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Preserving pathogens for wildlife conservation: a case for action on amphibian declines

Published online by Cambridge University Press:  25 September 2009

Jamie Voyles*
Affiliation:
School of Public Health, Tropical Medicine and Rehabilitation Sciences, Amphibian Disease Ecology Group, James Cook University, Townsville, Queensland 4811, Australia
Scott D. Cashins
Affiliation:
School of Marine and Tropical Biology, Amphibian Disease Ecology Group, James Cook University, Townsville, Australia.
Erica Bree Rosenblum
Affiliation:
Department of Biological Sciences, University of Idaho, Moscow, USA.
Robert Puschendorf
Affiliation:
School of Marine and Tropical Biology, Amphibian Disease Ecology Group, James Cook University, Townsville, Australia.
*
*School of Public Health, Tropical Medicine and Rehabilitation Sciences, Amphibian Disease Ecology Group, James Cook University, Townsville, Queensland 4811, Australia. E-mail jamie.voyles@gmail.com
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Abstract

Infectious disease is an important driver in biological systems but its importance in conservation has historically been underestimated. Recently, however, researchers have increasingly recognized the impact of diseases on wildlife populations and have grappled with disease-related conservation challenges. For example, the phenomenon of worldwide amphibian declines caused by the fungal disease chytridiomycosis has contributed to the creation of a global Amphibian Conservation Action Plan. The sense of urgency in the protection of amphibians and mitigation of the effects of chytridiomycosis is well-warranted but determining the best way to respond to chytridiomycosis is challenging. Current conservation strategies focus on the preservation of the amphibian hosts, their habitats and their genetic materials. However, we suggest that to confront disease threats fully, particularly in the case of amphibian declines, insight into host–pathogen coevolution may be critical and we must therefore also preserve the pathogen for basic disease research. Here we outline priority targets for virulence research and urge researchers and managers to isolate and archive the pathogen Batrachochytrium dendrobatidis to ensure viable long-term amphibian conservation.

Type
Short Communications
Copyright
Copyright © Fauna & Flora International 2009

Parasites can regulate host population densities, alter community dynamics and affect entire ecosystems (Scott, Reference Scott1988; Daszak et al., Reference Daszak, Cunningham and Hyatt2000; Hudson et al., Reference Hudson, Rizzoli and Bryan2002; de Castro & Bolker, Reference de Castro and Bolker2005; Whiles et al., Reference Whiles, Lips, Pringle, Kilham, Bixby and Brenes2006). Disease has obvious consequences for already-threatened animal populations (e.g. black-footed ferrets, Thorne & Williams, Reference Thorne and Williams1988) but it can also pose a significant threat to otherwise healthy populations (Scott, Reference Scott1988; Daszak et al., Reference Daszak, Cunningham and Hyatt2000; de Castro & Bolker, Reference de Castro and Bolker2005). Many amphibians, for example, are experiencing unprecedented declines because of the disease chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Berger et al., Reference Berger, Speare, Daszak, Green, Cunningham and Goggin1998; Lips et al., Reference Lips, Brem, Brenes, Reeve, Alford and Voyles2006; Mendelson et al., Reference Mendelson, Lips, Gagliardo, Rabb, Collins and Diffendorfer2006; Gascon et al., Reference Gascon, Collins, Moore, Church, McKay and Mendelson2007). The relatively recent discovery of B. dendrobatidis was precipitated by amphibian mass mortality events and disappearances in pristine locations around the world (Berger et al., Reference Berger, Speare, Daszak, Green, Cunningham and Goggin1998; Lips et al., Reference Lips, Brem, Brenes, Reeve, Alford and Voyles2006; Mendelson et al., Reference Mendelson, Lips, Gagliardo, Rabb, Collins and Diffendorfer2006; Gascon et al., Reference Gascon, Collins, Moore, Church, McKay and Mendelson2007). Although B. dendrobatidis is confined to the superficial layers of epidermis, infected frogs can die rapidly because of the physiological importance of amphibian skin (Berger et al., Reference Berger, Speare, Daszak, Green, Cunningham and Goggin1998; Voyles et al., Reference Voyles, Berger, Young, Speare, Webb and Warner2007). Current B. dendrobatidis distribution patterns generated by predictive models are based on the occurrence of the pathogen on the amphibians (Ron, Reference Ron2005; Puschendorf et al., Reference Puschendorf, Carnaval, VanDerWal, Zumbado-Ulate, Chaves, Bolaños and Alford2009). It is unclear whether B. dendrobatidis can persist independently of amphibian hosts, in an alternate life stage (Di Rosa et al., Reference Di Rosa, Simoncelli, Fagotti and Pascolini2007), by saprobic growth (Mitchell et al., Reference Mitchell, Churcher, Garner and Fisher2008) or in non-amphibian carriers. In spite of these unresolved possibilities, the loss of biodiversity (Lips et al., Reference Lips, Brem, Brenes, Reeve, Alford and Voyles2006; Mendelson et al., Reference Mendelson, Lips, Gagliardo, Rabb, Collins and Diffendorfer2006), subsequent ecosystem disturbance (Whiles et al., Reference Whiles, Lips, Pringle, Kilham, Bixby and Brenes2006) and the risk for naïve amphibian populations justify immediate conservation efforts.

