New Records of Morphological Anomalies in Anurans, with a Review for Brazil
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Herpetology Notes, volume 14: 31-41 (2021) (published online on 08 January 2021) New records of morphological anomalies in anurans, with a review for Brazil Franciele Cristina de Souza1,*, André Luiz Ferreira da Silva2, Camila Saraiva dos Anjos3, Tairine Freisleben Estevinho2, Mateus de Oliveira Lisboa4, and Marcelo Menin1 Changes in morphological and anatomical structures 2003). However, morphological alteration rates were of frogs have been reported for centuries (Henle et al., higher in agricultural areas when compared to protected 2017a). Those are called malformations when they occur areas as a result of damage caused by environmental in cellular and/or transcription processes that directly contaminants (Borges et al., 2019). Additionally, a study affect individuals in an initial phase of development of an introduced population of Rhinella jimi (Bufonidae) (Meteyer, 2000), while the term “deformity” usually in an oceanic island in Brazil showed that 52% of the indicates alterations of organs or structures that were tadpoles and about 45% of the adults exhibited anomalies originally formed correctly. According to Henle et that were mainly related to oral structures in tadpoles al. (2017b), malformations and deformities are often and to hind limbs in adults (Toledo and Ribeiro, 2010; difficult to tell apart without a detailed study of each Tolledo et al., 2014). Suggested hypotheses for these case, and hence the authors suggest using the term higher anomaly rates include parasite or virus infection, “anomaly” for this kind of permanent structural defect environmental contaminants, high level of ultraviolet-B (Johnson et al., 2001; Henle et al., 2017b). Anomalies radiation or inbreeding depression (Toledo and Ribeiro, in anurans can also be caused by external factors, such 2010). as parasitic infections, non-lethal predator attacks, and The impact of anomalies in amphibian populations has exposure to chemical pollutants or ultraviolet radiation been well documented in North America and in Europe (Johnson et al., 1999; Ouellet, 2000; Blaustein et al., (Henle et al., 2017a), but in Brazil there are fewer 2003; Reeves et al., 2013; Henle et al., 2017a; Borges anuran anomaly records, published mainly as single et al., 2019). event short notes and some articles on population impact Anomalies can affect amphibian populations at evaluations. Herein, we report anomaly observations on different rates. For some species the rate of individuals adults, newly-metamorphosed individuals and tadpoles with deformities or malformations in a healthy of nine anuran species in two localities in central population does not exceed 5% (Blaustein and Johnson, Amazon and southern Brazil. Additionally, we present an extensive literature review on anomalies in adults and tadpoles of anuran species occurring in Brazil. Between 2016 and 2019 we conducted field 1 Programa de Pós-Graduação em Zoologia and Laboratório de Taxonomia e Ecologia de Anfíbios e Répteis, Universidade observations in two non-flooded forests (Dense Federal do Amazonas, 69080-900, Manaus, Amazonas, Ombrophilous Forest) in the Reserva Florestal Adolpho Brazil. Ducke-RFAD (2.5730°S, 60.3724°W) and Dimona 2 Programa de Pós-Graduação em Zoologia, Laboratório Farm- Projeto Dinâmica Biológica de Fragmentos de Biodiversidade, Conservação e Ecologia de Animais Florestais-PDBFF (2.3904°S, 60.1708°W), both in the Silvestres, Universidade Federal do Paraná, 81531-980, municipality of Manaus, Amazonas State, and in one Curitiba, Paraná, Brazil. area of Mixed Ombrophilous Forest in the municipality 3 Programa de Pós-Graduação Biologia de Água Doce e Pesca Interior, Laboratório de Sistemática e Ecologia de Peixes, of São José dos Pinhais, Paraná State (Corta Vento Instituto Nacional de Pesquisas da Amazônia, 69067-375, Farm; 25.7024°S, 49.0720°W), Brazil. At RFAD Manaus, Amazonas, Brazil. adults and tadpoles were captured in the leaf litter of 4 Pontifícia Universidade Católica do Paraná, 80215-901, forest floor and in an artificial permanent reservoir at Curitiba, Paraná, Brazil. the edge of the forest (vegetation composed by Victoria * Corresponding author. E-mail: [email protected] amazonica (Nymphaeaceae), and Pistia stratiotes © 2020 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. (Araceae)). At Dimona Farm, tadpoles were captured 32 Franciele Cristina de Souza������� et al. in a natural temporary pond covered by Thurnia Allobates femoralis (Fig. 1A) and a tadpole of R. sphaerocephala (Thurniaceae), Urospatha sagitifolia marina (Fig. 1B) presented ectromely (amely) of the (Araceae) and Cyclantus sp. (Cyclanthaceae). At left forelimb and left hindlimb, respectively, where Corta Vento Farm adults were captured