Human habitat modification, not apex scavenger decline, drives isotopic niche variation in a carnivore community.

Top carnivores can influence the structure of ecological communities, primarily through competition and predation; however, communities are also influenced by bottom-up forces such as anthropogenic habitat disturbance. Top carnivore declines will likely alter competitive dynamics within and amongst sympatric carnivore species. Increasing intraspecific competition is generally predicted to drive niche expansion and/or individual specialisation, while interspecific competition tends to constrain niches. Using stable isotope analysis of whiskers, we studied the effects of Tasmanian devil Sarcophilus harrisii declines upon the population- and individual-level isotopic niches of Tasmanian devils and sympatric spotted-tailed quolls Dasyurus maculatus subsp. maculatus. We investigated whether time since the onset of devil decline (a proxy for severity of decline) and landscape characteristics affected the isotopic niche breadth and overlap of devil and quoll populations. We quantified individual isotopic niche breadth for a subset of Tasmanian devils and spotted-tailed quolls and assessed whether between-site population niche variation was driven by individual-level specialisation. Tasmanian devils and spotted-tailed quolls demonstrated smaller population-level isotopic niche breadths with increasing human-modified habitat, while time since the onset of devil decline had no effect on population-level niche breadth or interspecific niche overlap. Individual isotopic niche breadths of Tasmanian devils and spotted-tailed quolls were narrower in human-modified landscapes, likely driving population isotopic niche contraction, however, the degree of individuals' specialisation relative to one another remained constant. Our results suggest that across varied landscapes, mammalian carnivore niches can be more sensitive to the bottom-up forces of anthropogenic habitat disturbance than to the top-down effects of top carnivore decline.

Multi-locus homozygosity promotes actuarial senescence in a wild mammal.

Genome-wide homozygosity, caused for example by inbreeding, is expected to have deleterious effects on survival and/or reproduction. Evolutionary theory predicts that any fitness costs are likely to be detected in late life because natural selection will filter out negative impacts on younger individuals with greater reproductive value. Here we infer associations between multi-locus homozygosity (MLH), sex, disease and age-dependent mortality risks using Bayesian analysis of the life histories of wild European badgers Meles meles in a population naturally infected with Mycobacterium bovis (the causative agent of bovine tuberculosis [bTB]). We find important effects of MLH on all parameters of the Gompertz-Makeham mortality hazard function, but particularly in later life. Our findings confirm the predicted association between genomic homozygosity and actuarial senescence. Increased homozygosity is particularly associated with an earlier onset, and greater rates of actuarial senescence, regardless of sex. The association between homozygosity and actuarial senescence is further amplified among badgers putatively infected with bTB. These results recommend further investigation into the ecological and behavioural processes that result in genome-wide homozygosity, and focused work on whether homozygosity is harmful or beneficial during early life-stages.

Using high-resolution LiDAR-derived canopy structure and topography to characterise hibernaculum locations of the hazel dormouse.

The hazel dormouse is predominantly an arboreal species that moves down to the ground to hibernate in the autumn in temperate parts of its distributional ranges at locations not yet well understood. The main objective of this study is to test whether environmental characteristics surrounding hazel dormouse hibernacula can be identified using high-resolution remote sensing and data collected in situ. To achieve this, remotely sensed variables, including canopy height and cover, topographic slope, sky view, solar radiation and cold air drainage, were modelled around 83 dormouse hibernacula in England (n = 62) and the Netherlands (n = 21), and environmental characteristics that may be favoured by pre-hibernating dormice were identified. Data on leaf litter depth, temperature, canopy cover and distance to the nearest tree were collected in situ and analysed at hibernaculum locations in England. The findings indicated that remotely sensed data were effective in identifying attributes surrounding the locations of dormouse hibernacula and when compared to in situ information, provided more conclusive results. This study suggests that remotely sensed topographic slope, canopy height and sky view have an influence on hazel dormice choosing suitable locations to hibernate; whilst in situ data suggested that average daily mean temperature at the hibernaculum may also have an effect. Remote sensing proved capable of identifying localised environmental characteristics in the wider landscape that may be important for hibernating dormice. This study proposes that this method can provide a novel progression from habitat modelling to conservation management for the hazel dormouse, as well as other species using habitats where topography and vegetation structure influence fine-resolution favourability.

Regime shift tipping point in hare population collapse associated with climatic and agricultural change during the very early 20th century.

