Sharon Pratt ANZALDUA and Javier GOLDBERG.Hotspot of Adult Cuban Treefrog and Cane Toad Multi-organ Abnormality in Suburban South-west Florida[J].Asian Herpetological Research(AHR),2020,11(2):139-154.[doi:10.16373/j.cnki.ahr.190045]
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Hotspot of Adult Cuban Treefrog and Cane Toad Multi-organ Abnormality in Suburban South-west Florida
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Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

2020 VoI.11 No.2
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Hotspot of Adult Cuban Treefrog and Cane Toad Multi-organ Abnormality in Suburban South-west Florida
Sharon Pratt ANZALDUA1* and Javier GOLDBERG2
1 Private University, 27427 Horne Ave Bonita Springs, Florida 34135, USA
2 Instituto de Bio y Geociencias del NOA (IBIGEO-CONICET), CCT-Salta, 9 de Julio 14, Rosario de Lerma, Salta 4405, Argentina
gonad hermaphrodite malformation Osteopilus septentrionalis Rhinella marina
This study represents a continuation of the Florida hotspot of tadpole abnormality found in the South-west Florida suburban roadside drainage ditches in 2012 to determine if the adult frogs and toads frequenting the study sites were anatomically abnormal. The gross examination of all organs included 397 adult anurans and 40 metamorphs representing five anuran species: Osteopilus septentrionalis (N=364), Rhinella marina (N=60), Lithobates sphenocephala (N=7), Anaxyrus terrestris (N=5) and Anaxyrus americanus (N=1). The gonads, liver, kidney and intestines were abnormal at a frequency of 87.4%. The few normal anurans (12.6%) were females and young male adults. We found a significant difference in organ abnormality type and frequency between sexes. Almost all frog and toad males had testicular abnormality (92%) with only 6% with normal testes, whereas the female gonad abnormality was lower, at 41.6%. Hermaphroditism was found in both sexes at a frequency of 26.2%. The toads had a significantly higher frequency of hermaphroditism than the frogs. The toad hermaphroditism frequency was found to be 40%, whereas the frog hermaphroditism 23.3%. A hermaphrodite Cane toad male with a female phenotype coexisted with the normal male phenotype hermaphrodite. The fertility of 27 in situ pairs was assessed. The fertile testicular abnormal male and hermaphrodite pairs produced offspring with abnormal larval morphology. This information adds new evidence of the effect of chemicals on wild populations and the effect on non-target species which has always been underestimated.


Anway M. D., Leathers C., Skinner M. K. 2006. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult—onset disease. Endocrinology, 147: 5515–5523
Anzaldua Pratt S., Goldberg J. 2019. Hotspot of tadpole abnormality in suburban south-west Florida. Herpetol J, 29: 45–54
Abdel-moneim A., Coulter D. P., Mahapatra C. T., Sepulveda M. S. 2015. Intersex in fishes and amphibians: population implications, prence, mechanisms and molecular biomarkers. J Applied Toxic, 35: 1228–1240
Babic-Gojmerac T., Kniewald Z., Kniewald J. 1989. Testosterone metabolism in neuroendocrine organs in male rats under atrazine and dethylatrazine influence. Steroid Biochem, 33: 141–146
Barcenas-Ibarra A., de la Cueva H., Rojas-Lleonart I., Abreu-Grobois F. A., Lozano-Guzmán R. I., Cuevas E., García-Gasca A. 2015. First approximation to congenital malformation rates in embryos and hatchlings of sea turtles. Birth Defects Res A, 103: 203–224
Bernabo I., Guardia A., Macirella R., Brunelli E. 2017. Chronic exposure to fungicide pyrimethanil; muti-organ effects on Italian tree frog (Hyla-intermedia). Sci Reports, 7(1): 1179
Bonin J., Ouellet M., Rodrigue J., DesGranges J. L., Gagne F., Sharbel T. F., Lowcock L. A. 1997. Measuring the health of frogs in agricultural habitats subjected to pesticides. 246–257. In Green D.M. (Ed). Amphibians in decline: Canadian studies of a global problem. St. Louis (Soc study amphibians reptiles)
Brack W., Aissa S. A., Backhaus T., Dulio V., Escher B. I., Faust M., Hilscherova K., Hollender J., Hollert H., Muller C., Munthe J., Posthuma L., Seiler T. B., Slobodnik J., Teodorovic I., Tindall A. J., de Arag?o Umbuzeiro G., Zhang X., Altenburger R. 2019. Effect-based methods are key. The European Collaborative Project SOLUTIONS recommends integrating effect-based methods for diagnosis and monitoring of water quality. Environ Sci Eur, 31: 10
Bradford D. S., Lannoo M. J. 2005. Factors implicated in amphibian population declines in the United States. Chapter 23. Declining Amphibians: A United States Response to the Global Problem. UC Press Berkeley: 915–951
