Herpetology Notes, volume 14: 31-41 (2021) (published online on 08 January 2021)

New records of morphological anomalies in anurans, with a review for

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 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 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 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 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, , Hylodidae, , in jaw sheaths was treated as “jaw sheaths abnormal” Microhylidae, Odontophrynidae, , (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), (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 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), (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 fuscovarius (Lutz, 1925) (N = anuran populations, and are based on a great number 1 non-collected adult). of individuals (e.g. Toledo and Ribeiro, 2010; Tolledo New records of morphological anomalies in anurans, with a review for Brazil 33

Figure 1. Anurans with anomalies collected in the municipalities of Manaus, Amazonas State, and São José dos Pinhais, Paraná State, Brazil. (A) Ectromely (amely) in Allobates femorallis and (B) Rhinella marina. (C) Skin webbing and anomaly in the bones of the pelvic girdle in Boana geographica. (D) Black-eyed in Proceratophrys boiei and (E) Rhinella abei. (F) Anophthalmia in Proceratophrys boiei and (G) Rhinella proboscidea. (H) Ectromely of tibiafibula in Lithobates catesbeianus. (I) Ectromely of radius and ulna in Physalaemus cuvieri, (J) Scinax fuscovarius, and (K) Rhinella marina. (L) Brachymely and ectrodactyly in Proceratophrys boiei. Photos by: A. Camargo, C.S. Anjos, A.L.F. Silva and M.O. Lisboa.

et al., 2014; Ascoli-Morrete et al., 2019; Borges et Brazilian territory and harbours many species al., 2019). Our data added anomaly records for four (about 330 species; Hoogmoed and Galatti, 2019), the new species (R. abei, R. proboscidea, P. boiei, and L. presence of anomalies were previously reported for catesbeianus) to North and South Brazilian regions. only 14 of them (Table 1). Although the Amazon occupies more than 60% of the 34 Franciele Cristina de Souza et al.

The most widespread types of anomaly in adults and juveniles were ectrodactyly (27 records, 27 species), followed by brachydactyly (25 records, 23 species), ectromely partial or complete (23 records, 22 species), anophthalmy (16 records, 12 species), syndactyly (10 records, eight species), albinism (eight records, eight species), polymely (seven records, six species), and polydactyly (six records, six species). All other anomaly types were found in less than five species. In an extensive literature review on amphibian anomalies, Henle et al. (2017a) detected ectromely and ectrodactyly as the main types of skeletal anomalies in anuran and salamander populations around the world (authors considered brachydactyly as a specific form of ectrodactyly). Anophthalmia, presence of cysts, oedemas and bloating were the most common non-skeletal morphological anomalies in anuran species, while albinism and black- eyed were the most common colour anomalies (Henle Figure 2. X-ray image of an individual of Boana geographica et al., 2017a). (Hylidae) showing anomaly in the bones of the pelvic girdle Considering tadpoles (Table 1), we found 58 records and skin webbing. Photo: Victória D. Pereira e Silva. of 49 anuran species distributed in Bufonidae (six

Table 1. Anuran species with anomalies reported in Brazil. N = number of individuals. Stage: A= adults; J= juveniles/newly metamorphosed frogs; T = tadpoles. Species names follow Frost (2020).

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Table 1. Continued. 11 (A) Brachydactyly, ectrodactyly, ectromely, Sertão and Passo Fundo (Rio Grande do Sul) Ascoli-Morrete et al. (2019) syndactyly, polymely, Family/species N (Stage) Anomaly Municipality (State) Reference (Stevaux, 2002) 9 (J), Microcephaly, brachygnathia, deformed Archipelago of Fernando de Noronha Toledo and Ribeiro (2010) 62 (A) tympanum, black-eyed, perforated eye, (Pernambuco) opacity of the eye, anophthalmy, palpebrae fused to the skin, absent palpebrae, nictitant membrane fused to the superior palpebrae, deformed urostyle, partial albinism, open wound in the dorsum, brachydactyly, ectrodactyly, polydactyly, ectromely, clinodactyly, hypertrophy of the phalanges, syndactyly, skin webbing Rhinella jimi 217 (T) Jaw sheaths abnormal; keratinized denticles Archipelago of Fernando de Noronha Tolledo et al. (2014) absent; absence of jaw sheaths, tooth rows, (Pernambuco) labia; duplication of the teeth, stunted teeth, intersecting tooth rows; abnormal shape in the tooth rows