Management of infectious diseases is not easy; traditional conservation strategies, such as managing reservoir hosts, culling or vaccination, are not practical options where host management is not feasible or where vaccination is unavailable (Hudson et al., Reference Hudson, Rizzoli and Bryan2002). For amphibian conservation, one remediation prescribed by the Amphibian Conservation Action Plan and currently underway is the ‘rescue’ of amphibians from their natural habitats into ex situ breeding programmes before the disease emerges (Mendelson et al., Reference Mendelson, Lips, Gagliardo, Rabb, Collins and Diffendorfer2006; Gascon et al., Reference Gascon, Collins, Moore, Church, McKay and Mendelson2007). This strategy is controversial (Pounds et al., Reference Pounds, Carnaval, Puschendorf, Haddad and Masters2007) and many scientists recognize the conservation crux: re-establishment of amphibians into habitats where the pathogen is now endemic (Pounds et al., Reference Pounds, Carnaval, Puschendorf, Haddad and Masters2007; Schlaepfer, Reference Schlaepfer2007). Understanding host–pathogen interactions and coevolution may be critical for long-term conservation. However, with the current focus on preserving vulnerable amphibian hosts and their genetic material (Gascon et al., Reference Gascon, Collins, Moore, Church, McKay and Mendelson2007), the importance of pathogen collection and preservation is being overlooked. Chytridiomycosis is an important example of how access to pathogen isolates will be invaluable for disease research and conservation efforts.

Determinants of mortality from chytridiomycosis are multiple and complex. Pivotal factors include environmental conditions, population dynamics, host resistance and pathogen virulence. To date, most studies have focused on environmental factors (Woodhams et al., Reference Woodhams, Alford and Marantelli2003; Berger et al., Reference Berger, Speare, Hines, Marantelli, Hyatt and McDonald2004) and host resistance (Rollins-Smith et al., Reference Rollins-Smith, Doersam, Longcore, Taylor, Shamblin, Carey and Zasloff2002; Woodhams et al., Reference Woodhams, Ardipradja, Alford, Marantelli, Reinert and Rollins-Smith2007), whereas differential pathogen virulence has been largely neglected. Preliminary evidence suggests that B. dendrobatidis virulence may differ among isolates (Berger et al., Reference Berger, Marantelli, Skerratt and Speare2005; Retallick & Miera, Reference Retallick and Miera2007; Fisher et al., Reference Fisher, Bosch, Yin, Stead, Walker and Selway2009) but the underlying reasons for the variation are unknown. Furthermore, reduced mortality has been observed in populations after surviving initial emergence (Morgan et al., Reference Morgan, Vredenburg, Rachowicz, Knapp, Stice and Tunstall2007) and different populations, even within species, can experience differential susceptibility to chytridiomycosis (Briggs et al., Reference Briggs, Vredenburg, Knapp and Rachowicz2005). This variation in susceptibility to B. dendrobatidis suggests the possibility of increased host resistance, decreased parasite virulence or both.