Carr J. A., Gentles A., Smith E. E., Goleman W. L., Urquidi L. J., Thuett K., Kendall R. J., Giesy J. P., Gross T. S., Solomon K. R., Van Deer Kraak G. 2003. Response of larval Xenopus laevis to atrazine: assessment of growth, metamorphosis, and gonadal and laryngeal morphology. Environ Toxicol Chem, 22: 396–405
Colborn T., vom Seel E. S., Soto A. M. 1993. Developmental effects of endocrine disrupting chemicals in wildlife and humans. Environ Health Persp, 101378–101384
Crane M., Hallmark N., Legadic L., Ott K., Pickford D., Preuss T., Thompson H. M., Thorbek P., Weltje L., Weeler J. R. 2018. Assessing the population relevance of endocrine disrupting effects for the non-target vertebrates exposed to plant protection products. Integr Environ Assess Manag, 4113
da Silva A. P. A., de Oliveira C. D. L., Quirino A. M. S., da Silva F. D. M., de Aquino Saraiva R. 2018. Endocrine disruptors in aquatic environment: effects and consequences on the biodiversity of fish and amphibian species. Aquat Sci Technol, 6: 35–51
Daszak P. A., Berger L., Cunningham A. A., Hyatt A. D., Green D. E., Speare R. 1999. Emerging infectious disease and amphibian population declines. Emerg Infect Dis, 5: 735–748
Daszak P. A., Cunningham A. A., Hyatt A. D. 2003. Infectious disease and amphibian population declines. Divers Distrib, 9: 141–150
Fisher R. N., Shaffer H. B. 1996. The decline of amphibians in California’s Great Central Valley. Conserv Biol, 10: 1387–1397
Foran C. M., Peterson B. N., Benson W. H. 2002. Transgenerational and developmental exposure of Japanese medaka (Oryzias latipes) to ethinylestradiol results in endocrine and reproductive differences in the response to ethinylestradiol as adults. Toxicol Sci, 68: 389–402
Goldberg J. 2013. A first case of bilateral hermaphroditism in a wild-caught tadpole (Scinax fuscovarius). Herpetol J, 23: 167–169
Goldberg J. 2015. A case of gonadal segmented in tadpole Hypsiboas riojanus (Anura, Hylide). Whatever Herpetol, 29: 77–80
Google Maps. 2013.
Google Street View. 2013.
Gross T. S., Sepulveda M., Carr J. A., Giesy J. P., Hosmer A. J., Kendall R. J., Solomon K., Smith E. E., Van Der Kraak G. 2003. Atrazine exposure and the occurrence of reproductive abnormalities in field caught Bufo marinus from south Florida. Greater Everglades Ecosystem Restoration (GEER) Open File Report, 03–54
Hayes T., Haston K., Tsui M., Hoang A., Haeffele C., Vonk A. 2002. Feminization of male frogs in the wild. Nature, 419: 895–896
Hayes T., Haston K., Tsui M., Hoang A., Haeffele C., Vonk A. 2003. Atrazine-Induced Hermaphroditism at 0.1PPB in American Leopard Frogs (Rana pipiens): Laboratory and Field Evidence. Environ Health Persp, 111: 568–575
Hayes T., Stuart A., Mendoza M., Collins A., Noriega N., Vonk A., Johnston G., Liu R., Kpodzo D. 2006. Characterization of Atrazine-induced gonadal malformations in African clawed frogs (Xenopus laevis) and comparisons with effects of an androgen antagonist (cyproterone acetate) and exogeneous estrogen (17-estradiol): support for the demasculinization/feminization hypothesis. Environ Health Persp, 114 (Suppl 1): 134–141
Hecker M., Murphy M., Coady K., Villeneuve D., Jones P., Carr J., Solomon K., Smith E., Van Der Kraak G., Gross T., Du Preez L., Kendall R., Giesy J. 2006. Terminology of gonadal anomalies in fish and amphibians resulting from chemical exposures. Rev Environ Contam Toxicol, 187: 103–131
Hegde G., Krishnamurthy S. V., Berger G. 2019. Common frogs response to agrochemicals contamination in coffee plantations, Western Ghats, India. Chem Ecol, 35: 397–407
Heindall J. J. 2005. The fetal basis of adult disease: role of environmental exposures—introduction. Birth Defects Res A: Clin Mol Teratol, 73: 131–132
Henle K., Dubois A., Vershinin V. 2017. A review of anomalies in natural populations of amphibians and their potential causes. 57–164. In Henle K., Dubois A. (Eds.), Studies on anomalies in natural populations of amphibians. Mertensiella 25, Chimaira, Frankfurt, Main
Johnson S. 2013. The Cuban treefrog (Osteopilus septentrionalis) in Florida. UF/IFAS #WEC 218
Karami-Mohajeri S. K., Ahmadipour A., Hamid-Reza R., Abdollahi M. 2017. Adverse effects of organophosphorus pesticides on the liver: A brief summary of four decades of research. Arh Hig Rada Toksikol, 68: 261–275
Kniewald J., Jakominic M., Tomljenovic A., Simic B., Romae P., Vranesic D., Kniewald Z. 2000. Disorders of male rat reproductive tract under the influence of atrazine. J Appl Toxicol, 20: 61–68
Kubsad D., Nilsson E. E., King S. E., Sadler-Riggleman I., Beck D., Skinner M. K. 2019. Assessment of glyphosate induced epigenetic transgenerational inheritance of pathologies and sperm epimutations: Generational toxicology. Sci Rep, 9
Lannoo M. J. 2008. Malformed frogs: The collapse of aquatic ecosystems. Berkeley: UC Press, 1–270
Lee County Mosquito Control District. 2019.
