HFCs (heterozygosity-fitness correlations) measure the direct relationship between an individual's genetic diversity and fitness. The effects of parental heterozygosity and the environment on HFCs are currently under-researched. We investigated these in a high-density U.K. population of European badgers (Meles meles), using a multimodel capture-mark-recapture framework and 35 microsatellite loci. We detected interannual variation in first-year, but not adult, survival probability. Adult females had higher annual survival probabilities than adult males. Cubs with more heterozygous fathers had higher first-year survival, but only in wetter summers; there was no relationship with individual or maternal heterozygosity. Moist soil conditions enhance badger food supply (earthworms), improving survival. In dryer years, higher indiscriminate mortality rates appear to mask differential heterozygosity-related survival effects. This paternal interaction was significant in the most supported model; however, the model-averaged estimate had a relative importance of 0.50 and overlapped zero slightly. First-year survival probabilities were not correlated with the inbreeding coefficient (f); however, small sample sizes limited the power to detect inbreeding depression. Correlations between individual heterozygosity and inbreeding were weak, in line with published meta-analyses showing that HFCs tend to be weak. We found support for general rather than local heterozygosity effects on first-year survival probability, and g2 indicated that our markers had power to detect inbreeding. We emphasize the importance of assessing how environmental stressors can influence the magnitude and direction of HFCs and of considering how parental genetic diversity can affect fitness-related traits, which could play an important role in the evolution of mate choice.
The marbled cat Pardofelis marmorata is a poorly known wild cat that has a broad distribution across much of the Indomalayan ecorealm. This felid is thought to exist at low population densities throughout its range, yet no estimates of its abundance exist, hampering assessment of its conservation status. To investigate the distribution and abundance of marbled cats we conducted intensive, felid-focused camera trap surveys of eight forest areas and two oil palm plantations in Sabah, Malaysian Borneo. Study sites were broadly representative of the range of habitat types and the gradient of anthropogenic disturbance and fragmentation present in contemporary Sabah. We recorded marbled cats from all forest study areas apart from a small, relatively isolated forest patch, although photographic detection frequency varied greatly between areas. No marbled cats were recorded within the plantations, but a single individual was recorded walking along the forest/plantation boundary. We collected sufficient numbers of marbled cat photographic captures at three study areas to permit density estimation based on spatially explicit capture-recapture analyses. Estimates of population density from the primary, lowland Danum Valley Conservation Area and primary upland, Tawau Hills Park, were 19.57 (SD: 8.36) and 7.10 (SD: 1.90) individuals per 100 km2, respectively, and the selectively logged, lowland Tabin Wildlife Reserve yielded an estimated density of 10.45 (SD: 3.38) individuals per 100 km2. The low detection frequencies recorded in our other survey sites and from published studies elsewhere in its range, and the absence of previous density estimates for this felid suggest that our density estimates may be from the higher end of their abundance spectrum. We provide recommendations for future marbled cat survey approaches.
The major histocompatibility complex (MHC) plays a crucial role in the immune system, and in some species, it is a target by which individuals choose mates to optimize the fitness of their offspring, potentially mediated by olfactory cues. Under the genetic compatibility hypothesis, individuals are predicted to choose mates with compatible MHC alleles, to increase the fitness of their offspring. Studies of MHC-based mate choice in wild mammals are under-represented currently, and few investigate more than one class of MHC genes. We investigated mate choice based on the compatibility of MHC class I and II genes in a wild population of European badgers (Meles meles). We also investigated mate choice based on microsatellite-derived pairwise relatedness, to attempt to distinguish MHC-specific effects from genomewide effects. We found MHC-assortative mating, based on MHC class II, but not class I genes. Parent pairs had smaller MHC class II DRB amino acid distances and smaller functional distances than expected from random pairings. When we separated the analyses into within-group and neighbouring-group parent pairs, only neighbouring-group pairs showed MHC-assortative mating, due to similarity at MHC class II loci. Our randomizations showed no evidence of genomewide-based inbreeding, based on 35 microsatellite loci; MHC class II similarity was therefore the apparent target of mate choice. We propose that MHC-assortative mate choice may be a local adaptation to endemic pathogens, and this assortative mate choice may have contributed to the low MHC genetic diversity in this population.
