Amphibian chytridiomycosis
Submitting Institution
Institute of Zoology, LondonUnit of Assessment
Earth Systems and Environmental SciencesSummary Impact Type
EnvironmentalResearch Subject Area(s)
Environmental Sciences: Environmental Science and Management
Biological Sciences: Genetics
Agricultural and Veterinary Sciences: Veterinary Sciences
Summary of the impact
Amphibian population declines are recognised as one of the largest
biodiversity crises in modern
history. Professor Andrew Cunningham, Institute of Zoology (IOZ) headed
the team that identified
a novel chytrid fungus as the major cause of amphibian population declines
and species
extinctions. Our work is the basis for the scientific and conservation
responses to this disease, and
led to the fungus being listed by the OIE (World Organisation for Animal
Health). We have
established national surveillance programmes for the pathogen across the
EU and elsewhere,
identifying species at risk and developing mitigating measures to prevent
pathogen introduction
and species extinction.
Underpinning research
In the mid-1990s, Professor Andrew Cunningham at the Institute of Zoology
(IOZ) initiated
investigations into infectious causes of global amphibian mortality and
declines. As leader of the
Pathology and Diseases Working Group of the IUCN Declining Amphibian
Populations Task Force,
he co-discovered a novel chytrid fungus causing a disease of amphibians,
and showed that a
common infectious cause of amphibian mortality was associated with
population declines on two
continents. This work was described in Nature (394, 418-419) as
"an exemplary example of
international scientific collaboration". Following on from this, IOZ
researchers demonstrated that
the infectious agent, Batrachochytrium dendrobatidis (Bd),
a non-hyphal chytrid fungus that
produces the disease amphibian chytridiomycosis, is a major cause of
amphibian mortality,
population declines and species extinctions globally [1].
Since then, IOZ scientists have significantly advanced our understanding
of amphibian
chytridiomycosis through a wide range of projects. In 2003, Cunningham
worked with post-doctoral
researchers Trent Garner and Matthew Fisher on a NERC-funded project to
investigate the
ecological and genetic determinants of Bd emergence in European
amphibian populations. This
research demonstrated that chytridiomycosis is caused by a novel, emerging
fungus that arose
through substantial recombination and chromosomal copy number variation
and that post-emergence
disease dynamics are governed by an interaction between pathogen genotype,
host
species and community structure and a range of environmental factors,
including altitude, water
and air temperature, and salinity [2] [3]. Furthermore, IOZ
scientists showed that not all cases of
emergence result in amphibian declines or even mortality [2] and
conversely that exposure, even
in the absence of infection, can result in amphibian mortality.
Since 2004, projects co-founded by IOZ with Fisher, now a Professor at
Imperial College, have
revealed the extent of the global distribution of Bd and have
described infection in more than 500
amphibian species [4]. IOZ has been working in the Caribbean since
2003 and in Europe since
2007 to investigate the ecology and infection dynamics of Bd in
multi-species host communities.
This work has identified areas and amphibian taxonomic groups that are at
greater risk of disease
emergence and decline due to chytridiomycosis [5] and we have
shown how the introduction of
non-native species, translocations for conservation purposes and the
amphibian trade are all key
routes for the range expansion of Bd [6].
Our disease mitigation research is on-going, but has included
investigating safe treatments to cure
the disease in captive animals; whether field treatments can be used to
reduce the impact of the
disease on wild populations of Critically Endangered amphibians; whether
the impact of the
pathogen can be reduced through pre-exposure of animals to a hypovirulent
lineage of the fungus);
and whether restocking is a useful conservation tool following declines
due to chytridiomycosis [7].
References to the research
[1] Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL,
Slocombe R, Ragan
MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H.
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 Jul 21;95(15):9031-6.
http://www.pnas.org/content/95/15/9031.long
Cited >1100 times on Google Scholar
[2] Walker SF, Bosch J, Gomez V, Garner TWJ, Cunningham AA, Schmeller DS,
Ninyerola M,
Henk D, Ginestet C, Christian-Philippe A, Fisher MC. Factors driving
pathogenicity versus
prevalence of the amphibian pathogen Batrachochytrium dendrobatidis and
chytridiomycosis in
Iberia. Ecology Letters. 2010;13:372-82. http://dx.doi.org/10.1111/j.1461-0248.2009.01434.x.
Cited 55 times already on Google Scholar
[4] Garner TW, Perkins MW, Govindarajulu P, Seglie D, Walker S,
Cunningham AA, Fisher MC.
