New records of morphological anomalies in anurans, with a ...

Changes in morphological and anatomical structures of frogs have been reported for centuries (Henle et al., 2017a). Those are called malformations when they occur in cellular and/or transcription processes that directly affect individuals in an initial phase of development (Meteyer, 2000), while the term “deformity” usually indicates alterations of organs or structures that were originally formed correctly. According to Henle et al. (2017b), malformations and deformities are often difficult to tell apart without a detailed study of each case, and hence the authors suggest using the term “anomaly” for this kind of permanent structural defect (Johnson et al., 2001; Henle et al., 2017b). Anomalies in anurans can also be caused by external factors, such as parasitic infections, non-lethal predator attacks, and exposure to chemical pollutants or ultraviolet radiation (Johnson et al., 1999; Ouellet, 2000; Blaustein et al., 2003; Reeves et al., 2013; Henle et al., 2017a; Borges et al., 2019).

Anomalies can affect amphibian populations at different rates. For some species the rate of individuals with deformities or malformations in a healthy population does not exceed 5% (Blaustein and Johnson,

2003). However, morphological alteration rates were higher in agricultural areas when compared to protected areas as a result of damage caused by environmental contaminants (Borges et al., 2019). Additionally, a study of an introduced population of Rhinella jimi (Bufonidae) in an oceanic island in Brazil showed that 52% of the tadpoles and about 45% of the adults exhibited anomalies that were mainly related to oral structures in tadpoles and to hind limbs in adults (Toledo and Ribeiro, 2010; Tolledo et al., 2014). Suggested hypotheses for these higher anomaly rates include parasite or virus infection, environmental contaminants, high level of ultraviolet-B radiation or inbreeding depression (Toledo and Ribeiro, 2010).

The impact of anomalies in amphibian populations has been well documented in North America and in Europe (Henle et al., 2017a), but in Brazil there are fewer anuran anomaly records, published mainly as single event short notes and some articles on population impact evaluations. Herein, we report anomaly observations on adults, newly-metamorphosed individuals and tadpoles of nine anuran species in two localities in central 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 observations in two non-flooded forests (Dense Ombrophilous Forest) in the Reserva Florestal Adolpho Ducke-RFAD (2.5730°S, 60.3724°W) and Dimona Farm- Projeto Dinâmica Biológica de Fragmentos Florestais-PDBFF (2.3904°S, 60.1708°W), both in the municipality of Manaus, Amazonas State, and in one area of Mixed Ombrophilous Forest in the municipality of São José dos Pinhais, Paraná State (Corta Vento Farm; 25.7024°S, 49.0720°W), Brazil. At RFAD adults and tadpoles were captured in the leaf litter of forest floor and in an artificial permanent reservoir at the edge of the forest (vegetation composed by Victoria amazonica (Nymphaeaceae), and Pistia stratiotes (Araceae)). At Dimona Farm, tadpoles were captured

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

1 Programa de Pós-Graduação em Zoologia and Laboratório de Taxonomia e Ecologia de Anfíbios e Répteis, Universidade Federal do Amazonas, 69080-900, Manaus, Amazonas, Brazil.

2 Programa de Pós-Graduação em Zoologia, Laboratório de Biodiversidade, Conservação e Ecologia de Animais Silvestres, Universidade Federal do Paraná, 81531-980, Curitiba, Paraná, Brazil.

3 Programa de Pós-Graduação Biologia de Água Doce e Pesca Interior, Laboratório de Sistemática e Ecologia de Peixes, Instituto Nacional de Pesquisas da Amazônia, 69067-375, Manaus, Amazonas, Brazil.

4 Pontifícia Universidade Católica do Paraná, 80215-901, Curitiba, Paraná, Brazil.

* Corresponding author. E-mail: [email protected]

© 2020 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0.

Franciele Cristina de Souza et al. et al.32

in a natural temporary pond covered by Thurnia sphaerocephala (Thurniaceae), Urospatha sagitifolia (Araceae) and Cyclantus sp. (Cyclanthaceae). At Corta Vento Farm adults were captured in the leaf litter of the forest floor and in two artificial dams in an open area covered by Typhaceae, shrubs, small trees and Rubus niveus (Rosaceae). Adults were captured during the night both manually and with pitfall traps, while tadpoles were collected during the day with a hand net in temporary ponds and artificial reservoirs. Each species was identified according to Hero (1990) and Lima et al. (2012), together with our taxonomic expertise. We measured snout-vent length (SVL) of adults and metamorphosed individuals, and total length (TL) of tadpoles using a ruler (1 mm precision) or calliper (0.05 mm precision). Collected specimens were deposited at the Paulo Bürhnheim Zoological Collection of the Universidade Federal do Amazonas (CZPB-UFAM), section Anuran Larvae (tadpole lots: CZPB-LA 425/892, 426/893, 427/894) and at the Zoological Collection of Universidade Federal do Paraná (UFPR). We also extensively revised the literature in the search for malformations/deformities/anomalies in anurans (adults and tadpoles) in Brazil. Our definitions of malformations/anomalies follow Toledo and Ribeiro (2010), Tolledo et al. (2014) and Henle et al. (2017b). When inconsistencies were detected, we used Henle et al. (2017b). Ectromely was used for a partial or complete absence of a limb, and amely (one or several limbs completely lacking) was treated as a subcategory of ectromely; breaks, gaps and ridges in the denticles rows was treated as “tooth rows abnormal”; alterations in jaw sheaths was treated as “jaw sheaths abnormal” (Henle et al., 2017b).

In total, we observed anomalies in 12 individuals (tadpole, juveniles and adults) of nine anuran species: Allobates femoralis (Boulenger, 1884) (N = 1 newly-metamorphosed individual, SVL = 10.80 mm), Boana geographica (Spix, 1824) (N = 1 newly-metamorphosed individual, SVL = 21 mm), Rhinella proboscidea (Spix, 1824) (N = 1 tadpole, TL = 12.60 mm), Lithobates catesbeianus (Shaw, 1802) (N = 1 adult not collected), Physalaemus cuvieri Fitzinger, 1826 (N = 1 adult not collected), Proceratophrys boiei (Wied-Neuwied, 1824) (N = 3 adults, SVL = 42.2 and 43.1 mm, one individual not collected), Rhinella abei (Baldisseri et al., 2004) (N = 1 adult, SVL = 35.6 mm), Rhinella marina (Linnaeus, 1758) (N = 2, one tadpole and one newly metamorphosed individual, TL = 10.86 and SVL = 9.55, respectively), and Scinax fuscovarius (Lutz, 1925) (N = 1 non-collected adult).

