The role of non-declining amphibian species as alternative hosts for Batrachochytrium dendrobatidis in an amphibian community
Michelle P. Stockwell A B , Deborah S. Bower A , John Clulow A and Michael J. Mahony A
+ Author Affiliations
- Author Affiliations
A Conservation Biology Research Group, School of Environmental and Life Sciences, The University of Newcastle, Callaghan Drive, Callaghan, NSW 2308, Australia.
B Corresponding author. Email: Michelle.Stockwell@newcastle.edu.au
Wildlife Research 43(4) 341-347 https://doi.org/10.1071/WR15223
Submitted: 10 December 2015 Accepted: 21 April 2016 Published: 6 July 2016
Abstract
Context: Pathogens with reservoir hosts have been responsible for most disease-induced wildlife extinctions because the decline of susceptible hosts does not cause the decline of the pathogen. The existence of reservoirs for Batrachochytrium dendrobatidis limits population recovery and conservation actions for threatened amphibians. As such, the effect of reservoirs on disease risk within host community assemblages needs to be considered, but rarely is.
Aims: In this study we aimed to determine if amphibian species co-occurring with the green and golden bell frog Litoria aurea, a declining species susceptible to B. dendrobatidis, act as alternate hosts.
Methods: We quantified B. dendrobatidis infection levels, sub-lethal effects on body condition and terminal signs of disease in amphibian communities on Kooragang Island and Sydney Olympic Park in New South Wales, Australia, where two of the largest remaining L. aurea populations persist.
Key results: We found L. aurea carried infections at a similar prevalence (6–38%) to alternate species. Infection loads ranged widely (0.01–11 107.3 zoospore equivalents) and L. aurea differed from only one alternate host species (higher median load in Litoria fallax) at one site. There were no terminal or sub-lethal signs of disease in any species co-occurring with L. aurea.
Conclusion: Our results suggest that co-occurring species are acting as alternate hosts to L. aurea and whether their presence dilutes or amplifies B. dendrobatidis in the community is a priority for future research.
Implications: For L. aurea and many other susceptible species, confirming the existence of reservoir hosts and understanding their role in community disease dynamics will be important for optimising the outcomes of threat mitigation and habitat creation initiatives for their long-term conservation.
Additional keywords: chytridiomycosis, frog, disease, body-condition, infection.
References
Anderson, R. M., and May, R. M. (1986). The invasion, persistence and spread of infectious diseases within animal and plant communities. Philosophical Transactions of the Royal Society of London: Biological Sciences 314, 533–570.| 1:STN:280:DyaL2s7hvVCmug%3D%3D&md5=ea01b61a6c47311ddcbe599eab549a01CAS | 2880354PubMed |
Berger, L., Speare, R., Daszak, P., Green, D. E., Cunningham, A. A., Goggin, C. L., Slocombe, R., Ragan, M. A., Hyatt, A. D., McDonald, K. R., Hines, H. B., Lips, K. R., Marantelli, G., and Parkes, H. (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 United States of America 95, 9031–9036.
| Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFaltbc%3D&md5=440bbe20f7cd3649e9b5f095479f2f5eCAS | 9671799PubMed |
Berger, L., Speare, R., Hines, H., Marantelli, G., Hyatt, A. D., McDonald, K. R., Skerratt, L. F., Olsen, V., Clarke, J. M., Gillespie, G., Mahony, M., Sheppard, N., Williams, C., and Tyler, M. J. (2004). Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Australian Veterinary Journal 82, 434–439.
| Effect of season and temperature on mortality in amphibians due to chytridiomycosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cvkslalsg%3D%3D&md5=ff814dd07b1c52f4209ed89057946924CAS | 15354853PubMed |
Blaustein, A. R., Romansic, J. M., Scheessele, E. A., Han, B. A., Pessier, A. P., and Longcore, J. E. (2005). Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conservation Biology 19, 1460–1468.
| Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis.Crossref | GoogleScholarGoogle Scholar |
Bower, D. S., Pickett, E. J., Stockwell, M. P., Pollard, C. J., Garnham, J. I., Sanders, M. R., Clulow, J., and Mahony, M. J. (2014). Evaluating monitoring methods to guide adaptive management of a threatened amphibian (Litoria aurea). Ecology and Evolution 4, 1361–1368.
| Evaluating monitoring methods to guide adaptive management of a threatened amphibian (Litoria aurea).Crossref | GoogleScholarGoogle Scholar | 24834332PubMed |
Boyle, D. G., Olsen, V., Morgan, J. A. T., and Hyatt, A. D. (2004). Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms 60, 141–148.
| Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVOlsr0%3D&md5=902c75e4b0bed944647ea8e6a2adb9efCAS | 15460858PubMed |
Brannelly, L. A., Hunter, D. A., Lenger, D., Scheele, B. C., Skerratt, L. F., and Berger, L. (2015). Dynamics of Chytridiomycosis during the Breeding Season in an Australian Alpine Amphibian. PLoS One 10, e0143629.
| Dynamics of Chytridiomycosis during the Breeding Season in an Australian Alpine Amphibian.Crossref | GoogleScholarGoogle Scholar | 26629993PubMed |
Christy, M. (1996). The efficacy of using Passive Integrated Transponder (PIT) tags without anaesthetic in free-living frogs. Australian Zoologist 30, 139–142.
| The efficacy of using Passive Integrated Transponder (PIT) tags without anaesthetic in free-living frogs.Crossref | GoogleScholarGoogle Scholar |
Daly, G., Johnson, P., Malolakis, G., Hyatt, A., and Pietsch, R. (2008). Reintroduction of the green and golden bell frog Litoria aurea to Pambula on the south coast of New South Wales. Australian Zoologist 34, 261–270.
Darcovich, K., and O’Meara, J. (2008). An olympic legacy: green and golden bell frog conservation at Sydney Olympic Park. Australian Zoologist 34, 236–248.
| An olympic legacy: green and golden bell frog conservation at Sydney Olympic Park.Crossref | GoogleScholarGoogle Scholar |
Daszak, P. (1999). Extinction by infection. Trends in Ecology and Evolution 14, 279.
| 10370265PubMed |
Daszak, P., Cunningham, A. A., and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443–449.
| Emerging infectious diseases of wildlife – threats to biodiversity and human health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntl2jtw%3D%3D&md5=716f99b16fd6a6d0fd8198fe3c30c296CAS | 10642539PubMed |
Daszak, P., Strieby, A., Cunningham, A. A., Longcore, J. E., Brown, C.C., and Porter, D. (2004). Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. The Herpetological Journal 14, 201–207.
Davidson, E. W., Parris, M. J., Collins, J. P., Longcore, J. E., Pessier, A. P., and Brunner, J. (2003). Pathogenicity and transmission of chytridiomycosis in tiger salamanders (Ambystoma tigrinum). Copeia 2003, 601–607.
| Pathogenicity and transmission of chytridiomycosis in tiger salamanders (Ambystoma tigrinum).Crossref | GoogleScholarGoogle Scholar |
Davidson, C., Benard, M. F., Shaffer, H. B., Parker, J. M., O’Leary, C., Conlon, J. M., and Rollins-Smith, L. A. (2007). Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs. Environmental Science & Technology 41, 1771–1776.
| Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXns1Olsw%3D%3D&md5=2cb5aa8d35eb1b657b682995fc5f53d0CAS |
De Castro, F., and Bolker, B. (2005). Mechanisms of disease‐induced extinction. Ecology Letters 8, 117–126.
DECC (2000). Hygene protocol for the control of disease in frogs. Information Circular No. 6. DECC (Department of Environment and Climate Change, NSW), Sydney.
