Badgers and Badger Fleas: Strategies and Counter-Strategies

We examined the broad hypothesis that one function of grooming by the European badger (Meles meles) is to disadvantage (possibly by removal) parasitic badger fleas (Paraceris melis). We pursued two lines of investigation. First, we used infra‐red video analysis to examine the body areas reached by self‐ and allo‐grooming badgers. We expected that if grooming was important to disadvantage fleas then allo‐grooming would cover areas that could not be reached by self‐grooming. Badgers preferred dorsal allo‐grooming and ventral self‐grooming, and when combined, the overall amount of grooming per square centimetre of skin area provided even body coverage, pointing to a hygienic function, rather than a purely social function. Secondly, we examined fleas’ responses to simulated fur disturbance, characteristic of grooming. If grooming had no flea disadvantage effect, we would expect no response from fleas, and no directionality in their movement away from direct touch. The number of fleas encountered rapidly declined in successive 10‐s counts during simulated ‘grooming’ at the same site. When badgers were ‘groomed’ on alternate sides (mimicking the badgers’ rapid alternation of grooming position), there was a marked increase in fleas when grooming resumed on the original side. Similarly, when ‘grooming’ was suspended for 40 s, there was an initial increase in the number of fleas when ‘grooming’ was resumed. Disturbed fleas tended to run downwards relative to gravity and towards the posterior of the badger, following the direction of hair growth. This contrasted with the behaviour of fleas removed from badgers which tended to run upwards and jump. We concluded that the pattern of badger grooming and the fleas’ response to disturbance was consistent with a hypothesis that badgers and badger fleas have strategies and counter strategies to maximize and minimize contact (respectively) during grooming.     

Blood biochemistry reflects seasonal nutritional and reproductive constraints in the eurasian badger (Meles meles)

Physiological responses to nutritional and reproductive constraints were explored in a wild population of Eurasian badgers (Meles meles) inhabiting Wytham Woods, Oxfordshire, United Kingdom. We compared seasonal blood levels of lipid and protein compounds to variables describing the sex, age, body condition, wounds, testes position, and flea abundance of the badgers. We found seasonal variations in albumin/globulins and urea/creatinine ratios matched by differences in body condition. High creatinine, urea, and triglycerides levels were obtained in animals in poor nutritional condition and with low levels of body fat. The maintenance of urea/creatinine ratios indicates that the badger does not demonstrate a stage of protein conservation in periods of food scarcity during the summer or periods of cold weather. Hypercholesterolaemia, especially in fat animals, was confirmed. We also offer baseline levels of metabolites commonly used in clinical biochemistry for their further use in the analysis of the status and the management of wild badger populations.     

Culling-induced changes in badger (Meles meles) behaviour, social organisation and the epidemiology of bovine tuberculosis

In the UK, attempts since the 1970s to control the incidence of bovine tuberculosis (bTB) in cattle by culling a wildlife host, the European badger (Meles meles), have produced equivocal results. Culling-induced social perturbation of badger populations may lead to unexpected outcomes. We test predictions from the 'perturbation hypothesis', determining the impact of culling operations on badger populations, movement of surviving individuals and the influence on the epidemiology of bTB in badgers using data dervied from two study areas within the UK Government's Randomised Badger Culling Trial (RBCT). Culling operations did not remove all individuals from setts, with between 34-43% of badgers removed from targeted social groups. After culling, bTB prevalence increased in badger social groups neighbouring removals, particularly amongst cubs. Seventy individual adult badgers were fitted with radio-collars, yielding 8,311 locational fixes from both sites between November 2001 and December 2003. Home range areas of animals surviving within removed groups increased by 43.5% in response to culling. Overlap between summer ranges of individuals from Neighbouring social groups in the treatment population increased by 73.3% in response to culling. The movement rate of individuals between social groups was low, but increased after culling, in Removed and Neighbouring social groups. Increased bTB prevalence in Neighbouring groups was associated with badger movements both into and out of these groups, although none of the moving individuals themselves tested positive for bTB. Significant increases in both the frequency of individual badger movements between groups and the emergence of bTB were observed in response to culling. However, no direct evidence was found to link the two phenomena. We hypothesise that the social disruption caused by culling may not only increase direct contact and thus disease transmission between surviving badgers, but may also increase social stress within the surviving population, causing immunosuppression and enhancing the expression of disease.     