Rhinella marina (Linnaeus, 1758) 1 (T) Ectromely (amely) Manaus (Amazonas) This study Rhinella marina 1 (J) Ectromely Manaus (Amazonas) This study Rhinella marina 26 (A) Ectromely, brachydactyly, clinodactyly, Ilha Bailique, Macapá (Amapá) Bessa-Silva et al. (2016) polydactyly (Spix, 1824) 2 (T) Albinism Gália (São Paulo) Brassaloti and Bertoluci (2008) Rhinella ornata 1 (A) Brachydactyly Santo André (São Paulo) Trevine (2011) Rhinella ornata 2 (J), 37 Brachydactyly, phalangeal hypertrophy, Ilha da Marambaia, Ilha de Itacuruçá, Ilha Rebouças et al. (2019) (A) brachymely, ectrodactyly, polydactyly, Grande, Seropédica and Mangaratiba (Rio de curved bones, ectromely, tarsus hypertrophy Janeiro) Rhinella proboscidea (Spix, 1824) 1 (T) Anophthalmy Manaus (Amazonas) This study CRAUGASTORIDAE Pristimantis reichlei Padial and De la 1 (A) Eye colouration abnormal Senador Guiomard (Acre) Melo-Sampaio (2015) Riva, 2009

CYCLORAMPHIDAE Thoropa miliaris (Spix, 1824) 1 (A) Ectrodactyly Santa Teresa (Espírito Santo) Mônico et al. (2019) Toropa thaophora (Miranda-Ribeiro, 1 (T) Hyperkeratosis, loss of superficial epidermis, Ubatuba (São Paulo) Toledo et al. (2006a) 1923) remains of keratinized denticles, tooth rows abnormal HYLIDAE

Aparasphenodon arapapa Pimenta et al., 5 (J) Heterochromia, eye coloration abnormal Ilhéus (Bahia) Lourenço-de-Moraes et al. 2009 (2013) Aplastodiscus albosignatus (Lutz and 130 (T) Jaw sheaths abnormal, keratinized denticles Itanhaém (São Paulo) Navarro-Lozano et al. (2018) Lutz, 1938) absent Aplastodiscus albosignatus 1 (T) Hyperkeratosis, loss of superficial epidermis, Camanducaia (Minas Gerais) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Aplastodiscus cf. leucopygius 2 (T) Hyperkeratosis, loss of superficial epidermis, São Luiz do Paraitinga (São Paulo) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Aplastodiscus leucopygius (Cruz and 1 (A) Ectromely Santo André (São Paulo) Trevine (2011) Peixoto, 1985) Aplastodiscus leucopygius 1 (A) Ectrodactyly Santo André (São Paulo) Trevine (2011) Boana albomarginata (Spix, 1824) 2 (T) Albinism Duque de Caxias (Rio de Janeiro) Salles et al. (2013) Boana albopunctata (Spix, 1824) 1 (T) Hyperkeratosis, loss of superficial epidermis, Rio Claro (São Paulo) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Boana albopunctata 27 (T) Tail bifurcation, keratinized denticles absent Mineiros (Goiás) Borges et al. (2019) Boana albopunctata 33 (T) Jaw sheaths abnormal, keratinized denticles Itanhaém (São Paulo) Navarro-Lozano et al. (2018) absent Boana boans (Linnaeus, 1758) 1 (A) Back legs paralyzed, urostyle broken, Manaus (Amazonas) Magnusson et al. (1999) deformed ileum, broken leg, scars Boana faber (Wied-Neuwied, 1821) 1 (T) Jaw sheaths abnormal, keratinized denticles Morretes (Paraná) Vieira et al. (2012) absent Boana faber 1 (A) Anophthalmy Gália (São Paulo) Brassaloti and Bertoluci (2018) Boana faber 1 (A) Abnormal vocal sac Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) Boana faber 7 (T) Jaw sheaths