Bertoluci, Jaime

Brassaloti, Ricardo Augusto

English

Cadernos Espinosanos (E-Journal)

285Phyllomedusa - 17(2), December 2018PROOFSReceived 09 November 2018Accepted 12 December 2018Distributed December 2018Keywords: absence of eyes, deformity, malformation, Smith Frog.Palavras-chave: ausência de olhos, deformidade, malformação, sapo-ferreiro.Short CommuniCationA case of bilateral anophthalmy in an adult Boana faber (Anura: Hylidae) from southeastern BrazilRicardo Augusto Brassaloti and Jaime BertoluciEscola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo. Av. Pádua Dias 11, 13418-900, Piracicaba, SP, Brazil. E-mails: ricardo.brassaloti@usp.br, jaime.bertoluci@usp.br.Phyllomedusa 17(2):285–288, 2018© 2018 Universidade de São Paulo - ESALQ ISSN 1519-1397 (print) / ISSN 2316-9079 (online)doi: http://dx.doi.org/10.11606/issn.2316-9079.v17i2p285-288Morphological deformities, commonly osteological malformations of several types, occur in natural populations of amphibians around the world (e.g., Peloso 2016, Silva-Soares and Mônico 2017). Ouellet (2000) and Henle et al. (2017) provided comprehensive reviews on amphibian deformities and their possible causes. Anophthalmy, the absence of one or both eyes, has been documented in some anuran species (Henle et al. 2017 and references therein, Holer and Koleska 2018). We report here the occurrence of bilateral anophthalmy in an adult Blacksmith Frog, Boana faber (Wied-Neuwied, 1821), from a well-preserved forest area of southeastern Brazil.Boana faber is a medium-sized hylid frog widely distributed in eastern to southern Brazil, southeastern Paraguay, and Misiones, Argentina (Frost 2018).While conducting fieldwork related to the anuran faunas of four types of forest in southeastern Brazil (Bertoluci et al. 2007), RAB collected and adult female Boana faber with bilateral anophthalmy in the Estação Ecológica dos Caetetus, Gália Municipality, state of São Paulo, Brazil (22°24'11'' S, 49°42'05'' W); the station encompasses 2,178.84 ha (Tabanez et al. 2005). The animal was collected at about 660 m a.s.l. in an undisturbed area (Site 9 of Brassaloti et al. 2010; 22°23'27'' S, 49°41'31'' W; see this reference for a map). The female is a subadult (SVL 70 mm) and was collected on 13 May 2007 at 21:23 h while perched on vegetation about 1 m above ground along a stream; it died in captivity a few days later (Figure 1). We dissected the eye region for examination; the eye sockets were empty and there was no indication of optic nerves. Ovaries were not developed. The stomach had no prey, but a small quantity of faeces in the rectum revealed three tiny insects had been ingested (2 ants of the genus Wasmannia and an Auchenorrhyncha hemipteran) and some minute Acari; we assume that these were consumed accidentally. The specimen is deposited in the herpetological collection of the Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, with the number VESALQ 495.286Phyllomedusa - 17(2), December 2018Cases of bilateral anophthalmia are scarce in the literature. Narayana et al. (2017) found an adult bufonid Duttaphrynus melanostictus (Schneider, 1799) that lacked both eyes in Borneo. There are a few examples of anophthalmy in Brazilian anurans. Haddad et al. (1990) reported unilateral anophthalmy (always the left eye) in natural hybrids of the bufonids Rhinella icterica and R. ornata, and the hybridization itself was suggested as the probable cause of the abnormalities observed.The bufonid Rhinella jimi is an invasive species of the Archipelago of Fernando de Noronha in northeastern Brazil; in this area, many individuals had deformities of all kind, including partial and total anophthalmy (Toledo and Ribeiro 2009, Tolledo et al. 2014, Tolledo and Toledo 2015). It was suggested that the absence of predators on this invasive toad might have allowed deformed individuals to