The innate immune system provides the primary vertebrate defence system against pathogen invasion, but it is energetically costly and can have immune pathological effects. A previous study in sticklebacks found that intermediate major histocompatibility complex (MHC) diversity correlated with a lower leukocyte coping capacity (LCC), compared to individuals with fewer, or many, MHC alleles. The organization of the MHC genes in mammals, however, differs to the highly duplicated MHC genes in sticklebacks by having far fewer loci. Using European badgers (Meles meles), we therefore investigated whether innate immune activity, estimated functionally as the ability of an individual's leukocytes to produce a respiratory burst, was influenced by MHC diversity. We also investigated whether LCC was influenced by factors such as age-class, sex, body condition, season, year, neutrophil and lymphocyte counts, and intensity of infection with five different pathogens. We found that LCC was not associated with specific MHC haplotypes, MHC alleles, or MHC diversity, indicating that the innate immune system did not compensate for the adaptive immune system even when there were susceptible MHC alleles/haplotypes, or when the MHC diversity was low. We also identified a seasonal and annual variation of LCC. This temporal variation of innate immunity was potentially due to physiological trade-offs or temporal variation in pathogen infections. The innate immunity, estimated as LCC, does not compensate for MHC diversity suggests that the immune system may function differently between vertebrates with different MHC organizations, with implications for the evolution of immune systems in different taxa.
Games are an increasingly popular approach for conservation teaching. However, we know little about the effectiveness of the games on students' experiences and knowledge acquisition. Many current games are supplemental games (SG) that have no meaningful interaction with the subject matter. We adapted the experiential gaming (EG) model where students were immersed in goal-orientated tasks found in real-life situations, and they tackled questions to complete actions for their main task. Classroom-based games were created for eight different conservation topics for an annual Wildlife Conservation Course and an annual Diploma in International Wildlife Conservation Practice. Data were collected over two cycles, a total sample size of 55 multinational students. We used a combination of repeated-measures design and counterbalanced measures design; each student was subjected at least twice to each of the EG and didactic instruction (DI) treatments, and at least once to the SG approach. We compared students' perception, learning and behavioural responses to the treatments, including measures of student personality types and learning styles as explanatory variables. Findings revealed multiple benefits of the classroom EG compared to the DI approach, such as increased attention retention, increased engagement and added intrinsic motivation. The improved level of intrinsic motivation was mainly facilitated by increased social bonding between participants. Further, we show that this EG approach appeals to a wide range of learning styles and personalities. The performance of SG was generally intermediate between that of EG and DI. We propose EG as a beneficial complement to traditional classroom teaching and current gamified classes for conservation education.
Niche differentiation, the partitioning of resources along one or more axes of a species' niche hyper-volume, is widely recognised as an important mechanism for sympatric species to reduce interspecific competition and predation risk, and thus facilitate co-existence. Resource partitioning may be facilitated by behavioural differentiation along three main niche dimensions: habitat, food and time. In this study, we investigate the extent to which these mechanisms can explain the coexistence of an assemblage of five sympatric felids in Borneo. Using multi-scale logistic regression, we show that Bornean felids exhibit differences in both their broad and fine-scale habitat use. We calculate temporal activity patterns and overlap between these species, and present evidence for temporal separation within this felid guild. Lastly, we conducted an all-subsets logistic regression to predict the occurrence of each felid species as a function of the co-occurrence of a large number of other species and showed that Bornean felids co-occurred with a range of other species, some of which could be candidate prey. Our study reveals apparent resource partitioning within the Bornean felid assemblage, operating along all three niche dimension axes. These results provide new insights into the ecology of these species and the broader community in which they live and also provide important information for conservation planning for this guild of predators.