in the leaf there was no evidence of the limbs. The newly- litter of the forest floor and in two artificial dams in an metamorphosed individual of B. geographica (Fig. 1C) open area covered by Typhaceae, shrubs, small trees parasitized by the ectoparasitic crustacean Argulus sp. and Rubus niveus (Rosaceae). Adults were captured was obtained in the laboratory by rearing it from a pre- during the night both manually and with pitfall traps, metamorphic stage. After metamorphosis, we found while tadpoles were collected during the day with a anomalies in the pelvic girdle bones (extension and hand net in temporary ponds and artificial reservoirs. curvature of the right ilium) and skin membrane or skin Each species was identified according to Hero (1990) fusion (fusion of the skin restricting limb movement) and Lima et al. (2012), together with our taxonomic (Fig. 2), but we cannot ascertain that the parasite caused expertise. We measured snout-vent length (SVL) of the observed anomalies. One individual of P. boiei (Fig. adults and metamorphosed individuals, and total length 1D) and one of R. abei (Fig. 1E) presented black-eyed. (TL) of tadpoles using a ruler (1 mm precision) or Absence of the left eyeball (anophthalmy) was detected calliper (0.05 mm precision). Collected specimens were in an adult P. boiei (Fig. 1F) and in a tadpole of R. deposited at the Paulo Bürhnheim Zoological Collection proboscidea (Fig. 1G). Ectromely was observed in four of the Universidade Federal do Amazonas (CZPB- species and was divided in two categories: ectromely of UFAM), section Anuran Larvae (tadpole lots: CZPB- tibiafibula, with the left foot absent in L. catesbeianus LA 425/892, 426/893, 427/894) and at the Zoological (Fig. 1H), and ectromely of radius and ulna with the Collection of Universidade Federal do Paraná (UFPR). left hand absent in P. cuvieri (Fig. 1I), S. fuscovarius We also extensively revised the literature in the search (Fig. 1J) and R. marina (Fig. 1K). Lastly, another for malformations/deformities/anomalies in anurans individual of P. boiei (Fig. 1L) presented shortening of (adults and tadpoles) in Brazil. Our definitions of the right hindlimb, characterized as brachymely with malformations/anomalies follow Toledo and Ribeiro ectrodactyly of toes. (2010), Tolledo et al. (2014) and Henle et al. (2017b). In addition to our 12 observations we found 148 When inconsistencies were detected, we used Henle anomaly records on anuran adults, juveniles and et al. (2017b). Ectromely was used for a partial or tadpoles in Brazil in scientific literature (Table complete absence of a limb, and amely (one or several 1). The literature records and our observations limbs completely lacking) was treated as a subcategory encompass 104 species of 13 families (Aromobatidae, of ectromely; breaks, gaps and ridges in the denticles Brachycephalidae, Bufonidae, Craugastoridae, rows was treated as “tooth rows abnormal”; alterations Cycloramphidae, Hylidae, Hylodidae, Leptodactylidae, in jaw sheaths was treated as “jaw sheaths abnormal” Microhylidae, Odontophrynidae, Phyllomedusidae, (Henle et al., 2017b). Pipidae, and Ranidae; Frost, 2020). Anomalies occurred In total, we observed anomalies in 12 individuals across all Brazilian regions, but were concentrated (tadpole, juveniles and adults) of nine anuran species: in the South and Southeast regions. Hylidae was the Allobates femoralis (Boulenger, 1884) (N = 1 newly- family with the highest number of records (67 records metamorphosed individual, SVL = 10.80 mm), Boana in 40 species), followed by Leptodactylidae (24 records, geographica (Spix, 1824) (N = 1 newly-metamorphosed 16 species), Bufonidae (23 records, 13 species), individual, SVL = 21 mm), Rhinella proboscidea (Spix, Hylodidae (18 records, 14 species) Odontophrynidae 1824) (N = 1 tadpole, TL = 12.60 mm), Lithobates (10 records, seven species), Microhylidae (four catesbeianus (Shaw, 1802) (N = 1 adult not collected), records, four species), Brachycephalidae (four Physalaemus cuvieri Fitzinger, 1826 (N = 1 adult not records, two species), Aromobatidae (three records, collected), Proceratophrys boiei (Wied-Neuwied, two species), Cycloramphidae (two records, two 1824) (N = 3 adults, SVL = 42.2 and 43.1 mm, one species), Ranidae (two records and two species), individual not collected), Rhinella abei (Baldisseri et al., Craugastoridae, Phyllomedusidae, and Pipidae (one 2004) (N = 1 adult, SVL = 35.6 mm), Rhinella marina record and one species in each family). In general, (Linnaeus, 1758) (N = 2, one tadpole and one newly these records are based on single event observations, metamorphosed individual, TL = 10.86 and SVL = 9.55, but few studies estimated the impacts of anomalies on respectively), and Scinax fuscovarius (Lutz, 1925) (N = anuran populations, and are based on a great number 1 non-collected