Animal populations at northern latitudes may have cyclical dynamics that are degraded by climate change leading to trophic cascade. Hare populations at more southerly latitudes are characterized by dramatic declines in abundance associated with agricultural intensification. We focus on the impact of historical climatic and agricultural change on a mid-latitude population of mountain hares, Lepus timidus hibernicus. Using game bag records from multiple sites throughout Ireland, the hare population index exhibited a distinct regime shift. Contrary to expectations, there was a dynamical structure typical of northern latitude hare populations from 1853 to 1908, during which numbers were stable but cyclic with a periodicity of 8 years. This regime was replaced by dynamics more typical of southern latitude hare populations from 1909 to 1970, in which cycles were lost and numbers declined dramatically. Destabilization of the autumn North Atlantic Oscillation (NAO) led to the collapse of similar cycles in the hare population, coincident with the onset of agricultural intensification (a shift from small-to-large farms) in the first half of the 20th century. Similar, but more recent regime shifts have been observed in Arctic ecosystems and attributed to anthropogenic climate change. The present study suggests such shifts may have occurred at lower latitudes more than a century ago during the very early 20th century. It seems likely that similar tipping points in the population collapse of other farmland species may have occurred similarly early but went undocumented. As northern systems are increasingly impacted by climate change and probable expansion of agriculture, the interaction of these processes is likely to disrupt the pulsed flow of resources from cyclic populations impacting ecosystem function.

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

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 characterize 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 (h2 ) 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 h2 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.

Spatial and temporal dynamics of space use by free-ranging domestic dogs Canis familiaris in rural Africa.

Variation in the spatial ecology of animals influences the transmission of infections and so understanding host behavior can improve the control of diseases. Despite the global distribution of free-ranging domestic dogs Canis familiaris and their role as reservoirs for zoonotic diseases, little is known about the dynamics of their space use. We deployed GPS loggers on owned but free-ranging dogs from six villages in rural Chad, and tracked the movements of 174 individuals in the dry season and 151 in the wet season. We calculated 95% and core home ranges using auto-correlated kernel density estimates (AKDE95 and AKDEcore ), determined the degree to which their movements were predictable, and identified correlates of movement patterns. The median AKDE95 range in the dry season was 0.54 km2 and in the wet season was 0.31 km2 , while the median AKDEcore range in the dry season was 0.08 km2 and in the wet season was 0.04 km2 . Seasonal variation was, in part, related to owner activities; dogs from hunting households had ranges that were five times larger in the dry season. At least 70% of individuals were more predictably "at home" (<50 m from the household) throughout the day in the dry season, 80% of dogs demonstrated periodicity in activity levels (speed), and just over half the dogs exhibited periodicity in location (repeated space use). In the wet season, dogs mostly exhibited 24-h cycles in activity and location, with peaks at midday. In the dry season, dogs exhibited both 12- and 24-h cycles, with either a single peak at midday, or one peak between 06:00 and 12:00 and a second between 18:00 and 22:00. Strategies to control canine-mediated zoonoses can be improved by tailoring operations to the local spatial ecology of free-ranging dogs. Interventions using a door-to-door strategy in rural Chad would best conduct operations during the dry season, when access to dogs around their household more reliably exceeds 70% throughout the day. Given the importance of use in hunting for explaining variation in dog space-use, targeting approaches to disease control at the household level on the basis of owner activities offers potential to improve access to dogs.

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

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.

Stable isotopes are quantitative indicators of trophic niche.

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.

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

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.

The parakeet protectors: Understanding opposition to introduced species management.

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.

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

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.

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

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.

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.

Using Social Network Measures in Wildlife Disease Ecology, Epidemiology, and Management.

Contact networks, behavioral interactions, and shared use of space can all have important implications for the spread of disease in animals. Social networks enable the quantification of complex patterns of interactions; therefore, network analysis is becoming increasingly widespread in the study of infectious disease in animals, including wildlife. We present an introductory guide to using social-network-analytical approaches in wildlife disease ecology, epidemiology, and management. We focus on providing detailed practical guidance for the use of basic descriptive network measures by suggesting the research questions to which each technique is best suited and detailing the software available for each. We also discuss how using network approaches can be used beyond the study of social contacts and across a range of spatial and temporal scales. Finally, we integrate these approaches to examine how network analysis can be used to inform the implementation and monitoring of effective disease management strategies.

Determinants of woody encroachment and cover in African savannas.