Litvinchuk S. N. 2018. Testicular anomalies in the hybridogenetic frog Pelophylax esculentus (Amphibia: Aura: Ranidae). KnE Life Sci, 92–96
Lowcock L. A., Sharbel T. F., Bonin J., Ouellet M., Rodrigue J., DesGranges J. L. 1997. Flow cytometric assay for in vivo genotoxic effects of pesticides in green frogs (Rana clamitans). Aquat Toxicol, 38: 241–255
Molander L., Agerstrand M., Beronius A., Hanberg A., Ruden C. 2015. Science in risk assessment and policy (SciRAP): An online resource for uating and reporting in vivo (eco) toxicity studies. Hum Ecol Risk Assess, 21: 753–762
Mnif W., Hassine A. I. H., Bouaziz A., Bartegi A., Thomas O., Roig B. 2011. Effect of endocrine disruptor pesticides: a review. Int J Envir Res Pub Health, 8: 2265–2303
Martin O., Adams J., Beasley A., Belanger S., Breton R., Brock T., Buonsante V., Burgos M., Green J., Guiney P., Hall T., Hanson M., Harris M., Henry T., Huggett D., Junghans M., Laskowski R., Maack G., Moermond C., Panter G., Pease A., Poulsen V., Roberts M., Ruden C., Schlekat C., Schoeters I., Solomon K., Staveley J., Stubblefield B., Sumpter J., Warne M., Wentsel R., Wheeler J., Wolff B., Yamazaki K., Zahner H., Agerstrand M. 2019. Improving environmental risk assessments of chemicals: Steps towards evidence-based ecotoxicology. Environ Int, 128: 210–217
McCoy K. A., Bortnick L. J., Campbell C. M., Hamlin H. J., Guillette L. J., St Mary C. M. 2008. Agriculture alters gonadal form and function in the toad Bufo marinus. Environ. Health Persp, 116: 1526–1532
McCoy K. A., Hoang L. K., Guillette L. J. Jr, St Mary C. M. 2008. Renal pathologies in giant toads (Bufo marinus) vary with land use. Sci Total Environ, 407: 348–357
Murphy M. B., Hecker M., Coady K. K., Tompsett A. R., Jones P. D., Du Preez L. H., Everson G. J., Solomon K. R., Carr J. A., Smith E. E., Kendall R. J., Van Der Kraak G., Giesy J. P. 2006. Atrazine concentrations, gonadal gross morphology and histology in Ranid frogs collected in Michigan agricultural areas. Aquatic Toxicol, 76: 230–245
Meshaka W. E. Jr. 2001. The cuban treefrog in Florida: Life history of a successful colonizing species. Gainesville: University Press of Florida, 191
Meshaka W. E. Jr. 2011. A runway train in the making: the exotic amphibians, reptiles, turtles, and crocodilians of Florida. Herpetol Conserv Biol, 6 (Monograph 1): 1–101
Price S. J., Leung W. T. M., Owen R. P., Sergeant C., Cunningham F. B., Garner T. W. J., Nichols R. A. 2019. Effects of historic and projected climate change on the range and impacts of an emerging wildlife disease. Global Change Biol, 25: 2648–2660
Piprek R. P., Malgorzata K., Kubiak J. Z. 2014. Bidder’s organ-structure, development and function, Int J Dev Biol, 58: 819–827
Reeves M., Medley K., Pinkney A., Holyoak M., Johnson P., Lannoo M. J. 2013. Localized hotspots drive continental geography of abnormal amphibians on U.S. wildlife refuges. PLoS One, 8(11): e77467
Scheele B. C., Pasmans F., Lee F., Skerratt L. F., Berger L., Martel A., Beukema W., Aceve A. 2019. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science, 363: 1459–1463
Skelly D. K., Bolden S. R., Dion K. B. 2010. Intersex frogs concentrated in suburban and urban landscapes. Eco Health, 7: 374–379
Sparling D. W., Bickham J., Cowman D., Fellers G. M., Lacher T., Matson C. W., McConnell L. 2015. In situ effects of pesticides on amphibians in the Sierra Nevada. Ecotoxicol, 24: 262–278
Team Bufo: About us. 2011–2012:
U.S. EPA. (2019). Joint statement on mosquito control in the United States.


Last Update: 2020-06-25