Amphibian abnormalities and threats in pristine ecosystems in Sri Lanka

Main Article Content

G.K.V.P.T. Silva
W.A.D. Mahaulpatha
Anslem de Silva

Abstract

Amphibian abnormalities are caused by numerous etiologies prevailing in the environment.  Since amphibians are good bio indicators of the environment, amphibian abnormalities are popularly known as a veritable ecological screening tool to assess ecosystem health.  The present study was carried out encompassing within and outside the Horton Plains National Park areas, from January to November 2017.  Distribution of amphibian morphological abnormalities were assessed in and around the five lentic water bodies through gross visual encounter.  Six quadrates of 1m×2m were randomly placed in each sampling site.  Frequency and composition of amphibian abnormalities were assessed in a total of 694 amphibians, belonging to four families and 11 species.  Thereby, 4.5% and 80.87% abnormality indexes were accounted for respectively within and outside the park, comprehended surficial abnormalities, ectromelia and femoral projection abnormality types.  Surficial abnormalities were the most predominant in both localities, generally occurring at the hind limb region of pre-mature stages of Taruga eques.  Two lentic water bodies were identified as “abnormality hotspots†within and outside the Horton Plains National park; however, a multiplicity of possible combinations of potential causes of abnormalities were present in the environment.  Hence, finding the exact causes of amphibian abnormalities are an extremely difficult exercise in the field.  

Article Details

Section
Communications
Author Biographies

W.A.D. Mahaulpatha, Department of Zoology, Faculty of Applied Sciences, University of Sri Jayewardenepura Gangodawila, Nugegoda, Sri Lanka.

As a researcher and a professor in zoology in University of Sri Jayewardenepura, Prof. W.A.D Mahaulpatha has executed many researches in wildlife conservation and management including ornithology, herpetology and mammalogy and have more than hundred publications. As result of that she was got the Presidential award involuntarily in 2018.

Anslem de Silva, 315/1, Dolosbage Road, Gampola (Central Province), Sri Lanka.

Anslem de Silva, MSc. DSc. has contributed approximately 425 papers. This include app 50 books, the latest "Naturalist Guide to Reptiles of Sri Lanka' published in UK, 2017. Anslem received Presidents award for Scientific Publications four times. He is the current Regional Chairman of the Crocodile Specialist Group IUCN for South Asia and Iran.

References

Ankley, G.T., S.J. Degitz, S.A. Diamond & J.E. Tietge (2004). Assessment of environmental stressors potentially responsible for malformations in North American anuran amphibians. Ecotoxicology and Environmental Safety 58(1): 7–16. https://doi.org/10.1016/j.ecoenv.2004.01.004.

Ballengee, B. & S.K. Sessions (2009). Explanation for missing limbs in deformed amphibians. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 312(7): 770–779. https://doi.org/10.1002/jez.b.21296.

Blaustein, A.R. & P.T. Johnson (2003). The complexity of deformed amphibians. Frontiers in Ecology and the Environment 1(2): 87–94. https://doi.org/10.1890/1540-9295(2003)001[0087:TCODA]2.0.CO;2

Bowerman, J., P.T. Johnson & Bowerman (2010). Sublethal predators and their injured prey: linking aquatic predators and severe limb abnormalities in amphibians. Ecology 91(1): 242–251. https://doi.org/10.1890/08-1687.1

Bridges, C., E. Little, D. Gardiner, J. Petty & J. Huckins (2004). Assessing the toxicity and teratogenicity of pond water in North Central Minnesota to amphibians. Environmental Science and Pollution Research 11(4): 233–239. https://doi.org/10.1007/BF02979631

Budischak, S.A., L.K. Belden & W.A. Hopkins (2009). Relative toxicity of malathion to trematode-infected and noninfected Rana palustris tadpoles. Archives of Environmental Contamination and Toxicology 56(1): 123–128. https://doi.org/10.1007/s00244-008-9167-9

Burkhart, J.G., J.C. Helgen, D.J. Fort, K. Gallagher, D. Bowers, T.L. Propst, M. Gernes, J. Magner, M.D. Shelby & G. Lucier (1998). Induction of mortality and malformation in Xenopus laevis embryos by water sources associated with field frog deformities. Environmental Health Perspectives 106(12): 841. https://dx.doi.org/10.1289%2Fehp.106-1533234