persist in the population until the adult stage (Toledo and Ribeiro 2009).Dias and Carvalho-e-Silva (2012) reported unilateral anophthalmia and unilateral microphthalmia in two tadpoles of the proceratophryid Proceratophrys appendiculata at Parque Nacional da Serra dos Órgãos, state of Rio de Janeiro, Brazil; the cause of this deformity is unknown.It is surprising the individual Boana faber reported here attained adulthood being totally blind. Its survivorship could be related to the fact that B. faber preys mainly on adult arboreal frogs, such as the hylids Aplastodiscus perviridis, Scinax granulatus (Solé et al. 2004, 2005), and Scinax hayii (pers. obs.); each of these could be encountered in breeding choruses by a predator. Thus a blind frog might locate the breeding site acoustically by relying on both tympanum–columella–papilla basilaris (for air-borne sounds) and opercular muscle–operculum–papilla amphibiorum (for substrate-borne sounds) systems (Duellman and Trueb 1994) to locate individual prey. This would indicate that an individual frog is able to switch its foraging mechanism from visual to acoustic. In fact, Figure 1. The anophthalmic specimen of Boana faber in the field (A) and under captivity (B). Photos: RAB and JB.ABTolledo and Toledo (2015) demonstrated such a behavioral switch (and a correlated change in diet composition) from active, nocturnal hunting by eyesight to sit-and-wait predation based on tactile cues in blind Rhinella jimi in captivity. Insects and other arthropods are also commonly ingested by B. faber (Solé et al. 2004, 2005), and Brassaloti and Bertoluci287Phyllomedusa - 17(2), December 2018PROOFSdoubtless, the insects ingested by the blind frog may have kept it from starving.Unfortunately, the cause of deformity in this anuran is unknown. The core area of the site is well preserved, covered by a pristine vegetation, and harbors seemingly healthy anuran populations, as suggested by the report to the site of albino tadpoles of Rhinella ornata (Brassaloti and Bertoluci 2008), since in vertebrates albinism is characteristic of healthy populations (Bechtel 1995). Anophthalmy has been reported in anurans from presumably natural areas (e.g., Lythobates sylvaticus: Eaton et al. 2004). However, the deformed Boana faber was collected in an area with varying levels of disturbance because the reserve is located in an agricultural matrix where pesticides can accumulate in bodies of water (Tabanez et al. 2005). In fact, pesticides are known to cause deformities in embryos and larvae and to produce high rates of eye anomalies in adults (e.g., Bufo marinus; Fort et al. 2006).Acknowledgments.—We thank FAPESP for financial support (processes 04/15938-5 and 99/09635-0) and for a grant to RAB (process 06/55363-7), and IBAMA for the collection permit number 430/05. JB is a researcher of CNPq (process number 309017/2016-5). We thank Felipe Goulart Gonçalves for identifying insect remains, and Rudi Ricardo Laps and Juan C. Guix for reviewing the manuscript. Linda Trueb has improved the English and the readability of the manuscript.  ReferencesBechtel, H. B. 1995. Reptile and amphibian variants: colors, patterns and scales. Malabar, FL, Krieger Publishing. 224 pp.Bertoluci, J., R. A. Brassaloti, J. W. Ribeiro Júnior, V. M. F. N. Vilela, and H. O. Sawakuchi. 2007. Species composition and similarities among anuran assemblages of forest sites in southeastern Brazil. Scientia Agricola 64: 364–374.Brassaloti, R. A. and J. Bertoluci. 2008. Albinism in tadpoles of Rhinella ornata (Anura, Bufonidae) from southeastern Brazil. Herpetological Bulletin 106: 31–33.Brassaloti, R. A., D. C. Rossa-Feres, and J. Bertoluci. 2010. Anurofauna da Floresta Estacional Semidecidual da Estação Ecológica dos Caetetus, sudeste do Brasil. Biota Neotropica 10: http://www.biotaneotropica.org.br/v10n1/en/abstract?inventory+bn01810012010. Dias, P. H. S. and A. M. P. T. Carvalho-e-Silva. 