Links between energy budgets, somatic condition, and life history reveal heterogeneous energy management tactics in a group-living mesocarnivore.

BACKGROUND: Optimal management of voluntary energy expenditure is crucial to the survival and reproductive success of wild animals. Nevertheless, a growing appreciation of inter-individual variation in the internal state driving movement suggests that individuals may follow different, yet equally optimal tactics under the same environmental conditions. However, few studies in wild populations have investigated the occurrence and demographic context of different contemporaneous energetic expenditure tactics. Here, we explore this neglected aspect of energy budgeting in order to determine the effect of life-history traits such as age and reproductive status on the co-occurrence of different energy-budgeting tactics in wild populations. METHODS: We investigated inter-individual heterogeneity in energy expenditure within a wild population of European badgers (Meles meles) by quantifying individual overall dynamic body acceleration (ODBA, from tri-axial accelerometry collars) and total daily energy expenditure (DEE, from doubly-labelled water) during 6-9 day deployments and dosing periods over six different seasons (spring, summer, and autumn) in 2018-2019. We obtained ODBA values for 41 deployments (24 unique badgers) and DEE measurements for 41 dosings (22 unique badgers). We then evaluated correlations between these energetic metrics and computed individual ratios of ODBA/DEE as a proxy for the proportion of total energy spent on activity. We measured the impact of alternative ODBA/DEE ratios on body condition, and use survival models constructed using 29 years of demographic data from the same population to situate body-condition changes in the context of age and reproductive status. RESULTS: Both ODBA and DEE were highly variable between individuals and exhibited season-specific relationships with individual body condition and life-history factors. DEE scaled allometrically with body weight, but only in summer and autumn; post-reproductive female badgers were lighter than other badgers during the spring but expended on average 350 kJ/day more than predicted from allometric scaling. Older badgers expended significantly less energy on movement during the summer than did younger adults. The ratio of ODBA to DEE (OD) provides a measure of proportional investment into movement. This ratio correlated more significantly with next-season body condition than either energetic metric did independently. However, the majority of individuals with high OD ratios were either younger badgers or reproductive females, for which lower body condition typically presented less of a mortality risk in previous analyses of this population. CONCLUSIONS: Within a single population under the same environmental conditions, we found wide inter-individual variation in both mechanical and total energy expenditure. The adoption of different tactics aligns with relationships between life-history parameters and mortality risk previously studied within the population. Crucially, younger badgers and reproductive females appeared able to tolerate energy expenditure tactics that depleted their body condition more than other badgers. These findings provide a mechanism by which differences in individual energetic context set by life history can maintain heterogeneity in wild populations, providing a wide range of potential energetic tactics under changing environmental conditions.

Variation in Pheidole nodus (Hymenoptera: Formicidae) functional morphology across urban parks.

Background: Habitat fragmentation and consequent population isolation in urban areas can impose significant selection pressures on individuals and species confined to urban islands, such as parks. Despite many comparative studies on the diversity and structure of ant community living in urban areas, studies on ants' responses to these highly variable ecosystems are often based on assemblage composition and interspecific mean trait values, which ignore the potential for high intraspecific functional trait variation among individuals. Methods: Here, we examined differences in functional traits among populations of the generalist ant Pheidole nodus fragmented between urban parks. We used pitfall trapping, which is more random and objective than sampling colonies directly, despite a trade-off against sample size. We then tested whether trait-filtering could explain phenotypic differences among urban park ant populations, and whether ant populations in different parks exhibited different phenotypic optima, leading to positional shifts in anatomical morphospace through the regional ant meta-population. Results: Intraspecific morphological differentiation was evident across this urban region. Populations had different convex hull volumes, positioned differently over the morphospace. Conclusions: Fragmentation and habitat degradation reduced phenotypic diversity and, ultimately, changed the morphological optima of populations in this urban landscape. Considering ants' broad taxonomic and functional diversity and their important role in ecosystems, further work over a variety of ant taxa is necessary to ascertain those varied morphological response pathways operating in response to population segregation in urban environments.

Assessing chronic stress in wild mammals using claw-derived cortisol: a validation using European badgers (Meles meles).