Fox, J., and Weisberg, S. (2011). An {R} Companion to Applied Regression, Second Edition. (Sage Publishing: Thousand Oaks, CA) Available at http://socserv.socsci.mcmaster.ca/jfox/Books/Companion [1 September 2015]
Garner, T. W., Walker, S., Bosch, J., Leech, S., Marcus Rowcliffe, J., Cunningham, A. A., and Fisher, M. C. (2009). Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118, 783–791.
| Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis.Crossref | GoogleScholarGoogle Scholar |
Germano, J. M., Field, K. J., Griffiths, R. A., Clulow, S., Foster, J., Harding, G., and Swaisgood, R. R. (2015). Mitigation-driven translocations: are we moving wildlife in the right direction? Frontiers in Ecology and the Environment 13, 100–105.
| Mitigation-driven translocations: are we moving wildlife in the right direction?Crossref | GoogleScholarGoogle Scholar |
Hamer, A. J., Lane, S. J., and Mahony, M. J. (2007). Life-history of an endangered amphibian challenges the declining species paradigm. Australian Journal of Zoology 55, 79–88.
| Life-history of an endangered amphibian challenges the declining species paradigm.Crossref | GoogleScholarGoogle Scholar |
Haydon, D. T., Cleaveland, S., Taylor, L. H., and Laurenson, M. K. (2002). Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8, 1468–1473.
| Identifying reservoirs of infection: a conceptual and practical challenge.Crossref | GoogleScholarGoogle Scholar | 12498665PubMed |
Holt, R. A., and Pickering, J. (1985). Infectious disease and species coexistence: a model of Lotka-Volterra form. The American Naturalist 126, 196–211.
Hyatt, A., Boyle, D., Olsen, V., Boyle, D., Berger, L., Obendorf, D., Dalton, A., Kriger, K., Hero, M., and Hines, H. (2007). Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 73, 175–192.
| Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkslWhs7k%3D&md5=0e71d8586c439219147c8aad8b6be609CAS | 17330737PubMed |
Johnson, M. L., Berger, L., Philips, L., and Speare, R. (2003). Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 57, 255–260.
| Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1ShtL8%3D&md5=35a926238bee33e57eacf27b4bb13f04CAS | 14960039PubMed |
Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C. D., Holt, R. D., Hudson, P., Jolles, A., Jones, K. E., and Mitchell, C. E. (2010). Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652.
| Impacts of biodiversity on the emergence and transmission of infectious diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFSku7bE&md5=72fca4d1c68c4de0dec6da7bba6c4cf8CAS | 21124449PubMed |
Kinney, V. C., Heemeyer, J. L., Pessier, A. P., and Lannoo, M. J. (2011). Seasonal pattern of Batrachochytrium dendrobatidis infection and mortality in Lithobates areolatus: affirmation of Vredenburg’s “10,000 Zoospore Rule”. PLoS One 6, e16708.
| Seasonal pattern of Batrachochytrium dendrobatidis infection and mortality in Lithobates areolatus: affirmation of Vredenburg’s “10,000 Zoospore Rule”.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjslKmtbg%3D&md5=dc69f5382a131c709a40e8c951b438b9CAS | 21423745PubMed |
Lesnoff, M., and Lancelot, R. (2012). aod: analysis of overdispersed data. R package version 1.3, available at http://cran.r-project.org/package=aod.
Longcore, J. E., Pessier, A. P., and Nichols, D. K. (1999). Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91, 219–227.
| Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians.Crossref | GoogleScholarGoogle Scholar |
MacPhee, R. D., and Greenwood, A. D. (2013). Infectious disease, endangerment, and extinction. International Journal of Evolutionary Biology 2013, 1–9.
| Infectious disease, endangerment, and extinction.Crossref | GoogleScholarGoogle Scholar |
Mahony, M. (1996). The decline of the green and golden bell frog Litoria aurea viewed in the context of declines and disappearances of other Australian frogs. Australian Zoologist 30, 237–247.
| The decline of the green and golden bell frog Litoria aurea viewed in the context of declines and disappearances of other Australian frogs.Crossref | GoogleScholarGoogle Scholar |
Mahony, M. (1999). Review of the declines and disappearances within the bell frog species group (Litoria aurea species group) in Australia. In ‘Declines and Disappearances of Australian Frogs’. (Ed. A. Campbell.) pp. 81–93. (Environment Australia: Canberra.)