Allobates femoralis (Fig. 1A) and a tadpole of R. marina (Fig. 1B) presented ectromely (amely) of the left forelimb and left hindlimb, respectively, where there was no evidence of the limbs. The newly-metamorphosed individual of B. geographica (Fig. 1C) parasitized by the ectoparasitic crustacean Argulus sp. was obtained in the laboratory by rearing it from a pre-metamorphic stage. After metamorphosis, we found anomalies in the pelvic girdle bones (extension and curvature of the right ilium) and skin membrane or skin fusion (fusion of the skin restricting limb movement) (Fig. 2), but we cannot ascertain that the parasite caused the observed anomalies. One individual of P. boiei (Fig. 1D) and one of R. abei (Fig. 1E) presented black-eyed. Absence of the left eyeball (anophthalmy) was detected in an adult P. boiei (Fig. 1F) and in a tadpole of R. proboscidea (Fig. 1G). Ectromely was observed in four species and was divided in two categories: ectromely of tibiafibula, with the left foot absent in L. catesbeianus (Fig. 1H), and ectromely of radius and ulna with the left hand absent in P. cuvieri (Fig. 1I), S. fuscovarius (Fig. 1J) and R. marina (Fig. 1K). Lastly, another individual of P. boiei (Fig. 1L) presented shortening of the right hindlimb, characterized as brachymely with ectrodactyly of toes.

In addition to our 12 observations we found 148 anomaly records on anuran adults, juveniles and tadpoles in Brazil in scientific literature (Table 1). The literature records and our observations encompass 104 species of 13 families (Aromobatidae, Brachycephalidae, Bufonidae, Craugastoridae, Cycloramphidae, Hylidae, Hylodidae, Leptodactylidae, Microhylidae, Odontophrynidae, Phyllomedusidae, Pipidae, and Ranidae; Frost, 2020). Anomalies occurred across all Brazilian regions, but were concentrated in the South and Southeast regions. Hylidae was the family with the highest number of records (67 records in 40 species), followed by Leptodactylidae (24 records, 16 species), Bufonidae (23 records, 13 species), Hylodidae (18 records, 14 species) Odontophrynidae (10 records, seven species), Microhylidae (four records, four species), Brachycephalidae (four records, two species), Aromobatidae (three records, two species), Cycloramphidae (two records, two species), Ranidae (two records and two species), Craugastoridae, Phyllomedusidae, and Pipidae (one record and one species in each family). In general, these records are based on single event observations, but few studies estimated the impacts of anomalies on anuran populations, and are based on a great number of individuals (e.g. Toledo and Ribeiro, 2010; Tolledo

et al., 2014; Ascoli-Morrete et al., 2019; Borges et al., 2019). Our data added anomaly records for four new species (R. abei, R. proboscidea, P. boiei, and L. catesbeianus) to North and South Brazilian regions. Although the Amazon occupies more than 60% of the

Brazilian territory and harbours many frog species (about 330 species; Hoogmoed and Galatti, 2019), the presence of anomalies were previously reported for only 14 of them (Table 1).

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.

New records of morphological anomalies in anurans, with a review for Brazil 33

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 et al., 2017a).

Considering tadpoles (Table 1), we found 58 records 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).

Figure 2. X-ray image of an individual of Boana geographica (Hylidae) showing anomaly in the bones of the pelvic girdle and skin webbing. Photo: Victória D. Pereira e Silva.



Table 1. Continued.Rhinella icterica 11 (A) Brachydactyly, ectrodactyly, ectromely,

syndactyly, polymely, Sertão and Passo Fundo (Rio Grande do Sul) Ascoli-Morrete et al. (2019)

Family/species N (Stage) Anomaly Municipality (State) Reference

Rhinella jimi (Stevaux, 2002) 9 (J), 62 (A)

Microcephaly, brachygnathia, deformed tympanum, black-eyed, perforated eye, 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

Archipelago of Fernando de Noronha (Pernambuco)

Toledo and Ribeiro (2010)

Rhinella jimi 217 (T) Jaw sheaths abnormal; keratinized denticles absent; absence of jaw sheaths, tooth rows, labia; duplication of the teeth, stunted teeth, intersecting tooth rows; abnormal shape in the tooth rows

Archipelago of Fernando de Noronha (Pernambuco)

Tolledo et al. (2014)

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, polydactyly

Ilha Bailique, Macapá (Amapá) Bessa-Silva et al. (2016)

Rhinella ornata (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 (A)

Brachydactyly, phalangeal hypertrophy, brachymely, ectrodactyly, polydactyly, curved bones, ectromely, tarsus hypertrophy

Ilha da Marambaia, Ilha de Itacuruçá, Ilha Grande, Seropédica and Mangaratiba (Rio de Janeiro)

Rebouças et al. (2019)

Rhinella proboscidea (Spix, 1824) 1 (T) Anophthalmy Manaus (Amazonas) This study

CRAUGASTORIDAE

Pristimantis reichlei Padial and De la Riva, 2009

1 (A) Eye colouration abnormal Senador Guiomard (Acre) Melo-Sampaio (2015)

CYCLORAMPHIDAE Thoropa miliaris (Spix, 1824) 1 (A) Ectrodactyly Santa Teresa (Espírito Santo) Mônico et al. (2019)

Toropa thaophora (Miranda-Ribeiro, 1923)

1 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

Ubatuba (São Paulo) Toledo et al. (2006a)

HYLIDAE Aparasphenodon arapapa Pimenta et al.,

2009 5 (J) Heterochromia, eye coloration abnormal Ilhéus (Bahia) Lourenço-de-Moraes et al.