Measuring stress experienced by wild mammals is increasingly important in the context of human-induced rapid environmental change and initiatives to mitigate human-wildlife conflicts. Glucocorticoids (GC), such as cortisol, mediate responses by promoting physiological adjustments during environmental perturbations. Measuring cortisol is a popular technique; however, this often reveals only recent short-term stress such as that incurred by restraining the animal to sample blood, corrupting the veracity of this approach. Here we present a protocol using claw cortisol, compared with hair cortisol, as a long-term stress bio-indicator, which circumvents this constraint, where claw tissue archives the individual's GC concentration over preceding weeks. We then correlate our findings against detailed knowledge of European badger life history stressors. Based on a solid-phase extraction method, we assessed how claw cortisol concentrations related to season and badger sex, age and body-condition using a combination of generalized linear mixed models (GLMM) (n = 668 samples from 273 unique individuals) followed by finer scale mixed models for repeated measures (MMRM) (n = 152 re-captured individuals). Claw and hair cortisol assays achieved high accuracy, precision and repeatability, with similar sensitivity. The top GLMM model for claw cortisol included age, sex, season and the sex*season interaction. Overall, claw cortisol levels were significantly higher among males than females, but strongly influenced by season, where females had higher levels than males in autumn. The top fine scale MMRM model included sex, age and body condition, with claw cortisol significantly higher in males, older and thinner individuals. Hair cortisol was more variable than claw; nevertheless, there was a positive correlation after removing 34 outliers. We discuss strong support for these stress-related claw cortisol patterns from previous studies of badger biology. Given the potential of this technique, we conclude that it has broad application in conservation biology.

Ecotourist trail-use affects the taxonomic, functional and phylogenetic diversity of mammals in a protected area: lessons for conservation management.

Ecotourism, by definition, aims to engage peoples' interest in wildlife and the environment. The use of tourist roads and trails to access sites within protected areas (PAs) can detrimentally affect the behavior and distribution of species. The way mammals respond to anthropogenic pressures may differ across taxonomic, functional, and phylogenetic groups; nevertheless, how ecotourist trail-use affects these different diversity remains under-investigated. Here, we assessed 6 metrics of taxonomic, phylogenetic, and functional diversity for a mammal community in a PA in central China, recording how Trail use (using Trail type as a proxy) and habitat variables affected sightings and signs of mammals across 60 replicate 0.5 km transects. We then examined how Trail use affected the taxonomic, functional, and phylogenetic diversity indices of species (>1 kg). Using generalized liner mixed modeling, we identified that more used trail types had a greater adverse effect on all diversity richness indices than did less used trail types. Consequently, tourist pressure was associated with a general tendency to homogenize the site's mammal community. In contrast, the effects of Trail Types on all diversity evenness indices were non-significant. Furthermore, more developed and more heavily used trail types had a greater, significant negative effect on taxonomic, functional, and phylogenetic richness, whereas these richness indices were unaffected by minor trail types, used less intensively. As a general principle, lower biodiversity indices reduce ecosystem resilience, and so it is vital to better understand these responses to balance public access against biodiversity management in PAs.

Role of CT angiography and therapeutic anticoagulation in patients presenting to the emergency department with acute gastrointestinal bleeding.

INTRODUCTION: Acute gastrointestinal bleeding (GIB) is associated with morbidity and mortality. There can be a low threshold for practitioners to assess for active GIB and computed tomography angiography (CTA) examinations are performed frequently, even for stable patients and those who are therapeutically anticoagulated. We aimed to assess the predictive value of CTA for acute GIB and the influence of CTA on treatment. METHODS: Retrospective single-centre study over a 2-year period. RESULTS: A total of 227 patients with mean age 67.7 years (SD 17.86), 58.6% male. 84.4% were for lower GIB. 49 patients were on therapeutic anticoagulation (21.6%). 45 CTAs were positive (19.8%). 22 patients received embolisation, and 15 received acute endoscopic treatment. CTA sensitivity was 68.6% and specificity 89.1%. The PPV was 53.3% and NPV 93.9%. The odds ratio of a positive CTA requiring treatment for patients on therapeutic anticoagulation was 1.1 (P = 0.932) compared with the odds of patients not taking therapeutic anticoagulation 21.5 (P < 0.001). The risk ratio for requiring treatment if not taking anticoagulation was 6.2. A total of 19 patients (9.1%) met the definition of CI-AKI as a result of the CTA. A pre-existing eGFR of less than 20 was associated with significantly increased odds of developing CI-AKI (OR 3.95, P = 0.031, 95%CI 1.135-13.782). CONCLUSIONS: The presence of anticoagulation has a significant impact on the decision not to perform interventional treatments on patients with acute GIB when CTA is positive. Anticoagulant reversal and volume resuscitation are important front-line measures, and CTA may have a role for those anticoagulated who are haemodynamically unstable after resuscitation.

