Herpetology Notes, volume 13: 613-620 (2020) (published online on 05 August 2020)
Natural history notes of Sphaenorhynchus carneus (Cope, 1868) (Anura: Hylidae: Sphaenorhynchini) in the eastern Brazilian Amazon
Juliana Gonçalves Corrêa1, Pedro Ferreira França1, Carlos Eduardo Costa-Campos2,*, and Ricardo Alexandre Kawashita-Ribeiro1,3
Abstract. Sphaenorhynchus carneus is a small hylid distributed throughout the upper Amazon Basin. We carried out the fieldwork between June 2015 and May 2016, in a floodplain area in district of Ariri, municipality of Macapá, state of Amapá, Brazil. We conducted visual encounter and acoustic surveys during the day and night in five linear transects. We collected 98 individuals of S. carneus (86 adult males, 8 females, and 4 juveniles). Formicidae was the more abundant and frequent prey category in the stomachs of S. carneus (IRI = 82.15%). We found adult males, gravid females, and spawns from February to August, the rainy season in the region. Sphaenorhynchus carneus has diurnal and nocturnal activity. We observed calling males near females, usually on perches 15 cm higher than females. The distance between vocalising males varied from 30 cm to 2 m. The reproduction of species is related to the reproductive mode 1, with spawn composed of a single gelatinous translucent mass with a mean of 199 eggs (157 to 291) deposited on floating aquatic macrophytes. Studies in new localities should be carried out to allow a better understanding of the biology of this little-known species.
Keywords. Amapá, diet composition, trophic ecology, reproductive behaviour
Introduction years the knowledge about the most varied ecological aspects of anurans has significantly increased, Diet and reproduction traits are important aspects information concerning the natural history of many of the life history of amphibians that help us to plan species is still scarce. conservation strategies and management actions The genus Sphaenorhynchus Tschudi, 1838 currently (Duellman and Trueb, 1994; Verdade et al., 2012). comprises 14 species (sensu Araujo-Vieira et al., 2020) Anuran diet is mainly composed by arthropods and other of small greenish treefrogs widespread in the Amazon invertebrates (Toledo, 2005; Vitt and Caldwell, 2014). and Orinoco basins, and in the Brazilian Atlantic Forest They also have one of the most complex behavioural (Araujo-Vieira et al., 2019; 2020). Sphaenorhynchus repertoires and the highest diversity of reproductive carneus (Cope, 1868) is a small species (15–22.5 mm mode among vertebrates (Haddad and Prado, 2005; of snout-vent length in adults) that inhabits the floating Wells, 2007; Leivas et al., 2018). Although in the last vegetation interface zone of lentic environments, but can also live in permanent or temporary pools (Araujo- Vieira et al., 2019). The species is widely distributed in the upper Amazon Basin in southern Colombia, Peru, Ecuador, and, in Brazil, in the states of Amazonas and 1 Programa de Pós-Graduação em Biodiversidade, Universidade Amapá (Azevedo-Ramos et al., 2004; Corrêa et al., Federal do Oeste do Pará, Rua Vera Paz, s/n (Unidade 2015; Frost, 2020). Tapajós), 68040-255, Santarém, Pará, Brazil. Information about the natural history of S. carneus is 2 Laboratório de Herpetologia, Departamento de Ciências limited to some studies reporting acoustical parameters Biológicas e da Saúde, Universidade Federal do Amapá, of the advertisement call and calling sites (Höld, 1977, Rodovia JK Km 2, 68903-419, Macapá, Amapá, Brazil. Toledo et al., 2014), oviposition site (Bokermann, 1973; 3 Instituto de Ciências e Tecnologia das Águas, Universidade Federal do Oeste do Pará, Rua Vera Paz, s/n (Unidade Crump, 1974; Höld pers. comm. in Araujo-Vieira et Tapajós), 68040-255, Santarém, Pará, Brazil. al., 2019), notes on diet (Duellman, 1978; Rodriguez * Corresponding author. E-mail: [email protected] and Duellman, 1994), description of tadpoles (Suárez- 614 Juliana Gonçalves Corrêa et al.