The emerging amphibian pathogen Batrachochytrium dendrobatidis globally
infects introduced
populations of the North American bullfrog, Rana catesbeiana. Biol Lett.
2006 Sep 22;2(3):455-9.
http://dx.doi.org/10.1098/rsbl.2006.0494
Cited 182 times already on Google Scholar
[5] Bielby, J et al. Predicting susceptibility to future declines in the
world's frogs. Conservation
Letters 1 (2008): 82-90. DOI: 10.1111/j.1755-263X.2008.00015.x Cited 82
times already on
Google Scholar
[7] Walker SF, Bosch J, James TY, Litvintseva AP, Oliver Valls JA, Piña
S, García G, Rosa GA,
Cunningham AA, Hole S, Griffiths R, Fisher MC. Invasive pathogens threaten
species recovery
programs. Curr Biol. 2008 Sep 23;18(18):R853-4. http://dx.doi.org/10.1016/j.cub.2008.07.033
Key Grants
Fisher MC, Cunningham AA. Ecological and genetic determinants of Batrachochytrium
dendrobatidis emergence in European amphibian populations. NERC.
2003-6. £193,193.
Cunningham AA. Addressing a threat to Caribbean amphibians: capacity
building in Dominica;
Darwin Initiative for the Survival of Species; 2005-8; £204,834.
Fisher MC, Garner TWJ, Cunningham AA. Relationship between environmental,
ecological and
genetic drivers of emergence in amphibian chytridiomycosis. NERC. 2007-10.
£70,032.
Fisher MC, Garner TWJ, Donnelly C. Modelling the amphibian response to
infection by the chytrid
Batrachochytrium dendrobatidis. BBSRC. 2007-8. £128,195.
Cunningham AA. Investigation of amphibian chytridiomycosis: national
surveillance and local
monitoring. Natural England. 2007-8. £61,000.
Garner TWJ and six coapplicant European institutions. R.A.C.E. Risk
Assessment of
Chyridiomycosis to Europe's Amphibians. EU BiodivERsA
Programme, UK funding through NERC
and Defra. 2008-13. Total budget €1.5m, IOZ component £236,617.
Cunningham AA. Epidemiological aspects of amphibian chytridiomycosis
caused by
Batrachochytrium dendrobatidis. Defra. 2009-12. £264,000.
Bosch J, Garner TWJ, Fisher MC, Bielby J. Disease mitigation in declining
amphibian populations.
Fundación General CSIC Proyectos Cero. 2010-ongoing. €224,355.
Details of the impact
The underpinning research described above has prompted an international
effort to understand the
emergence, distribution, epidemiology, impact and control of Bd.
This work has illustrated how Bd
is unrivalled among pathogens in host range and its impact on
biodiversity. Before Bd, wildlife
disease was considered a specialist, peripheral subject of interest, but
is now firmly on the ecology
and conservation biology agendas.
Bd surveillance
As a result of his research into Bd, Cunningham was invited in
2006 to become a founder member
of the World Organisation for Animal Health (OIE) amphibian disease ad
hoc group. This group
reviewed available research (much from IOZ) and unanimously agreed to
recommend that
amphibian chytridiomycosis be listed by the OIE. This was agreed by the
OIE General Session in
May 2008, making amphibian chytridiomycosis (along with ranaviral disease)
the first OIE-listed
amphibian pathogen [a]. This listing made chytridiomycosis
internationally notifiable and thus
subject to OIE standards, which aim to assure the sanitary safety of
international trade in live
amphibians and their products. A total of 178 Member Countries are
Signatories to the OIE - these
countries are now obliged to instigate surveillance and control measures
for chytridiomycosis. As a
result, a network of government agencies, research institutions, NGOs and
other parties have
developed regional and national surveillance schemes. Our work has led to
diagnostic labs for Bd
detection being set up and staff trained by Cunningham, Garner and Becki
Lawson (IOZ Research
Fellow) in several countries [b].
Since 2009, the European surveillance effort has been coordinated through
the IOZ via the RACE
project, which involves NGOs, universities and government agencies in 15
EU Member and
Associate States [c]. Data from this and other projects, including
the UK national Bd surveillance
project (commissioned by the UK conservation agencies and Defra and
conducted by Cunningham
in 2008 and 2011), are open access and used by disease researchers across
the globe. The
results of our 2008 UK Bd surveillance, which involved the
training and engagement of hundreds of
citizen science volunteers, led to Natural England requiring any protected
amphibians being
translocated to be tested for, and free of, Bd prior to issuing a
translocation licence [d]. The
surveillance results also led to Defra commissioning IOZ to conduct a
three-year study to
investigate the epidemiology of the pathogen in the UK, which will be used
to inform UK
government policy on the control of Bd in the UK.