Chandrajith, R., N. Koralegedara, K.B. Ranawana, H.J. Tobschall & C.B. Dissanayake (2009). Major and trace elements in plants and soils in Horton Plains National Park, Sri Lanka: an approach to explain forest die back. Environmental Geology 57(1): 17–28. https://doi.org/10.1007/s00254-008-1278-0

Curtis, S. (2011). Water Bugs and Water Scorpions (Fact sheet). South Brisbane: Queensland Museum, 487pp.

de Silva, A. (2007). Amphibians of Sri Lanka: A Photographic Guide to Common Frogs, Toads and Caecilians. Kandy: Privately published.

de Silva, A. (2009). The incidence and pattern of malformations, abnormalities, injuries, and parasitic infection of amphibians in Sri Lanka (preliminary findings). Final Report: Amphibian Specialists Group, Seed Grant, 40.

de Silva, A. (2011). Some observations of malformation, eye disease, parasitic and viral infection and the effects of agrochemicals on amphibians in Sri Lanka. FrogLog, 24pp.

Dodd, C.K. (2010). Amphibian Ecology and Conservation: A Handbook of Techniques. Oxford University Press, New York, 584pp.

Dutta, S.K. & K. Manamendra-Arachchi (1996). The Amphibian Fauna of Sri Lanka. Colombo: Wildlife Heritage Trust of Sri Lanka, 230pp.

DWC (2007). Biodiversity Baseline Survey: Horton Plains National Park. Consultancy Services Report prepared by Green, M.J.B. (ed.), De Alwis, S.M.D.A.U., Dayawansa, P.N., How, R., Singhakumara, B.M.P., Weerakoon, D. and Wijesinghe, M.R. ARD Inc in association with Infotech IDEAS and GREENTECH Consultants. Sri Lanka Protected Areas Management and Wildlife Conservation Project (PAM &WCP/CONSULT/02/BDBS), Department of Wildlife Conservation, Ministry of Environment and Natural Resources, Colombo, 40pp.

Faruk, A., D. Belabut, N. Ahmad, R.J. Knell & T.W. Garner (2013). Effects of oilâ€palm plantations on diversity of tropical anurans. Conservation Biology 27(3): 615–624.

Gillilland, M.G. & P.M. Muzzall (1999). Helminths infecting froglets of the Northern Leopard Frog (Rana pipiens) from Foggy Bottom marsh, Michigan. Journal Helminthological Society Washington 66(12): 73–77. https://doi.org/10.1111/cobi.12062

Gillilland, M.G. & P.M. Muzzall (2002). Amphibians, trematodes, and deformities: an overview from southern Michigan. Comparative Parasitology 69(1): 81–85. https://doi.org/10.1654/1525-2647(2002)069[0081:ATADAO]2.0.CO;2

Goodman, B.A. & P.T. Johnson (2011). Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan. Plos One 6(5): 201–293. https://doi.org/10.1371/journal.pone.0020193

Green, M.J.B. (1990) (Comp.). IUCN Directory of South Asian Protected Areas. IUCN, Gland, Switzerland and Cambridge, U.K., xxiv+294pp.

Gunatilleke, I.A.U.N. & C.V.S. Gunatilleke (1990). Distribution of floristic richness and its conservation in Sri Lanka. Conservation Biology 21–31. https://doi.org/10.1111/j.1523-1739.1990.tb00262.x

Hamer, A.J., S.J. Lane & M.J. Mahony (2002). Management of freshwater wetlands for the endangered green and golden bell frog (Litoria aurea): roles of habitat determinants and space. Biological Conservation 106(3): 413–424. https://doi.org/10.1016/S0006-3207(02)00040-X

Harrison, J. (2011). A Field Guide to the Birds of Sri Lanka. Oxford University Press, Oxford, 219pp.

Imasuen, A.A., H.J. Ozemoka & M.S. Aisien (2012). Anurans as intermediate and paratenic hosts of helminth infections in the rainforest and derived savanna biotopes of southern Nigeria. International Journal of Zoology 5(3): 1­–7. https://doi.org/10.1155/2012/823970

Jayawardena, U.A., R.S. Rajakaruna, A.N. Navaratne & P.H. Amerasinghe (2010a). Toxicity of agrochemicals to common hourglass tree frog (Polypedates cruciger) in acute and chronic exposure. International Journal of Agriculture and Biology 12(5): 641–648.