Mayorga and Lynch, 2001), and distribution extensions data was obtained from Núcleo de Hidrometereologia e (Corrêa et al., 2015; Ramalho et al., 2016). Until Energias Renováveis/Instituto de Pesquisas Científicas now, the conservation status of S. carneus is listed in e Tecnológicas do Estado do Amapá (NHMET/IEPA) the IUCN as Least Concern (Azevedo-Ramos et al., database. 2004). Herein, we provide data on diet composition and Voucher specimens were killed with a 2% lidocaine reproduction of a population of S. carneus in an Amazon overdose, fixed in 10% formalin, and conserved in 70% basin area in the state of Amapá, northern Brazil, eastern alcohol (authorisation ICMBio/SISBio license #45990- Amazon Forest. 1). The specimens are housed in the Herpetological Collection of Universidade Federal do Amapá (CECC Material and Methods 0188–0257; 1143–1168). Pairs in amplexus were captured and maintained in plastic bags to collect Study area.—We collected data from a floodplain in spawns. The clutches obtained were preserved in 5% the district of Ariri (0.2993°N, 51.1298°W) located formalin and had eggs counted. near the Km 33 on the BR 156 highway, north of the municipality of Macapá, state of Amapá. The area is Data analysis.—For the diet analysis, we used 94 flooded by the Matapí river basin and is composed of individuals (86 males and 8 females) and performed Amazonian savannah with large areas of gallery forest an abdominal dissection on each of them to remove the and floodplains forest (Silva et al., 2016). The climate stomach and extract the available content. We identified is Equatorial (Am) following Koppen’s classification each prey item with a stereomicroscope at order level (Alvares et al., 2013). The region is going through an and, when possible, at lower taxonomic categories, intense urbanisation process, whereby most of its forest using the identification keys available in Rafael et cover was affected. al. (2012). Ants were identified at subfamily level following Baccaro et al. (2015). Preys were confirmed Identification.—We distinguished S. carneus from by the entomologist Raimundo N.P. Souto from the other sympatric species that occur in the study area, Laboratory of Arthropods. Prey items in advanced especially S. lacteus (Daudin, 1800), by the following stages of digestion were considered as unidentifiable. combination of characters: 1) snout-vent length varying We measured the length (l) and width (w) in from 15 to 18 mm in males and 22 to 23 mm in females; millimetres (mm) of intact segment of a prey and 2) pale green dorsal colouration with a golden stripe, calculated their volumes (V) using the ellipsoid delimited above and below by brown-reddish lines from formula (Colli et al., 1992). We calculated numerical the posterior corner of eye to the groin; 3) ventral region and volumetric percentages of each prey type for each and vocal sac whitish green; 4) armpit and groin pale individual. The index of relative importance (IRI) for blue; 5) iris silvery, with elliptical pupil; 6) fingers and each prey category was calculated using data obtained toes yellowish green (Rodriguez and Duellman, 1994). from the mean of the percentage of prey occurrence Data collection.—Fieldwork was conducted from (F%), numerical percentage (N%), and volumetric June 2015 to May 2016 including months from the rain percentage (V%) (see Pinkas et al., 1971). We used (December to August) and dry season (September to regression analysis between snout-vent length (SVL) in November). We sampled five linear transects of 250 m millimetres (mm) and the volume of stomach contents of extension at distance of 500 m during the day (15:00 (total volume of preys consumed for each individual) to 17:00 h) and night (18:00 to 20:00 h) using visual to test whether larger frogs were able to consume more encounter and acoustic surveys (Crump and Scott-Jr, preys or larger preys. All analyses were made using 1994). Five observers slowly walked in each transect Systat 12.0 software (Systat, 2007). recording all individuals observed, calling males and For the reproductive modes, we used the methodology others species in activity. Searching effort corresponded and classification proposed by Haddad and Prado to 4 person-hours per day and per transect. The transects (2005). Calling sites were characterised, for each had the same sampling effort of 20 person-hours, total male, considering substrate type (shrub, arboreal, or of 240 person-hours. terrestrial), position of the individual in relation to the We identified adults of S. carneus by the presence of water surface, height of the vocalisation site in relation vocal sacs in males and oocytes in females. In addition, to the water surface, distance to margin and between other sympatric species were registered for a community vocalising males. characterisation of the study area. The climatological We counted the number of eggs per spawn and thirty Natural history notes of Sphaenorhynchus carneus in the eastern Brazilian Amazon 615 eggs per clutch had their diameters measured with an ocular micrometre (0.01 mm precision) in a Zeiss stereomicroscope (see Hartmann et al., 2010).