Increasing frequency of bite wounds with increasing population density in Eurasian badgers, Meles meles

Eurasian badgers sometimes live in territorial, mixed-sex groups; the adaptive significance of this is not understood, but members generally interact amicably. None the less, badgers occasionally fight and inflict sometimes severe wounds on one another. Based on 498 badger life histories, from first emergence as a cub until death, documented during a 10-year trapping study at Wytham Woods, Oxfordshire, U.K., the patterns and rates of bite wounding and consequential scarring were examined. Male badgers received more wounds and more severe wounds than did females. Wounding rates for both sexes increased significantly with age, and there was evidence that heavier individuals received most wounds. No seasonal pattern in wounding rates was apparent. During the study, the badger population size increased three-fold and wounding rates, particularly in males, showed a density-dependent increase. The rate of bite wounding increased with group size, and this increase was more marked among males than among females. Among males, but not females, the rate of bite wounding also increased with the number of badgers living in adjoining territories.     

Comparative study on the consequences of culling badgers (Meles meles) on biometrics, population dynamics and movement

1.  Capture–mark–recapture data were used to describe the process of recovery from a typical badger removal operation (BRO) at North Nibley, Gloucestershire, UK, which was carried out as part of the government's strategy to control bovine tuberculosis. Data on biometrics, demographics and movement from this low-density disturbed population were compared with those of two nearby high-density undisturbed populations (Wytham Woods and Woodchester Park, UK) in order to study fundamental principles of population dynamics and density-dependence.
2.  Badgers moved more between social groups at North Nibley than in the other study areas, particularly in the immediate aftermath of the removal operation.
3.  Recolonization of the vacated habitat occurred in the first instance by young females.
4.  Although in the first year after the BRO no cubs had been reared in any of the culled groups, and although the shortage of sexually mature boars may have limited the reproductive output of sows in the following year, the population took only 3 years to recover to its (already lowered) preremoval density.
5.  Losses from the adult (and cub) population due to mortality or emigration were smaller at North Nibley than at the other sites.
6.  There was much evidence that during 1995 and 1996 density-dependent effects constrained the reproductive output of the high-density populations, and some support for the hypothesis that badgers exhibit the non-linear 'large mammal' type of functional response to density.
7.  Badgers at North Nibley were younger, heavier and in better condition than badgers at Wytham Woods and Woodchester Park.
8.  We argue that the disease dynamics are likely to be different in disturbed compared with undisturbed badger populations, and that this could affect the effectiveness of BROs.     

The inadvertent introduction into Australia of Trypanosoma nabiasi, the trypanosome of the European rabbit (Oryctolagus cuniculus), and its potential for biocontrol

Wild rabbits (Oryctolagus cuniculus) in Australia are the descendents of 24 animals from England released in 1859. We surveyed rabbits and rabbit fleas (Spilopsyllus cuniculi) in Australia for the presence of trypanosomes using parasitological and PCR-based methods. Trypanosomes were detected in blood from the European rabbits by microscopy, and PCR using trypanosome-specific small subunit ribosomal RNA (SSU rRNA) gene primers and those in rabbit fleas by PCR. This is the first record of trypanosomes from rabbits in Australia. We identified these Australian rabbit trypanosomes as Trypanosoma nabiasi, the trypanosome of the European rabbit, by comparison of morphology and SSU rRNA gene sequences of Australian and European rabbit trypanosomes. Phylogenetic analysis places T. nabiasi in a clade with rodent trypanosomes in the subgenus Herpetosoma and their common link appears to be transmission by fleas. Despite the strict host specificity of trypanosomes in this clade, phylogenies presented here suggest that they have not strictly cospeciated with their vertebrate hosts. We suggest that T. nabiasi was inadvertently introduced into Australia in the 1960s in its flea vector Spilopsyllus cuniculi, which was deliberately introduced as a potential vector of the myxoma virus. In view of the environmental and economic damage caused by rabbits in Australia and other islands, the development of a virulent or genetically modified T. nabiasi should be considered to control rabbits.     

