Precision wildlife medicine: applications of the human‐centred precision medicine revolution to species conservation

The current species extinction crisis is being exacerbated by an increased rate of emergence of epizootic disease. Human‐induced factors including habitat degradation, loss of biodiversity and wildlife population reductions resulting in reduced genetic variation are accelerating disease emergence. Novel, efficient and effective approaches are required to combat these epizootic events. Here, we present the case for the application of human precision medicine approaches to wildlife medicine in order to enhance species conservation efforts. We consider how the precision medicine revolution, coupled with the advances made in genomics, may provide a powerful and feasible approach to identifying and treating wildlife diseases in a targeted, effective and streamlined manner. A number of case studies of threatened species are presented which demonstrate the applicability of precision medicine to wildlife conservation, including sea turtles, amphibians and Tasmanian devils. These examples show how species conservation could be improved by using precision medicine techniques to determine novel treatments and management strategies for the specific medical conditions hampering efforts to restore population levels. Additionally, a precision medicine approach to wildlife health has in turn the potential to provide deeper insights into human health and the possibility of stemming and alleviating the impacts of zoonotic diseases. The integration of the currently emerging Precision Medicine Initiative with the concepts of EcoHealth (aiming for sustainable health of people, animals and ecosystems through transdisciplinary action research) and One Health (recognizing the intimate connection of humans, animal and ecosystem health and addressing a wide range of risks at the animal–human–ecosystem interface through a coordinated, collaborative, interdisciplinary approach) has great potential to deliver a deeper and broader interdisciplinary‐based understanding of both wildlife and human diseases.     

Effects of environmental factors on the distribution of flagship species in Bomfobiri Wildlife Sanctuary,Kumawu, Ghana: Implications for conservation and ecotourism development

Sustainable ecotourism development and conservation depend on understanding factors that affect flagship species. This study analysed environmental factors and their effects on flagship species: African buffalo (Syncerus caffer), red-river hog (Potamochoerus porcus), olive baboon (Papio anubis), duiker (Cephalophus spp.), and crocodile (Crocodylus niloticus) distribution in Bomfobiri Wildlife Sanctuary (BWS). Secondary data (camp reports 2017–2019) showed flagship species distribution across four vegetation types in 14 sites. Field observations were used to reconstruct camp report information using GPS coordinates to show animal distribution. Environmental factors were assessed based on the scope and severity of their threats to the species. PAST ver.3.06 was used to analyse animal and vegetation data. A total of 995 individual animals were recorded. Riverine forest (n = 325) had the highest, followed by semi-deciduous (n = 316), and woodland Savanna (n = 192). Bushfire was the major predictive factor on animal distribution, followed by grazing pressure, farming activities, elevation, and erosion. These findings imply that an increased scale of disturbances reduces the chance of sighting flagship animals. A higher concentration of these species in riverine and semi-deciduous forests calls for increased patrols as a conservation measure. Constructing viewing platforms and hiking trails in areas of higher animal activity would improve ecotourism development.     

Two’s company,three’s a crowd: Exploring how host–parasite–microbiota interactions may influence disease susceptibility and conservation of wildlife

A large body of research has demonstrated that host‐associated microbiota—the archaeal, bacterial, fungal and viral communities residing on and inside organisms—are critical to host health (Cho & Blaser, 2012). Although the vast majority of these studies focus on humans or model organisms in laboratory settings (Pascoe, Hauffe, Marchesi, & Perkins, 2017), they nevertheless provide important conceptual evidence that the disruption of host‐associated microbial communities (termed “dysbiosis”) among wild animals may reduce host fitness and survival under natural environmental conditions. Among the myriad of environmental factors capable of inducing dysbiosis among wild animals (Trevelline, Fontaine, Hartup, & Kohl, 2019), parasitic infections represent a potentially potent, yet poorly understood, factor influencing microbial community dynamics and animal health. The study by DeCandia et al. in this issue of Molecular Ecology is a rare example of a host–parasite–microbiota interaction that impacts the health, survival and conservation of a threatened wild animal in its natural habitat. Using culture‐independent techniques, DeCandia et al. found that the presence of an ectoparasitic mite (Otodectes cynotis) in the ear canal of the Santa Catalina Island fox (Urocyon littoralis catalinae) was associated with significantly reduced ear canal microbial diversity, with the opportunistic pathogen Staphylococcus pseudintermedius dominating the community. These findings suggest that parasite‐induced inflammation may contribute to the formation of ceruminous gland tumours in this subspecies of Channel Island fox. As a rare example of a host–parasite–microbiota interaction that may mediate a lethal disease in a population of threatened animals, their study provides an excellent example of how aspects of disease ecology can be integrated into studies of host‐associated microbiota to advance conservation science and practice.     

