Assessing host response to disease treatment: how chytrid-susceptible frogs react to increased water salinity
Kaya L. Klop-Toker A B , Jose W. Valdez A , Michelle P. Stockwell A , Matthew E. Edgar A , Loren Fardell A , Simon Clulow A , John Clulow A and Michael J. Mahony A
+ Author Affiliations
- Author Affiliations
A Conservation Biology Research Group, School of Environmental and Life Science, Biology Building, University of Newcastle, Callaghan 2308, NSW, Australia.
B Corresponding author. Email: kaya.klop-toker@uon.edu.au
Wildlife Research 44(8) 648-659 https://doi.org/10.1071/WR16145
Submitted: 1 August 2016 Accepted: 26 August 2017 Published: 26 February 2018
Abstract
Context: The severity and prevalence of the amphibian fungal pathogen, Batrachochytrium dendrobatidis (Bd) is correlated with several environmental variables, including salinity, temperature, and moisture content, which influence the pathogen’s growth and survival. Habitats that contain these environmental variables at levels outside of those optimal for Bd growth and survival may facilitate the survival of susceptible host species. Therefore, manipulation of environmental salinity is a potential management strategy to help conserve Bd-susceptible species. However, host behaviour also influences disease dynamics, and the success of habitat manipulation programs depends on how hosts use this altered habitat.
Aims: To assess if the Bd-susceptible green and golden bell frog, Litoria aurea, will select waterbodies with a salinity increased to S = 3; if this selection is affected by infection; and if a frog’s time in a waterbody of this salinity affects infection load or blood physiology.
Methods: We conducted a filmed choice experiment and a 3-year field study where infected and uninfected frogs could choose between fresh or saline waterbodies.
Key results: In both the laboratory experiment and field study, Bd-infected L. aurea spent a significantly greater amount of time in or closer to a waterbody than uninfected frogs. Experimentally infected frogs tended to prefer the saline water over fresh, but their choice of water usage did not differ statistically from uninfected frogs. In the field, frogs began to avoid ponds when salinities rose above S = 5.
Conclusions: Because both wild and captive, and infected and uninfected L. aurea readily selected waterbodies with a salinity of S = 3, this salinity could potentially be used as a passive method for reducing the severity of Bd when managing this species. However, further testing is needed to understand the efficacy of this treatment, and care must be taken to prevent salinities rising above S = 5, because this level seems to produce an avoidance response and therefore may not be suitable in every location.
Implications: Manipulation of aquatic habitats may be a worthwhile focus for Bd management in habitats where water level fluctuations are minimal.
Additional keywords: Batrachochytrium dendrobatidis, behaviour, chytridiomycosis, disease management, facilitation, habitat modification.
References
Becker, C. G., and Zamudio, K. R. (2011). Tropical amphibian populations experience higher disease risk in natural habitats. Proceedings of the National Academy of Sciences of the United States of America 108, 9893–9898.| Tropical amphibian populations experience higher disease risk in natural habitats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvVynu7Y%3D&md5=f21c100ad0f2d9e24797024c0fa7f6daCAS |
Berger, L., Speare, R., Daszak, P., Green, D. E., Cunningham, A. A., Goggin, C. L., Slocombe, R., Ragan, M. A., Hyatt, A. D., and McDonald, K. R. (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=36c7095df6e32c1989c1092202004ad3CAS |
Berger, L., Speare, R., Hines, H., Marantelli, G., Hyatt, A., McDonald, K., Skerratt, L., Olsen, V., Clarke, J., and Gillespie, G. (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=9141fdb3ade296c0f4c5db7b0a578ccdCAS |
Beyer, S. E., Phillips, C. A., and Schooley, R. L. (2015). Canopy cover and drought influence the landscape epidemiology of an amphibian chytrid fungus. Ecosphere 6, 78.
| Canopy cover and drought influence the landscape epidemiology of an amphibian chytrid fungus.Crossref | GoogleScholarGoogle Scholar |
Bosch, J., Sanchez-Tomé, E., Fernández-Loras, A., Oliver, J. A., Fisher, M. C., and Garner, T. W. (2015). Successful elimination of a lethal wildlife infectious disease in nature. Biology Letters 11, 20150874.
| Successful elimination of a lethal wildlife infectious disease in nature.Crossref | GoogleScholarGoogle Scholar |
Bower, D. S., Stockwell, M. P., Pollard, C. J., Pickett, E. J., Garnham, J. I., Clulow, J., and Mahony, M. J. (2013). Life stage specific variation in the occupancy of ponds by Litoira aurea, a threatened amphibian. Austral Ecology 38, 543–547.
