Opinion
Surveillance for Emerging Biodiversity Diseases of
Wildlife
Laura F. Grogan1*, Lee Berger1, Karrie Rose2, Victoria Grillo3, Scott D. Cashins1, Lee F. Skerratt1
1 One Health Research Group, School of Public Health, Tropical Medicine and Rehabilitation Sciences, James Cook University, Townsville, Queensland, Australia,
2 Australian Registry of Wildlife Health, Taronga Conservation Society Australia, Mosman, New South Wales, Australia, 3 Wildlife Health Australia (formerly Australian
Wildlife Health Network), Georges Heights, New South Wales, Australia
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
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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]).
Citation: Grogan LF, Berger L, Rose K, Grillo V, Cashins SD, et al. (2014) Surveillance for Emerging Biodiversity
Diseases of Wildlife. PLoS Pathog 10(5): e1004015. doi:10.1371/journal.ppat.1004015
Editor: Glenn F. Rall, The Fox Chase Cancer Center, United States of America
Published May 29, 2014
Copyright: ß 2014 Grogan et al. This is an open-access article distributed under the terms of the Creative
Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium,
provided the original author and source are credited.
Funding: LFG and LB were supported by Australian Research Council grants LP110200240 and FT100100375.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the
manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: laura.grogan@my.jcu.edu.au
1
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Figure 1. Chytridiomycosis: a catastrophic biodiversity disease causing amphibian declines. Chytridiomycosis emerged in the 1970s but
was not detected until the 1990s. (A) An alpine tree frog (Litoria verreauxii alpina) with severe chytridiomycosis, showing skin reddening and an
inability to maintain normal upright posture; (B) skin surface of a stony creek frog (formerly Litoria lesueuri). Many cells are infected with sporangia,
pushing discharge tubes (arrow) to the skin surface (scanning electron micrograph). Scale bar = 10 mm.
doi:10.1371/journal.ppat.1004015.g001
A number of regional frameworks are
already established, while others are new
and emerging. With improved funding,
regional frameworks for wildlife health will
be better equipped to provide direction,
facilities, and expertise for surveillance.
These centers typically involve collaboration of veterinarians, ecologists, wildlife
biologists, microbiologists, and molecular
biologists. They require salaries for field
staff, epidemiologists, and pathologists;
funding for diagnostic testing; and data
management systems to collect and analyze surveillance data. Agreement on
methodologies, risk assessment pathways,
and contingency plans for emerging infectious biodiversity diseases across these
regional frameworks will support prompt
responses to outbreaks [43].
Current biodiversity disease surveillance
is often ad hoc and relies on passive
surveillance (data collected from community submissions) or activities that overlap
with human and livestock diseases. This
approach is unable to elucidate the impact
of disease on the population because only
the diseased subpopulation is detected,
and it is less likely to detect subtle clinical
signs or alterations in species fitness, such
as reduced fecundity, despite potentially
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large population impacts [44–52]. Some
diseases may also be underrepresented due
to the cryptic or noncharismatic nature of
the hosts, the remote nature of the
location, or apathy or acceptance of
consequences once a diagnosis has been
reached [47,53–55].
Considering the potential deficiencies of
current approaches to detect emerging
biodiversity diseases, a new, transdisciplinary, systematic surveillance approach is needed. Essential elements of this approach are
established in many countries, but are not
specifically being utilized to detect biodiversity diseases. The following aspects
could be incorporated into this approach:
1) Combine current strategies (integrate passive and active or general
and targeted techniques with outbreak
investigations that characterize
emerging pathogens or multifactorial
disease pathways to enable implementation of effective control) [56]. Surveillance techniques in use for human
and domestic animal diseases that
may be adapted include:
a.
Disease-specific screening for incursions of important pathogens.
2
b.
Use of sentinel species or individuals
at sentinel locations (such as key
wildlife trade sites) [27,53,57].
Species could be ranked for use
as sentinels by evaluating:
i.
ii.
Species value based on conservation status, taxonomy, ecosystem representation, and
phylogenetic uniqueness.
Sentinel value based on ecological role (keystone species
and predators/scavengers),
ease of observation and representative sampling, current
level of study, and probability as a disease-emergence
host [58].
2) Target both known and unknown pathogens and hosts
and regions predicted to be at
high risk for disease emergence
through predictive modeling.
Retrospective and risk factor analyses show correlations between the
incidence of disease emergence in
general and socioeconomic and
ecological factors (for example,
May 2014 | Volume 10 | Issue 5 | e1004015
highly biodiverse developing regions constitute infectious-disease–
emergence hotspots which could be
targeted [28,59–61]). Deterministic
models based on
general pathogen characteristics
and sensitivity analysis, combined
with metagenomic studies, hold
potential for predicting future disease emergence [62–65].
3) Ensure spatial and taxonomic
representation to prevent the loss
of biodiversity in important taxonomic clades or small regions with high
levels of endemism [66].
4) Focus on multiple biological
levels, such as ecosystems and species
[67].
5) Integrate essential baseline ecological data collection for an un-
derstanding of the population
impact of disease. Mark-recapture
studies provide long-term data
on population dynamics and are
appropriate for wildlife population impact assessment, despite imperfect detection [68]. Integration
of epidemiological transmission models with disease, population, and
environmental data will better elucidate the roles of infectious disease,
anthropogenic environmental disturbance, and other factors in driving
changes in population structure, distribution, or size [69].
6) Incorporate self-evaluative mechanisms to ensure adaptability
and prioritization strategies.
Strategies should evolve as diagnostic
and ecological monitoring techniques
emerge, and as global circumstances
change [1,70,71]. Frameworks for
structured decision making and prioritization will ensure that surveillance
approaches remain cost effective
[72,73].
In conclusion, we suggest that improved
integration, capacity, and a systematic
approach to disease surveillance in wildlife
are imperative for future biodiversity conservation.
Acknowledgments
The authors thank A. Roberts, S. Young, R.
Puschendorf, and D. Mendez for helpful
comments on the manuscript.
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