Exploring wildlife predation in the Limpopo Province of South Africa: A double‐hurdle approach

Predation is a well‐known problem in South Africa with large losses in the small and large livestock sectors. Predation in the wildlife ranching industry has also become more of a concern, as the financial losses due to predation on valuable antelope species are large. Predation data for small, large, and scarce/colour‐variant antelope species were collected using a structured questionnaire from wildlife ranchers in the Limpopo province, South Africa. We explore the factors that influence predation on these species by determining whether the perceptions of predation and consequent managerial decisions affect predation. The use of nonlethal control methods can be successfully employed to reduce the probability of predation occurrences, however, a combination of lethal and nonlethal control methods were used to reduce the level of predation. The type of antelope species will determine the type of predation control method to be employed. Therefore, the antelope species should be taken into account when making predation management decisions.     

Living on the edge: Multiscale habitat selection by cheetahs in a human‐wildlife landscape

Animals select habitats that will ultimately optimize their fitness through access to favorable resources, such as food, mates, and breeding sites. However, access to these resources may be limited by bottom‐up effects, such as availability, and top‐down effects, such as risk avoidance and competition, including that with humans. Competition between wildlife and people over resources, specifically over space, has played a significant role in the worldwide decrease in large carnivores. The goal of this study was to determine the habitat selection of cheetahs (Acinonyx jubatus) in a human‐wildlife landscape at multiple spatial scales. Cheetahs are a wide‐ranging, large carnivore, whose significant decline is largely attributed to habitat loss and fragmentation. It is believed that 77% of the global cheetah population ranges outside protected areas, yet little is known about cheetahs’ resource use in areas where they co‐occur with people. The selection, or avoidance, of three anthropogenic variables (human footprint density, distance to main roads and wildlife areas) and five environmental variables (open habitat, semiclosed habitat, edge density, patch density and slope), at multiple spatial scales, was determined by analyzing collar data from six cheetahs. Cheetahs selected variables at different scales; anthropogenic variables were selected at broader scales (720–1440 m) than environmental variables (90–180 m), suggesting that anthropogenic pressures affect habitat selection at a home‐range level, whilst environmental variables influence site‐level habitat selection. Cheetah presence was best explained by human presence, wildlife areas, semiclosed habitat, edge density and slope. Cheetahs showed avoidance for humans and steep slopes and selected for wildlife areas and areas with high proportions of semiclosed habitat and edge density. Understanding a species’ resource requirements, and how these might be affected by humans, is crucial for conservation. Using a multiscale approach, we provide new insights into the habitat selection of a large carnivore living in a human‐wildlife landscape.     