abnormal, keratinized denticles Itanhaém (São Paulo) Navarro-Lozano et al. (2018) absent Boana fasciata (Günther, 1858) 2 (A) Anophthalmy Boca do Acre (Amazonas) and Buriti do Ramalho et al. (2017) Tocantins (Tocantins) Boana freicanecae (Carnaval and Peixoto, 40 (T) Jaw sheaths abnormal, keratinized denticles Jaqueira (Pernambuco) Carnaval and Peixoto (2004) 2004) absent, tooth rows abnormal Boana geographica (Spix, 1824) 1 (J) Anomaly in the bones of the pelvic girdle, Manaus (Amazonas) This study cutaneous fusion Boana geographica 1 (A) Sacrum asymmetric Undetermined (Amazonas) Peloso (2016) Boana leptolineata (Braun and Braun, 2 (A) Missing adhesive disc, ectrodactyly Sertão and Passo Fundo (Rio Grande do Sul) Ascoli-Morrete et al. (2019) 1977) Boana pulchella (Duméril and Bibron, 1 (A) Ectrodactyly Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) 1841) Family/species N (Stage) Anomaly Municipality (State) Reference Boana semilineata (Spix, 1824) 1 (T) Hyperkeratosis, loss of superficial epidermis, Camanducaia (Minas Gerais) Toledo et al. (2006a) tooth rows abnormal Boana semilineata 2 (T) Albinism Jaqueira and Igarassu (Pernanbuco) Santos et al. (2010) Boana semilineata 15 (T) Leucism Itamarajú (Bahia) Mira-Mendes and Varela Rios (2016) circumdata (Cope, 1871) 1 (T) Hyperkeratosis, loss of superficial epidermis, Petropólis (Rio de Janeiro) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Bokermannohyla hylax (Heyer, 1985) 1 (T) Hyperkeratosis, loss of superficial epidermis, São Luiz do Paraitinga (São Paulo) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Bokermannohyla hylax 1 (A) Mandibular hypoplasia Santo André (São Paulo) Trevine (2011) Bokermannohyla martinsi (Bokermann, 22 (T) Tail lesions Catas Altas (Minas Gerais) Lima et al. (2015) 1964) Bokermannohyla nanuzae (Bokermann 15 (T) Tail lesions Catas Altas (Minas Gerais) Lima et al. (2015) and Sazima, 1973) Bokermannohyla saxicola (Bokermann, 1 (T) Tail bifurcation Ubatuba (São Paulo) Silva and Toledo (2010) 1964) greeningi Boulenger, 1896 1 (A) Brachydactyly Cafarnaum (Bahia) Silva-Soares and Mônico (2017) Corythomantis greeningi 1 (A) Ectromely (amely) Cabrobó (Pernambuco) Faria et al. (2018) Dendropsophus meridianus (Lutz, 1954) 1 (?) Supernumerary vertebrae, sacrum Rio de Janeiro (Rio de Janeiro) Prigioni and Langone (1985) asymmetric Dendropsophus minutus (Peters, 1872) 1 (A) Syndactyly Santo André (São Paulo) Trevine (2011) Dendropsophus minutus 2 (T) Alterations in the tail (not specified) Mineiros (Goiás) Borges et al. (2019) Dendropsophus minutus 3 (A) Brachydactyly, syndactyly, ectrodactyly Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) Dendropsophus minutus 1 (A) Axanthism Guaramiranga (Ceará) Araújo et al. (2020) Itapotihyla langsdorffii (Duméril and 1 (A) Jaw shape abnormal Santa Teresa (Espírito Santo) Mônico et al. (2016a) Bibron, 1841) Lysapsus bolivianus Gallardo, 1961 1 (A) Anophthalmy Macapá (Amapá) Sousa and Costa-Campos (2017) 36 Franciele Cristina de Souza������� et al.

