Trends in Parasitology
Volume 31, Issue 4, April 2015, Pages 149-159
Journal home page for Trends in Parasitology

Review
Special Issue: Wildlife Parasitology
Emerging infectious diseases of wildlife: a critical perspective

https://doi.org/10.1016/j.pt.2015.01.007Get rights and content

Highlights

  • We critically review the evidence for current vertebrate wildlife disease emergence.

  • Sufficient data on prior absence or difference are lacking for many infectious agents.

  • Host exposure to domestic infection sources is the primary driver of fish disease emergence.

  • Human-assisted exposure to wild infection sources is the primary driver for other taxa.

We review the literature to distinguish reports of vertebrate wildlife disease emergence with sufficient evidence, enabling a robust assessment of emergence drivers. For potentially emerging agents that cannot be confirmed, sufficient data on prior absence (or a prior difference in disease dynamics) are frequently lacking. Improved surveillance, particularly for neglected host taxa, geographical regions and infectious agents, would enable more effective management should emergence occur. Exposure to domestic sources of infection and human-assisted exposure to wild sources were identified as the two main drivers of emergence across host taxa; the domestic source was primary for fish while the wild source was primary for other taxa. There was generally insufficient evidence for major roles of other hypothesized drivers of emergence.

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

References (79)

  • L. Berger

    Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America

    Proc. Natl. Acad. Sci. U.S.A.

    (1998)
  • J.E. Longcore

    Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians

    Mycologia

    (1999)
  • A. Martel

    Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians

    Proc. Natl. Acad. Sci. U.S.A.

    (2013)
  • A. Storfer

    Phylogenetic concordance analysis shows an emerging pathogen is novel and endemic

    Ecol. Lett.

    (2007)
  • M.J. Gray

    Ecology and pathology of amphibian ranaviruses

    Dis. Aquat. Organ.

    (2009)
  • S.L. LaDeau

    West Nile virus emergence and large-scale declines of North American bird populations

    Nature

    (2007)
  • A.M. Kilpatrick

    Globalization, land use, and the invasion of West Nile virus

    Science

    (2011)
  • P.R. Hosseini

    Spatial spread of an emerging infectious disease: conjunctivitis in house finches

    Ecology

    (2006)
  • W.M. Hochachka

    Multiple host transfers, but only one successful lineage in a continent-spanning emergent pathogen

    Proc. Biol. Sci.

    (2013)
  • J. Liu

    Highly pathogenic H5N1 influenza virus infection in migratory birds

    Science

    (2005)
  • P. Calistri

    West Nile virus transmission in 2008 in North-Eastern Italy

    Zoonoses Public Health

    (2010)
  • H. Weissenbock

    Emergence of Usutu virus, an African mosquito-borne Flavivirus of the Japanese encephalitis virus group, Central Europe

    Emerg. Infect. Dis.

    (2002)
  • A. Vázquez

    Usutu virus – potential risk of human disease in Europe

    Euro Surveill.

    (2011)
  • J. Keawcharoen

    Avian influenza H5N1 in tigers and leopards

    Emerg. Infect. Dis.

    (2004)
  • S.I. Roberton

    Avian influenza H5N1 in viverrids: implications for wildlife health and conservation

    Proc. Biol. Sci.

    (2006)
  • X. Qi

    Molecular characterization of highly pathogenic H5N1 avian influenza A viruses isolated from raccoon dogs in China

    PLoS ONE

    (2009)
  • L.A. Reperant

    Avian influenza viruses in mammals

    Rev. Sci. Tech.

    (2009)
  • D.M. Tompkins

    Ecological replacement of native red squirrels by invasive greys driven by disease

    Ecol. Lett.

    (2003)
  • C.J. McInnes

    First cases of squirrelpox in red squirrels (Sciurus vulgaris) in Scotland

    Vet. Rec.

    (2009)
  • C.J. McInnes

    The emergence of squirrelpox in Ireland

    Anim. Conserv.

    (2013)
  • D.S. Blehert

    Bat white-nose syndrome: an emerging fungal pathogen?

    Science

    (2009)
  • J.M. Lorch

    Experimental infection of bats with Geomyces destructans causes white-nose syndrome

    Nature

    (2011)
  • S.E. Saunders

    Occurrence, transmission, and zoonotic potential of chronic wasting disease

    Emerg. Infect. Dis.

    (2012)
  • E.S. Almberg

    Persistence of canine distemper virus in the Greater Yellowstone Ecosystem's carnivore community

    Ecol. Appl.

    (2010)
  • E.S. Almberg

    Parasite invasion following host reintroduction: a case study of Yellowstone's wolves

    Philos. Trans. R. Soc. Lond. B: Biol. Sci.

    (2012)
  • M.B. Fournier

    Cyprinid herpesvirus 3: an interesting virus for applied and fundamental research Emerg

    Infect. Dis.

    (2010)
  • R.J. Whittington

    Iridovirus infections in finfish – critical review with emphasis on ranaviruses

    J. Fish Dis.

    (2010)
  • P.J. Walker et al.

    Emerging viral diseases of fish and shrimp

    Vet. Res.

    (2010)
  • J.M. Grizzle et al.

    Review of largemouth bass virus

    Fisheries

    (2003)
  • Cited by (209)

    View all citing articles on Scopus
    View full text