Tiger subspecific taxonomy is controversial because of morphological and genetic variation found between now fragmented populations, yet the extent to which phenotypic plasticity or genetic variation affects phenotypes of putative tiger subspecies has not been explicitly addressed. In order to assess the role of phenotypic plasticity in determining skull variation, we compared skull morphology among continental tigers from zoos and the wild. In turn, we examine continental tiger skulls from across their wild range, to evaluate how the different environmental conditions experienced by individuals in the wild can influence morphological variation. Fifty-seven measurements from 172 specimens were used to analyse size and shape differences among wild and captive continental tiger skulls. Captive specimens have broader skulls, and shorter rostral depths and mandible heights than wild specimens. In addition, sagittal crest size is larger in wild Amur tigers compared with those from captivity, and it is larger in wild Amur tigers compared with other wild continental tigers. The degree of phenotypic plasticity shown by the sagittal crest, skull width and rostral height suggests that the distinctive shape of Amur tiger skulls compared with that of other continental tigers is mostly a phenotypically plastic response to differences in their environments.
Extra-group paternity (EGP) occurs commonly among group-living mammals and plays an important role in mating systems and the dynamics of sexual selection; however, socio-ecological and genetic correlates of EGP have been underexplored. We use 23 years of demographic and genetic data from a high-density European badger (Meles meles) population, to investigate the relationship between the rate of EGP in litters and mate availability, mate incompatibility and mate quality (heterozygosity). Relatedness between within-group assigned mothers and candidate fathers had a negative quadratic effect on EGP, whereas the number of neighbouring-group candidate fathers had a linear positive effect. We detected no effect of mean or maximum heterozygosity of within-group candidate fathers on EGP. Consequently, EGP was associated primarily with mate availability, subject to within-group genetic effects, potentially to mitigate mate incompatibility and inbreeding. In badgers, cryptic female choice, facilitated by superfecundation, superfoetation and delayed implantation, prevents males from monopolizing within-group females. This resonates with a meta-analysis in group-living mammals, which proposed that higher rates of EGP occur when within-group males cannot monopolize within-group females. In contrast to the positive meta-analytic association, however, we found that EGP associated negatively with the number of within-group assigned mothers and the number of within-group candidate fathers; potentially a strategy to counter within-group males committing infanticide. The relationship between the rate of EGP and socio-ecological or genetic factors can therefore be intricate, and the potential for cryptic female choice must be accounted for in comparative studies.
Zoo animals are crucial for conserving and potentially re-introducing species to the wild, yet it is known that the morphology of captive animals differs from that of wild animals. It is important to know how and why zoo and wild animal morphology differs to better care for captive animals and enhance their survival in reintroductions, and to understand how plasticity may influence morphology, which is supposedly indicative of evolutionary relationships. Using museum collections, we took 56 morphological measurements of skulls and mandibles from 617 captive and wild lions and tigers, reflecting each species' recent historical range. Linear morphometrics were used to identify differences in size and shape. Skull size does not differ between captive and wild lions and tigers, but skull and mandible shape does. Differences occur in regions associated with biting, indicating that diet has influenced forces acting upon the skull and mandible. The diets of captive big cats used in this study predominantly consisted of whole or partial carcasses, which closely resemble the mechanical properties of wild diets. Thus, we speculate that the additional impacts of killing, manipulating and consuming large prey in the wild have driven differentiation between captive and wild big cats.
There is currently no available information regarding the veterinary management of Sunda clouded leopards (Neofelis diardi), either in captivity or in the wild. In this study, 12 Sunda clouded leopards were anesthetized between January 2008 and February 2014 for medical exams, and/or GPS-collaring. Seven wild-caught individuals were kept in captivity and 5 free-ranging animals were captured by cage traps. Two anesthesia combinations were used: medetomidine-ketamine (M-K) or tiletamine-zolazepam (T-Z). Atipamezole (0.2 mg/kg im) was used as an antagonist for medetomidine. Medetomidine (range: 0.039-0.054 mg/kg) and ketamine (range: 3-4.39 mg/kg) were administered during 5 immobilizations, resulting in median induction times of 7 min. After a median anesthesia time of 56 min, atipamezole was injected, observing effects of antagonism at a median time of 12 min. T-Z (range: 6.8-10.8 mg/kg) was administered on 7 occasions. Median induction times observed with this combination were shorter than with M-K (4 min vs 7 min; P=0.04), and anesthesia and recovery times were significantly longer (244 and 35 min vs 56 and 16 min, respectively; P=0.02). Lower heart rates were measured in the M-K group, while lower rectal temperatures were found in the T-Z group. Both combinations resulted in safe and reliable immobilizations, although given the favorable anesthesia and recovery times of M-K, we recommend this approach over T-Z for the veterinary handling of Sunda clouded leopards.