Boana leptolineata (Braun and Braun, 2 (A) Missing adhesive disc, ectrodactyly Sertão and Passo Fundo (Rio Grande do Sul) Ascoli-Morrete et al. (2019) Table1977) 1. Continued. Boana pulchella (Duméril and Bibron, 1 (A) Ectrodactyly Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) 1841) Family/species N (Stage) Anomaly Municipality (State) Reference Boana semilineata (Spix, 1824) 1 (T) Hyperkeratosis, loss of superficial epidermis, Camanducaia (Minas Gerais) Toledo et al. (2006a) tooth rows abnormal Boana semilineata 2 (T) Albinism Jaqueira and Igarassu (Pernanbuco) Santos et al. (2010) Boana semilineata 15 (T) Leucism Itamarajú (Bahia) Mira-Mendes and Varela Rios (2016) Bokermannohyla circumdata (Cope, 1871) 1 (T) Hyperkeratosis, loss of superficial epidermis, Petropólis (Rio de Janeiro) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Bokermannohyla hylax (Heyer, 1985) 1 (T) Hyperkeratosis, loss of superficial epidermis, São Luiz do Paraitinga (São Paulo) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Bokermannohyla hylax 1 (A) Mandibular hypoplasia Santo André (São Paulo) Trevine (2011) Bokermannohyla martinsi (Bokermann, 22 (T) Tail lesions Catas Altas (Minas Gerais) Lima et al. (2015) 1964) Bokermannohyla nanuzae (Bokermann 15 (T) Tail lesions Catas Altas (Minas Gerais) Lima et al. (2015) and Sazima, 1973) Bokermannohyla saxicola (Bokermann, 1 (T) Tail bifurcation Ubatuba (São Paulo) Silva and Toledo (2010) 1964) Corythomantis greeningi Boulenger, 1896 1 (A) Brachydactyly Cafarnaum (Bahia) Silva-Soares and Mônico (2017) Corythomantis greeningi 1 (A) Ectromely (amely) Cabrobó (Pernambuco) Faria et al. (2018) Dendropsophus meridianus (Lutz, 1954) 1 (?) Supernumerary vertebrae, sacrum Rio de Janeiro (Rio de Janeiro) Prigioni and Langone (1985) asymmetric Dendropsophus minutus (Peters, 1872) 1 (A) Syndactyly Santo André (São Paulo) Trevine (2011) Dendropsophus minutus 2 (T) Alterations in the tail (not specified) Mineiros (Goiás) Borges et al. (2019) Dendropsophus minutus 3 (A) Brachydactyly, syndactyly, ectrodactyly Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) Dendropsophus minutus 1 (A) Axanthism Guaramiranga (Ceará) Araújo et al. (2020) Itapotihyla langsdorffii (Duméril and 1 (A) Jaw shape abnormal Santa Teresa (Espírito Santo) Mônico et al. (2016a) Bibron, 1841) Lysapsus bolivianus Gallardo, 1961 1 (A) Anophthalmy Macapá (Amapá) Sousa and Costa-Campos (2017) Ololygon albicans (Bokermann, 1967) 1 (T) Hyperkeratosis, loss of superficial epidermis, Petrópolis (Rio de Janeiro) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Ololygon aromothyella (Faivovich, 2005) 1 (A) Abnormal pigment, brachydactyly, Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) ectrodactyly Ololygon brieni (De Witte, 1930) 1 (A) Ectromely Santo André (São Paulo) Trevine (2011) Ololygon rizibilis (Bokermann, 1964) 1 (A) Ectrodactyly Santo André (São Paulo) Trevine (2011) Osteocephalus leprieurii (Duméril and 1 (A) Anophthalmy Plácido de Castro (Acre) Ramalho et al. (2017) Bibron, 1841) Phyllodytes wuchereri (Peters, 1873) 5 (T) Tail lesions Elísio Medrado (Bahia) Magalhães et al. (2015) Pseudis paradoxa (Linnaeus, 1758) 1 (A) Polymely Amapá (Amapá) Oliveira-Souza et al. (2020) Scinax curicica Pugliesse et al., 2004 1 (T) Tail bifurcation Ubatuba (SãoPaulo) Silva and Toledo (2010) Scinax fuscomarginatus (Lutz, 1925) 1 (T) Ectromely (amely) Riachinho (Minas Gerais) Pirani and Moura (2012) Scinax fuscovarius (Lutz, 1925) 1 (A) Melanism Undetermined (probably Rio de Janeiro) Lutz (1973) Scinax fuscovarius 1 (J) Flavism São Francisco do Sul (Santa Catarina) Henle et al. (2017b) Scinax fuscovarius 29 (T) Anophthalmy, microphthalmy, aphakia Ipiguá and Mirassol (São Paulo) Sánchez-Domene et al. (2018) (absence of eye lens), sub-development (small amorphous and not emerged eye) Scinax fuscovarius 1 (A) Abnormal eye (not specified) Passo Fundo (Rio Grande do Sul) Ascoli-Morrete et al. (2019) Scinax fuscovarius 26 (T) Irregular or double fins, ridges in caudal fins Rio Verde (Goiás) Borges et al. (2019) Scinax fuscovarius 1 (A) Ectromely São José dos Pinhais (Paraná) This study Scinax hayii (Barbour, 1909) 1 (A) Melanism Cubatão (São Paulo) Lutz (1973) Scinax hayii 1 (A) Melanism Angra dos Reis (Rio de Janeiro) Lutz (1973) Scinax hayii 1 (A) Melanism Itatiaia (Rio de Janeiro) Lutz (1973) Scinax hayii 13 (T) Jaw sheaths abnormal, keratinized denticles Itanhaém (São Paulo) Navarro-Lozano et al. (2018) absent Scinax ruber (Laurenti, 1768) 1 (?) Cysts Probably Corumbá (Mato Grosso do Sul) Sambon, 1928 Scinax ruber 1 (A) Black eyed Amapá (Amapá) Sousa and Costa-Campos (2017) Scinax squalirostris (Lutz, 1925) 1 (T) Tail bifurcation Ubatuba (São Paulo) Silva and Toledo (2010) Scinax squalirostris 1 (A) Schizodactyly Botucatu (São Paulo) Jorgewich-Cohen et al. (2019) Scinax squalirostris 1 (A) Ectrodactyly (missing adhesive disc) Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) Sphaenorhynchus dorisae (Goin, 1957) 1 (A) Anophthalmy Uarini (Amazonas) Carvalho et al. (2008) Trachycephalus mesophaeus (Hensel, 1 (T) Albinism Ub atuba (São Paulo) Sazima (1974) 1867) Trachycephalus mesophaeus 1 (T) Tail bifurcation Ubatuba (São Paulo) Silva and Toledo (2010) Trachycephalus typhonius (Linnaeus, 1 (A) Axial flexure, polymely Undetermined (probably São Paulo) Vizotto et al. (1977) apud Henle 1758) et al. (2017a, b) HYLODIDAE