Infection with a Recently Discovered Gammaherpesvirus Variant in European Badgers, Meles meles, is Associated with Higher Relative Viral Loads in Blood.

Herpesviruses are ubiquitous pathogens infecting most animals. Although host immunity continually coevolves to combat virulence, viral variants with enhanced transmissibility or virulence occasionally emerge, resulting in disease burdens in host populations. Mustelid gammaherpesvirus 1 (MusGHV-1) is the only herpesvirus species identified thus far in European badgers, Meles meles. No MusGHV-1 associated pathomorbidity has been reported, but reactivation of MusGHV-1 in genital tracts is linked to impaired female reproductive success. An analysis of a short sequence from the highly conserved DNA polymerase (DNApol) gene previously identified two variants in a single host population. Here we compared genetic variance in blood samples from 66 known individuals of this same free-ranging badger population using a partial sequence comprising 2874 nucleotides of the DNApol gene, among which we identified 15 nucleotide differences resulting in 5 amino acid differences. Prevalence was 86% (59/66) for the common and 17% (11/66) for the novel variant, with 6% (4/66) of badgers presenting with coinfection. MusGHV-1 variants were distributed unevenly across the population, with individuals infected with the novel genotype clustered in 3 of 25 contiguous social groups. Individuals infected with the novel variant had significantly higher MusGHV-1 viral loads in their blood (p = 0.002) after adjusting for age (juveniles > adults, p < 0.001) and season (summer > spring and autumn, p = 0.005; mixed-effect linear regression), likely indicating higher virulence of the novel variant. Further genome-wide analyses of MusGHV-1 host resistance genes and host phenotypic variations are required to clarify the drivers and sequelae of this new MusGHV-1 variant.

The Huanan Seafood Wholesale Market in Wuhan was the early epicenter of the COVID-19 pandemic.

Understanding how severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) emerged in 2019 is critical to preventing future zoonotic outbreaks before they become the next pandemic. The Huanan Seafood Wholesale Market in Wuhan, China, was identified as a likely source of cases in early reports, but later this conclusion became controversial. We show here that the earliest known COVID-19 cases from December 2019, including those without reported direct links, were geographically centered on this market. We report that live SARS-CoV-2-susceptible mammals were sold at the market in late 2019 and that within the market, SARS-CoV-2-positive environmental samples were spatially associated with vendors selling live mammals. Although there is insufficient evidence to define upstream events, and exact circumstances remain obscure, our analyses indicate that the emergence of SARS-CoV-2 occurred through the live wildlife trade in China and show that the Huanan market was the epicenter of the COVID-19 pandemic.

Adverse weather during in utero development is linked to higher rates of later-life herpesvirus reactivation in adult European badgers, Meles meles.

Maternal immune and/or metabolic conditions relating to stress or nutritional status can affect in utero development among offspring with subsequent implications for later-life responses to infections. We used free-ranging European badgers as a host-pathogen model to investigate how prenatal weather conditions affect later-life herpesvirus genital tract reactivation. We applied a sliding window analysis of weather conditions to 164 samples collected in 2018 from 95 individuals born between 2005-2016. We test if the monthly mean and variation in rainfall and temperature experienced by their mother during the 12 months of delayed implantation and gestation prior to parturition subsequently affected individual herpes reactivation rates among these offspring. We identified four influential prenatal seasonal weather windows that corresponded with previously identified critical climatic conditions affecting badger survival, fecundity and body condition. These all occurred during the pre-implantation rather than the post-implantation period. We conclude that environmental cues during the in utero period of delayed implantation may result in changes that affect an individual's developmental programming against infection or viral reactivation later in life. This illustrates how prenatal adversity caused by environmental factors, such as climate change, can impact wildlife health and population dynamics-an interaction largely overlooked in wildlife management and conservation programmes.

