Surveillance for Emerging Biodiversity Diseases of Wildlife

Effective surveillance is crucial for early detection and successful mitigation of emerging diseases [1]. The current global approach to surveillance for wildlife diseases affecting biodiversity (‘‘biodiversity diseases’’) is still inadequate as demonstrated by the slow characterization and response to the two recent devastating epidemics, chytridiomycosis and whitenose syndrome [2–5]. Current surveillance for wildlife disease usually targets diseases that affect humans or livestock, not those impacting wildlife populations. Barriers to effective surveillance for biodiversity diseases include a relative lack of social and political will and the inherent complexity and cost of implementing surveillance for multiple and diverse free-ranging populations. Here we evaluate these challenges and the inadequacies of current surveillance techniques, and we suggest an integrated approach for effective surveillance. Despite challenges in quantifying the role of disease in species declines [6], there are numerous clear examples of diseases (infectious, toxic, multifactorial, or of undetermined origin) that have caused severe population impacts; for example, avian malaria and poxvirus in Hawaii, diclofenac poisoning in Indian vultures, rinderpest in Africa, bighorn sheep pneumonia, chronic wasting disease, crayfish plague, avian trichomonosis, and Tasmanian devil facial tumor disease [7–15]. The emergence of the amphibian fungal skin disease chytridiomycosis is a pertinent example in which a lack of effective disease surveillance contributed to global biodiversity loss (Figure 1) [16–18]. Epidemiological investigation did not commence until 15 years after initial declines [19]. Despite recent listing of chytridiomycosis as a notifiable disease by the World Organization for Animal Health (OIE), the extended time before diagnosis very likely contributed to the decline and extinction of at least 200 species of frogs globally, helping to make amphibians the most endangered vertebrate class [3,20]. Here we define ‘‘biodiversity disease’’ as ‘‘a disease that has caused, or is predicted to cause, a decline in a wild species sufficient to worsen its conservation status.’’ This term can be applied to kingdoms other than Animalia, but those are outside the scope of the current paper. Our aim is to improve wildlife biodiversity disease surveillance, which could have important socioeconomic benefits, including reducing long-term disease management costs, protecting biodiversity and ecosystem services, and contributing to prespillover surveillance for public health and agricultural diseases [21–31]. Preventing disease-linked species extirpation will stabilize ecosystems, curtailing cascades of trophic coextinctions and global biodiversity loss [32–34]. Biodiversity and ecosystem stability are also increasingly linked with decreased risk of disease emergence [25,35–39]. Current funding priorities for wildlife health surveillance tend to rely on overlap with human and livestock diseases [1]. Cost-benefit analyses applied to zoonotic and agricultural diseases in funding prioritization models, including, for example, the ‘‘willingness to pay’’ framework based on societal values and the concept of paying for ‘‘ecosystem services,’’ typically do not adequately address the consequences of biodiversity loss [4,40,41]. Appropriately quantifying the value of biodiversity would assist leveraging more appropriate resource allocation. Responsibility for wildlife health is often spread across multiple agencies, levels of government, universities, and nongovernment agencies. This fragmentation of accountability may contribute to lower prioritization of biodiversity disease surveillance and control compared with human and livestock health threats, which are managed by specific departments. To promote effective implementation of surveillance programs, a greater focus on emerging biodiversity diseases is needed in international policy and practice and more support must be given to existing regional wildlife health frameworks, recognizing their crucial role in identifying and managing biodiversity diseases. This recognition should encourage coordination at international, national, and local levels, as well as resourcing on-the-ground surveillance. Several international bodies concerned with animal health are appropriately situated to take on this coordinating role, and collaborations between bodies such as OIE and the World Conservation Union (IUCN) may provide the necessary transdisciplinary expertise required [3]. The OIE has already taken steps in this direction by listing notifiable and nonnotifiable infectious diseases, highlighting current issues through their Working Group on Wildlife Diseases, and developing their ‘‘Training Manual on Wildlife Diseases and Surveillance’’ [42]. International coordination can result in rapid disease assessments, prioritization of resources, and targeted response via regional frameworks for wildlife health (for example, the successfully coordinated, multiagency response to highly pathogenic avian influenza virus, H5N1 [4]).