Distribution and Impacts of Tasmanian Devil Facial Tumor Disease

The Tasmanian devil, Sarcophilus harrisii, is the largest extant marsupial carnivore. In 1996, a debilitating facial tumor was reported. It is now clear that this is an invariably lethal infectious cancer. The disease has now spread across the majority of the range of the species and is likely to occur across the entire range within 5 to 10 years. The disease has lead to continuing declines of up to 90% and virtual disappearance of older age classes. Mark-recapture analysis and a preliminary epidemiological model developed for the population with the best longitudinal data both project local extinction in that area over a timeframe of 10 to 15 years from disease emergence. However, the prediction of extinction from the model is sensitive to the estimate of the latent period, which is poorly known. As transmission appears to occur by biting, much of which happens during sexual encounters, the dynamics of the disease may be typical of sexually transmitted diseases. This means that transmission is likely to be frequency-dependent with no threshold density for disease maintenance. Extinction over the entire current range of the devil is therefore a real possibility and an unacceptable risk.     

MHC gene copy number variation in Tasmanian devils: implications for the spread of a contagious cancer

Tasmanian devils face extinction owing to the emergence of a contagious cancer. Devil facial tumour disease (DFTD) is a clonal cancer spread owing to a lack of major histocompatibility complex (MHC) barriers in Tasmanian devil populations. We present a comprehensive screen of MHC diversity in devils and identify 25 MHC types and 53 novel sequences, but conclude that overall levels of MHC diversity at the sequence level are low. The majority of MHC Class I variation can be explained by allelic copy number variation with two to seven sequence variants identified per individual. MHC sequences are divided into two distinct groups based on sequence similarity. DFTD cells and most devils have sequences from both groups. Twenty per cent of individuals have a restricted MHC repertoire and contain only group I or only group II sequences. Counterintuitively, we postulate that the immune system of individuals with a restricted MHC repertoire may recognize foreign MHC antigens on the surface of the DFTD cell. The implication of these results for management of DFTD and this endangered species are discussed.     

The impact of disease on the survival and population growth rate of the Tasmanian devil

1. We investigated the impact of a recently emerged disease, Devil Facial Tumour Disease (DFTD), on the survival and population growth rate of a population of Tasmanian devils, Sarcophilus harrisii, on the Freycinet Peninsula in eastern Tasmania. 2. Cormack-Jolly-Seber and multistate mark-recapture models were employed to investigate the impact of DFTD on age- and sex-specific apparent survival and transition rates. Disease impact on population growth rate was investigated using reverse-time mark-recapture models. 3. The arrival of DFTD triggered an immediate and steady decline in apparent survival rates of adults and subadults, the rate of which was predicted well by the increase in disease prevalence in the population over time. 4. Transitions from healthy to diseased state increased with disease prevalence suggesting that the force of infection in the population is increasing and that the epidemic is not subsiding. 5. The arrival of DFTD coincided with a marked, ongoing decline in the population growth rate of the previously stable population, which to date has not been offset by population compensatory responses.     

Transmissible cancer in Tasmanian devils: localized lineage replacement and host population response

Tasmanian devil facial tumour disease (DFTD) is a clonally transmissible cancer threatening the Tasmanian devil (Sarcophilus harrisii) with extinction. Live cancer cells are the infectious agent, transmitted to new hosts when individuals bite each other. Over the 18 years since DFTD was first observed, distinct genetic and karyotypic sublineages have evolved. In this longitudinal study, we investigate the associations between tumour karyotype, epidemic patterns and host demographic response to the disease. Reduced host population effects and low DFTD infection rates were associated with high prevalence of tetraploid tumours. Subsequent replacement by a diploid variant of DFTD coincided with a rapid increase in disease prevalence, population decline and reduced mean age of the population. Our results suggest a role for tumour genetics in DFTD transmission dynamics and epidemic outcome. Future research, for this and other highly pathogenic emerging infectious diseases, should focus on understanding the evolution of host and pathogen genotypes, their effects on susceptibility and tolerance to infection, and their implications for designing novel genetic management strategies. This study provides evidence for a rapid localized lineage replacement occurring within a transmissible cancer epidemic and highlights the possibility that distinct DFTD genetic lineages may harbour traits that influence pathogen fitness.     