Early-life seasonal, weather and social effects on telomere length in a wild mammal.

Early-life environmental conditions can provide a source of individual variation in life-history strategies and senescence patterns. Conditions experienced in early life can be quantified by measuring telomere length, which can act as a biomarker of survival probability in some species. Here, we investigate whether seasonal changes, weather conditions and group size are associated with early-life and/or early-adulthood telomere length in a wild population of European badgers (Meles meles). We found substantial intra-annual changes in telomere length during the first 3 years of life, where within-individual effects showed shorter telomere lengths in the winter following the first spring and a trend for longer telomere lengths in the second spring compared to the first winter. In terms of weather conditions, cubs born in warmer, wetter springs with low rainfall variability had longer early-life (3-12 months old) telomeres. Additionally, cubs born in groups with more cubs had marginally longer early-life telomeres, providing no evidence of resource constraint from cub competition. We also found that the positive association between early-life telomere length and cub survival probability remained when social and weather variables were included. Finally, after sexual maturity, in early adulthood (i.e., 12-36 months) we found no significant association between same-sex adult group size and telomere length (i.e., no effect of intrasexual competition). Overall, we show that controlling for seasonal effects, which are linked to food availability, is important in telomere length analyses, and that variation in telomere length in badgers reflects early-life conditions and also predicts first year cub survival.

Comparing Ant Assemblages and Functional Groups across Urban Habitats and Seasons in an East Asia Monsoon Climate Area.

China's East Asia monsoon zone is undergoing rapid land-use conversion and urbanization. Safeguarding remaining biodiversity requires reducing, mitigating, and/or eliminating the negative impacts of human-induced landscape modification. In this study, we sampled ground-dwelling ants at 40 plots over 12 continuous months in a suburban area in southwestern China to examine whether and how vegetation composition and habitat fragmentation affected species richness and assemblage composition for the general ant community and, specifically, for principal functional groups (including Opportunists and Generalized Myrmicinae). Warmer seasons were associated with a higher capture rate for all functional groups. Patterns of ant species richness among Opportunists were more sensitive to vegetation and fragmentation than for Generalized Myrmicinae, and these effects generally varied with season. Patterns of ant assemblage composition for Opportunists were exclusively sensitive to vegetation, whereas Generalized Myrmicinae were sensitive to both vegetation and fragmentation with variation among seasons. Overall, our findings highlight the important role of seasonality, vegetation composition, and habitat fragmentation in mediating the impacts of human-induced landscape modification on urbanized ant communities, which make an essential functional contribution to biodiversity in the East Asia monsoon zone.

Stress-Related Herpesvirus Reactivation in Badgers Can Result in Clostridium Proliferation.

Clostridium perfringens is an important food-borne zoonotic pathogen and a member of the commensal gut microbiome of many mammals. Predisposing factors such as coinfection with other pathogens or diet change can, however, cause overgrowth and subsequent disease development. Here we investigated the occurrence of C. perfringens in a free-ranging badger population with up to 100% prevalence of herpesvirus infection. Herpesvirus reactivation is known to be associated with increased susceptibility bacterial infections. PCR screening of rectal swabs from 69 free-ranging badgers revealed 15.9% (11/69, 95% CI = 9.1-26.3%) prevalence of detectable C. perfringens (Type A) DNA in the digestive tracts of assymptomatic animals. The results of Fisher's exact test revealed C. perfringens detection was not biased by age, sex and seasons. However, badgers with genital tract gammaherpesvirus (MusGHV-1) reactivation (p = 0.007) and infection with a specific MusGHV-1 genotype (p = 0.019) were more prone to of C. perfringens proliferation, indicating coinfection biased dynamics of intestinal C. perfringens. An inclusion pattern analysis further indicated that, causally, MusGHV-1 reactivation potentiated C. perfringens detection. Whether or not specific MusGHV-1 genotype infection or reactivation plays a role in C. perfringens overgrowth or disease development in badgers will require further investigation. Nevertheless, a postmortem examination of a single badger that died of fatal disease, likely associated with C. perfringens, revealed MusGHV-1 detection in the small intestine.

Prosecution records reveal pangolin trading networks in China, 2014-2019.