Bovine tuberculosis (Mycobacterium bovis) in British farmland wildlife: the importance to agriculture

Bovine tuberculosis (bTB) is an important disease of cattle and an emerging infectious disease of humans. Cow- and badger-based control strategies have failed to eradicate bTB from the British cattle herd, and the incidence is rising by about 18%per year. The annual cost to taxpayers in Britain is currently 74 million UK pounds. Research has focused on the badger as a potential bTB reservoir, with little attention being paid to other mammals common on farmland. We have conducted a systematic survey of wild mammals (n=4393 individuals) present on dairy farms to explore the role of species other than badgers in the epidemiology of bTB. Cultures were prepared from 10397 samples (primarily faeces, urine and tracheal aspirates). One of the 1307 bank voles (Clethrionomys glareolus) live-sampled, and three of the 43 badgers (Meles meles), yielded positive isolates of Mycobacterium bovis. This is the first time the bacterium has been isolated from the bank vole. The strain type was the same as that found in cattle and badgers on the same farm. However, our work indicates that the mean prevalence of infectious individuals among common farmland wildlife is extremely low (the upper 95% confidence interval is < or =2.0 for all of the abundant species). Mathematical models illustrate that it is highly unlikely the disease could be maintained at such low levels. Our results suggest that these animals are relatively unimportant as reservoirs of bTB, having insufficient within-species (or within-group) transmission to sustain the infection, though occasional spill-overs from cattle or badgers may occur.     

Epidemic and maintenance of rabies in chinese ferret badgers (Melogale moschata) indicated by epidemiology and the molecular signatures of rabies viruses

An epidemic of Chinese ferret badger-associated human rabies was investigated in Wuyuan county, Jiangxi province and rabies viruses isolates from ferret badgers in different districts in Jiangxi and Zhejiang provinces were sequenced with their nucleotides and amino acids and aligned for epidemiological analysis. The results showed that the human rabies in Wuyuan are only associated with ferret badger bites; the rabies virus can be isolated in a high percentage of ferret badgers in the epidemic areas in Jiangxi and Zhejiang provinces; the isolates share the same molecular features in nucleotides and have characteristic amino acid signatures, i.e., 2 sites in the nucleoprotein and 3 sites in the glycoprotein, that are distinct from virus isolates from dogs in the same region. We conclude that rabies in Chinese ferret badgers has formed an independent transmission cycle and ferret badgers may serve as another important rabies reservoir independent of dog rabies in China.     

Age, sex, and condition as predictors of moult and the efficacy of a novel fur-clip technique for individual marking of the European badger (Meles meles)

The European badger ( Meles meles ) moults once a year. In our study site in lowland England, pelage replacement of the guard hairs and a protracted period of fur growth (follicular anagen) occur between May and early November, with a peak in July. The precise timing of the moult depends on the age and condition of the badger. Yearling badgers undergo moult significantly earlier than adults. Adult females that have lactated, moult significantly later than other classes of adult, delaying the moult until autumn which corresponds to an annual period of food abundance. Lactation was significantly associated with poor condition in these badgers. It was not possible to determine whether delayed moult was due to poor condition per se , or due to some other physiological consequence of lactation, e.g. hormonal changes. We hypothesize that delay of moult in laclating/poor condition individuals has the adaptive consequence of delaying the metabolic costs of pelage replacement from a time of energy deficit until a time of relative plenty.
These findings are of practical importance to a novel solution to the problem of individually marking badgers during observational studies. The technique involves clipping the dark band near the tips of the badger's guard hairs to reveal the white under-fur and produce patterning of the coat. The highly contrasting marks were well suited to visual identification during observations under low light and infra-red illumination, and they allowed a large number of individuals (over 80 in our study) to be distinctively marked. The mark persists until the badger undergoes its single annual moult, or until three months of the active phase of fur growth have passed. Clip marks on adults made in late August had the greatest longevity, with 80% still visible after nine months. Though clipping had no significant effect on body condition in our study site, it should be cautiously applied with individuals in poor condition or in cold climates.     