Using species distribution models to define nesting habitat of the eastern metapopulation of double‐crested cormorants

When organisms with similar phenotypes have conflicting management and conservation initiatives, approaches are needed to differentiate among subpopulations or discrete groups. For example, the eastern metapopulation of the double‐crested cormorant (Phalacrocorax auritus) has a migratory phenotype that is culled because they are viewed as a threat to commercial and natural resources, whereas resident birds are targeted for conservation. Understanding the distinct breeding habitats of resident versus migratory cormorants would aid in identification and management decisions. Here, we use species distribution models (SDM: Maxent) of cormorant nesting habitat to examine the eastern P. auritus metapopulation and the predicted breeding sites of its phenotypes. We then estimate the phenotypic identity of breeding colonies of cormorants where management plans are being developed. We transferred SDMs trained on data from resident bird colonies in Florida and migratory bird colonies in Minnesota to South Carolina in an effort to identify the phenotype of breeding cormorants there based on the local landscape characteristics. Nesting habitat characteristics of cormorant colonies in South Carolina more closely resembled those of the Florida phenotype than those of birds of the Minnesota phenotype. The presence of the resident phenotype in summer suggests that migratory and resident cormorants will co‐occur in South Carolina in winter. Thus, there is an opportunity for separate management strategies for the two phenotypes in that state. We found differences in nesting habitat characteristics that could be used to refine management strategies and reduce human conflicts with abundant winter migrants and, at the same time, conserve less common colonies of resident cormorants. The models we use here show potential for advancing the study of geographically overlapping phenotypes with differing conservation and management priorities.     

Golden bananas in the field: elevated fruit pro‐vitamin A from the expression of a single banana transgene

Vitamin A deficiency remains one of the world's major public health problems despite food fortification and supplements strategies. Biofortification of staple crops with enhanced levels of pro‐vitamin A (PVA) offers a sustainable alternative strategy to both food fortification and supplementation. As a proof of concept, PVA‐biofortified transgenic Cavendish bananas were generated and field trialed in Australia with the aim of achieving a target level of 20 μg/g of dry weight (dw) β‐carotene equivalent (β‐CE) in the fruit. Expression of a Fe'i banana‐derived phytoene synthase 2a (MtPsy2a) gene resulted in the generation of lines with PVA levels exceeding the target level with one line reaching 55 μg/g dw β‐CE . Expression of the maize phytoene synthase 1 (ZmPsy1) gene, used to develop ‘Golden Rice 2’, also resulted in increased fruit PVA levels although many lines displayed undesirable phenotypes. Constitutive expression of either transgene with the maize polyubiquitin promoter increased PVA accumulation from the earliest stage of fruit development. In contrast, PVA accumulation was restricted to the late stages of fruit development when either the banana 1‐aminocyclopropane‐1‐carboxylate oxidase or the expansin 1 promoters were used to drive the same transgenes. Wild‐type plants with the longest fruit development time had also the highest fruit PVA concentrations. The results from this study suggest that early activation of the rate‐limiting enzyme in the carotenoid biosynthetic pathway and extended fruit maturation time are essential factors to achieve optimal PVA concentrations in banana fruit.     

Translocation of the Eastern Bristlebird 1: radio‐tracking of post‐release movements

Summary Translocating birds to a new area of habitat to restore or supplement depleted populations may pose a significant threat to the translocated individuals. While for many species, translocated individuals appear to move larger distances than resident animals, species with poor dispersal capacity may be restricted in movements and translocation methods may need to accommodate differences in movements to ensure success. In this study, designed to provide insights to inform our broader programme of translocations in New South Wales, Australia, we investigated post‐release movements in the endangered, semi‐flightless Eastern Bristlebird (Dasyornis brachypterus). We predicted that movements would be minimal, with few differences between males and females, similar to published information for a resident un‐manipulated population. Following the release of 45 birds at a host location at Jervis Bay, NSW, over a 3‐year programme, we followed individuals for up to 2 weeks using radio‐tracking. The translocated birds had larger maximum movements and moved through much larger home ranges than non‐translocated individuals from the resident population. Translocated birds moved 300 m further after release when conspecifics were present. Males moved further than females and tended to have larger home ranges, although average daily displacement did not differ. We concluded that the semi‐flightlessness of the species does not result in minimal movements. Release at a small number of locations in the new habitat was considered appropriate for the species, as animals seem to move enough to find new unoccupied areas in a relatively short period. This work provided us with increasing confidence to continue with further translocations.     