International policy
Although amphibians are not listed in the Appendices of the Convention on
Migratory Species,
chytridiomycosis was one of the diseases that alerted the Convention on
Migratory Species (CMS)
Scientific Council to the importance of disease as a conservation threat
to wildlife, prompting the
adoption of two CMS Resolutions: 9.8 Responding to the Challenge of
Emerging and Re-Emerging
Diseases in Migratory Species, Including Highly Pathogenic Avian Influenza
H5N1 (2008), and
10.22 Wildlife Disease and Migratory Species (2011). Resolution 9.8 led to
the creation of the
UNEP-CMS and FAO Co-convened Scientific Task Force on Wildlife and
Ecosystem Health. In
2012, Cunningham was technical editor for the disease factsheet on
amphibian chytridiomycosis
which formed part of the Ramsar Wetland Disease Manual (Ramsar Technical
Report No. 7),
produced by the Wildfowl & Wetlands Trust for the Ramsar Convention
(an international treaty on
the conservation of wetlands) [e].
Mitigating the effects of Bd
Research by Cunningham, Garner and their students have developed chemical
antifungal
treatments for Bd (primarily using Itraconazole) for captive
animals and these are now used by
zoos (e.g. by the Team Leader in Herpetology, ZSL London Zoo) and others
across the world.
Working with Defra, we produced a national risk assessment for Bd
in the UK - the first of its kind
in the world [f].
In 2008, Cunningham convened an international workshop in Dominica, from
which
representatives of nine governments in the region attended. This workshop
produced a
Chytridiomycosis Management Plan for the Lesser Antilles Region [g].
This plan markedly raised
awareness about amphibian conservation and wildlife disease amongst
wildlife departments and
others in the region, leading to conservation measures in the region [h].
Biosecurity measures used in amphibian conservation programs in the
Caribbean, across Europe,
and in China were first developed by Cunningham and are communicated to a
wider audience as
best practice guidelines for field researchers working in aquatic
environments and are available on
the websites of a variety of GOs and NGOs [i].
Sources to corroborate the impact
[a] Final Report of the OIE 76th General Session • Paris, 25-30 May 2008.
http://www.oie.int/doc/ged/D11922.PDF
See p.66-7
[b] Our work training for Bd diagnosis can be verified by a
supporting statement from the Curator
of Herpetology Collection at the Hungarian Natural History Museum. Copy
available on
request.
[c] http://www.bd-maps.eu/
[d] The impact of our work on Natural England policy and practice can be
verified by a supporting
statement from the Conservation Director, Amphibian & Reptile
Conservation. Copy available
on request.
[e] The relevant resolutions are available at
http://www.cms.int/bodies/COP/cop10/resolutions_adopted/10_22_diseases_e.pdf,
http://www.ramsar.org/pdf/lib/rtr7-disease.pdf
see p.176 and
http://www.ramsar.org/pdf/cop11/res/cop11-res12-e.pdf,
and Cunningham's contribution can be
verified by a supporting statement from Head of Wildlife Health2028
Wildfowl & Wetlands
Trust,2028 Slimbridge. Copy available on request.
[f] Peel AJ, Hartley M, Cunningham AA. Qualitative risk analysis of
introducing Batrachochytrium
dendrobatidis to the UK through the importation of live amphibians. Dis
Aquat Organ. 2012 Mar
20;98(2):95-112. http://dx.doi.org/10.3354/dao02424.
Use by Defra can be verified by
European Specialist in Wildlife Population Health at Zoo and Wildlife
Solutions Ltd.
[g] http://www.mountainchicken.org/wp-content/uploads/2010/11/Chytridiomycosis-Management-Plan.pdf
[h] Conservation impacts resulting from the Chytridiomycosis Management
Plan for the Lesser
Antilles Region can be verified by a supporting statement from the
Director of Forestry, Wildlife
and Parks, Ministry of Agriculture and Forestry, Commonwealth of Dominica.
Copy available on
request.
[i] www.snh.gov.uk/docs/B349121.pdf