In a precautionary response to the current coronavirus (COVID-19) pandemic, China's Ministries permanently banned eating and trading in terrestrial wild (non-livestock) animals on 24 February 2020, and extensively updated the list of Fauna under Special State Protection (LFSSP) in 2020 and 2021, in which pangolins (Manidae spp.) were upgraded to the highest protection level. Examining 509 pangolin prosecution records from China Judgements online prior to these changes (01/01/14-31/12/19), we identified that Guangdong, Guangxi and Yunnan Provinces were hotspots for trade in whole pangolins and their scales. Interrupting trade in these three principal southern provinces would substantially fragment the pangolin trade network and reduce supply of imports from other south-east Asian countries. In the context of the revised legislation and strategies intended to prevent wildlife trade, we conclude that targeting interventions at key trade nodes could significantly reduce illegal trade in pangolins, and that this approach could also be effective with other taxa.

Patterns of Genital Tract Mustelid Gammaherpesvirus 1 (Musghv-1) Reactivation Are Linked to Stressors in European Badgers (Meles Meles).

Gammaherpesvirus reactivation can promote diseases or impair reproduction. Understanding reactivation patterns and associated risks of different stressors is therefore important. Nevertheless, outside the laboratory or captive environment, studies on the effects of stress on gammaherpesvirus reactivation in wild mammals are lacking. Here we used Mustelid gammaherpesvirus 1 (MusGHV-1) infection in European badgers (Meles meles) as a host-pathogen wildlife model to study the effects of a variety of demographic, physiological and environmental stressors on virus shedding in the genital tract. We collected 251 genital swabs from 150 free-ranging individuals across three seasons and screened them for the presence of MusGHV-1 DNA using PCR targeting the DNA polymerase gene. We explored possible links between MusGHV-1 DNA presence and seven variables reflecting stressors, using logistic regression analysis. The results reveal different sets of risk factors between juveniles and adults, likely reflecting primary infection and reactivation. In adults, virus shedding was more likely in badgers in poorer body condition and younger than 5 years or older than 7; while in juveniles, virus shedding is more likely in females and individuals in better body condition. However, living in social groups with more cubs was a risk factor for all badgers. We discuss possible explanations for these risk factors and their links to stress in badgers.

Seed dispersers shape the pulp nutrients of fleshy-fruited plants.

The dispersal-syndrome hypothesis posits that fruit traits are a product of selection by frugivores. Although criticized as adaptationist, recent studies have suggested that traits such as fruit or seed size, colour and odour exhibit signatures that imply selection by animal mutualists. These traits imply nutritional rewards (e.g. lipid, carbohydrate), attracting frugivores; however, this remains incompletely resolved. Here, we investigated whether fruit nutrients (lipid, sugar, protein, vitamin C, water content) moderate the co-adaptation of key disperser-group mutualisms. Multivariate techniques revealed that fruit nutrients assembled non-randomly and grouped according to key dispersal modes. Bird-dispersed fruits were richer in lipids than mammal-dispersed fruits. Mixed-dispersed fruits had significantly higher vitamin C than did mammal- or bird-dispersed fruits separately. Sugar and water content were consistently high irrespective of dispersal modes, suggesting that these traits appeal to both avian and mammalian frugivores to match high-energy requirements. Similarly, protein content was low irrespective of dispersal modes, corroborating that birds and mammals avoid protein-rich fruits, which are often associated with toxic levels of nitrogenous secondary compounds. Our results provide substantial over-arching evidence that seed disperser assemblages co-exert fundamental selection pressures on fruit nutrient trait adaptation, with broad implications for structuring fruit-frugivore mutualism and maintaining fruit trait diversity.

Animal sales from Wuhan wet markets immediately prior to the COVID-19 pandemic.

Here we document 47,381 individuals from 38 species, including 31 protected species sold between May 2017 and November 2019 in Wuhan's markets. We note that no pangolins (or bats) were traded, supporting reformed opinion that pangolins were not likely the spillover host at the source of the current coronavirus (COVID-19) pandemic. While we caution against the misattribution of COVID-19's origins, the wild animals on sale in Wuhan suffered poor welfare and hygiene conditions and we detail a range of other zoonotic infections they can potentially vector. Nevertheless, in a precautionary response to COVID-19, China's Ministries temporarily banned all wildlife trade on 26th Jan 2020 until the COVID-19 pandemic concludes, and permanently banned eating and trading terrestrial wild (non-livestock) animals for food on 24th Feb 2020. These interventions, intended to protect human health, redress previous trading and enforcement inconsistencies, and will have collateral benefits for global biodiversity conservation and animal welfare.