(2013)

Aplastodiscus albosignatus (Lutz and Lutz, 1938)

130 (T) Jaw sheaths abnormal, keratinized denticles absent

Itanhaém (São Paulo) Navarro-Lozano et al. (2018)

Aplastodiscus albosignatus 1 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

Camanducaia (Minas Gerais) Toledo et al. (2006a)

Aplastodiscus cf. leucopygius 2 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

São Luiz do Paraitinga (São Paulo) Toledo et al. (2006a)

Aplastodiscus leucopygius (Cruz and Peixoto, 1985)

1 (A) Ectromely Santo André (São Paulo) Trevine (2011)

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, remains of keratinized denticles, tooth rows abnormal

Rio Claro (São Paulo) Toledo et al. (2006a)

Boana albopunctata 27 (T) Tail bifurcation, keratinized denticles absent Mineiros (Goiás) Borges et al. (2019)

Boana albopunctata 33 (T) Jaw sheaths abnormal, keratinized denticles absent


Boana boans (Linnaeus, 1758) 1 (A) Back legs paralyzed, urostyle broken, deformed ileum, broken leg, scars

Manaus (Amazonas) Magnusson et al. (1999)

Boana faber (Wied-Neuwied, 1821) 1 (T) Jaw sheaths abnormal, keratinized denticles absent

Morretes (Paraná) Vieira et al. (2012)

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 absent


Boana fasciata (Günther, 1858) 2 (A) Anophthalmy Boca do Acre (Amazonas) and Buriti do Tocantins (Tocantins)

Ramalho et al. (2017)

Boana freicanecae (Carnaval and Peixoto, 2004)

40 (T) Jaw sheaths abnormal, keratinized denticles absent, tooth rows abnormal

Jaqueira (Pernambuco) Carnaval and Peixoto (2004)

Boana geographica (Spix, 1824) 1 (J) Anomaly in the bones of the pelvic girdle, cutaneous fusion

Manaus (Amazonas) This study

Boana geographica 1 (A) Sacrum asymmetric Undetermined (Amazonas) Peloso (2016) Boana leptolineata (Braun and Braun,

1977) 2 (A) Missing adhesive disc, ectrodactyly Sertão and Passo Fundo (Rio Grande do Sul) Ascoli-Morrete et al. (2019)

Boana pulchella (Duméril and Bibron, 1841)

1 (A) Ectrodactyly Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019)


Boana semilineata (Spix, 1824) 1 (T) Hyperkeratosis, loss of superficial epidermis, 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, remains of keratinized denticles, tooth rows abnormal

Petropólis (Rio de Janeiro) Toledo et al. (2006a)

Bokermannohyla hylax (Heyer, 1985) 1 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal


Bokermannohyla hylax 1 (A) Mandibular hypoplasia Santo André (São Paulo) Trevine (2011)

Bokermannohyla martinsi (Bokermann, 1964)

22 (T) Tail lesions Catas Altas (Minas Gerais) Lima et al. (2015)

Bokermannohyla nanuzae (Bokermann and Sazima, 1973)


Bokermannohyla saxicola (Bokermann, 1964)

1 (T) Tail bifurcation Ubatuba (São Paulo) Silva and Toledo (2010)

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 asymmetric

Rio de Janeiro (Rio de Janeiro) Prigioni and Langone (1985)

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 Bibron, 1841)

1 (A) Jaw shape abnormal Santa Teresa (Espírito Santo) Mônico et al. (2016a)

Lysapsus bolivianus Gallardo, 1961 1 (A) Anophthalmy Macapá (Amapá) Sousa and Costa-Campos (2017)


Table 1. Continued.Boana leptolineata (Braun and Braun,

1977) 2 (A) Missing adhesive disc, ectrodactyly Sertão and Passo Fundo (Rio Grande do Sul) Ascoli-Morrete et al. (2019)

Boana pulchella (Duméril and Bibron, 1841)

1 (A) Ectrodactyly Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019)


Boana semilineata (Spix, 1824) 1 (T) Hyperkeratosis, loss of superficial epidermis, 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, remains of keratinized denticles, tooth rows abnormal

Petropólis (Rio de Janeiro) Toledo et al. (2006a)

Bokermannohyla hylax (Heyer, 1985) 1 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal


Bokermannohyla hylax 1 (A) Mandibular hypoplasia Santo André (São Paulo) Trevine (2011)

Bokermannohyla martinsi (Bokermann, 1964)


Bokermannohyla nanuzae (Bokermann and Sazima, 1973)


Bokermannohyla saxicola (Bokermann, 1964)

1 (T) Tail bifurcation Ubatuba (São Paulo) Silva and Toledo (2010)

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 asymmetric

Rio de Janeiro (Rio de Janeiro) Prigioni and Langone (1985)

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 Bibron, 1841)

1 (A) Jaw shape abnormal Santa Teresa (Espírito Santo) Mônico et al. (2016a)

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, remains of keratinized denticles, tooth rows abnormal

Petrópolis (Rio de Janeiro) Toledo et al. (2006a)

Ololygon aromothyella (Faivovich, 2005) 1 (A) Abnormal pigment, brachydactyly, ectrodactyly

Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019)

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 Bibron, 1841)

1 (A) Anophthalmy Plácido de Castro (Acre) Ramalho et al. (2017)

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 (absence of eye lens), sub-development (small amorphous and not emerged eye)

Ipiguá and Mirassol (São Paulo) Sánchez-Domene et al. (2018)

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 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, 1867)

1 (T) Albinism Ubatuba (São Paulo) Sazima (1974)

Trachycephalus mesophaeus 1 (T) Tail bifurcation Ubatuba (São Paulo) Silva and Toledo (2010)

Trachycephalus typhonius (Linnaeus, 1758)

1 (A) Axial flexure, polymely Undetermined (probably São Paulo) Vizotto et al. (1977) apud Henle et al. (2017a, b)

HYLODIDAE Crossodactylus caramaschii Bastos and

Pombal, 1995 8 (T) Jaw sheaths abnormal, keratinized denticles

absent Itanhaém (São Paulo) Navarro-Lozano et al. (2018)


Crossodactylus gaudichaudii Duméril and Bibron, 1841

4 (A) Cysts Angra dos Reis (Rio de Janeiro) Hatano et al. (2007)

Crossodactylus timbuhy Pimenta et al., 2014

1 (J) Ectromely, ectrodactyly, brachydactyly Santa Teresa (Espírito Santo) Mônico et al. (2019)

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 absent


Hylodes dactylocinus Pavan et al., 2001 1 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

Peruíbe (São Paulo) Toledo et al. (2006a)

Hylodes magalhaesi (Bokermann, 1964) 5 (T) Jaw sheaths abnormal, keratinized denticles absent

Camanducaia (Minas Gerais) Toledo et al. (2006b)

Hylodes meridionalis (Mertens, 1927) 1 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