Determining the factors that influence disease development will lead to a greater understanding of the disease and thus direct more effective conservation action. For example, we may be able to distinguish a novel pathogen from a pathogen that has increased in virulence (Daszak et al., Reference Daszak, Cunningham and Hyatt2000; Rachowicz et al., Reference Rachowicz, Hero, Alford, Taylor, Morgan and Vredenburg2005), assess potential disease risk (Kuiken et al., Reference Kuiken, Leighton, Fouchier, LeDuc, Peiris and Schudel2005), track pathogen movements (Kuiken et al., Reference Kuiken, Leighton, Fouchier, LeDuc, Peiris and Schudel2005; Kang et al., Reference Kang, Blair, Geiser, Khang, Park and Gahegan2006) or incorporate disease resistance into breeding programmes (Schlaepfer, Reference Schlaepfer2007). Substantial advancements in virulence research are achievable but depend on access to pathogen isolates from diverse spatio-temporal origins. We suggest three priority targets for pathogen collection and cryopreservation: (1) isolates from geographically and taxonomically diverse hosts, (2) isolates preserved during and following pathogen emergence, and (3) isolates collected at finer scales from populations exhibiting differential responses to infection. Such isolates will be a key resource for laboratory experiments and genetic studies aiming to identify pathogenicity factors (Rosenblum et al., Reference Rosenblum, Stajich, Maddox and Eisen2008) in chytridiomycosis or for any disease that threatens wildlife populations.

In the case of amphibian declines due to chytridiomycosis, the ability to confront the disease threat fully will hinge on coordinating multiple mitigation strategies including careful screening for the pathogen in naïve populations (Skerratt et al., Reference Skerratt, Berger, Hines, McDonald, Mendez and Speare2008; Cashins et al., in press) and in the international amphibian trade (Australian Government Department of the Environment and Heritage, 2006; Gascon et al., Reference Gascon, Collins, Moore, Church, McKay and Mendelson2007), identifying and preserving vulnerable amphibians (Mendelson et al., Reference Mendelson, Lips, Gagliardo, Rabb, Collins and Diffendorfer2006; Gascon et al., Reference Gascon, Collins, Moore, Church, McKay and Mendelson2007) and, most importantly, advancing basic disease research (Australian Government Department of the Environment and Heritage, 2006; Mendelson et al., Reference Mendelson, Lips, Gagliardo, Rabb, Collins and Diffendorfer2006; Gascon et al., Reference Gascon, Collins, Moore, Church, McKay and Mendelson2007). Understanding pathogen virulence is important to this endeavour and we urge managers and researchers to participate in a collaborative effort to archive B. dendrobatidis. Established methodologies for isolating (Longcore et al., Reference Longcore, Pessier and Nichols1999) and cryo-archiving (Boyle et al., Reference Boyle, Hyatt, Daszak, Berger, Longcore and Porter2003) B. dendrobatidis are available in multiple languages at the Global Bd Banking Project website (2009). In developing this website as an international forum, we aim to share the necessary resources to preserve B. dendrobatidis and to collate information on global isolates into a single database to facilitate virulence research. Confronting disease threats and implementing effective conservation action will require a better understanding of the disease, the host and the pathogen.

Biographical sketches

Jamie Voyles is interested in ecosystem health and the evolution of virulence in host-pathogen systems, focusing on pathogenesis of chytridiomycosis and virulence of Batrachochytrium dendrobatidis in amphibians. Scott D. Cashins studies disease ecology, focusing on transmission and seasonal dynamics of Batrachochytrium dendrobatidis in tadpoles in rainforest habitats of North Queensland, Australia. Erica B. Rosenblum's research interests centre on the mechanisms of adaptive evolution, using functional genomics tools to elucidate the genetic basis of pathogenicity of chytridiomycosis. Robert Puschendorf is interested in disease ecology and the influence of environmental factors on host-pathogen interactions, especially on dynamics of Batrachochytrium dendrobatidis across habitats in Costa Rica and Australia.