Alternative reproductive strategies provide a flexible mechanism for assuring mating success in the European badgers (Meles meles): An investigation from hormonal measures.

Selection-pressures differ with population density, but few studies investigate how this can affect reproductive physiology. European badger (Meles meles) density varies from solitary to group-living across their range, with reported mating periods throughout the entire year to specific seasonal periods. Badger reproduction is evolutionarily distinct, interrupting the direct progression from conception to gestation with delayed implantation (DI), allowing for superfecundation (SF). To establish the tactical mating flexibility afforded by DI*SF, we used cross-sectional population-level seasonal variation of circulating sex-steroids for 97 females from a high-density population. Oestradiol was highest in spring among non-parous females, then lower in summer, and remained low during following seasons, suggesting that the mating period was restricted to just spring. Oestrone was consistently higher than oestradiol; it was elevated in spring, lowest during summer, peaked in autumn, and remained elevated for pregnant females in winter. This suggests that oestrone sustains pre-implanted blastocysts throughout DI. Progesterone was low throughout, except during winter pregnancy, associated with implantation and luteal development. In contrast to multiple mating periods reported by lower-density studies, our oestradiol data suggest that, at high-density, females exhibit only one mating period (congruent with testosterone patterns in males studied previously in this same population). While additional mating periods during DI enhance fertility assurance at low-density, at high-density, we propose that when coitus is frequent, fertilisation is assured, precluding the need for further cycles and associated mating risks. This endocrinologically flexible DI*SF mating strategy likely represents a form of balancing selection, allowing badgers to succeed at a range of regional densities.

Understanding wildlife crime in China: Socio-demographic profiling and motivation of offenders.

Wildlife crime presents a growing threat to the integrity of ecological communities. While campaigns have raised consumer awareness, little is known about the socio-demographic profile of wildlife offenders, or how to intervene. Using data from China Judgements Online (2014-2018), we documented 4,735 cases, involving 7,244 offenders who smuggled, hunted, transported, sold and/or purchased protected species in contravention of China's Criminal Law. Offenders were predominantly men (93.0% of 7,143 offenders), aged 30-44 (43.9% of 4,699), agricultural workers (48.4% of 3,960), with less schooling (78.6% of 4,699 < senior secondary school). Socio-economic profiles related to crime seriousness, the type of illegal activity, motivation and taxon involved. These generalizations reveal scope to tailor specific intervention and mitigation approaches to offender profiles, through public information campaigns, proactive incentives opposed by punitive disincentives, and provision of alternative incomes.

A non-invasive method to assess the reproductive status of the European badger (Meles meles) from urinary sex-steroid metabolites.

Due to their unique reproductive physiology and behaviour, European badgers (Meles meles) are often used as a model to study mammalian reproduction. For reproductive endocrinology, circulating hormone levels are conventionally measured directly from blood samples. However, routine blood sampling is often not practical for wild animals and may induce stress affecting measurement accuracy. Non-invasive alternatives are thus of interest. Circulating hormones are metabolized through different routes, either by the kidneys, to be excreted through urine, or by the liver, to be excreted through faeces. These metabolites can thus be used as a proxy of hormone measurements, provided the species-specific metabolic characteristics are known. Here we tested the suitability of measuring urinary metabolites of circulating plasma sex-steroid hormones (testosterone in males and oestrogen in females) with enzyme immunoassays to assess the reproductive status of the European badger (Meles meles). Biological validation evidenced that urinary testosterone metabolite (UTM) and urinary total oestrogen metabolite (UEM) excretion patterns both corresponded with seasonal badger reproductive patterns on a population level, signaling correlation over a broad time frame. On an individual level, concurrent sampling of urine and plasma showed that male plasma testosterone and UTM levels correlated significantly across seasons, but no short term correlation was evident for total oestrogen and UEM in females. Thus, in badgers, urinary sex-steroid metabolites can be used reliably in the short term to assess male reproductive status at the individual level, but only at the broader population level for females.