Westernmost Record of the Fringed Leaf Frog, Cruziohyla Craspedopus (Funkhouser, 1957) (Anura: Phyllomedusidae) in Brazil

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Herpetology Notes, volume 13: 1021-1024 (2020) (published online on 14 December 2020)

Westernmost record of the Fringed Leaf Frog, Cruziohyla craspedopus (Funkhouser, 1957) (Anura: Phyllomedusidae) in Brazil

Wirven Lima da Fonseca1,2, Igor Oliveira3, Radraque Rodrigues Correa1, Andesson de Souza Oliveira1, Reginaldo Assêncio Machado1, and Paulo Sérgio Bernarde1,*

The genus Cruziohyla Faivovich, Haddad, Garcia, to low branches to breed, laying eggs on vegetation Frost, Campbell, and Wheeler 2005 comprises three overhanging water-filled cavities in logs (Hoogmoed forest species (C. calcarifer, C. craspedopus and and Cadle, 1991; Rodriguez and Duellman, 1994; C. sylviae) distributed through Caribbean slopes of Block et al., 2003). Due to its singular habitat use, C. Honduras Nicaragua, Costa Rica and Panama in craspedopus is poorly sampled in the Brazilian Amazon, Central America, and Pacific lowlands of Colombia and being known to few localities (Moraes and Pavan, Ecuador, in South America (Frost, 2019). The Fringed 2017). Venancio et al. (2014) recorded this species Leaf Frog Cruziohyla craspedopus was described by in the municipality of Tarauacá in the state of Acre. Funkhouser (1957), from Chicherota, Rio Bobonaza, Herein we report C. craspedopus occurring in the Alto province of Pastaza (Ecuador). Its common name refers Juruá Valley, Acre state, being the westernmost record to the extensive skin flanges present on its limbs (Gray, of Brazil, and extends the nearest known location of 2018). This species is distinguishable by having lavender Tarauacá (Venancio et al., 2014) by 152.67 kilometres. green dorsum with scattered irregular, lichenous, greyish On 19 March 2019, we found one male individual of white spots; all ventral surfaces of fringes and the belly C. craspedopus (snout-vent length [SVL] = 53 mm) are bright yellow or orange-yellowblack; pronounced (7.6232ºS, 72.7882ºW) during a fieldwork study in the calcars are present on the flanks and legs; and the iris river Moa, Cruzeiro do Sul, Acre state, Brazil (Fig. 1). is bicoloured, with a silvery-grey centre contoured by This individual was on shrub branches (Fig. 2) at 1.5 m yellow-orange (Hoogmoed and Cadle, 1991; Rodriguez and Duellman, 1994). Cruziohyla craspedopus occurs in Amazonian lowlands of Colombia, Ecuador, Peru, and Brazil (Frost, 2019). This frog species inhabits the canopy of the lowland rainforest most of the time, and walks down

1 Laboratório de Herpetologia, Centro Multidisciplinar, Campus Floresta, Universidade Federal do Acre, Cruzeiro do Sul, Acre, 69980000, Brazil. 2 Programa de Pós-graduação em Ecologia e Manejo de Recursos Naturais, Universidade Federal do Acre, Rio Branco, Acre, 69920900, Brazil. 3 EtnoLab - Etnociências, Ecologia e Conservação, Centro de Educação e Letras, Campus Floresta, Universidade Federal Figure 2. Adult male of Cruziohyla craspedopus recorded do Acre, Cruzeiro do Sul, Acre, 69980000, Brazil. in Cruzeiro do Sul, Acre state, Brazil. Photograph by Paulo * Corresponding author. E-mail: [email protected] Bernarde. 1022 Wirven Lima da Fonseca et al.

