species and populations. However, in some groups, such as terrestrial mammals, it is difficult to disentangle individual niche variation from spatial variation in resource availability. In the present study, we investigate individual variation in the foraging niche of the European badger (Meles meles), a social carnivore that lives in a shared group territory, but forages predominantly alone. Using stable isotope analysis, we distinguish the extent to which foraging variation in badgers is determined by social and spatial constraints and by individual differences within groups. We found a tendency for individual badgers within groups to differ markedly and consistently in their isotope values, suggesting that individuals living with access to the same resources occupied distinctive foraging niches. Although sex had a significant effect on isotope values, substantial variation within groups occurred independently of age and sex. Individual differences were consistent over a period of several months and in some instances were highly consistent across the two years of the study, suggesting long-term individual foraging specialisations. Individual specialisation in foraging may, therefore, persist in populations of territorial species not solely as a result of spatial variation in resources, but also arising from individuals selecting differently from the same available resources. Although the exact cause of this behaviour is unknown, we suggest that specialisation may occur due to learning trade-offs which may limit individual niche widths. However, ecological factors at the group level, such as competition, may also influence the degree of specialisation. Abstract
. Author URL
Kelly DJ, Robertson A, Murphy D, Fitzsimons T, Costello E, Gormley E, Corner LAL, Marples NM
(2012). Trophic Enrichment Factors for Blood Serum in the European Badger (Meles meles). PLoS ONE
Trophic Enrichment Factors for Blood Serum in the European Badger (Meles meles)
Ecologists undertaking stable isotopic analyses of animal diets require trophic enrichment factors (TEFs) for the specific animal tissues that they are studying. Such basic data are available for a small number of species, so values from trophically or phylogenetically similar species are often substituted for missing values. By feeding a controlled diet to captive European badgers (Meles meles) we determined TEFs for carbon and nitrogen in blood serum. TEFs for nitrogen and carbon in blood serum were +3.0±0.4‰ and +0.4±0.1‰ respectively. The TEFs for serum in badgers are notably different from those published for the red fox (Vulpes vulpes). There is currently no data for TEFs in the serum of other mustelid species. Our data show that species sharing similar niches (red fox) do not provide adequate proxy values for TEFs of badgers. Our findings emphasise the importance of having species-specific data when undertaking trophic studies using stable isotope analysis. © 2012 Kelly et al. Abstract
Robertson A, McDonald RA, Delahay RJ, Kelly SD, Bearhop S (2012). Whisker growth in wild Eurasian badgers Meles meles: implications for stable isotope and bait marking studies. European Journal of Wildlife Research, 1-10.