| Life stage specific variation in the occupancy of ponds by Litoira aurea, a threatened amphibian.Crossref | GoogleScholarGoogle Scholar |
Bower, D. S., Pickett, E. J., Garnham, J. I., Deboo, M. L., McCurry, M. R., Mengerink, R. M., Mahony, M. J., and Clulow, J. (2014). Diet of a threatened pond frog differs over a small spatial scale. Endangered Species Research 23, 93–98.
| Diet of a threatened pond frog differs over a small spatial scale.Crossref | GoogleScholarGoogle Scholar |
Boyle, D. G., Boyle, D. B., 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.
| 1:CAS:528:DC%2BD2cXptVOlsr0%3D&md5=5dc844bd2ffb21924c22010c900e1a39CAS |
Bramwell, R. (2011). Do salinity and pH help protect natterjack toads from chytridiomycosis, a disease caused by the amphibian fungus Batrachochytrium dendrobatidis (Bd). Masters thesis, Imperial College London.
Brannelly, L. A., Richards-Zawacki, C. L., and Pessier, A. P. (2012). Clinical trials with itraconazole as a treatment for chytrid fungal infections in amphibians. Diseases of Aquatic Organisms 101, 95–104.
| Clinical trials with itraconazole as a treatment for chytrid fungal infections in amphibians.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtV2nur8%3D&md5=84fc2b8e7c8b67520564e36a53f5524fCAS |
Briggs, C. J., Knapp, R. A., and Vredenburg, V. T. (2010). Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences of the United States of America 107, 9695–9700.
| Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntFGqsbw%3D&md5=52009296e4690cd2966194ecfb86fe51CAS |
Caldwell, J. P. (1997). Pair bonding in spotted poison frogs. Nature 385, 211.
| Pair bonding in spotted poison frogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXls1KntQ%3D%3D&md5=fa86a4746ee65a8839af15e9e1071e88CAS |
Campbell, C. R., Voyles, J., Cook, D. I., and Dinudom, A. (2012). Frog skin epithelium: electrolyte transport and chytridiomycosis. The International Journal of Biochemistry & Cell Biology 44, 431–434.
| Frog skin epithelium: electrolyte transport and chytridiomycosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtV2ks7k%3D&md5=eb80c38249191e78a83351959c8636d0CAS |
Carey, C., Bruzgul, J. E., Livo, L. J., Walling, M. L., Kuehl, K. A., Dixon, B. F., Pessier, A. P., Alford, R. A., and Rogers, K. B. (2006). Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3, 5–21.
| Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis).Crossref | GoogleScholarGoogle Scholar |
Chatfield, M. W., and Richards-Zawacki, C. L. (2011). Elevated temperature as a treatment for Batrachochytrium dendrobatidis infection in captive frogs. Diseases of Aquatic Organisms 94, 235–238.
| Elevated temperature as a treatment for Batrachochytrium dendrobatidis infection in captive frogs.Crossref | GoogleScholarGoogle Scholar |
Christy, M. T., and Dickman, C. R. (2002). Effects of salinity on tadpoles of the green and golden bell frog (Litoria aurea). Amphibia-Reptilia 23, 1–11.
| Effects of salinity on tadpoles of the green and golden bell frog (Litoria aurea).Crossref | GoogleScholarGoogle Scholar |
Feder, M. E., and Burggren, W. W. (1992). ‘Environmental Physiology of the Amphibians.’ (Chicago University Press: Chicago).
Fisher, M. C., Garner, T. W. J., and Walker, S. F. (2009). Global emergence of Batrachocytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annual Review of Microbiology 63, 291–310.
| Global emergence of Batrachocytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlSitLjM&md5=32289a2c473d0e08d37d5bcac07a3693CAS |
Forrest, M. J., and Schlaepfer, M. A. (2011). Nothing a hot bath won’t cure: infection rates of amphibian chytrid fungus correlate negatively with water temperature under natural field settings. PLoS One 6, e28444.
| Nothing a hot bath won’t cure: infection rates of amphibian chytrid fungus correlate negatively with water temperature under natural field settings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksFCgsw%3D%3D&md5=e6aec7f1530047ec20e260d47652e5c8CAS |
Hamer, A. J., and Mahony, M. J. (2010). Rapid turnover in site occupancy of a pond-breeding frog demonstrates the need for landscape-level management. Wetlands 30, 287–299.