McCallum, H., and Dobson, A. (1995). Detecting disease and parasite threats to endangered species and ecosystems. Trends in Ecology and Evolution 10, 190–194.
| 1:STN:280:DC%2BC3M7itFahtw%3D%3D&md5=556a130e511043356a621e1382f70102CAS | 21237000PubMed |
McFadden, M., Duffy, S., Harlow, P., Hobcroft, D., Webb, C., and Ward-Fear, G. (2008). A review of the green and golden bell frog Litoria aurea breeding program at Taronga Zoo. Australian Zoologist 34, 291–296.
| A review of the green and golden bell frog Litoria aurea breeding program at Taronga Zoo.Crossref | GoogleScholarGoogle Scholar |
Miller, E., and Huppert, A. (2013). The effects of host diversity on vector-borne disease: the conditions under which diversity will amplify or dilute the disease risk. PLoS One 8, e80279.
| The effects of host diversity on vector-borne disease: the conditions under which diversity will amplify or dilute the disease risk.Crossref | GoogleScholarGoogle Scholar | 24303003PubMed |
Parker, J. M., Mikaelian, I., Hahn, N., and Diggs, H. E. (2002). Clinical diagnosis and treatment of epidermal chytridiomycosis in African clawed frogs (Xenopus tropicalis). Comparative Medicine 52, 265–268.
| 1:CAS:528:DC%2BD38XltVGmu7c%3D&md5=3e41fbfa95e5cdb538dbac833ef03683CAS | 12102573PubMed |
Pickett, E. J., Stockwell, M. P., Bower, D. S., Garnham, J. I., Pollard, C. J., Clulow, J., and Mahony, M. J. (2013). Achieving no net loss in habitat offset of a threatened frog required high offset ratio and intensive monitoring. Biological Conservation 157, 156–162.
| Achieving no net loss in habitat offset of a threatened frog required high offset ratio and intensive monitoring.Crossref | GoogleScholarGoogle Scholar |
Piotrowski, J. S., Annis, S. L., and Longcore, J. E. (2004). Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96, 9–15.
| Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians.Crossref | GoogleScholarGoogle Scholar | 21148822PubMed |
R Core Team. (2010). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
Retallick, R. W., and Miera, V. (2007). Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sub-lethal effects of infection. Diseases of Aquatic Organisms 75, 201–207.
| Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sub-lethal effects of infection.Crossref | GoogleScholarGoogle Scholar | 17629114PubMed |
Richards-Zawacki, C. L. (2010). Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. Proceedings of the Royal Society of London. Series B, Biological Sciences 277, 519–528.
| Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs.Crossref | GoogleScholarGoogle Scholar |
Sapsford, S. J., Roznik, E. A., Alford, R. A., and Schwarzkopf, L. (2014). Visible implant elastomer marking does not affect short-term movements or survival rates of the treefrog Litoria rheocola. Herpetologica 70, 23–33.
| Visible implant elastomer marking does not affect short-term movements or survival rates of the treefrog Litoria rheocola.Crossref | GoogleScholarGoogle Scholar |
Schmidt, K. A., and Ostfeld, R. S. (2001). Biodiversity and the dilution effect in disease ecology. Ecology 82, 609–619.
| Biodiversity and the dilution effect in disease ecology.Crossref | GoogleScholarGoogle Scholar |
Schmidt, K., and Schwarzkopf, L. (2010). Visible implant elastomer tagging and toe-clipping: effects of marking on locomotor performance of frogs and skinks. The Herpetological Journal 20, 99–105.