The difficulty of using species distribution modelling for the conservation of refugee species – the example of European bison

Refugee species have been confined to suboptimal habitat through historic anthropogenic factors. If this is unknown, management might actively conserve these species in suboptimal habitat assuming it represents optimal habitat. Similarly, species distribution modelling (SDM) might misguide conservation management of refugee species by only using presence data from suboptimal habitats. We illustrate this by commenting on a recent SDM for European bison that reconstructed the historic distribution of the species. We challenge the interpretation of this model by suggesting an alternative historic biogeography based on the refugee species concept. We argue that, in the case of refugee species, historic reconstructions using SDM cannot be used as a template for conservation management. Rather, experimental re‐introduction programmes should provide us with population performance and life history data from a range of suboptimal to optimal habitats. Such data could be used in mechanistic niche modelling to predict potential distribution of refugee species.     

The protected flora of long‐established cemeteries in Hungary: Using historical maps in biodiversity conservation

The role of anthropogenically influenced habitats in conserving elements of the original wildlife has increased worldwide simultaneously with the disappearance of natural sites. Burial places are able to conserve original elements of the wildlife, and this fact has been known for at least a century. To this day, little is known about long‐time changes and the effect of long‐time management methods in cemeteries on the flora they harbor. The utility of historical maps in research focused on natural values, as well as in answering questions related to conservation was recently demonstrated, but the use of digitized historical maps in biodiversity research of the Carpathian Basin is very limited. In the present paper, we aimed to predict the conservation potential of long‐established and newly established cemeteries of Hungarian settlements with various population sizes based on the digitized maps of the 2nd Military Survey of the Austrian Empire (1819–1869), by categorizing cemeteries into 3 distinct (anthropogenic habitat, cemetery, or natural habitat) types. To build our models, we used records of the protected flora from Hungarian cemeteries, based on data of thematic botanical surveys of 991 cemeteries. Out of the surveyed cemeteries, 553 (56%) harbored protected plants, totaling 306.617 estimated individuals of 92 protected species, belonging to 28 plant families. These species represent 12% of the entire protected flora of Hungary. Hungarian cemeteries play a key role mainly in preserving steppe and dry grassland plant species. Long‐established and large cemeteries harbor more protected plant species than small and newly established ones. Human population size of the settlements correlated negatively with the number of protected species and individuals. Moreover, woodland cover and proportion of grassland also significantly positively affected the number of protected plant species in cemeteries.     

Measuring the efficiency of fen restoration on carabid beetles and vascular plants: a case study from north‐eastern Germany

The aim of the study was to assess the effects of fen rewetting on carabid beetle and vascular plant assemblages within riverine fens along the river Peene in north‐eastern Germany. Drained (silage grassland), rewetted (restored formerly drained silage grassland), and near‐natural (fairly pristine) stands were compared. Eighty‐four beetle species (7,267 individuals) and 135 plant species were recorded. The richness of vascular plant species and the number of endangered species were highest on near‐natural fens. Fourteen years of rewetting did not increase plant species numbers compared with drained fens. For carabid beetles, however, species richness and the number of stenotopic species were highest on rewetted fens. Rewetting caused the replacement of generalist carabids by wetland specialists, but did not provide suitable habitat for specialist fen carabids or for plant species of oligo‐ or mesotrophic fen communities. Therefore, raising the water table on fens with nutrient‐rich, degraded peat was not sufficient for restoring species assemblages of intact fens, although water level was the most important environmental factor separating species assemblages. Our study illustrated that insects and plants may respond differentially to restoration, stressing the need to consider different taxa when assessing the efficiency of fen restoration. Furthermore, species assemblages of intact fens could not be restored within 14 years, highlighting the importance of conserving pristine habitat.     