Savanna ecosystems are an integral part of the African landscape and sustain the livelihoods of millions of people. Woody encroachment in savannas is a widespread phenomenon but its causes are widely debated. We review the extensive literature on woody encroachment to help improve understanding of the possible causes and to highlight where and how future scientific efforts to fully understand these causes should be focused. Rainfall is the most important determinant of maximum woody cover across Africa, but fire and herbivory interact to reduce woody cover below the maximum at many locations. We postulate that woody encroachment is most likely driven by CO2 enrichment and propose a two-system conceptual framework, whereby mechanisms of woody encroachment differ depending on whether the savanna is a wet or dry system. In dry savannas, the increased water-use efficiency in plants relaxes precipitation-driven constraints and increases woody growth. In wet savannas, the increase of carbon allocation to tree roots results in faster recovery rates after disturbance and a greater likelihood of reaching sexual maturity. Our proposed framework can be tested using a mixture of experimental and earth observational techniques. At a local level, changes in precipitation, burning regimes or herbivory could be driving woody encroachment, but are unlikely to be the explanation of this continent-wide phenomenon.

Wild small mammals as sentinels for the environmental transmission of antimicrobial resistance.

Antimicrobial resistance (AMR) represents a serious threat to human health worldwide. We have tested the use of free-living small mammals (mice, voles and shrews) as sentinels of variation in the distribution of AMR in the environment and the potential for transmission from the natural environment to animal hosts. Escherichia coli isolated from the faeces of small mammals trapped at paired coastal and inland sites were tested for resistance to four antibiotics: trimethoprim, ampicillin, ciprofloxacin and cefotaxime. Coastal individuals were over twice as likely to carry AMR E. coli than inland individuals (79% and 35% respectively), and both between-site and between-species variation was observed. Animals from coastal populations also excreted increased numbers of AMR E. coli and a greater diversity of E. coli phylotypes, including human-associated pathogenic strains. Small mammals appear to be useful bioindicators of fine-scale spatial variation in the distribution of AMR and, potentially, of the risks of AMR transmission to mammalian hosts, including humans.

Demographic buffering and compensatory recruitment promotes the persistence of disease in a wildlife population.

Demographic buffering allows populations to persist by compensating for fluctuations in vital rates, including disease-induced mortality. Using long-term data on a badger (Meles meles Linnaeus, 1758) population naturally infected with Mycobacterium bovis, we built an integrated population model to quantify impacts of disease, density and environmental drivers on survival and recruitment. Badgers exhibit a slow life-history strategy, having high rates of adult survival with low variance, and low but variable rates of recruitment. Recruitment exhibited strong negative density-dependence, but was not influenced by disease, while adult survival was density independent but declined with increasing prevalence of diseased individuals. Given that reproductive success is not depressed by disease prevalence, density-dependent recruitment of cubs is likely to compensate for disease-induced mortality. This combination of slow life history and compensatory recruitment promotes the persistence of a naturally infected badger population and helps to explain the badger's role as a persistent reservoir of M. bovis.

Age-related declines in immune response in a wild mammal are unrelated to immune cell telomere length.

Senescence has been hypothesized to arise in part from age-related declines in immune performance, but the patterns and drivers of within-individual age-related changes in immunity remain virtually unexplored in natural populations. Here, using a long-term epidemiological study of wild European badgers (Meles meles), we (i) present evidence of a within-individual age-related decline in the response of a key immune-signalling cytokine, interferon-gamma (IFNγ), to ex vivo lymphocyte stimulation, and (ii) investigate three putative drivers of individual variation in the rate of this decline (sex, disease and immune cell telomere length; ICTL). That the within-individual rate of age-related decline markedly exceeded that at the population level suggests that individuals with weaker IFNγ responses are selectively lost from this population. IFNγ responses appeared to decrease with the progression of bovine tuberculosis infection (independent of age) and were weaker among males than females. However, neither sex nor disease influenced the rate of age-related decline in IFNγ response. Similarly, while ICTL also declines with age, variation in ICTL predicted neither among- nor within-individual variation in IFNγ response. Our findings provide evidence of within-individual age-related declines in immune performance in a wild mammal and highlight the likely complexity of the mechanisms that generate them.

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.

Association of quantitative interferon-γ responses with the progression of naturally acquired Mycobacterium bovis infection in wild European badgers (Meles meles).

Bovine tuberculosis is one of the biggest challenges facing cattle farming in Great Britain. European badgers (Meles meles) are a reservoir host for the causal agent, Mycobacterium bovis. There have been significant recent advances in diagnostic testing for tuberculosis in humans, cattle and badgers, with the development of species-specific assays for interferon-γ (IFN-γ), an important cytokine in tuberculous infections. Using data collected from longitudinal studies of naturally infected wild badgers, we report that the magnitude of the IFN-γ response to M. bovis antigens at the disclosing test event was positively correlated with subsequent progression of disease to a seropositive or excreting state. In addition, we show that the magnitude of the IFN-γ response, despite fluctuation, declined with time after the disclosing event for all badgers, but remained significantly higher in those animals with evidence of disease progression. We discuss how our findings may be related to the immunopathogenesis of natural M. bovis infection in badgers.