Crossodactylus caramaschii Bastos and 8 (T) Jaw sheaths abnormal, keratinized denticles Itanhaém (São Paulo) Navarro-Lozano et al. (2018) Pombal, 1995 absent Family/species N (Stage) Anomaly Municipality (State) Reference Crossodactylus gaudichaudii Duméril and 4 (A) Cysts Angra dos Reis (Rio de Janeiro) Hatano et al. (2007) Bibron, 1841 Crossodactylus timbuhy Pimenta et al., 1 (J) Ectromely, ectrodactyly, brachydactyly Santa Teresa (Espírito Santo) Mônico et al. (2019) 2014 Hylodes asper (Müller, 1924) 1 (A) Ectromely Santo André (São Paulo) Trevine (2011) Hylodes cardosoi Lingnau et al., 2008 6 (T) Jaw sheaths abnormal, keratinized denticles Morretes (Paraná) Vieira et al. (2012) absent Hylodes dactylocinus Pavan et al., 2001 1 (T) Hyperkeratosis, loss of superficial epidermis, Peruíbe (São Paulo) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Hylodes magalhaesi (Bokermann, 1964) 5 (T) Jaw sheaths abnormal, keratinized denticles Camanducaia (Minas Gerais) Toledo et al. (2006b) absent Hylodes meridionalis (Mertens, 1927) 1 (T) Hyperkeratosis, loss of superficial epidermis, Lauro Müller (Santa Catarina) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Hylodes meridionalis 1 (T) Hyperkeratosis, loss of superficial epidermis, São Francisco de Paula (Rio Grande do Sul) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Hylodes meridionalis 1 (J) Albinism Itati (Rio Grande do Sul) Pereira et al. (2020) Hylodes cf. ornatus 113 (T) Jaw sheaths abnormal, keratinized denticles Jundiaí (São Paulo) Vieira et al. (2013) absent Hylodes perplicatus (Miranda-Ribeiro, 1 (T) Hyperkeratosis, loss of superficial epidermis, São Bento do Sul (Santa Catarina) Toledo et al. (2006a) 1926) remains of keratinized denticles, tooth rows abnormal Hylodes phyllodes Heyer and Cocroft, 1 (T) Hyperkeratosis, loss of superficial epidermis, São Luiz do Paraitinga (São Paulo) Toledo et al. (2006a) 1986 remains of keratinized denticles, tooth rows abnormal Hylodes phyllodes 43 (A) Cysts Angra dos Reis (Rio de Janeiro) Hatano et al. (2007) Trachycephalus mesophaeus (Hensel, 1 (T) Albinism Ubatuba (São Paulo) Sazima (1974) 1867) NewTrachycephalus records mesophaeus of morphological 1 (T)anomalies Tail bifurcation in anurans, with a reviewUbatuba for (São Brazil Paulo) Silva and Toledo (2010) 37 Trachycephalus typhonius (Linnaeus, 1 (A) Axial flexure, polymely Undetermined (probably São Paulo) Vizotto et al. (1977) apud Henle 1758) et al. (2017a, b) HYLODIDAE Table 1. Continued. Crossodactylus caramaschii Bastos and 8 (T) Jaw sheaths abnormal, keratinized denticles Itanhaém (São Paulo) Navarro-Lozano et al. (2018) Pombal, 1995 absent Family/species N (Stage) Anomaly Municipality (State) Reference Crossodactylus gaudichaudii Duméril and 4 (A) Cysts Angra dos Reis (Rio de Janeiro) Hatano et al. (2007) Bibron, 1841 Crossodactylus timbuhy Pimenta et al., 1 (J) Ectromely, ectrodactyly, brachydactyly Santa Teresa (Espírito Santo) Mônico et al. (2019) 2014 Hylodes asper (Müller, 1924) 1 (A) Ectromely Santo André (São Paulo) Trevine (2011) Hylodes cardosoi Lingnau et al., 2008 6 (T) Jaw sheaths abnormal, keratinized denticles Morretes (Paraná) Vieira et al. (2012) absent Hylodes dactylocinus Pavan et al., 2001 1 (T) Hyperkeratosis, loss of superficial epidermis, Peruíbe (São Paulo) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Hylodes magalhaesi (Bokermann, 1964) 5 (T) Jaw sheaths abnormal, keratinized denticles Camanducaia (Minas Gerais) Toledo et al. (2006b) absent Hylodes meridionalis (Mertens, 1927) 1 (T) Hyperkeratosis, loss of superficial epidermis, Lauro Müller (Santa Catarina) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Hylodes meridionalis 1 (T) Hyperkeratosis, loss of superficial epidermis, São Francisco de Paula (Rio Grande do Sul) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Hylodes meridionalis 1 (J) Albinism Itati (Rio Grande do Sul) Pereira et al. (2020) Hylodes cf. ornatus 113 (T) Jaw sheaths abnormal, keratinized denticles Jundiaí (São Paulo) Vieira et al. (2013) absent Hylodes perplicatus (Miranda-Ribeiro, 1 (T) Hyperkeratosis, loss of superficial epidermis, São Bento do Sul (Santa Catarina) Toledo et al. (2006a) 1926) remains of keratinized denticles, tooth rows abnormal Hylodes phyllodes Heyer and Cocroft, 1 (T) Hyperkeratosis, loss of superficial epidermis, São Luiz do Paraitinga (São Paulo) Toledo et al. (2006a) 1986 remains of keratinized denticles, tooth rows abnormal Hylodes phyllodes 43 (A) Cysts Angra dos Reis (Rio de Janeiro) Hatano et al. (2007) Hylodes aff. phyllodes 1 (A) Ectromely Santo André (São Paulo) Trevine (2011) Hylodes aff. sazimai Haddad and Pombal, 1 (T) Hyperkeratosis, loss of superficial epidermis, São Luiz do Paraitinga (São Paulo) Toledo et al. (2006a) 1995 remains of keratinized denticles, tooth rows abnormal Megaelosia cf. boticariana 2 (T) Hyperkeratosis, loss of superficial epidermis, Caçapava (São Paulo) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal Megaelosia massarti (De Witte, 1930) 2 (T) Hyperkeratosis, loss of superficial epidermis, Santo André (São Paulo) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal LEPTODACTYLIDAE