Isotopic niche variation in Tasmanian devils Sarcophilus harrisii with progression of devil facial tumor disease

Devil facial tumor disease (DFTD) is a transmissible cancer affecting Tasmanian devils Sarcophilus harrisii. The disease has caused severe population declines and is associated with demographic and behavioral changes, including earlier breeding, younger age structures, and reduced dispersal and social interactions. Devils are generally solitary, but social encounters are commonplace when feeding upon large carcasses. DFTD tumors can disfigure the jaw and mouth and so diseased individuals might alter their diets to enable ingestion of alternative foods, to avoid conspecific interactions, or to reduce competition. Using stable isotope analysis (δ¹³C and δ¹⁵N) of whiskers, we tested whether DFTD progression, measured as tumor volume, affected the isotope ratios and isotopic niches of 94 infected Tasmanian devils from six sites in Tasmania, comprising four eucalypt plantations, an area of smallholdings and a national park. Then, using tissue from 10 devils sampled before and after detection of tumors and 8 devils where no tumors were detected, we examined whether mean and standard deviation of δ¹³C and δ¹⁵N of the same individuals changed between healthy and diseased states. δ¹³C and δ¹⁵N values were generally not related to tumor volume in infected devils, though at one site, Freycinet National Park, δ¹⁵N values increased significantly as tumor volume increased. Infection with DFTD was not associated with significant changes in the mean or standard deviation of δ¹³C and δ¹⁵N values in individual devils sampled before and after detection of tumors. Our analysis suggests that devils tend to maintain their isotopic niche in the face of DFTD infection and progression, except where ecological conditions facilitate a shift in diets and feeding behaviors, demonstrating that ecological context, alongside disease severity, can modulate the behavioral responses of Tasmanian devils to DFTD.     

Seasonal,demographic and density‐related patterns of contact between Tasmanian devils (Sarcophilus harrisii): Implications for transmission of devil facial tumour disease

Abstract Devil facial tumour disease (DFTD), is an emerging infectious cancer thought to be spread by biting. It is causing ongoing, severe population decline of the Tasmanian devil (Sarcophilus harrisii), the largest surviving marsupial carnivore and there are concerns that DFTD may lead to extinction of the devil. Whether extinction is likely depends on contact rates and their relationship to host density. We investigated contact rates using two different datasets. The first consisted of field observations of contact and biting behaviour around prey carcasses and, the second was a 3‐year longitudinal series of injuries in a marked devil population. During feeding interactions at carcasses, contact rates were significantly positively associated with population density and subadults delivered more bites than adult males and females. Injuries from the marked devil population did not differ between adult males and females. In two of the three years, penetrating biting (resulting in injury) increased markedly during the mating season and was more frequent in adults than in subadults. Among injured devils with wounds penetrating the dermal layer, adults were more frequently bitten in the head (the location of primary tumours) in the mating season than in other seasons, and had more head bites than subadults. Our results suggest that the mating season may be the key period for disease transmission. If most penetrating bites occur during mating interactions, DFTD transmission is likely to be frequency dependent, which means that there would be no threshold host density for disease persistence, and disease‐induced extinction is possible.     

Relaxation of risk-sensitive behaviour of prey following disease-induced decline of an apex predator,the Tasmanian devil

Apex predators structure ecosystems through lethal and non-lethal interactions with prey, and their global decline is causing loss of ecological function. Behavioural changes of prey are some of the most rapid responses to predator decline and may act as an early indicator of cascading effects. The Tasmanian devil (Sarcophilus harrisii), an apex predator, is undergoing progressive and extensive population decline, of more than 90% in long-diseased areas, caused by a novel disease. Time since local disease outbreak correlates with devil population declines and thus predation risk. We used hair traps and giving-up densities (GUDs) in food patches to test whether a major prey species of devils, the arboreal common brushtail possum (Trichosurus vulpecula), is responsive to the changing risk of predation when they forage on the ground. Possums spend more time on the ground, discover food patches faster and forage more to a lower GUD with increasing years since disease outbreak and greater devil population decline. Loss of top–down effects of devils with respect to predation risk was evident at 90% devil population decline, with possum behaviour indistinguishable from a devil-free island. Alternative predators may help to maintain risk-sensitive anti-predator behaviours in possums while devil populations remain low.     

Contact networks in a wild Tasmanian devil (Sarcophilus harrisii) population: using social network analysis to reveal seasonal variability in social behaviour and its implications for transmission of devil facial tumour disease

The structure of the contact network between individuals has a profound effect on the transmission of infectious disease. Using a novel technology – proximity sensing radio collars – we described the contact network in a population of Tasmanian devils. This largest surviving marsupial carnivore is threatened by a novel infectious cancer. All devils were connected in a single giant component, which would permit disease to spread throughout the network from any single infected individual. Unlike the contact networks for many human diseases, the degree distribution was not highly aggregated. Nevertheless, the empirically derived networks differed from random networks. Contact networks differed between the mating and non-mating seasons, with more extended male–female associations in the mating season and a greater frequency of female–female associations outside the mating season. Our results suggest that there is limited potential to control the disease by targeting highly connected age or sex classes.     