The ecological importance of crocodylians: towards evidence‐based justification for their conservation

Large‐bodied predators are well represented among the world's threatened and endangered species. A significant body of literature shows that in terrestrial and marine ecosystems large predators can play important roles in ecosystem structure and functioning. By contrast, the ecological roles and importance of large predators within freshwater ecosystems are poorly understood, constraining the design and implementation of optimal conservation strategies for freshwater ecosystems. Conservationists and environmentalists frequently promulgate ecological roles that crocodylians are assumed to fulfil, but often with limited evidence supporting those claims. Here, we review the available information on the ecological importance of crocodylians, a widely distributed group of predominantly freshwater‐dwelling, large‐bodied predators. We synthesise information regarding the role of crocodylians under five criteria within the context of modern ecological concepts: as indicators of ecological health, as ecosystem engineers, apex predators, keystone species, and as contributors to nutrient and energy translocation across ecosystems. Some crocodylians play a role as indicators of ecosystem health, but this is largely untested across the order Crocodylia. By contrast, the role of crocodylian activities in ecosystem engineering is largely anecdotal, and information supporting their assumed role as apex predators is currently limited to only a few species. Whether crocodylians contribute significantly to nutrient and energy translocation through cross‐ecosystem movements is unknown. We conclude that most claims regarding the importance of crocodylians as apex predators, keystone species, ecosystem engineers, and as contributors to nutrient and energy translocation across ecosystems are mostly unsubstantiated speculation, drawn from anecdotal observations made during research carried out primarily for other purposes. There is a paucity of biological research targeted directly at: understanding population dynamics; trophic interactions within their ecological communities; and quantifying the short‐ and long‐term ecological impacts of crocodylian population declines, extirpations, and recoveries. Conservation practices ideally need evidence‐based planning, decision making and justification. Addressing the knowledge gaps identified here will be important for achieving effective conservation of crocodylians.     

Landscape‐scale accessibility of livestock to tigers: implications of spatial grain for modeling predation risk to mitigate human–carnivore conflict

Innovative conservation tools are greatly needed to reduce livelihood losses and wildlife declines resulting from human–carnivore conflict. Spatial risk modeling is an emerging method for assessing the spatial patterns of predator–prey interactions, with applications for mitigating carnivore attacks on livestock. Large carnivores that ambush prey attack and kill over small areas, requiring models at fine spatial grains to predict livestock depredation hot spots. To detect the best resolution for predicting where carnivores access livestock, we examined the spatial attributes associated with livestock killed by tigers in Kanha Tiger Reserve, India, using risk models generated at 20, 100, and 200‐m spatial grains. We analyzed land‐use, human presence, and vegetation structure variables at 138 kill sites and 439 random sites to identify key landscape attributes where livestock were vulnerable to tigers. Land‐use and human presence variables contributed strongly to predation risk models, with most variables showing high relative importance (≥0.85) at all spatial grains. The risk of a tiger killing livestock increased near dense forests and near the boundary of the park core zone where human presence is restricted. Risk was nonlinearly related to human infrastructure and open vegetation, with the greatest risk occurring 1.2 km from roads, 1.1 km from villages, and 8.0 km from scrubland. Kill sites were characterized by denser, patchier, and more complex vegetation with lower visibility than random sites. Risk maps revealed high‐risk hot spots inside of the core zone boundary and in several patches in the human‐dominated buffer zone. Validation against known kills revealed predictive accuracy for only the 20 m model, the resolution best representing the kill stage of hunting for large carnivores that ambush prey, like the tiger. Results demonstrate that risk models developed at fine spatial grains can offer accurate guidance on landscape attributes livestock should avoid to minimize human–carnivore conflict.     