Adenomera ajurauna (Berneck et al., 1 (A) Ectrodactyly Santo André (São Paulo) Trevine (2011) 2008) Adenomera marmorata Steindachner, 1 (A) Albinism Recife (Pernambuco) Pereira and Santos (2012) 1867 Adenomera cf. marmorata 1 (A) Brachydactyly Santo André (São Paulo) Trevine (2011) Leptodactylus fuscus (Schneider, 1799) 15 (T) Irregular or double fins, tooth rows Rio Verde (Goiás) Borges et al. (2019) abnormal, keratinized denticles absent, ectromely (amely), anophthalmy, intestinal loop Leptodactylus latrans (Steffen, 1815) 2 (A) Ectromely and/or ectrodactyly --- Amaro and Sena (1968) apud Polymely and/or polydactyly Ouellet (2000) Leptodactylus latrans 1 (T) Albinism Uberlândia (Minas gerais) Rodrigues and Filho (2004) Leptodactylus mystacinus (Burmeister, 1 (A) Brachydactyly Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) 1861) Leptodactylus podicipinus (Cope, 1862) 2 (A) Ectrodactyly, brachydactyly, ectromely Santana (Amapá) Sousa and Costa-Campos (2016) Leptodactylus podicipinus 1 (A) Brachydactyly Macapá (Amapá) Santos et al. (2017) Leptodactylus troglodytes Lutz, 1926 1 (A) Albinism São Lourenço da Mata (Pernambuco) Santos and Silva (2010) Leptodactylus vastus Lutz, 1930 1 (A) Corneal lipidosis São Gonçalo do Amarante, (Ceará) Braga et al. (2013) Physalaemus biligonigerus (Cope, 1861) 1 (A) Ectrodactyly Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) Physalaemus centralis Bokermann, 1962 5 (T) Irregular or double fins, keratinized denticles Rio Verde (Goiás) Borges et al. (2019) absent, ocular alterations (not specified) Physalaemus cuvieri Fitzinger, 1826 14 (A) Brachydactyly, ectrodactyly, ectromely, Mato Castelhano and Sertão (Rio Grande do Ascoli-Morrete et al. (2019) syndactyly, polyphalangy Sul) Physalaemus cuvieri 18 (T) Tooth rows abnormal, keratinized denticles Mineiros and Rio Verde (Goiás) Borges et al. (2019) absent, intestinal loop, nasal asymmetry, ocular alteration (not specified) Physalaemus cuvieri 1 (A) Ectromely São José dos Pinhais (Paraná) This study Physalaemus cuvieri 1 (A) Albinism Morro do Pilar (Minas Gerais) Carvalho et al. (2012) Physalaemus cuvieri 4 (T) Jaw sheaths abnormal, keratinized denticles Itanhaém (São Paulo) Navarro-Lozano et al. (2018) absent Physalaemus aff. gracilis (Boulenger, 25 (A) Brachydactyly, ectrodactyly, ectromely, Mato Castelhano, Passo Fundo and Sertão (Rio Ascoli-Morrete et al. (2019) 1883) syndactyly, polyphalangy, microphthalmy, Grande do Sul) anophthalmy Physalaemus moreirae (Miranda-Ribeiro, 3 (A) Ectromely Santo André (São Paulo) Trevine (2011) 1937) Family/species N (Stage) Anomaly Municipality (State) Reference Physalaemus moreirae 1 (A) Syndactyly Santo André (São Paulo) Trevine (2011) Physalaemus nattereri (Steindachner, 14 (T) Irregular or double fins Rio Verde (Goiás) Borges et al. (2019) 1863) Pseudopaludicola mystacalis (Cope, 1 (A) Flavism (partial) Nísia Floresta (Rio Grande do Norte) Fernandes et al. (2014) 1887) Pseudopaludicola sp. 1 (T) Alteration in oral disc (not specified) Rio Verde (Goiás) Borges et al. (2019) MICROHYLIDAE