The earliest European badger (Meles meles), from the Late Villafranchian site of Fuente Nueva 3 (Orce, Granada, SE Iberian Peninsula)

Paleontological and molecular data suggest that the divergence of the European and Asian badgers (Meles meles and Meles leucurus, respectively) from their ancestor Meles thorali might have taken place in the Middle to Late Villafranchian boundary (ca. 1.8 Ma). However, the available record of Late Villafrachian European badgers is scanty and poorly known, and this hypothesis needs more paleontological data in order to be tested. The badger hemimandible from the Iberian locality of Fuente Nueva 3, a locality placed in the beginning of the Late Villafranchian, supports the idea of an early divergence between European and Asian badgers.     

Use of cattle farm resources by badgers (Meles meles) and risk of bovine tuberculosis (Mycobacterium bovis) transmission to cattle

Nocturnal observations, radio telemetry and time-lapse camera surveillance were used to investigate visits by badgers (Meles meles L.) to two cattle farms. During 59 half-nights (ca. 295 h) of observation and 17 nights (ca. 154 h) of camera surveillance, 139 separate visits to farm buildings, by at least 26 individually identifiable badgers from two social groups, were recorded. The badgers, which included three individuals infected with bovine tuberculosis (Mycobacterium bovis), used cowsheds, feedsheds, barns, haystacks, slurry pits, cattle troughs and farmyards to exploit a range of food resources, including cattle feed and silage. Cattle feed was contaminated with badger faeces and badgers also came into close contact with cattle. The minimum number of badgers visiting farm buildings per night was negatively correlated with local 24 h rainfall. We conclude that exploitation by badgers of resources provided by cattle farms constitutes a potentially important mechanism for tuberculosis transmission from badgers to cattle.     

Absence of antibodies against canine distemper virus in free-ranging populations of the Eurasian badger in Great Britain

Canine distemper virus (CDV) is a serious disease of wild carnivores throughout the world. In Europe, infection has been detected in several carnivores including the Eurasian badger (Meles meles). In the present study 182 badger blood samples were collected from an intensively studied population of wild badgers in southwestern England (January-July, 1997), and a further 286 from throughout southern Britain (June 1996-November 1998). A neutralizing peroxidase-linked antibody test was used for the detection of antibodies against CDV. All the samples were negative for CDV antibodies, suggesting that in contrast to mainland Europe, the disease may be either absent or maintained at low levels in British badgers.     

Weather influences trapping success for tuberculosis management in European badgers (<Emphasis Type="Italic">Meles meles</Emphasis>)

European badgers (Meles meles) in Ireland and the UK are a reservoir for Mycobacterium bovis, the causative agent of bovine tuberculosis (TB). A number of interventions have been evaluated in attempts to control bovine TB within badger populations, and many of which rely on the capture of badgers. One strategy being implemented within Ireland is intramuscular vaccination using Bacillus Calmette-Guérin (BCG), as an alternative to badger culling. The success of vaccination as a disease control strategy depends on the ability to capture badgers and administer vaccines; thus, trapping success is crucial to effectively vaccinate the population (maximize vaccine coverage). A field vaccine trial was conducted in County Kilkenny, Ireland, from 2010–2013. We used data from this trial to evaluate the association between weather (precipitation and temperature data), badger sett characteristics, and badger trapping success. Approximately 10% of capture efforts resulted in a badger capture. Our results indicate that badger captures were the highest in drizzle, rain, and heavy rain weather conditions, and when minimum temperatures ranged from 3–8 °C. Badger captures were the highest at main setts (large burrow systems), and when sett activity scores were high (qualitative classes 4 or 5). Using local precipitation and temperature data in conjunction with observed sett characteristics provides wildlife managers with guidelines to optimize trapping success. Implementing capture operations under optimal conditions should increase the trapping success of badgers and allow for increased delivery of vaccines to manage bovine TB.     

