Trends in Parasitology
ReviewSpecial Issue: Wildlife ParasitologyEmerging infectious diseases of wildlife: a critical perspective
Introduction
Be they impacting people, agriculture, or wildlife, emerging infectious diseases (disease-causing agents that rapidly increase in geographical range, host range, or prevalence) are acknowledged to be occurring at an increased rate globally 1, 2, 3. Management to successfully mitigate these threats requires identifying and understanding their drivers. However, it is increasingly recognized that many reports of currently and recently emerging disease-causing agents may have insufficient supporting evidence to substantiate their status as such 4, 5. In such cases, frequently limited resources for research and management may be misallocated with respect to where they could make the most valuable impact. In addition, the ‘noise’ generated by spurious cases may obscure accurate assessments of emergence drivers and thus be misleading in considerations of suitable and effective management actions to decrease risk of emergence.
Here we conduct to the best of our knowledge the most critical review and assessment to date of the current and recent vertebrate wildlife emerging infectious disease literature (see Box 1 for the methodology used). Our aim is threefold. First, we separate agents for which there is sufficient evidence of emergence from those for which there is insufficient evidence to support such a conclusion and interrogate the patterns observed with respect to host and agent taxa and the timing and geography of emergence. Second, based on only those agents with sufficient evidence, we objectively identify and rank in terms of importance the causes and drivers of disease emergence in vertebrate wildlife, to provide robust guidelines for management to mitigate such threats to wild populations (see Box 2 for all of the potential drivers of disease emergence indicated by the full review). Third, we provide direction to researchers regarding where efforts would be best focused to further increase our understanding of, and thus our ability to prevent, such disease emergence.
Section snippets
Amphibians and reptiles
Nine disease-causing infectious agents of amphibians and reptiles were identified with evidence of potential emergence from 2000 onward (Table S1 in the supplementary material online). Amphibians were the most affected group (with six potential agents) followed by turtles (with three). Almost half of the potential emergences are ongoing from the past century and there is no obvious temporal bias in those reported this century (Figure 1). There is also no strong evidence of any agent taxon bias,
Birds
Eight disease-causing infectious agents of birds were identified with evidence of potential emergence from 2000 onward (Table S2 in the supplementary material online), counting Lineages 1 and 2 of West Nile virus as distinct emergences. Six of these agents solely or mainly impact passerine birds while two impact waterfowl. A large proportion were initially reported from North America or Europe, also with a temporal bias in reporting; while two are ongoing from the past century, the other six
Eutherian mammals
Eighteen disease-causing infectious agents of eutherian mammals were identified with evidence of potential emergence from 2000 onward (Table S3 in the supplementary material online). While the most common host orders were the Carnivora (both terrestrial and aquatic) and Cetacea, potential emergences were reported from a wide host range. As with birds, a large proportion of potential emergences were initially reported from North America or Europe, again with a temporal bias in reporting; while
Fish
Twenty-eight disease-causing infectious agents of fish were identified with evidence of potential emergence from 2000 onward (Table S4 in the supplementary material online). Agents were recorded across freshwater, estuarine, and marine host species, but with a bias toward economically important fish in temperate waters (salmonids, cyprinids, and catfish) and those that are farmed for food production or ornamental trade. There is very poor representation of emerging infectious diseases of
Marsupials and monotremes
Seven disease-causing infectious agents of marsupials and monotremes were identified with evidence of potential emergence from 2000 onward (Table S5 in the supplementary material online); four are ongoing from the past century and there is no obvious temporal bias in those reported this century (Figure 1). Six of these agents impact marsupials (spanning kangaroos, wallabies, bandicoots, wombats, and the Tasmanian devil) and one impacts monotremes (platypus in Tasmania). Of the six
Taxonomic identity of emerging infectious agents
In the complete set of agents with sufficient evidence of emergence (N = 34), there is a clear skew toward microparasites across all host taxa; 76% were microparasites and 14% macroparasites, with over half of the microparasites being viruses (Figure 2). Exceptions to the dominance of viral agents were observed in the marsupials and monotremes host taxa set (with one mite and one transmissible cancer being the only agents with sufficient evidence of emergence) and in the amphibians and reptiles
Host taxon patterns of agent emergence
Reports from fish account for over half of the agents with sufficient evidence of emergence, with other host taxa accounting for approximately 5–15% each (Table 2). This may reflect a real greater rate of disease emergence in fish, a higher level of surveillance of fish populations, or simply that there are more species of fish in the world than of the other host taxa (Table 2). However, in terms of emergences with sufficient evidence per species known, it is the marsupial and monotreme host
Temporal and geographical patterns of agent emergence
For the agents with sufficient evidence of emergence, almost two-thirds were agents that initially emerged in the past century that were/are continuing to spread from 2000 onward. Of the remainder, four were first reported during the period 2000–2004, seven during 2005–2009, and only one during 2010–2014 (undoubtedly at least partly reflecting a time lag in clinical identification and publication in the peer-reviewed literature). Interestingly, there is a high proportion of potentially emerging
Drivers of agent emergence
There is a clear difference between fish and the other host taxa in which drivers played the greatest role in the emergence of disease-causing infectious agents (Figure 3). For the cases in fish with sufficient evidence (N = 19; Table 1), host exposure to infectious agents from domestic populations (aquaculture, stocks for release, and the ornamental fish trade) is recognized as the primary cause in 14 (74%). With exposure to domestic populations playing a lesser role in agent emergence in other
Evidence of absence or absence of evidence?
The more compelling examples of wildlife disease emergence are those with multiple lines of evidence all supporting the hypothesis of emergence and the proposed drivers. For example, the cases for chytridiomycosis, DFTD, West Nile virus, mycoplasmal conjunctivitis, white-nose syndrome, and A(H5N1) emergence are all supported by a combination of high-quality spatiotemporal surveillance data, molecular evidence of emergence source, and outbreak investigations that together are more than
Concluding remarks
Our consideration of wildlife disease emergence (Box 3) is undoubtedly biased; the requirement of ‘sufficient evidence’ for our assessment of drivers will have a bias toward agents for which emergence is easier to demonstrate; that is, those with obvious disease as opposed to more cryptic impacts, those showing monotonic increases in host or geographical range (or disease incidence or impact) as opposed to more sporadic outbreak dynamics, and those that are localized and specialists as opposed
Acknowledgments
This review was inspired by the ‘Management of Wildlife Diseases – Shifting the Paradigm’ symposium at the 25th International Congress for Conservation Biology (ICCB). Funding was provided by the New Zealand Ministry for Business, Innovation, and Employment to D.M.T., a US NSF-NIH Ecology and Evolution of Infectious Diseases grant (EF1413925) to S.C., Australian Research Council grant DP110103069 and a US NSF-NIH Ecology and Evolution of Infectious Diseases grant to M.E.J., a Discovery Grant
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