Dermatonotus muelleri (Boettger, 1885) 7 (T) Irregular or double fins, absence of dermal Rio Verde (Goiás) Borges et al. (2019) flaps Elachistocleis bicolor (Guérin-Méneville, 1 (A) Brachydactyly Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) 1838) Elachistocleis carvalhoi Caramaschi, 2010 1 (A) Albinism Altamira (Pará) Toledo et al. (2011) Elachistocleis sp. 1 (T) Tail bifurcation Jaboticatubas (Minas Gerais) Silva and Toledo (2010) ODONTOPHRYNIDAE

Odontophrynus americanus (Duméril and 6 (A) Anophthalmy, brachydactyly, ectrodactyly, Mato Castelhano and Sertão (Rio Grande do Ascoli-Morrete et al. (2019) Bibron, 1841) syndactyly Sul) Odontophrynus carvalhoi Savage and Cei, 1 (A) Anophthalmy Guaramiranga (Ceará) Brito et al. (2011) 1965 Odontophrynus maisuma Rosset, 2008 1 (A) Ectrodactyly and brachydactyly Laguna (Santa Catarina) Mônico and Vargas (2020) Proceratophrys appendiculata (Günther, 2 (T) Anophthalmy, microphthalmy, keratinized Teresópolis (Rio de Janeiro) Dias and Carvalho-e-Silva 1873) denticles absent (2012) Physalaemus cuvieri 18 (T) Tooth rows abnormal, keratinized denticles Mineiros and Rio Verde (Goiás) Borges et al. (2019) absent, intestinal loop, nasal asymmetry, ocular alteration (not specified) Physalaemus cuvieri 1 (A) Ectromely São José dos Pinhais (Paraná) This study Physalaemus cuvieri 1 (A) Albinism Morro do Pilar (Minas Gerais) Carvalho et al. (2012) Physalaemus cuvieri 4 (T) Jaw sheaths abnormal, keratinized denticles Itanhaém (São Paulo) Franciele CristinaNavarro-Lozano de Souz et al. (2018)a������� et al. 38 absent Physalaemus aff. gracilis (Boulenger, 25 (A) Brachydactyly, ectrodactyly, ectromely, Mato Castelhano, Passo Fundo and Sertão (Rio Ascoli-Morrete et al. (2019) 1883) syndactyly, polyphalangy, microphthalmy, Grande do Sul) Table 1. Continued. anophthalmy Physalaemus moreirae (Miranda-Ribeiro, 3 (A) Ectromely Santo André (São Paulo) Trevine (2011) 1937) Family/species N (Stage) Anomaly Municipality (State) Reference Physalaemus moreirae 1 (A) Syndactyly Santo André (São Paulo) Trevine (2011) Physalaemus nattereri (Steindachner, 14 (T) Irregular or double fins Rio Verde (Goiás) Borges et al. (2019) 1863) Pseudopaludicola mystacalis (Cope, 1 (A) Flavism (partial) Nísia Floresta (Rio Grande do Norte) Fernandes et al. (2014) 1887) Pseudopaludicola sp. 1 (T) Alteration in oral disc (not specified) Rio Verde (Goiás) Borges et al. (2019) MICROHYLIDAE

Dermatonotus muelleri (Boettger, 1885) 7 (T) Irregular or double fins, absence of dermal Rio Verde (Goiás) Borges et al. (2019) flaps Elachistocleis bicolor (Guérin-Méneville, 1 (A) Brachydactyly Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) 1838) Elachistocleis carvalhoi Caramaschi, 2010 1 (A) Albinism Altamira (Pará) Toledo et al. (2011) Elachistocleis sp. 1 (T) Tail bifurcation Jaboticatubas (Minas Gerais) Silva and Toledo (2010) ODONTOPHRYNIDAE

Odontophrynus americanus (Duméril and 6 (A) Anophthalmy, brachydactyly, ectrodactyly, Mato Castelhano and Sertão (Rio Grande do Ascoli-Morrete et al. (2019) Bibron, 1841) syndactyly Sul) Odontophrynus carvalhoi Savage and Cei, 1 (A) Anophthalmy Guaramiranga (Ceará) Brito et al. (2011) 1965 Odontophrynus maisuma Rosset, 2008 1 (A) Ectrodactyly and brachydactyly Laguna (Santa Catarina) Mônico and Vargas (2020) Proceratophrys appendiculata (Günther, 2 (T) Anophthalmy, microphthalmy, keratinized Teresópolis (Rio de Janeiro) Dias and Carvalho-e-Silva 1873) denticles absent (2012) Proceratophrys appendiculata 1 (J) Polymely Teresópolis (Rio de Janeiro) Dias and Carvalho-e-Silva (2012) Proceratophrys bigibbosa (Peters, 1872) 2 (A) Brachydactyly, ectrodactyly Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019) Proceratophrys boiei (Wied-Neuwied, 1 (A) Brachymely and ectrodactyly São José dos Pinhais (Paraná) This study 1824) Proceratophrys boiei 1 (A) Black-eyed São José dos Pinhais (Paraná) This study Proceratophrys boiei 1 (A) Anophthalmy São José dos Pinhais (Paraná) This study Proceratophrys schirchi (Miranda- 1 (J) Microphtalmy Santa Teresa (Espírito Santo) Mônico et al. (2019) Ribeiro, 1937) PHYLLOMEDUSIDAE Phrynomedusa cf. marginata 1 (T) Hyperkeratosis, loss of superficial epidermis, São Luiz do Paraitinga (São Paulo) Toledo et al. (2006a) remains of keratinized denticles, tooth rows abnormal PIPIDAE