Lack of genetic diversity across diverse immune genes in an endangered mammal,the Tasmanian devil (Sarcophilus harrisii)

The Tasmanian devil (Sarcophilus harrisii) is threatened with extinction due to the spread of devil facial tumour disease. Polymorphisms in immune genes can provide adaptive potential to resist diseases. Previous studies in diversity at immune loci in wild species have almost exclusively focused on genes of the major histocompatibility complex (MHC); however, these genes only account for a fraction of immune gene diversity. Devils lack diversity at functionally important immunity loci, including MHC and Toll‐like receptor genes. Whether there are polymorphisms at devil immune genes outside these two families is unknown. Here, we identify polymorphisms in a wide range of key immune genes, and develop assays to type single nucleotide polymorphisms (SNPs) within a subset of these genes. A total of 167 immune genes were examined, including cytokines, chemokines and natural killer cell receptors. Using genome‐level data from ten devils, SNPs within coding regions, introns and 10 kb flanking genes of interest were identified. We found low polymorphism across 167 immune genes examined bioinformatically using whole‐genome data. From this data, we developed long amplicon assays to target nine genes. These amplicons were sequenced in 29–220 devils and found to contain 78 SNPs, including eight SNPS within exons. Despite the extreme paucity of genetic diversity within these genes, signatures of balancing selection were exhibited by one chemokine gene, suggesting that remaining diversity may hold adaptive potential. The low functional diversity may leave devils highly vulnerable to infectious disease, and therefore, monitoring and preserving remaining diversity will be critical for the long‐term management of this species. Examining genetic variation in diverse immune genes should be a priority for threatened wildlife species. This study can act as a model for broad‐scale immunogenetic diversity analysis in threatened species.     

Occurrence of Charcoal Rot Caused by Macrophomina phaseolina,an Emerging Disease of Adzuki Bean in China

Adzuki bean (Vigna angularis) is an important legume crop in China. Soil‐borne charcoal rot caused by Macrophomina phaseolina (Tassi) Goid is an important and devastating disease of many crops including legumes. During late August and early September, 2014, symptoms similar to charcoal rot were observed on adzuki bean plants in Yulin City of Shanxi Province, and Fangshan County of Beijing, China. This study was conducted to determine the causal agent of the emerging disease on adzuki bean. Four fungal isolates were obtained and identified as M. phaseolina based on morphological and molecular characteristics, including species‐specific primer detection and sequences of internal transcribed spacer (ITS) of nuclear ribosomal DNA. The resulting sequences showed 99% identity with more than 60 M. phaseolina strains from diverse hosts. The virulence on adzuki bean was verified using pathogenicity tests, producing symptoms similar to those observed in the fields. To our knowledge, this is the first report of M. phaseolina causing charcoal rot on adzuki bean.     

Ecosystem Management in the Context of Large, Infrequent Disturbances

Large, infrequent disturbances (LIDs) can have significant impacts yet seldom are included in management plans. Although this neglect may stem from relative unfamiliarity with a kind of event that rarely occurs in the experience or jurisdiction of individual managers, it may also reflect the assumption that LIDs are so large and powerful as to be beyond the ability of managers to affect. However, some LIDs can be affected by management, and for many of those that cannot be affected, the resilience or recovery of the system disrupted by the disturbance can be influenced to meet management goals. Such results can be achieved through advanced planning that allows for LIDs, whether caused by natural events, human activities, or a combination of the two. Management plans for LIDs may adopt a variety of goals, depending on the nature of the system and the nature of the anticipated disturbance regime. Managers can choose to influence (a) the system prior to the disturbance, (b) the disturbance itself, (c) the system after the disturbance, or (d) the recovery process. Prior to the disturbance, the system can be managed in ways that alter its vulnerability or change how it will respond to a disturbance. The disturbance can be managed through no action, preventive measures, or manipulations that can affect the intensity or frequency of the disturbance. Recovery efforts can focus on either managing the state of the system immediately after the disturbance or managing the ongoing process of recovery. This review of the management implications of LIDs suggests that management actions should be tailored to particular disturbance characteristics and management goals. Management actions should foster survival of residuals and spatial heterogeneity that promote the desired recovery pattern and process. Most importantly, however, management plans need to recognize LIDs and include the potential for such disturbances to occur. Received 14 July 1998; accepted 16 September 1998     