Lauro Müller (Santa Catarina) Toledo et al. (2006a)

Hylodes meridionalis 1 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

São Francisco de Paula (Rio Grande do Sul) Toledo et al. (2006a)

Hylodes meridionalis 1 (J) Albinism Itati (Rio Grande do Sul) Pereira et al. (2020)

Hylodes cf. ornatus 113 (T) Jaw sheaths abnormal, keratinized denticles absent

Jundiaí (São Paulo) Vieira et al. (2013)

Hylodes perplicatus (Miranda-Ribeiro, 1926)


São Bento do Sul (Santa Catarina) Toledo et al. (2006a)

Hylodes phyllodes Heyer and Cocroft, 1986



Hylodes phyllodes 43 (A) Cysts Angra dos Reis (Rio de Janeiro) Hatano et al. (2007)

New records of morphological anomalies in anurans, with a review for Brazil 37Trachycephalus mesophaeus (Hensel,

1867) 1 (T) Albinism Ubatuba (São Paulo) Sazima (1974)

Trachycephalus mesophaeus 1 (T) Tail bifurcation Ubatuba (São Paulo) Silva and Toledo (2010)

Trachycephalus typhonius (Linnaeus, 1758)

1 (A) Axial flexure, polymely Undetermined (probably São Paulo) Vizotto et al. (1977) apud Henle et al. (2017a, b)

HYLODIDAE Crossodactylus caramaschii Bastos and

Pombal, 1995 8 (T) Jaw sheaths abnormal, keratinized denticles

absent Itanhaém (São Paulo) Navarro-Lozano et al. (2018)


Crossodactylus gaudichaudii Duméril and Bibron, 1841

4 (A) Cysts Angra dos Reis (Rio de Janeiro) Hatano et al. (2007)

Crossodactylus timbuhy Pimenta et al., 2014

1 (J) Ectromely, ectrodactyly, brachydactyly Santa Teresa (Espírito Santo) Mônico et al. (2019)

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 absent


Hylodes dactylocinus Pavan et al., 2001 1 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

Peruíbe (São Paulo) Toledo et al. (2006a)

Hylodes magalhaesi (Bokermann, 1964) 5 (T) Jaw sheaths abnormal, keratinized denticles absent

Camanducaia (Minas Gerais) Toledo et al. (2006b)

Hylodes meridionalis (Mertens, 1927) 1 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

Lauro Müller (Santa Catarina) Toledo et al. (2006a)

Hylodes meridionalis 1 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

São Francisco de Paula (Rio Grande do Sul) Toledo et al. (2006a)

Hylodes meridionalis 1 (J) Albinism Itati (Rio Grande do Sul) Pereira et al. (2020)

Hylodes cf. ornatus 113 (T) Jaw sheaths abnormal, keratinized denticles absent

Jundiaí (São Paulo) Vieira et al. (2013)

Hylodes perplicatus (Miranda-Ribeiro, 1926)


São Bento do Sul (Santa Catarina) Toledo et al. (2006a)

Hylodes phyllodes Heyer and Cocroft, 1986



Hylodes phyllodes 43 (A) Cysts Angra dos Reis (Rio de Janeiro) Hatano et al. (2007)

Table 1. Continued.

Hylodes aff. phyllodes 1 (A) Ectromely Santo André (São Paulo) Trevine (2011)

Hylodes aff. sazimai Haddad and Pombal, 1995



Megaelosia cf. boticariana 2 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

Caçapava (São Paulo) Toledo et al. (2006a)

Megaelosia massarti (De Witte, 1930) 2 (T) Hyperkeratosis, loss of superficial epidermis, remains of keratinized denticles, tooth rows abnormal

Santo André (São Paulo) Toledo et al. (2006a)

LEPTODACTYLIDAE Adenomera ajurauna (Berneck et al.,

2008) 1 (A) Ectrodactyly

Santo André (São Paulo) Trevine (2011)

Adenomera marmorata Steindachner, 1867

1 (A) Albinism Recife (Pernambuco) Pereira and Santos (2012)

Adenomera cf. marmorata 1 (A) Brachydactyly Santo André (São Paulo) Trevine (2011)

Leptodactylus fuscus (Schneider, 1799) 15 (T) Irregular or double fins, tooth rows abnormal, keratinized denticles absent, ectromely (amely), anophthalmy, intestinal loop

Rio Verde (Goiás) Borges et al. (2019)

Leptodactylus latrans (Steffen, 1815) 2 (A) Ectromely and/or ectrodactyly Polymely and/or polydactyly

--- Amaro and Sena (1968) apud Ouellet (2000)

Leptodactylus latrans 1 (T) Albinism Uberlândia (Minas gerais) Rodrigues and Filho (2004)

Leptodactylus mystacinus (Burmeister, 1861)

1 (A) Brachydactyly Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019)

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 absent, ocular alterations (not specified)

Rio Verde (Goiás) Borges et al. (2019)

Physalaemus cuvieri Fitzinger, 1826 14 (A) Brachydactyly, ectrodactyly, ectromely, syndactyly, polyphalangy

Mato Castelhano and Sertão (Rio Grande do Sul)

Ascoli-Morrete et al. (2019)

Physalaemus cuvieri 18 (T) Tooth rows abnormal, keratinized denticles absent, intestinal loop, nasal asymmetry, ocular alteration (not specified)

Mineiros and Rio Verde (Goiás) Borges et al. (2019)

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 absent


Physalaemus aff. gracilis (Boulenger, 1883)

25 (A) Brachydactyly, ectrodactyly, ectromely, syndactyly, polyphalangy, microphthalmy, anophthalmy

Mato Castelhano, Passo Fundo and Sertão (Rio Grande do Sul)


Physalaemus moreirae (Miranda-Ribeiro, 1937)



Physalaemus moreirae 1 (A) Syndactyly Santo André (São Paulo) Trevine (2011)

Physalaemus nattereri (Steindachner, 1863)

14 (T) Irregular or double fins Rio Verde (Goiás) Borges et al. (2019)

Pseudopaludicola mystacalis (Cope, 1887)

1 (A) Flavism (partial) Nísia Floresta (Rio Grande do Norte) Fernandes et al. (2014)

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

flaps Rio Verde (Goiás) Borges et al. (2019)

Elachistocleis bicolor (Guérin-Méneville, 1838)

1 (A) Brachydactyly Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019)