Pipa carvalhoi (Miranda-Ribeiro, 1937) 1 (A) Ectromely São Roque do Canaã (Espírito Santo) Mônico et al. (2016b) RANIDAE

Lithobates catesbeianus (Shaw, 1802) 1 (A) Ectromely São José dos Pinhais (Paraná) This study Lithobates palmipes (Spix, 1824) 1 (A) Albinism Paranaíta (Mato Grosso) Toledo et al. (2011)

Borges et al. (2019) did not detail the type of alterations in each species. We included some anomalies described in the paper when it was possible to identify them. When we did not identify the type of alteration, we maintained a general classification made by the authors: alterations in the oral disc (including interrupted, overlapping, folded, complete or partial absence of the denticles; absence of keratinization in the denticles; denticles of different sizes; as well as alterations of the papillae) or alterations in the tail (including irregular and double fins, ridges in caudal fins, and tail bifurcation).

species), Cycloramphidae (one species), Hylidae (21 oral disc, such as depigmentation of beaks and denticles, species), Hylodidae (11 species), Leptodactylidae (six sheaths and tooth rows abnormal, are attributed to the species), Microhylidae (two species), Odontophrynidae infection by Batrachochytrium dendrobatidis (e.g. (one species), and Phyllomedusidae (one species). Toledo et al., 2006a, b; Vieira et al., 2012, 2013). These reported alterations were related mainly to the Although we cannot determine the causes of the oral disc (complete absence of denticles, absence of observed anomalies, we provide novel observations denticle row, overlap in denticle rows, abnormal or lack in the Amazon and in the . The of keratinization in tooth rows or jaw sheaths, gaps in recorded individual morphological anomalies can denticle rows, absence of dermal flaps, abnormal shape be caused by several factors (Henle et al., 2017a), of denticle rows), tail (double caudal membrane, ridges including unsuccessful attacks by predators (e.g., in the superior and inferior margins of the caudal fins, dragonfly nymphs; Ballengée and Sessions, 2009) tail with bifurcated extremity), amely, anophthalmy, or environmental degradation (e.g., Borges et al., microphthalmy, aphakia, alterations in the intestinal 2019). Nonetheless, new and more detailed studies are loop, nasal asymmetry and albinism (Table 1; this study). necessary to determine the anomaly rates and its effects Torsion in the vertebral column and tail was reported in adult and tadpole populations of the species presented in hybrids of Rhinella icterica and here. (Haddad et al., 1990). Most of the anomalies found in New records of morphological anomalies in anurans, with a review for Brazil 39

Acknowledgments. We are grateful to Museu da Amazônia (Lutz, 1930 Amphibia - Anura: Leptodactylidae). Archives of (MUSA); the entire team of Reserva Florestal Adolpho Ducke: Veterinary Science 18: 470–472. Rubenildo, Rosinaldo, Attman and Maria for field work assistance; Brassaloti, R.A., Bertoluci, J. (2008): Albinism in tadpoles of Projeto Dinâmica Biológica de Fragmentos Florestais (PDBFF) Rhinella ornata (Anura, Bufonidae) from southeastern Brazil. for the assistance and the logistical support during field activities; Herpetological Bulletin 106: 31–33. Michelle Robin for the English revision; Victória D.P. Silva and Brassaloti, R.A., Bertoluci, J. (2018): A case of bilateral Alexssander Camargo by the photographs; Jansen Zuanon, Mirco anophthalmy in an adult Boana faber (Anura: Hylidae) from Solé and Renato Nali for suggestions in the previous version southeastern Brazil. 17: 285–288. of the manuscript; Klaus Henle for suggestions and for permit Brito, L., Aguiar, F., Cascon, P. (2011): Odontophrynus carvalhoi access to a personal database on anuran anomalies; Coordenação (Carvalho’s escuerzo): Malformation. Herpetological Bulletin de Aperfeiçoamento de Pessoal de Nível Supeiror (CAPES, 118: 38–40. Finance code 001); Conselho Nacional de Desenvolvimento Carnaval, A.C.O.Q., Peixoto, O.L. (2004): A new species of Científico e Tecnológico (CNPq) for granting of a PCI-D during Hyla from northeastern Brazil (Amphibia, Anura, Hylidae). 2018 to FCS (process# 314006/2017-6), a doctoral scholarship Herpetologica 60: 387–395. to CSA (process# 141793/2016-3) and a research productivity Carvalho, V.T., Novelle, S.M.H., Lopes, L.P.C., Vogt, R.C. (2008): grant for MM; Fundação de Amparo à Pesquisa do Estado do Sphaenorhynchus dorisae (Spotted Hatchet-faced Treefrog). Amazonas (FAPEAM) for a doctoral scholarship to FCS and Ocular anomaly. 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Accepted by Renato Nali