Risk of Disease Transmission between Conservation Personnel and the Mountain Gorillas: Results from an Employee Health Program in Rwanda

Humans and gorillas share 97% of their genetic makeup which means the risk of disease transmission between the two is potentially high. Humans with high exposure and whose exposure-related activity can most easily be managed are park conservation personnel. In June 2001, the Morris Animal Foundations Mountain Gorilla Veterinary Project initiated a health program for all employees working in Rwandas Parc National des Volcans in collaboration with in-country government and nongovernmental agencies. The goal is to improve the health of conservation personnel and reduce the risk of zoonotic disease transmission between employees and the parks mountain gorillas. Employees annually receive a clinical examination and laboratory testing, and provide a clinical history, In 2002, analyses were performed on the dataset of 127 employees to identify potential risk factors associated with positive laboratory tests. Considering all fecal tests combined, 70.1% were positive for one or more pathogenic organisms. A high percentage (> 80%) tested positive on viral antibody titer testing for various communicable diseases including measles, chickenpox, and hepatitis. On multivariate analysis, the main risk factor for testing positive for any pathogenic organism was use of a pit latrine at home. Vaccination against childhood communicable diseases and improved human waste disposal could be critical control points for preventing disease transmission to mountain gorillas. Program results have been shared with local health officials to aid in their efforts to improve village health and sanitation standards, and with park employers as a basis for ongoing employee health education.The Mountain Gorilla Veterinary Project 2002 Employee Health Group members are listed in Appendix 1. by area of contribution.     

Integration of Ecosystem Services into Ecological Risk Assessment for Implementation in Ecosystem-Based River Management: A Case Study of the Yellow River,China

Ecological risk assessment (ERA) is a scientific tool used to support ecosystem-based management (EBM), but most current ERA methods consider only a few indices of particular species or components. Such limitations restrict the scope of results so that they are insufficient to reflect the integrated risk characterization of an ecosystem, thereby inhibiting the application of ERA in EBM. We incorporate the concept of ecosystem services into ERA and develop an improved ERA framework to create a comprehensive risk map of an ecosystem, accounting for multiple human activities and ecosystem services. Using the Yellow River as a case study, we show how this framework enables the implementation of integrated risk characterization and prioritization of the most important ecological risk issues in the ecosystem-based river management of the Yellow River. This framework can help practitioners facilitate better implementation of ERA within EBM in rivers or any target ecosystem.     

The Evolution of Conservation Management Philosophy: Science, Environmental Change and Social Adjustments in Kruger National Park

In this ‘perspectives’ article, we share experiences gained from the century-old Kruger National Park (KNP) in South Africa to illustrate the dynamic complexity of biophysical and socio-political systems, the interactions that occur between them, and the consequences for ecosystem-scale functions and resources and for their management. As in KNP, the social-ecological milieu surrounding many national parks and protected areas is changing rapidly. There will be significant managerial adjustments as human populations grow and the needs for resources accelerate. The changes, driven largely by global-scale environmental shifts as well as by new knowledge, are intimately intertwined with evolving societal perceptions, values, and expectations. Many KNP resource-related issues of the past century originated more internally and were largely environmental, whereas the emerging issues are more external and largely social. Here, we illustrate how interrelated scientific and managerial advances in integrating biophysical and social systems are acting to conserve and rehabilitate resources within KNP, and to aid in their conservation. Where appropriate, we relate these advances to similar examples in the region or other protected areas in the world. Strategies to address emerging issues are identified and discussed—and their combined effects on resource conservation and management are evaluated. In our experience the approach to conservation within KNP has been successful, despite well-intended but damaging management actions in the past. We believe that the perceived success stems from a willingness to continually incorporate new knowledge into management, to foster close working and personal associations among scientists, managers, and rangers, to acquire an intimate knowledge and understanding of the social-ecological system by the administrators as well as by the staff, and to be actively ‘forward’ thinking in an increasingly complex and uncertain world. We accept that many decisions taken today will be challenged by future managers and scientists, and we expect that some will be found wanting as emerging knowledge and continued learning shape future decisions. Further, evolving political, social, and environmental contexts may mean that protected areas will need to be managed in different ways. Therefore, we emphasize the importance of minimizing the permanency and impact of decisions so that today’s actions do not compromise future decisions when meaningful changes need to be made.