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

Bibron, 1841) 6 (A) Anophthalmy, brachydactyly, ectrodactyly,

syndactyly Mato Castelhano and Sertão (Rio Grande do Sul)


Odontophrynus carvalhoi Savage and Cei, 1965

1 (A) Anophthalmy Guaramiranga (Ceará) Brito et al. (2011)

Odontophrynus maisuma Rosset, 2008 1 (A) Ectrodactyly and brachydactyly Laguna (Santa Catarina) Mônico and Vargas (2020)

Proceratophrys appendiculata (Günther, 1873)

2 (T) Anophthalmy, microphthalmy, keratinized denticles absent

Teresópolis (Rio de Janeiro) Dias and Carvalho-e-Silva (2012)

species), Cycloramphidae (one species), Hylidae (21 species), Hylodidae (11 species), Leptodactylidae (six species), Microhylidae (two species), Odontophrynidae (one species), and Phyllomedusidae (one species). These reported alterations were related mainly to the oral disc (complete absence of denticles, absence of denticle row, overlap in denticle rows, abnormal or lack of keratinization in tooth rows or jaw sheaths, gaps in denticle rows, absence of dermal flaps, abnormal shape of denticle rows), tail (double caudal membrane, ridges in the superior and inferior margins of the caudal fins, tail with bifurcated extremity), amely, anophthalmy, microphthalmy, aphakia, alterations in the intestinal loop, nasal asymmetry and albinism (Table 1; this study). Torsion in the vertebral column and tail was reported in hybrids of Rhinella icterica and Rhinella crucifer (Haddad et al., 1990). Most of the anomalies found in

oral disc, such as depigmentation of beaks and denticles, sheaths and tooth rows abnormal, are attributed to the infection by Batrachochytrium dendrobatidis (e.g. Toledo et al., 2006a, b; Vieira et al., 2012, 2013).

Although we cannot determine the causes of the observed anomalies, we provide novel observations in the Amazon and in the Atlantic Forest. The recorded individual morphological anomalies can be caused by several factors (Henle et al., 2017a), including unsuccessful attacks by predators (e.g., dragonfly nymphs; Ballengée and Sessions, 2009) or environmental degradation (e.g., Borges et al., 2019). Nonetheless, new and more detailed studies are necessary to determine the anomaly rates and its effects in adult and tadpole populations of the species presented here.


Table 1. Continued.

Physalaemus cuvieri 18 (T) Tooth rows abnormal, keratinized denticles absent, intestinal loop, nasal asymmetry, ocular alteration (not specified)

Mineiros and Rio Verde (Goiás) Borges et al. (2019)

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 absent


Physalaemus aff. gracilis (Boulenger, 1883)

25 (A) Brachydactyly, ectrodactyly, ectromely, syndactyly, polyphalangy, microphthalmy, anophthalmy

Mato Castelhano, Passo Fundo and Sertão (Rio Grande do Sul)


Physalaemus moreirae (Miranda-Ribeiro, 1937)



Physalaemus moreirae 1 (A) Syndactyly Santo André (São Paulo) Trevine (2011)

Physalaemus nattereri (Steindachner, 1863)

14 (T) Irregular or double fins Rio Verde (Goiás) Borges et al. (2019)

Pseudopaludicola mystacalis (Cope, 1887)

1 (A) Flavism (partial) Nísia Floresta (Rio Grande do Norte) Fernandes et al. (2014)

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

flaps Rio Verde (Goiás) Borges et al. (2019)

Elachistocleis bicolor (Guérin-Méneville, 1838)

1 (A) Brachydactyly Mato Castelhano/Sertão (Rio Grande do Sul) Ascoli-Morrete et al. (2019)

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

Bibron, 1841) 6 (A) Anophthalmy, brachydactyly, ectrodactyly,

syndactyly Mato Castelhano and Sertão (Rio Grande do Sul)


Odontophrynus carvalhoi Savage and Cei, 1965

1 (A) Anophthalmy Guaramiranga (Ceará) Brito et al. (2011)

Odontophrynus maisuma Rosset, 2008 1 (A) Ectrodactyly and brachydactyly Laguna (Santa Catarina) Mônico and Vargas (2020)

Proceratophrys appendiculata (Günther, 1873)

2 (T) Anophthalmy, microphthalmy, keratinized denticles absent

Teresópolis (Rio de Janeiro) Dias and Carvalho-e-Silva (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, 1824)

1 (A) Brachymely and ectrodactyly São José dos Pinhais (Paraná) This study

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-Ribeiro, 1937)

1 (J) Microphtalmy Santa Teresa (Espírito Santo) Mônico et al. (2019)

PHYLLOMEDUSIDAE

Phrynomedusa cf. marginata 1 (T) Hyperkeratosis, loss of superficial epidermis, 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).

Acknowledgments. We are grateful to Museu da Amazônia (MUSA); the entire team of Reserva Florestal Adolpho Ducke: Rubenildo, Rosinaldo, Attman and Maria for field work assistance; Projeto Dinâmica Biológica de Fragmentos Florestais (PDBFF) for the assistance and the logistical support during field activities; Michelle Robin for the English revision; Victória D.P. Silva and Alexssander Camargo by the photographs; Jansen Zuanon, Mirco Solé and Renato Nali for suggestions in the previous version of the manuscript; Klaus Henle for suggestions and for permit access to a personal database on anuran anomalies; Coordenação de Aperfeiçoamento de Pessoal de Nível Supeiror (CAPES, Finance code 001); Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for granting of a PCI-D during 2018 to FCS (process# 314006/2017-6), a doctoral scholarship to CSA (process# 141793/2016-3) and a research productivity grant for MM; Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM) for a doctoral scholarship to FCS and financial support in the preparation of the manuscript (PosGrad FAPEAM 2019); and Instituto Chico Mendes de Conservação da Biodiversidade for collection permits (SISBIO/ICMBio # 53377-1, 61852-1, 40224-3, 9247-1, 72946).

References

Alves, J., Mônico, A.T., Vasconcelos, L., Silva-Soares, T. (2018): Rhinella schneideri (Sapo-boi; Cururu Toad) Hindlimb malformation. Herpetological Review 49: 312.

Amaro, A., Sena, S. (1968): Ocorrências de anomalias em anfíbios. Atas da Sociedade de Biologia do Rio de Janeiro 12: 95–96.