Figure 1. Occurrence map of Cruziohyla craspedopus in Brazil. � �� Mato Grosso (Rodrigues et al., 2011); 3 = Porto Velho, Rondônia (Meneghelli et al., 2011); 4 = Tarauacá, Acre (Venancio et al., 2014); 5 = Jacareanga, Pará (Bitar et al., 2015); 6 = Itaituba, Pará (Moraes and Pavan, 2017); Red star = Cruzeiro do Sul, Acre (This study). ��dor and Peru.

high. The locality is a seasonally flooded floodplain area 2000, Pristimantis aureolineatus (Guayasamin, Ron, with canopy about 20-35 m (Bernarde et al., 2011). Cisneros-Heredia, Lamar, and McCracken, 2006, Based on the existent records (Moraes and Pavan, Ranitomeya ventrimaculata (Shreve, 1935)] that use the 2017) it is possible to notice that C. craspeopus is upper canopy stratum are under estimated (Guayasamin broadly distributed through the Amazonian areas in a et al. 2006). Anuran species’ richness of Alto Juruá variety of habitats. The species is currently known to region that were previously known are: 126 species at occur in the southern, eastern, central, and western Serra do Divisor National Park (Souza, 2009), 80 at portions of the Amazon, in a range from 70 to 240 m Riozinho da Liberdade Extractive Reserve (Bernarde et above sea level (Venancio et al., 2014; Moraes and al., 2011), 57 at Porto Walter (Fonseca et al., 2019), and Pavan, 2017). Commonly, registers of C. craspedopus 50 species at the present locality (Bernarde et al., 2013). are occasional and occur during breeding events on However, C. craspedopus was not recorded in these the rainy season when individuals are observed in previous studies, evidencing the difficulty on sampling amplexus or calling activities (Table 1). We observed the species. this species in a floodplain area, a type of habitat where Although C. craspedopus is probably more abundant C. craspedopus was not previously reported, and also than showed by previous records, this species not during a breeding event. The rarity of this species distribution is influenced by its own biological features, is probably due to its behaviour of spending most of the such as specificities of habitat use and breeding activity time in the forest canopy (Hoogmoed and Cadle, 1991; that may limit populational increase (Hogmoed and Rodriguez and Duellman, 1994; Block et al., 2003). Cadle, 1991; Turrel et al., 2016). Habitats often used by Several studies with amphibians in tropical forests show C. craspedopus are phytotelm water-filled cavities in that the lower stratum is the most commonly sampled, hollow logs, and depressions at ground level (Hogmoed and therefore some species [e.g., Osteocephalus and Cadle, 1991; Rodrigues et al., 2011; Turrel et al., deridens Jungfer, Ron, Seipp, and Almendáriz, 2000, 2016; Moraes and Pavan, 2017). Rodrigues et al. (2011) O. fuscifacies Jungfer, Ron, Seipp, and Almendáriz, and Moraes and Pavan (2017) recorded clutches and Westernmost record of the Fringed Leaf Frog in Brazil 1023 1

Table 1. Occurrence records of Cruziohyla craspedopus in Brazil. Table 1. Occurrence records of Cruziohyla craspedopus in Brazil.

Locality Coordinates* Habitat Site Breeding Months Municipality of Castanho, km 3.3547oS, 59.8605oW Forest On a hollow log above a water- Pair in amplexus February 22 on the BR319 road – AM1 filled cavity São Nicolau farm, municipality 9.8547oS, 58.2494oW Primary forest Inside a bucket of pitfall trap Pair in amplexus September and of Cotriguaçu – MT and clutches December (200 m a.s.l.)2 Estação Ecológica do Cuniã – 8.1065oS, 63.4833oW Primary forest On a large leaf of Caranaí palm Male calling November RO (87 m a.s.l.)3 (Lepidocaryum tenue Mart.) 180 cm above a temporary pond Tarauacá – AC (240m a.s.l.)4 7.9781oS, 71.4517oW Primary forest On a palm leaf, at approximately 4 Male calling January m height, near a large temporary pond Jacareanga – PA5 6.0885oS, 57.6831oW Upland forest On a palm leaf at 1.5 m from the Juvenile April ground specimen Parque Nacional da Amazônia, 4.7077°S, 56.4414°W Terra Firme forest Inside a bucket of pitfall trap Pair in amplexus October Itaituba – PA (70 m a.s.l.)6