| Rapid turnover in site occupancy of a pond-breeding frog demonstrates the need for landscape-level management.Crossref | GoogleScholarGoogle Scholar |
Hamer, A. J., Lane, S., and Mahony, M. J. (2002). Management of freshwater wetlands for the endangered green and golden bell frog (Litoria aurea): roles of habitat determinants and space. Biological Conservation 106, 413–424.
| Management of freshwater wetlands for the endangered green and golden bell frog (Litoria aurea): roles of habitat determinants and space.Crossref | GoogleScholarGoogle Scholar |
Heard, G. W., Scroggie, M. P., Clemann, N., and Ramsey, D. S. (2014). Wetland characteristics influence disease risk for a threatened amphibian. Ecological Applications 24, 650–662.
| Wetland characteristics influence disease risk for a threatened amphibian.Crossref | GoogleScholarGoogle Scholar |
Jakob, E. M., Marshall, S. D., and Uetz, G. W. (1996). Estimating fitness: a comparison of body condition indices. Oikos 77, 61–67.
| Estimating fitness: a comparison of body condition indices.Crossref | GoogleScholarGoogle Scholar |
James, M. S., Stockwell, M. P., Clulow, J., Clulow, S., and Mahony, M. J. (2015). Investigating behaviour for conservation goals: conspecific call playback can be used to alter amphibian distributions within ponds. Biological Conservation 192, 287–293.
| Investigating behaviour for conservation goals: conspecific call playback can be used to alter amphibian distributions within ponds.Crossref | GoogleScholarGoogle Scholar |
Johnson, M. L., and Speare, R. (2003). Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infectious Diseases 9, 922–925.
| Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications.Crossref | GoogleScholarGoogle Scholar |
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=d45a5ee0b0b2ff4555d3a1433a13f1deCAS |
Kearney, B. D., Byrne, P. G., and Reina, R. D. (2012). Larval tolerance to salinity in three species of Australian anuran: an indication of saline specialisation in Litoria aurea. PLoS One 7, e43427.
| Larval tolerance to salinity in three species of Australian anuran: an indication of saline specialisation in Litoria aurea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Ggu7fN&md5=9095241da2abf6e09e4cd39278412a85CAS |
Kindermann, C., Narayan, E. J., and Hero, J.-M. (2012). Urinary corticosterone metabolites and chytridiomycosis disease prevalence in a free-living population of male Stony Creek frogs (Litoria wilcoxii). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 162, 171–176.
| Urinary corticosterone metabolites and chytridiomycosis disease prevalence in a free-living population of male Stony Creek frogs (Litoria wilcoxii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsFOnsbg%3D&md5=4069fef8f870b711369eba777399f368CAS |
Kriger, K. M., and Hero, J. M. (2007). Large‐scale seasonal variation in the prevalence and severity of chytridiomycosis. Journal of Zoology 271, 352–359.
Licht, L. E. (1986). Comparative escape behavior of sympatric Rana aurora and Rana pretiosa. American Midland Naturalist 115, 239–247.
| Comparative escape behavior of sympatric Rana aurora and Rana pretiosa.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.)
Mahony, M. J., Hamer, A. J., Pickett, E. J., McKenzie, D. J., Stockwell, M. P., Garnham, J. I., Keely, C. C., Deboo, M. L., O’Meara, J., and Pollard, C. J. (2013). Identifying conservation and research priorities in the face of uncertainty: a review of the threatened bell frog complex in eastern Australia. Herpetological Conservation and Biology 8, 519–538.
Murray, K. A., Retallick, R. W., Puschendorf, R., Skerratt, L. F., Rosauer, D., McCallum, H. I., Berger, L., Speare, R., and VanDerWal, J. (2011). Assessing spatial patterns of disease risk to biodiversity: implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis. Journal of Applied Ecology 48, 163–173.
| Assessing spatial patterns of disease risk to biodiversity: implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis.Crossref | GoogleScholarGoogle Scholar |
Peterson, J. D., Steffen, J. E., Reinert, L. K., Cobine, P. A., Appel, A., Rollins-Smith, L., and Mendonça, M. T. (2013). Host stress response is important for the pathogenesis of the deadly amphibian disease, chytridiomycosis, in Litoria caerulea. PLoS One 8, e62146.