Araújo, K.C., Cavalcante, L.A., Oliveira, D.B., Andrade, E.B. (2020): Axanthism in the treefrog Dendropsophus minutus (Anura: Hylidae) from a montane forest relict in Northeastern Brazil. Herpetology Notes 13: 257–259.

Ascoli-Morrete, T., Signor, E., Santos-Pereira, M., Zanella, N. (2019): Morphological abnormalities in anurans from southern Brazil. Austral Ecology 44: 1025–1029.

Ballengée, B., Sessions, S.K. (2009): Explanation for missing limbs in deformed amphibians. Journal of Experimental Zoology, Part B, Molecular and Developmental Evolution 312B: 770–779.

Barros, L.P.V., Muniz, R.F., Kloss-Degen, J.P., Castro, T.M., Oliveira, J.C.F., Rocha, C.F.D. (2018): Albinism in a juvenile of Rhinella crucifer Wied-Neuwied, 1821 (Anura: Bufonidae) from southeastern Brazil. Herpetology Notes 11: 599–600.

Bessa-Silva, A.R., Vallinoto, M., Sodré, D., Cunha, D.B., Hadad, D., Asp, N.E. et al. (2016): Patterns of genetic variability in island populations of the Cane Toad (Rhinella marina) from the mouth of the Amazon. PLoS ONE 11: e0152492.

Blaustein, A.R., Johnson, P.T.J. (2003): The complexity of deformed amphibians. Frontiers in Ecology and Environment 1: 87–94.

Blaustein, A.R., Romansic, J.M., Kiesecker, J. M., Hatch, A.C. (2003): Ultraviolet radiation, toxic chemicals and amphibian population declines. Diversity and Distributions 9: 123–140.

Borges, R.E., Santos, L.R.S., Assis, R.A., Benvindo-Souza, M., Franco-Belussi, L., Oliveira, C. (2019): Monitoring the morphological integrity of Neotropical anurans. Environmental Science and Pollution Research 26: 2623–2634.

Braga, R.R., Bezerra, C.H., Leite, M.J.B., Rodrigues, J.F.M., Borges-Nojosa, D.M. (2013): Lipidose corneal em Leptodactylus vastus

(Lutz, 1930 Amphibia - Anura: Leptodactylidae). Archives of Veterinary Science 18: 470–472.

Brassaloti, R.A., Bertoluci, J. (2008): Albinism in tadpoles of Rhinella ornata (Anura, Bufonidae) from southeastern Brazil. Herpetological Bulletin 106: 31–33.

Brassaloti, R.A., Bertoluci, J. (2018): A case of bilateral anophthalmy in an adult Boana faber (Anura: Hylidae) from southeastern Brazil. Phyllomedusa 17: 285–288.

Brito, L., Aguiar, F., Cascon, P. (2011): Odontophrynus carvalhoi (Carvalho’s escuerzo): Malformation. Herpetological Bulletin 118: 38–40.

Carnaval, A.C.O.Q., Peixoto, O.L. (2004): A new species of Hyla from northeastern Brazil (Amphibia, Anura, Hylidae). Herpetologica 60: 387–395.

Carvalho, V.T., Novelle, S.M.H., Lopes, L.P.C., Vogt, R.C. (2008): Sphaenorhynchus dorisae (Spotted Hatchet-faced Treefrog). Ocular anomaly. Herpetological Review 39: 211–212.

Carvalho Jr, R.R., Araújo, S.R., Pereira, L.K. (2012): Physalaemus cuvieri (Cuvier’s Foam Froglet). Albinism. Herpetological Review 43: 468–469.

Correia, L.L., Almeida, J.P.F.A., Lisboa, B.S., Nascimento, F.A.C. (2018): Brachydactyly in the toad Rhinella granulosa (Bufonidae) from the Caatinga of Brazil: a rare case with all limbs affected. Herpetology Notes 11: 445–448.

Dias, P.H.S., Carvalho-e-Silva, A.M.P.T. (2012): Records of abnormalities in Proceratophrys appendiculata (Günther, 1873) (Anura; Cycloramphidae; Alsodinae). Herpetology Notes 5: 197–199.

Di-Bernardo, M., Maneyro, R., Grillo, H. (2006): New species of Melanophryniscus (Anura: Bufonidae) from Rio Grande do Sul, Southern Brazil. Journal of Herpetology 40: 261–266.

Faria, M.D., Ribeiro, L.B., Nicola, P.A., Pereira, L.C.M., Gradela, A., Constantino, A.C. (2018): Absence of the right forelimb in Corythomantis greeningi Boulenger, 1896: case report. Acta Veterinaria Brasilica 12: 45–48.

Fernandes, V., Magalhães, F.M., Pererira, T.C.S.O., Santana, D.J. (2014): Pseudopaludicola mystacalis. Coloration. Herpetological Review 45: 114.

Ferreira, R.B., Zocca, C.Z., Mageski, M.M., Lírio, F.C.F. (2014): Rhinella crucifer (Sapo Cururuzinho; Striped Toad). Hindlimb malformation. Herpetological Review 45: 307.

Frost, D.R. (2020): Amphibian Species of the World: an Online Reference. Version 6.1. Available at: https://amphibiansoftheworld.amnh.org/index.php. Accessed on 20 September 2020.

Haddad, C.F.B., Cardoso, A.J., Castanho, L.M. (1990): Hibridação natural entre Bufo ictericus e Bufo crucifer (Amphibia: Anura). Revista Brasileira de Biologia 50: 739–744.

Hatano, F.H., Gettinger, D., Van Sluys, M., Rocha, C.F.D. (2007): Parasitism of Hylodes phyllodes (Anura: Cycloramphidae) by Hannemania sp. (Acari: Trombicuudae) in an area of Atlantic Forest, Ilha Grande, southeastern Brazil. Parasite 14: 107–112.

Henle, K., Dubois, A., Vershinin, V. (2017a): A review of anomalies in natural populations of amphibians and their potential causes. Mertensiella 25: 57–164.

Henle, K., Dubois, A., Vershinin, V. (2017b): Commented glossary, terminology and synonymies of anomalies in natural populations of amphibians. Mertensiella 25: 9–48.


Hero, J.M. (1990): An illustrated key to tadpoles occurring in the Central Amazon rainforest, Manaus, Amazonas, Brasil. Amazoniana 11: 201–262.