2012. Records of abnormalities in Proceratophrys appendiculata (Günther, 1873) (Anura; Cycloramphidae; Alsodinae). Herpetology Notes 5: 197–199.Duellman, W. E. and L. Trueb. 1994. Biology of Amphibians. Johns Hopkins University Press. 670 pp.Eaton, B. R., S. Eaves, C. Stevens, A. Puchniak, and C. A. Paszkowski. 2004. Deformity levels in wild populations of the wood frog (Rana sylvatica) in three ecoregions of Western Canada. Journal of Herpetology 38: 283–287.Fort, D. J., R. L. Rogers, B. O. Buzzard, G. D. Anderson, and J. P. Bacon. 2006. Deformities in cane toad (Bufo marinus) populations in Bermuda: Part III. Microcosm-based exposure pathway assessment. Applied Herpetology 3: 257–277. Frost, D. R. 2018. Amphibian Species of the World: an Online Reference. Version 6.0. Electronic Database accessible at http://research.amnh.org/herpetology/amphibia/index.html. American Museum of Natural History, New York, USA. Captured on 15 October 2018.Haddad, C. F. B., A. J. Cardoso, and L. M. Castanho. 1990. Hibridação natural entre Bufo ictericus e Bufo crucifer (Amphibia: Anura). Revista Brasileira de Biologia 50: 739–744.Henle, K., A. Dubois, and V. Vershinin. 2017. A review of anomalies in natural populations of amphibians and their potential causes. Mertensiella 25: 57–164. Holer, T. and D. Koleska. 2018. A case of unilateral anophthalmia in an adult Pelophylax kl. esculentus (Linnaeus, 1758). Herpetozoa 31: 103–104.Narayana, B. L., B. Naresh, and S. Hussain. 2017. A case of anophthalmia in Duttaphrynus melanostictus (Schneider, 1799) from Telangana, India. Sauria 39: 52–53.Ouellet, M. 2000. Amphibian deformities: current state of knowledge. Pp. 617–661 in D. W. Sparling, G. Linder, and C. A. Bishop (eds.), Ecotoxicology of Amphibians and Reptiles. Pensacola. SETAC Press. Peloso, P. L. V. 2016. Osteological malformation in the tree frog Hypsiboas geographicus (Anura: Hylidae). Phyllomedusa 15: 91–93.A case of bilateral anophthalmy in Boana faber288Phyllomedusa - 17(2), December 2018Silva-Soares, T. and A. T. Mônico. 2017. Hind limb malformation in the tree frog Corythomantis greeningi (Anura: Hylidae). Phyllomedusa 16: 117–120.Solé, M., B. Pelz, and A. Kwet. 2004. Hyla faber (Smith Frog). Diet. Herpetological Review 35: 159.Solé, M., O. Beckmann, B. Pelz, A. Kwet, and W. Engels. 2005. Stomach-flushing for diet analysis in anurans: an improved protocol evaluated in a case study in Araucaria forests, southern Brazil. Studies on Neotropical Fauna and Environment 40: 23–28.Tabanez, M.F., G. Durigan, A. Keuroghlian, A. F. Barbosa, C. A. Freitas, C. E. F. Silva, D. A. Silva, D. P. Eaton, G. Brisolla, H. H. Faria, I. F. A. Mattos, I. M. T. Lobo, M. R. Barbosa, M. Rossi, M. G. Souza, R. B. Machado, R. M. Pfeifer, V. S. Ramos, W. J. Andrade, and W. A. Contieri. 2005. Plano de manejo da Estação Ecológica dos Caetetus. IF Série Registros 29: 1–103.Toledo, L. F. and R. S. Ribeiro. 2009. The archipelago of Fernando de Noronha: an intriguing malformed toad hotspot in South America. EcoHealth 6: 351–357.Tolledo, J. and L. F. Toledo. 2015. Blind toads in paradise: the cascading effects of vision loss on a tropical archipelago. Journal of Zoology 296: 167–176.Tolledo, J., E. T. Silva, C. H. L. Nunes-de-Almeida, and. L. F. Toledo. 2014. Anomalous tadpoles in a Brazilian oceanic archipelago: implications of oral anomalies on foraging behaviour, food intake and metamorphosis. Herpetological Journal 24: 237–243.Editor: Franco Leandro SouzaBrassaloti and Bertoluci

A case of bilateral anophthalmy in an adult Boana faber (Anura: Hylidae) from southeastern Brazil

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A case of bilateral anophthalmy in an adult Boana faber (Anura: Hylidae) from southeastern Brazil

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