Jayawardena, U.A., R.S. Rajakaruna, A.N. Navaratne & P.H. Amerasinghe (2010b). Monostome cercariae induced malformations in amphibians: effect of infection at the prelimb-bud stage tadpoles of Polypedates cruciger blyth. Journal of the National Science Foundation of Sri Lanka 38(4): 241–248. http://doi.org/10.4038/jnsfsr.v38i4.2651

Johnson, P.T. & J. Bowerman (2010). Do predators cause frog deformities? The need for an ecoâ€epidemiological approach. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 314(7): 515–518. https://doi.org/10.1002/jez.b.21369

Johnson, P.T. & J.M. Chase (2004). Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7(7): 521–526. https://doi.org/10.1111/j.1461-0248.2004.00610.x

Johnson, P.T. & R.B. Hartson (2009). All hosts are not equal: explaining differential patterns of malformations in an amphibian community. Journal of Animal Ecology 78(1): 191–201. https://doi.org/10.1111/j.1365-2656.2008.01455.x

Johnson, P.T., K.B. Lunde, R.W. Haight, J. Bowerman & A.R. Blaustein (2001a). Ribeiroia ondatrae (Trematoda: Digenea) infection induces severe limb malformations in Western toads (Bufo boreas). Canadian Journal of Zoology 79(3): 370–379. https://doi.org/10.1139/cjz-79-3-370

Johnson, P.T., K.B. Lunde, E.G. Ritchie, J.K. Reaser & A.E. Launer (2001b). Morphological abnormality patterns in a California amphibian community. Herpetologica 57(3): 336–352. https://doi.org/ 291822102

Johnson, P.T., K.B. Lunde, E.M. Thurman, E.G. Ritchie, S.N. Wray, D.R. Sutherland, J.M. Kapfer, T.J. Frest, J. Bowerman & A.R. Blaustein (2002). Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the Western United States. Ecological Monographs 72(2): 151–168. https://doi.org/10.1890/0012-9615(2002)072[0151: PROILT]2.0.CO;2

Johnson, P.T., E.R. Preu, D.R. Sutherland, J.M. Romansic, B. Han & A.R. Blaustein (2006). Adding infection to injury: synergistic effects of predation and parasitism on amphibian malformations. Ecology 87(9): 2227–2235. https://doi.org/10.1890/0012-9658(2006)87[2227:AITISE]2.0.CO;2

Johnson, P.T., D.R. Sutherland, J.M. Kinsella & K.B. Lunde (2004). Review of the trematode genus Ribeiroia (Psilostomidae): Ecology, life history and pathogenesis with special emphasis on the amphibian malformation problem. Advances in Parasitology 57(5): 191–253. https://doi.org/10.1016/S0065-308X (04)57003-3

Kiesecker, J.M., L.K. Belden, K. Shea & M.J. Rubbo (2004). Amphibian decline and emerging disease: What can sick frogs teach us about new and resurgent diseases in human populations and other species of wildlife? American Scientist 92(2): 138–147.

Lajmanovich, R.C., M.T. Sandoval & P.M. Peltzer (2003). Induction of mortality and malformation in Scinax nasicus tadpoles exposed to glyphosate formulations. Bulletin of Environmental Contamination and Toxicology 70(3): 612–618. https://doi.org/10.1007/s00128-003-0029-x

Lannoo, M. (2008). Malformed Frogs: The Collapse of Aquatic Ecosystems. University of California Press, Berkeley, 288pp.

Linder, G. (2003). Multiple stressor effects in relation to declining amphibian populations. West Consohocken: American Society for Testing & Materials International, https://doi.org/10.1520/STP1443-EB

Lunde, K.B. & P.T. Johnson (2012). A practical guide for the study of malformed amphibians and their causes. Journal of Herpetology 46(4): 429–441. https://doi.org/10.2307/23327156

Manamendra-Arachchi, K. & R. Pethiyagoda (2006). Sri Lankawe Ubhayajeevin. WHT Publications (Pvt) Ltd, Colombo.

McCallum, M.L., W.E. Moser, B.A. Wheeler & S.E. Trauth (2011). Amphibian infestation and host size preference by the leech Placobdella picta (Verrill, 1872) (Hirudinida: Rhynchobdellida: Glossiphoniidae) from the Eastern Ozarks, USA. Herpetology Notes 4(6): 147–151. https://doi.org/10.1107/2415134

Meegaskumbura, M., G. Bowatte, K. Manamendra-Arachchi & S. Meegaskumbura (2011). Amphibian research in Sri Lanka. FrogLog 4(2): 26.

Meteyer, C.U. (2000). Field Muide to malformations of Frogs and Toads, with Radiographic Interpretations. US Fish and Wildlife Service, 16pp.