Hybridisation in European ungulates: an overview of the current status,causes, and consequences

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Management of coastal ecosystems in eastern Sumatra: the case of Berbak Wildlife Reserve,Jambi Province

The eastern lowlands of Sumatra comprise about 88 000 square kilometres, or approximately eighteen percent of the island's total area. Most of these lowlands were originally peatswamp forest, freshwater swamp forest and mangrove. A significant proportion of the area is subject to tidal influence.The lowlands have experienced a variety of land uses, firstly by the native people, who were mainly hunter-gatherers, later by the Buginese and Banjarese immigrants from Sulawesi and Kalimantan respectively, and more recently by transmigrants from Java, Bali and Madura.Land uses have involved principally agriculture, logging and fishing, and a wide range of associated activities. As in most attempts to settle and convert wetlands to other uses, there have been many problems. The Berbak Wildlife Reserve located on the southeast coast of the Province of Jambi provides a microcosm of these problems. The issues and impacts evident in Berbak include nearly all of the issues and impacts affecting wetland areas elsewhere in the eastern lowlands and provide a useful case study.The Asian Wetland Bureau and the Indonesian Directorate General of Forest Protection and Nature Conservation have carried out a two-year project which includes development of management of the Reserve and the preparation of an Environmental Profile for the lowland wetlands of Jambi Province as a background for regional planning. These components of the project are aimed at investigating and resolving management problems affecting the Reserve, and may be extrapolated to the solution of similar problems in other parts of the Sumatran lowlands.     

Using an Ecosystem Modeling Approach to Explore Possible Ecosystem Impacts of Fishing in the Beibu Gulf,Northern South China Sea

Using the Ecopath with Ecosim software, a trophic structure model of the Beibu Gulf was constructed to explore the energy flows and provide a snapshot of the ecosystem operations. Input data were mainly from the trawl survey data collected from October 1998 to September 1999 and related literatures. The impacts of various fishing pressure on the biomass were examined by simulation at different fishing mortality rates. The model consists of 20 functional groups (boxes), each representing organisms with a similar role in the food web, and only covers the major trophic flows in the Beibu Gulf ecosystem. It was found that the food web of the Beibu Gulf was dominated by the primary producers path, and phytoplankton was the primary producer mostly used as a food source. The fractional trophic levels ranged from 1.0 to 4.02, and the marine mammals occupied the highest trophic level. Using network analysis, the ecosystem network was mapped into a linear food chain, and six discrete trophic levels were found with a mean transfer efficiency of 11.2%. The Finn cycling index was 9.73%. The path length was 1.821. The omnivory index was 0.197. The ecosystem had some degree of instability due to exploitation and other human activities, according to Odum’s theory of ecosystem development. A 10-year simulation was performed for each fishery scenario. The fishing mortality rate was found to have a strong impact on the biomass. By keeping the fishing mortality rate at the current level for all fishing sectors, scenario 1 had a drastic decrease in the large fish groups. The biomass of the small and medium pelagic fish would increase to some extent. The biomass of the small and low trophic level species, jellyfish, prawns and benthic crustaceans would be stable. The total biomass of the fishery resources would have a 10% decrease from the current biomass after 10 years. In contrast, the reduced fishing mortality rate induced the recovery of biomass (scenarios 2–4). In scenario 2, the biomass of the large demersal fish and the large pelagic fish would increase to over 16 times and 10 times, respectively, of their current level. In scenario 4, the biomass of the large pelagic fish would increase to over 3 times of its current level. The total biomass of the fish groups, especially the high trophic level groups, would become significantly higher after 10 years, which illustrates the contribution on biomass recovery by relaxing the fishing pressure. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. Author contributions: Xiaoping Jia designed research; Zuozhi Chen and Yongsong Qiu performed research; Zuozhi Chen, Yongsong Qiu, and Shannan Xu analyzed data; and Zuozhi Chen and Shannan Xu wrote the article.     

Ecological Risk Assessment of China's Freshwater Ecosystems Applying the Relative Risk Model: Toward an Ecosystem-Based Water Management in China

The relative risk model (RRM) was applied to evaluate the ecological risk characterization of the freshwater ecosystems in China, from both overall and region-specific levels. Ten large-scale river basins (further broken into 15 risk regions) in China were chosen as the study objects; 10 sources, two habitats, and seven endpoints were identified as risk components. The results reveal the status of ecosystem conditions, key ecological risk issues, and the spatial heterogeneity of the freshwater ecosystems in China. The policy implications for the ecosystem-based water management contained in the results are discussed. The results obtained in this article provide a deeper understanding of the ecological risk characterization of the freshwater ecosystems in China, and aid in promoting the applications of the RRM as the tool for ecosystem-based water management.