Dry deciduous dipterocarp forests (DDF) cover about 15%-20% of Southeast Asia and are the most threatened forest type in the region. The jungle cat (Felis chaus) is a DDF specialist that occurs only in small isolated populations in Southeast Asia. Despite being one of the rarest felids in the region, almost nothing is known about its ecology. We investigated the ecology of jungle cats and their resource partitioning with the more common leopard cats (Prionailurus bengalensis) in a DDF-dominated landscape in Srepok Wildlife Sanctuary, Cambodia. We used camera-trap data collected from 2009 to 2019 and DNA-confirmed scats to determine the temporal, dietary and spatial overlap between jungle cats and leopard cats. The diet of jungle cats was relatively diverse and consisted of murids (56% biomass consumed), sciurids (15%), hares (Lepus peguensis; 12%), birds (8%), and reptiles (8%), whereas leopard cats had a narrower niche breadth and a diet dominated by smaller prey, primarily murids (73%). Nonetheless, dietary overlap was high because both felid species consumed predominantly small rodents. Both species were primarily nocturnal and had high temporal overlap. Two-species occupancy modelling suggested jungle cats were restricted to DDF and had low occupancy, whereas leopard cats had higher occupancy and were habitat generalists. Our study confirmed that jungle cats are DDF specialists that likely persist in low numbers due to the harsh conditions of the dry season in this habitat, including annual fires and substantial decreases in small vertebrate prey. The lower occupancy and more diverse diet of jungle cats, together with the broader habitat use of leopard cats, likely facilitated the coexistence of these species. The low occupancy of jungle cats in DDF suggests that protection of large areas of DDF will be required for the long-term conservation of this rare felid in Southeast Asia.
The orangutan is the world's largest arboreal mammal, and images of the red ape moving through the tropical forest canopy symbolise its typical arboreal behaviour. Records of terrestrial behaviour are scarce and often associated with habitat disturbance. We conducted a large-scale species-level analysis of ground-based camera-trapping data to evaluate the extent to which Bornean orangutans Pongo pygmaeus come down from the trees to travel terrestrially, and whether they are indeed forced to the ground primarily by anthropogenic forest disturbances. Although the degree of forest disturbance and canopy gap size influenced terrestriality, orangutans were recorded on the ground as frequently in heavily degraded habitats as in primary forests. Furthermore, all age-sex classes were recorded on the ground (flanged males more often). This suggests that terrestrial locomotion is part of the Bornean orangutan's natural behavioural repertoire to a much greater extent than previously thought, and is only modified by habitat disturbance. The capacity of orangutans to come down from the trees may increase their ability to cope with at least smaller-scale forest fragmentation, and to cross moderately open spaces in mosaic landscapes, although the extent of this versatility remains to be investigated.
Aichi Target 11 committed governments to protect ≥17% of their terrestrial environments by 2020, yet it was rarely achieved, raising questions about the post-2020 Global Biodiversity Framework goal to protect 30% by 2030. Asia is a challenging continent for such targets, combining high biodiversity with dense human populations. Here, we evaluated achievements in Asia against Aichi Target 11. We found that Asia was the most underperforming continent globally, with just 13.2% of terrestrial protected area (PA) coverage, averaging 14.1 ± SE 1.8% per country in 2020. 73.1% of terrestrial ecoregions had <17% representation and only 7% of PAs even had an assessment of management effectiveness. We found that a higher agricultural land in 2015 was associated with lower PA coverage today. Asian countries also showed a remarkably slow average annual pace of 0.4 ± SE 0.1% increase of PA extent. These combined lines of evidence suggest that the ambitious 2030 targets are unlikely to be achieved in Asia unless the PA coverage to increase 2.4-5.9 times faster. We provided three recommendations to support Asian countries to meet their post-2020 biodiversity targets: complete reporting and the wider adoption "other effective area-based conservation measures"; restoring disturbed landscapes; and bolstering transboundary PAs.