Ostler, H.B. (ed.) (2004). Diseases of the Eye and Skin: A Colour Atlas. Lippincott Williams & Wilkins, Philadelphia, 416pp.

Ouellet, M., J. Bonin, J. Rodrigue, J.L. Desgranges & S. Lair (1997). Hindlimb deformities (ectromelia, ectrodactyly) in free-living anurans from agricultural habitats. Journal of Wildlife Diseases 33(1): 95–104. https://doi.org/10.7589/0090-3558-33.1.95

Peltzer, P.M., R.C. Lajmanovich, L.C. Sanchez, A.M. Attademo, C.M. Junges, C.L Bionda, A.L. Martino & A. Basso (2011). Morphological abnormalities in amphibian populations. Herpetological Conservation and Biology 6(3): 432–442. https://doi.org/20.1633/0055-7541

Piha, H., M. Pekkonen & J. Merila (2006). Morphological abnormalities in amphibians in agricultural habitats: a case study of the common frog Rana temporaria. Copeia 2006(4): 810–817.

Quek, A., L.Y. Tan, L.K. Wang & E. Clews (2014). A Guide to Freshwater Fauna of Ponds in Singapore. Tropical Marine Science Institute, The National University of Singapore. Downloaded on 14 July 2017; https://emid.nus.edu.sg/Inland/vguide pond.pdf.

Rajakaruna, R.S., V.A.M.P.K. Samarawickrama & K.B. Ranawana (2007). Amphibian declines and possible etiologies: the case for Sri Lanka. Journal of Natural Science Foundation 35(1): 3–8. https://doi.org/10.4038/jnsfsr.v35i1.3655

Rajakaruna, R.S., P.M.J.R. Piyatissa, U.A. Jayawardena, A.N. Navaratne & P.H. Amerasinghe (2008). Trematode infection induced malformations in the common hourglass treefrogs. Journal of Zoology 275(1): 89–95. https://doi.org/10.1111/j.1469-7998.2008.00416.x

Reeves, M.K., C.L. Dolph, H. Zimmer, R.S. Tjeerdema & K.A. Trust (2008). Road proximity increases risk of skeletal abnormalities in wood frogs from National Wildlife Refuges in Alaska. Environmental Health Perspectives 116(8): 1009–1014. https://doi.org/10.1289/ehp.10963.

Schalk, G., M.R. Forbes & P.J. Weatherhead (2002). Developmental plasticity and growth rates of green frog (Rana clamitans) embryos and tadpoles in relation to a leech (Macrobdella decora) predator. Copeia 2002(2): 445–449.

Schotthoefer, A.M., A.V. Koehler, C.U. Meteyer & R.A. Cole (2003). Influence of Ribeiroia infection on limb development and survival of northern leopard frogs: effects of host stage and parasite exposure level. Canadian Journal of Zoology 81(5): 1144–1153. https://doi.org/10.1139/z03-099

Sparling, D.W. (2010). Water-quality Criteria for amphibians, pp. 105–120. In: Amphibian Ecology and Conservation - A Handbook of Techniques. Oxford University Press, New York, 584pp.

Spolyarich, N., R.V. Hyne, S.P. Wilson, C.G. Palmer & M. Byrne (2011). Morphological abnormalities in frogs from a rice-growing region in NSW, Australia, with investigations into pesticide exposure. Environmental Monitoring and Assessment 173(1): 397–407. https://doi.org/10.1007/s10661-010-1395-6

Stopper, G.F., L. Hecker, R.A. Franssen & S.K. Sessions (2002). How trematodes cause limb deformities in amphibians. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 294(3): 252–263. https://doi.org/10.1002/jez.10173

Thiemann, G.W. & R.J. Wassersug (2000). Patterns and consequences of behavioural responses to predators and parasites in Rana tadpoles. Biological Journal of the Linnean Society 71(3): 513–528. https://doi.org/10.1006/bijl.2000.0459

Urbina, G., C. Jenny & S.P. Galeano (2009). Abundance, activity patterns and microhabitat of Rhinella macrorhina, an endemic toad from the cloud forests of the Colombian Central Andes. The Herpetological Journal 19(1): 35–40. https://doi.org/10.3202/belm.10274.

Wheeler, C.A. & H.H. Welsh Jr. (2008). Mating strategy and breeding patterns of the foothill yellow-legged frog (Rana boylii). Herpetological Conservation and Biology 3(2): 128–142.