Hoogmoed, M.S., Galatti, U. (2019): Censo da Biodiversidade da Amazônia Brasileira – MPEG: Anura. Available at http://www.museugoeldi. br/censo/. Accessed on 16 May 2020.

Johnson, P.T. J., Lunde, K.B., Ritchie, E. G., Launer, A.E. (1999): The effect of trematode infection on amphibian limb development and survivorship. Science 284: 802–804.

Johnson, P.T.J., Lunde, K.B., Ritchie, E.G., Reaser, J.L., Launer, A.E. (2001): Morphological abnormality patterns in a California amphibian community. Herpetologica 57: 336–352.

Jorgewich-Cohen, G., Cavalcanti, I.R.S., Kanasiro, A. (2019): Abnormalities in hylid frogs: a case study of schizodactyly in the striped snouted treefrog, Scinax squalirostris (Lutz, 1925) (Amphibia: Anura: Hylidae). Herpetology Notes 12: 1015–1018.

Lima, A.P., Magnusson, W.E., Menin, M., Erdtmann, L.K., Rodrigues, D.J., Keller, C., Hödl, W. (2012): Guia de Sapos da Reserva Adolpho Ducke, Amazônia Central / Guide to the Frogs of the Reserva Adolpho Ducke, Central Amazonia. 2nd. ed. Manaus, Brazil, Editora INPA.

Lima, R.C.L., Dias, J.E.M., Lima, N.G.S., Torres, P.F., Eterovick, P.C. (2015): Escape response of tadpoles of two species of Bokermannohyla (Anura, Hylidae) to simulated threat. Journal of Herpetology 49: 176–183.

Lourenço-de-Moraes, R., Lantyer-Silva, A.S.F., Toledo, L.F., Solé, M. (2013): Tadpole, oophagy, advertisement call, and geographic distribution of Aparasphenodon arapapa Pimenta, Napoli and Haddad 2009 (Anura, Hylidae). Journal of Herpetology 47: 575–579.

Lutz, B. (1973): Brazilian species of Hyla. Austin and London, University of Texas Press.

Magalhães, F.M., Juncá, F.A., Garda, A.A. (2015): Tadpole and vocalisations of Phyllodytes wuchereri (Anura: Hylidae) from Bahia, Brazil. Salamandra 51: 83–90.

Magnusson, W.E., Lima, A.P., Hero, J.-M., Araújo, M.C. (1999): The rise and fall of a population of Hyla boans: reproduction in a neotropical gladiator Frog. Journal of Herpetology 33: 647–656.

Melo-Sampaio, P.R. (2015): Pristimantis reichlei. Eye coloration. Herpetological Review 46: 614.

Meteyer, C.U. (2000): Field guide to malformations of frogs and toads with radiographic interpretations. Biological Science Report USGS/BRD/BSR–2000–0005: 1–16.

Mira-Mendes, C.V., Rios, C.H.V. (2016): Hypsiboas semilineatus. Leucism. Herpetological Review 47: 277.

Mônico, A.T., Ferreira, R.B., Lauvers, W.D., Mattos, R.O., Clemente-Carvalho, R.B.G. (2016a): Itapotihyla langsdorffii (Perereca Castanhola; Ocellated Treefrog). Head abnormality. Herpetological Review 47: 278–279.

Mônico, A.T., Silva-Soares, T., Clemente-Carvalho, R.B.G. (2016b): Pipa carvalhoi (Carvalho’s Surinam Toad; Sapo d’água). Hindlimb malformation. Herpetological Review 47: 115.

Mônico, A.T., Silva-Soares, T., Koch, E.D. (2019): Malformation in three anuran species from a preserved remnant of Atlantic Forest

in southeastern Brazil. Neotropical Biology and Conservation 14: 213–220.

Mônico, A.T., Vargas, N.D. (2020): Odontophrynus maiuma. Hindlimb malformation. Herpetological Review 51: 567–568.

Moraes, L.J.C.L., Kaefer, I.L. (2015): Leucism in the Amazonian diurnal frog Anomaloglossus stepheni (Martins, 1989) (Anura: Aromobatidae). Herpetology Notes 8: 179–181.

Navarro-Lozano, A., Sánchez-Domene, D., Rossa-Feres, D.C., Bosch, J., Sawaya, R.J. (2018): Are oral deformities in tadpoles accurate indicators of anuran chytridiomycosis? PLoS ONE 13: 1–9.

Oliveira-Souza, A.E., Lima, P.H.G., Afonso, D.D., Santana, M.M.S., Pinheiro, R.T, Pedroso-Santos, F., et al. (2020): First record of polymelia in the Paradox Frog Pseudis paradoxa (Linnaeus, 1758) from Northern Brazil. International Journal of Zoology and Animal Biology 3: 1–3.

Ouellet, M. (2000): Amphibian deformities: current state of knowledge. In: Ecotoxicology of Amphibians and Reptiles, p. 617–661. Sparling, D.W., Linder, G., Bishop, C.A., Krest S.K., Eds., Pensacola, SETAC Technical Publications Series.

Pasquarelli, P., Mendes, E.G., Costacurta, L. (1981): Natural polymely in the toad Bufo ictericus ictericus Spix, 1824 (Amphibia-Anura). Zoologische Anzeiger 206: 292–296.

Peloso, P.L.V. (2016): Osteological malformation in the tree frog Hypsiboas geographicus (Anura: Hylidae). Phyllomedusa 15: 91–93.

Pereira, E.N., Santos, E.M. (2012): Leptodacylus aff. marmoratus. Albinism. Herpetological Review 43: 323.

Pereira, D., Freire, M.D., Ferrari, L., Colombo, P. (2020): Hylodes meridionalis (Torrent Frog). Albinism. Herpetological Review 51: 98–99.

Pirani, M.R., Moura, M.R. (2012): Scinax fuscomarginatus (Brown-bordered Snouted Treefrog). Amelia. Herpetological Review 43: 471–472.

Prigioni, C.M., Langone, J.A. (1985): Anomalias anatomicas registradas en anfibios de la coleccion herpetologica del Museo Nacional de Historia Natural. Actas de las Jornadas de Zoologia del Uruguay 1: 73–75.

Ramalho, W.P., Maffei, F., Guerra, V., Silva, D.P., Matos, L.R.A., Vieira, L.J.S. (2017): Anophthalmia in adults of two Amazonian treefrogs (Anura: Hylidae). The Herpetological Bulletin 139: 43–44.