Skerratt, L. F., Berger, L., Speare, R., Cashins, S., McDonald, K. R., Phillott, A. D., Hines, H. B., and Kenyon, N. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125–134.
| Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs.Crossref | GoogleScholarGoogle Scholar |
Smith, K., Acevedo‐Whitehouse, K., and Pedersen, A. (2009). The role of infectious diseases in biological conservation. Animal Conservation 12, 1–12.
| The role of infectious diseases in biological conservation.Crossref | GoogleScholarGoogle Scholar |
Stockwell, M. P., Clulow, S., Clulow, J., and Mahony, M. (2008). The impact of the amphibian chytrid fungus Batrachochytrium dendrobatidis on a green and golden bell frog Litoria aurea reintroduction program at the Hunter Wetlands Centre Australia in the Hunter Region of NSW. Australian Zoologist 34, 379–386.
| The impact of the amphibian chytrid fungus Batrachochytrium dendrobatidis on a green and golden bell frog Litoria aurea reintroduction program at the Hunter Wetlands Centre Australia in the Hunter Region of NSW.Crossref | GoogleScholarGoogle Scholar |
Stockwell, M. P., Clulow, J., and Mahony, M. J. (2010). Host species determines whether infection load increases beyond disease-causing thresholds following exposure to the amphibian chytrid fungus. Animal Conservation 13, –71.
| Host species determines whether infection load increases beyond disease-causing thresholds following exposure to the amphibian chytrid fungus.Crossref | GoogleScholarGoogle Scholar |
Stockwell, M. P., Clulow, J., and Mahony, M. J. (2012). Sodium chloride inhibits the growth and infective capacity of the amphibian chytrid fungus and increases host survival rates. PLoS One 7, e36942.
| Sodium chloride inhibits the growth and infective capacity of the amphibian chytrid fungus and increases host survival rates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xns1GhtLg%3D&md5=b0dea0770f5af638869c38a1a01267b9CAS | 22590639PubMed |
Stockwell, M. P., Clulow, J., and Mahony, M. J. (2015). Evidence of a salt refuge: chytrid infection loads are suppressed in hosts exposed to salt. Oecologia 177, 901–910.
| Evidence of a salt refuge: chytrid infection loads are suppressed in hosts exposed to salt.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MzgtFansg%3D%3D&md5=d8694faf525eb4de2cc9a8c1a3fb73d5CAS | 25416999PubMed |
Voyles, J., Young, S., Berger, L., Campbell, C., Voyles, W. F., Dinudom, A., Cook, D., Webb, R., Alford, R. A., and Skerratt, L. F. (2009). Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326, 582–585.
| Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1ymsrbP&md5=78497021a16c16006f08302350e85944CAS | 19900897PubMed |
Vredenburg, V. T., Knapp, R. A., Tunstall, T. S., and Briggs, C. J. (2010). Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences of the United States of America 107, 9689–9694.
| Dynamics of an emerging disease drive large-scale amphibian population extinctions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntFGqsb8%3D&md5=d118785d7b8f55cb38f546d9862a2f0aCAS | 20457913PubMed |
Weldon, C., du Preez, L. H., Hyatt, A. D., Muller, R., and Speare, R. (2004). Origin of the amphibian chytrid fungus. Emerging Infectious Diseases 10, 2100–2105.
| Origin of the amphibian chytrid fungus.Crossref | GoogleScholarGoogle Scholar | 15663845PubMed |
White, A., and Pyke, G. H. (2008). Frogs on the hop: translocations of green and golden bell frogs Litoria aurea in greater Sydney. Australian Zoologist 34, 249–260.
| Frogs on the hop: translocations of green and golden bell frogs Litoria aurea in greater Sydney.Crossref | GoogleScholarGoogle Scholar |
Woodhams, D. C., and Alford, R. A. (2005). Ecology of chytridiomycosis in rainforest stream frog assemblages of tropical Queensland. Conservation Biology 19, 1449–1459.
| Ecology of chytridiomycosis in rainforest stream frog assemblages of tropical Queensland.Crossref | GoogleScholarGoogle Scholar |
Woodhams, D., Ardipradja, K., Alford, R., Marantelli, G., Reinert, L., and Rollins‐Smith, L. (2007a). Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Animal Conservation 10, 409–417.
| Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses.Crossref | GoogleScholarGoogle Scholar |
Woodhams, D. C., Ardipraja, K., Alford, R. A., Marantelli, G., Reinert, L. K., and Rollins-Smith, L. A. (2007b). Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Animal Conservation 10, 409–417.
| Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses.Crossref | GoogleScholarGoogle Scholar |