Population ecology and prevalence of tuberculosis in Badgers in an area of Staffordshire

Forty-five badgers representing five social groups were removed from an area in Staffordshire where tuberculosis had occurred in cattle. Prior to removal, the tuberculosis status of the badger population was investigated by screening faeces samples, collected at fortnightly intervals, and badger social-group territories were determined by bait-marking. Samples for cultural and biological examination were taken from the live badgers before euthanasia and detailed post-mortem examination. The adult badger population density was 6-2/km2 and Mycobacterium bovis was isolated from samples taken post mortem from eight (17-8%) badgers. The results are reviewed in relation to previous findings.     

The distribution of Eurasian badger, Meles meles, setts in a high-density area: field observations contradict the sett dispersion hypothesis

Are setts significant determinants of badger socio‐spatial organisation, and do suitable sett sites represent a limited resource, potentially affecting badger distributions? The factors determining diurnal resting den, or sett, location and selection by Eurasian badgers Meles meles L. were investigated in Wytham Woods, Oxfordshire. 279 sett sites were located. The habitat parameters that were associated with the siting of these setts were analysed and associations were sought between sett location and character and the body condition and body weight of resident badgers Habitat characteristics in the vicinity of setts were significantly different from randomly selected points. Badgers preferentially selected sites with sandy, well‐drained soils, situated on NW‐facing, convex and moderately inclined slopes at moderate altitude. There was no evidence that sett morphology (number of entrances, sett area, number of hinterland latrines) was affected by the surrounding sett site habitat characteristics. Mean body weight was significantly higher for badgers occupying territories with setts in sandy soils, situated on NW‐facing slopes, than in territories with less optimal sett characteristics. Contrary to the hypothesis that the availability of sett sites was limiting, and therefore that sett dispersion dictates the spatial and social organisation of their populations, the badgers were clearly able to excavate new setts. On our measures, these new setts were not inferior to old established ones, despite occupying subsequently exploited sites; the badgers utilising these new setts had neither lighter body weights nor poorer body condition scores. During the period of our study badgers have manifestly been able to dig numerous new setts; as satisfactory sites still remain available, this indicates that suitable sett sites have not yet become a limiting resource. There was no relationship between sett age and the characteristics of the site in which it was dug, as suitable sites were not limiting. Significantly, population expansion during the decade 1987–1997 was not constrained by lack of setts, rather the main proliferation in setts occurred after the population size had peaked in 1996. Some implications for the management and conservation of the Eurasian badger are considered.     

Factors affecting population density, group size and territory size of the European badger, Meles meles

This paper discusses the relationship between the distribution and biomass of the main prey of European badgers, Meles meles and the badgers group size, territory size and population density. The distribution of areas rich in earthworms, Lumbricus spp., is correlated with badger range size, whilst badger group size increases with the biomass of worms per badger territory and badger density increases with overall worm biomass. Regulation of badger density in an area is likely to take place through regulation of group size, in the absence of other factors such as persecution and lack of suitable sett-sites.     