References

Australian Government Department of the Environment and Heritage (2006) Threat Abatement Plan: Infection of Amphibians With Chytrid Fungus Resulting in Chytridiomycosis. Canberra, Commonwealth of Australia. Http://www.environment.gov.au/biodiversity/threatened/publications/tap/chytrid [accessed 9 November 2008].Google Scholar
Berger, L., Marantelli, G., Skerratt, L.F. & Speare, R. (2005) Virulence of the amphibian chytrid fungus Batrachochytrium dendrobatidis varies with the strain. Diseases of Aquatic Organisms, 68, 4750.CrossRefGoogle ScholarPubMed
Berger, L., Speare, R., Daszak, P., Green, D.E., Cunningham, A.A., Goggin, C.L. et al. . (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the USA, 95, 9031.CrossRefGoogle ScholarPubMed
Berger, L., Speare, R., Hines, H.B., Marantelli, G., Hyatt, A.D., McDonald, K.R. et al. . (2004) Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Australian Veterinary Journal, 82, 434439.CrossRefGoogle ScholarPubMed
Boyle, D.G., Hyatt, A.D., Daszak, P., Berger, L., Longcore, J.E., Porter, D. et al. . (2003) Cryo-archiving of Batrachochytrium dendrobatidis and other chytridiomycetes. Diseases of Aquatic Organisms, 56, 5964.CrossRefGoogle ScholarPubMed
Briggs, C.J., Vredenburg, V.T., Knapp, R.A. & Rachowicz, L.J. (2005) Investigating the population-level effects of chytridiomycosis: an emerging infectious disease of amphibians. Ecology, 86, 31493159.CrossRefGoogle Scholar
Cashins, S.D., Skerratt, L.F. & Alford, R.A. (in press) Effect of sample collection techniques on sensitivity of real time PCR assay for detecting the amphibian pathogen Batrachochytrium dendrobatidis. Veterinary Microbiology.Google Scholar
Daszak, P., Cunningham, A.A. & Hyatt, A.D. (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science, 287, 443449.CrossRefGoogle ScholarPubMed
de Castro, F. & Bolker, B. (2005) Mechanisms of disease-induced extinction. Ecology Letters, 8, 117126.CrossRefGoogle Scholar
Di Rosa, I., Simoncelli, F., Fagotti, A. & Pascolini, R. (2007) Ecology: the proximate cause of frog declines? Nature, 447, E4E5.CrossRefGoogle ScholarPubMed
Fisher, M.C., Bosch, J., Yin, Z., Stead, D.A., Walker, J., Selway, L. et al. . (2009) Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Molecular Ecology, 18, 415429.CrossRefGoogle ScholarPubMed
Gascon, C., Collins, J.P., Moore, R.D., Church, D.R., McKay, J.E. & Mendelson, J.R. (2007) Amphibian Conservation Action Plan, Proceedings: IUCN/SSC Amphibian Conservation Summit 2005. IUCN, Gland, Switzerland.Google Scholar
Global Bd Banking Project (2009) Http://www.bdbank.org [accessed 6 August 2009].Google Scholar
Hudson, P.J., Rizzoli, A. & Bryan, G. (2002) The Ecology of Wildlife Diseases. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Kang, S., Blair, J.E., Geiser, D.M., Khang, C.H., Park, S.Y., Gahegan, M. et al. . (2006) Plant pathogen culture collections: it takes a village to preserve these resources vital to the advancement of agricultural security and plant pathology. Phytopathology, 96, 920925.CrossRefGoogle Scholar
Kuiken, T., Leighton, F.A., Fouchier, R.A., LeDuc, J.W., Peiris, J.S., Schudel, A. et al. . (2005) Pathogen surveillance in animals. Science, 309, 16801681.CrossRefGoogle ScholarPubMed
Lips, K.R., Brem, F., Brenes, R., Reeve, J.D., Alford, R.A., Voyles, J. et al. . (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences of the USA, 103, 31653170.CrossRefGoogle Scholar
Longcore, J.E., Pessier, A.P. & Nichols, D.K. (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia, 91, 219227.CrossRefGoogle Scholar