The importance of marginal population hotspots of cold‐adapted species for research on climate change and conservation

Areas hosting hotspots of low‐latitude marginal populations of cold‐adapted plant species could be key areas for understanding geographical attributes that result in refugia during climatic shifts as well as the conservation of genetic diversity in the face of climate change. Low‐latitude populations of cold‐adapted plants are important because they may harbour the combination of alleles that foster persistence in a warmer climate. Consequently, identification of areas where arctic‐alpine, circumpolar and circumboreal species reach the low‐latitude ends of their distribution will present a unique opportunity to uncover processes that shaped current biogeographical patterns, as well as prepare for future scenarios. Here, we identify 35 main marginal population hotspots (19 and 16 areas in North America and Europe, respectively) of 183 plant taxa. These hotspots represent areas where southern marginal populations of cold‐adapted species co‐occur. The identification of hotspots was based on geographic overlap of southernmost locations of the target species, in a 50 × 50 km grid. With a threshold of two species in a single grid cell or in two contiguous cells, the analysis revealed that hotspots are in most cases located in the southern portion of major mountain chains. However, hotspots also occur in lowland areas at high latitudes (Fennoscandia, Alaska, Hudson Bay) which do not necessarily correspond to known cold‐ or warm‐stage refugia (e.g. Alps). Rockies and Sierra Nevada both in California and Spain, Apennines, and the southern Scandes, maintain their hotspot status even with more stringent cut‐off thresholds (>3 and >5 species per cell group). From a conservation point of view, our analysis reveals that only a small portion of the hotspots are currently included within protected areas. We discuss the importance of marginal population hotspots to future research on climate change and, finally, outline how conservation strategies can capitalize on the knowledge gained from studying climate change effects on cold‐adapted plants.     

Reconstructing demographic events from population genetic data: the introduction of bumblebees to New Zealand

Four British bumblebee species (Bombus terrestris, Bombus hortorum, Bombus ruderatus and Bombus subterraneus) became established in New Zealand following their introduction at the turn of the last century. Of these, two remain common in the United Kingdom (B. terrestris and B. hortorum), whilst two (B. ruderatus and B. subterraneus) have undergone marked declines, the latter being declared extinct in 2000. The presence of these bumblebees in New Zealand provides an unique system in which four related species have been isolated from their source population for over 100 years, providing a rare opportunity to examine the impacts of an initial bottleneck and introduction to a novel environment on their population genetics. We used microsatellite markers to compare modern populations of B. terrestris, B. hortorum and B. ruderatus in the United Kingdom and New Zealand and to compare museum specimens of British B. subterraneus with the current New Zealand population. We used approximate Bayesian computation to estimate demographic parameters of the introduction history, notably to estimate the number of founders involved in the initial introduction. Species-specific patterns derived from genetic analysis were consistent with the predictions based on the presumed history of these populations; demographic events have left a marked genetic signature on all four species. Approximate Bayesian analyses suggest that the New Zealand population of B. subterraneus may have been founded by as few as two individuals, giving rise to low genetic diversity and marked genetic divergence from the (now extinct) UK population.     

Conservation biogeography of the US–Mexico border: a transcontinental risk assessment of barriers to animal dispersal

Aim Humans have dramatically transformed landscapes along the US–Mexico border. We aim to assess the risk of barriers that may significantly impede animal migrations within this ecologically sensitive region. Location United States and Mexico. Methods We examined the intersection of current and possible future barriers along the border with the geographic ranges of 313 amphibian, reptile and non‐volant mammal species. We considered the areas of intensive human land use and ～ 600 km of pedestrian fence as current barriers along the border. We evaluated the impacts of two scenarios of dispersal barriers – continuation of existing and construction of new barriers – and identified species vulnerable to global and local extinction. Results Among the species most at risk from current barriers are four species listed as threatened globally or by both nations, 23 species for which the larger of their two national subranges is < 10⁵ km² and 29 species whose ranges cross the border only marginally. Three border regions, California, Madrean archipelago and Gulf coast, emerge as being of particular concern. These regions are characterized by high overall species richness and high richness of species at risk from existing barriers and from construction of potential new barriers. Main conclusions New barriers along the border would increase the number of species at risk, especially in the three identified regions, which should be prioritized for mitigation of the impacts of current barriers. The species we identified as being potentially at risk merit further study to determine impacts of border dispersal barriers.