North Spain (Burgos) wild mammals ectoparasites

Twenty-seven species of arthropods were collected from 105 wild mammals, six wolves Canis lupus (Linnaeus, 1758) included. A total of 87 animals (82.8%) harboured some ectoparasites. Ticks were found in 60% of the samples, fleas in 51.4%, chewing-lice in 3.8%, and others (Mesostigmata and hippoboscids) in 3.8%. Moreover, 42.5% were single infestation and 57.5% mixed. Some of the species were new records for a host in spanish country such as Trichodectes canis (De Géer, 1778), Ixodes trianguliceps (Birula, 1895), Ceratophyllus (Monopsyllus) S. sciurorum (Schrank, 1803) and Paraceras melis melis (Walker, 1856) on several mammals. Two species were new records for Spain: Chaetopsylla matina (Jordan, 1925) and Archaeopsylla erinacei erinacei (Bouché, 1835).     

The flea epifauna of a suburban fox (Vulpes vulpes) population

Five hundred and thirteen fleas, of eight different species, were collected from a sample of 252 foxes killed in suburban London. 25–8% of foxes carried fleas, with a mean of 204 fleas per fox. Levels of infestation of male and female hosts did not differ significantly. Possible sources of the fleas infesting foxes are discussed with respect to their seasonal occurrence and fox prey composition. No evidence was found to support the suggestion that foxes obtain the majority of their fleas from prey items, although occasional heavy infestations of some flea species were probably derived from recent meals. Although Pulex irritans, Paraceras m. melis and Ctenocephalides canis , which contributed 35 % of the flea epifauna, could be considered parasitic on the fox, it seems probable that foxes pick up the majority of their fleas from the habitat through which they move. Thus, two particularly heavily infested categories of foxes were found: (1) juveniles during July-September, their fleas probably being accumulated during exploratory and play activities, and (2) all animals during the period October-December.     

Local feeding specialization by badgers (Meles meles) in a mediterranean environment

A case of local feeding specialization in the European badger (Meles meles), a carnivore species with morphological, physiological and behavioural traits proper to a trophic generalist, is described. For the first time, we report a mammalian species, the European rabbit (Oryctolagus cuniculus), as the preferred prey of badgers. Secondary prey are consumed according to their availability, compensating for temporal fluctuations in the abundance of rabbit kittens. We discuss how both predator (little ability to hunt) and prey (profitability and predictability) features, may favour the observed specialization, as predicted by foraging theory. Badgers show a trend to specialize on different prey in different areas throughout the species range. It is suggested that changes in prey features can reverse the badger feeding strategy at the population level. Such dynamic behavioural responses make difficult to label badgers as generalists or specialists at the species level.     

In situ adaptive response to climate and habitat quality variation: spatial and temporal variation in European badger (Meles meles) body weight

Variation in climatic and habitat conditions can affect populations through a variety of mechanisms, and these relationships can act at different temporal and spatial scales. Using post‐mortem badger body weight records from 15 878 individuals captured across the Republic of Ireland (7224 setts across ca. 15 000 km²; 2009–2012), we employed a hierarchical multilevel mixed model to evaluate the effects of climate (rainfall and temperature) and habitat quality (landscape suitability), while controlling for local abundance (unique badgers caught/sett/year). Body weight was affected strongly by temperature across a number of temporal scales (preceding month or season), with badgers being heavier if preceding temperatures (particularly during winter/spring) were warmer than the long‐term seasonal mean. There was less support for rainfall across different temporal scales, although badgers did exhibit heavier weights when greater rainfall occurred one or 2 months prior to capture. Badgers were also heavier in areas with higher landscape habitat quality, modulated by the number of individuals captured per sett, consistent with density‐dependent effects reducing weights. Overall, the mean badger body weight of culled individuals rose during the study period (2009–2012), more so for males than for females. With predicted increases in temperature, and rainfall, augmented by ongoing agricultural land conversion in this region, we project heavier individual badger body weights in the future. Increased body weight has been associated with higher fecundity, recruitment and survival rates in badgers, due to improved food availability and energetic budgets. We thus predict that climate change could increase the badger population across the Republic of Ireland. Nevertheless, we emphasize that, locally, populations could still be vulnerable to extreme weather variability coupled with detrimental agricultural practice, including population management.