Mendelson, J.R. III, Lips, K.R., Gagliardo, R.W., Rabb, G.B., Collins, J.P., Diffendorfer, J.E. et al. . (2006) Confronting amphibian declines and extinctions. Science, 313, 48.CrossRefGoogle ScholarPubMed
Mitchell, K.M., Churcher, T.S., Garner, T.W.J. & Fisher, M.C. (2008) Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction. Proceedings of the Royal Society B, 275, 329334.CrossRefGoogle ScholarPubMed
Morgan, J.A.T., Vredenburg, V.T., Rachowicz, L.J., Knapp, R.A., Stice, M.J., Tunstall, T. et al. . (2007) Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the USA, 104, 13845.CrossRefGoogle ScholarPubMed
Pounds, J.A., Carnaval, A.C., Puschendorf, R., Haddad, C.F.B. & Masters, K.L. (2007) Action on amphibian extinctions: going beyond the reductive. Science (E-Letter, 28 August 2007), 313.Google Scholar
Puschendorf, R., Carnaval, A.C., VanDerWal, J., Zumbado-Ulate, H., Chaves, G., Bolaños, F. & Alford, R.A. (2009) Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: proposing climatic refuges as a conservation tool. Diversity and Distributions, 15, 401408.CrossRefGoogle Scholar
Rachowicz, L.J., Hero, J.M., Alford, R.A., Taylor, J.W., Morgan, J.A.T., Vredenburg, V.T. et al. . (2005) The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conservation Biology, 19, 14411448.CrossRefGoogle Scholar
Retallick, R.W.R. & Miera, V. (2007) Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sub-lethal effects of infection. Diseases of Aquatic Organisms, 75, 201207.CrossRefGoogle ScholarPubMed
Rollins-Smith, L.A., Doersam, J.K., Longcore, J.E., Taylor, S.K., Shamblin, J.C., Carey, C. & Zasloff, M.A. (2002) Antimicrobial peptide defenses against pathogens associated with global amphibian declines. Developmental and Comparative Immunology, 26, 6372.CrossRefGoogle ScholarPubMed
Ron, S. (2005) Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica, 37, 209221.CrossRefGoogle Scholar
Rosenblum, E.B., Stajich, J.E., Maddox, N. & Eisen, M.B. (2008) Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the USA, 105, 17034.CrossRefGoogle ScholarPubMed
Schlaepfer, M.A. (2007) Is there a role for evolutionary management in addressing the threat of chytridiomycosis? Science (E-Letter, 23 March 2007), 313.Google Scholar
Scott, M.E. (1988) The impact of infection and disease on animal populations: implications for conservation biology. Conservation Biology, 2, 4056.CrossRefGoogle Scholar
Skerratt, L.F., Berger, L., Hines, H.B., McDonald, K.R., Mendez, D. & Speare, R. (2008) Survey protocol for detecting chytridiomycosis in all Australian frog populations. Ecohealth, 80, 8594.Google ScholarPubMed
Thorne, E. & Williams, E.S. (1988) Disease and endangered species: the black-footed ferret as a recent example. Conservation Biology, 2, 6674.CrossRefGoogle Scholar
Voyles, J., Berger, L., Young, S., Speare, R., Webb, R., Warner, J. et al. . (2007) Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Diseases of Aquatic Organisms, 77, 113118.CrossRefGoogle ScholarPubMed
Whiles, M.R., Lips, K.R., Pringle, C.M., Kilham, S.S., Bixby, R.J., Brenes, R. et al. . (2006) The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Frontiers in Ecology and the Environment, 4, 2734.CrossRefGoogle Scholar
Woodhams, D.C., Alford, R.A. & Marantelli, G. (2003) Emerging disease of amphibians cured by elevated body temperature. Diseases of Aquatic Organisms, 55, 6567.CrossRefGoogle ScholarPubMed
Woodhams, D.C., Ardipradja, K., Alford, R.A., Marantelli, G., Reinert, L.K. & Rollins-Smith, L.A. (2007) Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Animal Conservation, 10, 409417.CrossRefGoogle Scholar