Rebouças, R., Silva, H.R., Solé, M. (2019): Malformations in insular and coastal populations of toads in Rio de Janeiro, Southeastern Brazil. South American Journal of Herpetology 14: 12–18.

Reeves, M.K., Medley, K.A., Pinkney, A.E., Holyoak, M., Johnson, P.T.J., Lannoo, M.J. (2013): Localized hotspots drive continental geography of abnormal amphibians on U.S. wildlife refuges. PLoS ONE 8: 1–14.

Rodrigues, A.P., Oliveira Filho, J.C. (2004): Leptodactylus ocellatus (Rã-manteiga). Tadpole albinism. Herpetological Review 35: 373.

Salles, R.O.L., Xisto, T., Ferreira, T., Nascimento, B. (2013): Albinism in a tadpole of Hypsiboas albomarginatus (Spix, 1824) (Anura: Hylidae) from Southeastern Brazil. Herpetology Notes 6: 577–578.


Sambon, L.W. (1928): The parasitic acarians of animals and the part they play in the causation of the eruptive fevers and other diseases of man. Annals of Tropical Medicine & Parasitology 22: 67–132.

Sánchez-Domene, D., Navarro-Lozano, A., Acayaba, R., Picheli, K., Montagner, C., Rossa-Feres, D.C., et al. (2018): Eye malformation baseline in Scinax fuscovarius larvae populations that inhabit agroecosystem ponds in southern Brazil. Amphibia-Reptilia 39: 325–334.

Santos, E.M., Silva, T.C.B. (2010): Albinismo parcial em Leptodactylus troglodytes (Amphibia, Anura, Leptodactylidae). Boletim do Museu de Biologia Mello Leitão (Nova Série) 28: 159–163.

Santos, F.P, Sanches, P.R, Sousa, J.C., Costa-Campos, C.E. (2017): Morphological abnormality in Leptodactylus podicipinus (Cope, 1862) (Anura: Leptodactylidae) in an urban area of north Brazil, Eastern Amazon. Boletín de la Asociación Herpetológica Española 28: 70–72.

Santos, S.P.L., Amorim, F.O., Santos, E.M. (2010): Hypsiboas semilineatus (NCN). Albinism. Herpetological Review 41: 474.

Sazima, I. (1974): An albino hylid frog, Phrynohyas mesophaea (Hensel). Journal of Herpetology 8: 264–265.

Silva, N.R., Toledo, L.F. (2010): Bokermannohyla saxicola (NCN), Scinax curicica (Lanceback Treefrog), Scinax squalirostris (Snouted Treefrog), Trachycephalus mesophaeus (Golden-eyed Treefrog), and Elachistocleis sp. (Oval Frog). Morphology. Herpetological Review 41: 333–334.

Silva-Soares, T., Mônico, A. (2017): Hind limb malformation in the tree frog Corythomantis greeningi (Anura: Hylidae). Phyllomedusa 16: 117–120.

Sousa, J.C., Costa-Campos, C.E. (2016): Leptodactylus podicipinus (Pointedbelly Frog). Malformations. Herpetological Review 47: 112–113.

Sousa, J.C., Costa-Campos, C.E. (2017): Records of ocular anomaly in two species of anurans in the eastern Amazon region. Herpetology Notes 10: 413–415.

Tavares-Pinheiro, R., Costa-Campos, C.E., Kaefer, I.L. (2020): A leucistic brilliant-thighed poison frog Allobates femoralis (Dendrobatoidea). Herpetology Notes 13: 321–323.

Toledo, L.F., Britto, F.B., Araújo, O.G.S., Giasson, L.M.O., Haddad, C.F.B. (2006a): The occurrence of Batrachochytrium dendrobatidis in Brazil and the inclusion of 17 new cases of infection. South American Journal of Herpetology 1: 185–191.

Toledo, L.F., Haddad, C.F.B., Carnaval, A.O.C.Q., Britto, F.B. (2006b): A Brazilian anuran (Hylodes magalhaesi: Leptodactylidae) infected by Batrachochytrium dendrobatidis: a conservation concern. Amphibian and Reptile Conservation 4: 17–21.

Toledo, L.F., Ribeiro, R. S. (2010): The Archipelago of Fernando de Noronha: an intriguing malformed toad hotspot in South America. EcoHealth 6: 351–357.

Toledo, L.F., Silva, N.R., Araújo, O.G.S. (2011): Albinism in two Amazonian frogs: Elachistocleis carvalhoi (Microhylidae) and Lithobates palmipes (Ranidae). Herpetology Notes 4: 145–146.

Tolledo, J., Silva, E.T., Nunes-de-Almeida, C.H.L., Toledo, L.F. (2014): Anomalous tadpoles in a Brazilian oceanic archipelago: implications of oral anomalies on foraging behaviour, food intake and metamorphosis. Herpetological Journal 24: 237–243.

Trevine, V.C. (2011): Levantamento da Herpetofauna do Parque Natural Municipal Nascentes de Paranapiacaba, Santo André, SP. Unpublished Master’s thesis, Universidade Estadual Paulista Júlio de Mesquita Filho, Rio Claro, Brazil.

Vieira, C.A., Almeida, C.H.L.N., Lambertini, C., Leite D. S., Toledo, L.F. (2012): First record of Batrachochytrium dendrobatidis in Paraná, Brazil. Herpetological Review 43: 93–94.

Vieira, C.A., Toledo, L.F., Longcore, J.E., Longcore, J.R. (2013): Body length of Hylodes cf. ornatus and Lithobates catesbeianus tadpoles, depigmentation of mouthparts, and presence of Batrachochytrium dendrobatidis are related. Brazilian Journal Biology 73: 195–199.

Vizotto, L.D., Taddei, V.A., Cais, A. (1977): Pseudomelia em Phyrnohyas hebes (Cope, 1862) (Anura-Hylidae). Naturalia 3: 35–43.

Voitena, J.F., Pastore, I., Prokoski, K., Filadepho, A.L., Birck, A.J., Afonso, A.M., et al. (2013): Polimelia em sapo-boi (Rhinella paracnemis): Relato de caso. Revista Científica Eletrônica de Medicina Veterinária 11: 1–9.

Accepted by Renato Nali


New records of morphological anomalies in anurans, with a ...

Documents

Transcript of New records of morphological anomalies in anurans, with a ...