| Host stress response is important for the pathogenesis of the deadly amphibian disease, chytridiomycosis, in Litoria caerulea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntVWgs7w%3D&md5=7316507ebe25ce0417cd98bbe762469fCAS |
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 |
Puschendorf, R., Hoskin, C. J., Cashins, S. D., McDonald, K., Skerratt, L. F., Vanderwal, J., and Alford, R. A. (2011). Environmental refuge from disease‐driven amphibian extinction. Conservation Biology 25, 956–964.
| Environmental refuge from disease‐driven amphibian extinction.Crossref | GoogleScholarGoogle Scholar |
Pyke, G., and White, A. (2001). A review of the biology of the green and golden bell frog Litoria aurea. Australian Zoologist 31, 563–598.
| A review of the biology of the green and golden bell frog Litoria aurea.Crossref | GoogleScholarGoogle Scholar |
Rowley, J. J., and Alford, R. A. (2007). Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis. Diseases of Aquatic Organisms 77, 1–9.
| Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis.Crossref | GoogleScholarGoogle Scholar |
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 |
Spieler, M., and Linsenmair, K. E. (1998). Migration patterns and diurnal use of shelter in a ranid frog of a West African savannah: a telemetric study. Amphibia-Reptilia 19, 43–64.
| Migration patterns and diurnal use of shelter in a ranid frog of a West African savannah: a telemetric study.Crossref | GoogleScholarGoogle Scholar |
Stockwell, M., 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., Clulow, J., and Mahony, M. (2010). Host species determines whether infection load increases beyond disease‐causing thresholds following exposure to the amphibian chytrid fungus. Animal Conservation 13, 62–71.
| 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=81819eaa39f04b129fce1ae8ddde735aCAS |
Stockwell, M., Clulow, J., and Mahony, M. (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=7d0101e9c794070cbcea96ebb5bce3caCAS |
Stockwell, M., Garnham, J., Bower, D., Clulow, J., and Mahony, M. (2016). Low disease-causing threshold in a frog species susceptible to chytridiomycosis. FEMS Microbiology Letters 363, fnw111.
| Low disease-causing threshold in a frog species susceptible to chytridiomycosis.Crossref | GoogleScholarGoogle Scholar |
Threlfall, C., Jolley, D., Evershed, N., Goldingay, R., and Buttemer, W. (2008). Do green and golden bell frogs Litoria aurea occupy habitats with fungicidal properties? Australian Zoologist 34, 350–360.
| Do green and golden bell frogs Litoria aurea occupy habitats with fungicidal properties?Crossref | GoogleScholarGoogle Scholar |
Tyler, M. J. (1979). The impact of European man upon Australasian amphibians. In ‘The Status of Endangered Australasian Wildlife’. (Ed. M. J. Tyler.) pp. 177–184. (Royal Zoological Society of South Australia: Adelaide.)
Uchiyama, M., and Konno, N. (2006). Hormonal regulation of ion and water transport in anuran amphibians. General and Comparative Endocrinology 147, 54–61.
| Hormonal regulation of ion and water transport in anuran amphibians.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVOit7g%3D&md5=1bfdffca7c3ec55f7f1080acd55b4a13CAS |
Voyles, J., Berger, L., Young, S., Speare, R., Webb, R., Warner, J., Rudd, D., Campbell, R., and Skerratt, L. F. (2007). Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Diseases of Aquatic Organisms 77, 113–118.
| Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yiu7rP&md5=b7e5478d882c4a5ecaaf4eca2b3de4ecCAS |
White, A., and Pyke, G. (1996). Distribution and conservation status of the green and golden bell frog Litoria aurea in New South Wales. Australian Zoologist 30, 177–189.
| Distribution and conservation status of the green and golden bell frog Litoria aurea in New South Wales.Crossref | GoogleScholarGoogle Scholar |
White, A., and Pyke, G. (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., Alford, R. A., and Marantelli, G. (2003). Emerging disease of amphibians cured by elevated body temperature. Diseases of Aquatic Organisms 55, 65–67.
| Emerging disease of amphibians cured by elevated body temperature.Crossref | GoogleScholarGoogle Scholar |
Woodhams, D. C., Bosch, J., Briggs, C. J., Cashins, S., Davis, L. R., Lauer, A., Muths, E., Puschendorf, R., Schmidt, B. R., and Sheafor, B. (2011). Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Frontiers in Zoology 8, 8.
| Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis.Crossref | GoogleScholarGoogle Scholar |