Baixo Rio Moa, Cruzeiro do 7.6232ºS; 72.7882ºW Floodplain forest On shrub branches at 1.5 m high Male not calling March Sul – AC (188 m a.s.l.)7 * The coordinates were transformed from the original data of each article using the WGS84 Datum; 1 = Lima et al. (2003); 2 = Rodrigues et al. (2011); 3 = Meneghelli et al. (2011); 4 = Venancio et al. (2014); 5 = Bitar et al. (2015); 6 = Moraes and Pavan (2017); 7 = this study.

mating pairs in pitfall buckets and covers that were filled currently under a population decline process (Ângulo with rainwater. This is evidence that, although this type et al., 2004), which makes studies on distribution and of trap is designed to sample anurans from litter, arboreal ecology of this species of paramount. species may be also occasionally captured (e.g., Boana geographica, Trachycephalus cunauaru, Scinax ruber, Acknowledgements. We are thankful for the funding provided by Phyllomedusa tomopterna, and P. vaillanti; Bernarde Coordenação de Aperfeiçoamento de Pessoal de Nível Superior and Macedo, 2008). In such cases, these species are - Brasil (CAPES) - Finance Code 001 and Federal University of Acre (EDITAL UFAC/PROPEG Nº 03/2018 - Institutional likely searching for shelter or breeding sites (Rodrigues support for research groups), to CNPq by the Institutional et al., 2011; Moraes and Pavan, 2017). Turrel et al. Scientific Initiation Scholarship Program (PIBIC/UFAC), authors (2016) studied a population of C. craspedopus in Madre RRC and ASO, and to Marcelo Nogueira de Carvalho Kokubum de Dios, Peru, by using artificial breeding sites. The for the corrections and suggestions on the manuscript. We thank behaviour of C. craspedopus of living in forest canopies the Instituto Chico Mendes de Conservação da Biodiversidade and its reproductive pattern seem to be determinant for (ICMBio) for providing collection permits (SISBIO/12.178). its rarity in sample activities. However, this species actually may have wider geographical distribution than References currently known (Hoogmoed and Cadle, 1991; Turrel Ângulo, A., Coloma, L.A., Ron, S., Hoogmoed, M., Castro, F., et al., 2016). Sample methods designed to optimise Rueda, J.V., et al. (2004): Cruziohyla craspedopus.�� the vertical cover of tropical forest strata have the Red List of Threatened Species. Available at: http://www. potential to improve our comprehension on amphibian iucnredlist.org/ details/55291/0. Accessed on 10 April 2019. Bernarde, P.S., Macedo, L.C. (2008): Impacto do desmatamento e communities of such environments (Guayasamin et formação de pastagens sobre a anurofauna de serapilheira em al., 2006). However, having access to forest canopy is Rondônia. Iheringia 98(4): 454–459. a dangerous activity for researchers and also requires Bernarde, P.S., Machado, R.A., Turci, L.C.B. (2011): Herpetofauna specific and expensive training (Turrel et al., 2016). da área do Igarapé Esperança na Reserva Extrativista Riozinho Owing to this, such methods are rarely applied, da Liberdade, Acre – Brasil. Biota Neotropica 11(3): 117–144. resulting in sample bias. To investigate the reproductive Bernarde, P.S., Albuquerque, S., Miranda, D.B., Turci, L.C.B. biology of elusive species as C. craspedopus, the use of (2013): Herpetofauna da floresta do baixo rio Moa em Cruzeiro do Sul, Acre – Brasil. Biota Neotropica 13(1): 220–244. artificial breeding sites placed in occurring localities of Bitar, Y.O.C., Silva, K.R.A., Filho, H.F.S., Pinheiro, L.C. the species seems to be a promising approach (Turrel (2015): Amphibia, Anura, Hylidae, Cruziohyla craspedopus et al., 2016). Moreover, although C. craspedopus is (Funkhouser, 1957): distribution extension and first record from currently considered “least concern” by IUCN, it is the state of Pará, Brazil. �� 11(2): 1–3. 1024 Wirven Lima da Fonseca et al.

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Accepted by Andre Bruinjé