Results We captured a total of 98 individuals of S. carneus (86 males, 8 females, and 4 juveniles), with the lowest number of individuals being recorded in February (N = 1) and the highest number in May 2016 (N = 23). Adult individuals of S. carneus were recorded only during the rainy season (July to August 2015 and February to May 2016; Fig. 1). Figure 1. Adults (males and females) and juveniles of Among the analysed stomachs, 21 were empty. Sphaenorhynchus carneus recorded in floodplain of district We found 587 preys belonging to three categories: Ariri, municipality of Macapá, state of Amapá, Brazil, in Coleoptera, Diptera, and Hymenoptera (Table 1). relation to rainfall variation during the years 2015-2016. Formicidae were the most abundant and frequent item in the stomach of S. carneus (N% = 96.11%, IRI = 82.15%). We did not find a significant correlation between SVL and size of the volume of stomach contents (R2 = 0.214, at 15:00 h and lasting until 20:00 h (Table 2). During p = 0.836). daylight hours, only Lysapsus bolivianus Gallardo, Sphaenorhynchus carneus have diurnal and nocturnal 1961 used the same calling sites as S. carneus. At activity, with emission of acoustic signals beginning night, S. carneus calling activity diminished, and other
Table 1. Food items of the diet of the Sphaenorhynchus carneus from floodplain of the Ariri District, municipality of Macapá, state of Amapá. Prey abundance of (N); Relative abundance of prey (N%); Prey occurrence frequency (F); Relative frequency of prey occurrence (F%); Prey volume (V); Relative volume prey (V%); Relative importance index (IRI).
3UH\FDWHJRU\ 1 1 ) ) 9 9 ,5, &ROHRSWHUD +\GURSKLOLGDH 'LSWHUD +\PHQRSWHUD )RUPLFLGDH 0\UPLFLQDH &HSKDORWHVVS &UHPDWRJDVWHUVS 2FKHWRP\UPH[VS 6ROHQRSVLVVS )RUPLFLQDH 1\ODQGHULDVS 'ROLFKRGHULQDH 7DSLQRPDPHODQRFHSKDOXP 3VHXGRP\UPLFLQDH 3VHXGRP\UPH[IHUUXJLQHD 3VHXGRP\UPH[VLPSOH[ 3VHXGRP\UPH[WHUPLWDULXV 3RQHULQDH 7RWDO 616 Juliana Gonçalves Corrêa et al.
Table 2. Calling activity of Sphaenorhynchus carneus from floodplain of the district of Ariri, municipality of Macapá, state of Amapá.
+RXUPRQWK -XQ -XO $XJ 6HS 2FW 1RY 'HF -DQ )HE 0DU $SU 0D\ 7RWDO
species that used the same calling sites of the floodplain (Poaceae), Leersia hexandra Sw. (Poaceae) up to 30 cm area [e.g. Pseudis paradoxa (Linnaeus, 1758) and higher than the water surface or in aquatic macrophytes Sphaenorhynchus lacteus] continued their calling Nymphoides indica (L.) Kuntze (Menyanthaceae) and activities. We recorded six species of sympatric anurans Salvinia auriculata Aubl (Salviniaceae), for a distance calling in the water margin and five species using the up to six meters from the margin (Fig. 2A, B). adjacent floodplain as calling sites (Table 3). Sphaenorhynchus carneus has the reproductive Males were observed emitting advertisement calls (see mode 1 (oviposition and tadpoles development Hödl, 1977; Toledo et al., 2014) near females generally occurring in lentic environments). Males did not actively on perches 15 cm higher than those with females. In the search for females and did not exhibit parental care. absence of females, distance between vocalising males Neither territorial competition nor amplexus dispute varied from 30 cm to 2 m. We observed adult males, was observed between males. Amplexus in S. carneus gravid females, and spawns of S. carneus from February is axial and female oviposition sites are on emergent to August, which corresponds to the rainy season in the vegetation composed of Nymphoides indica (L.) region (Table 3). Kuntze (Menyanthaceae) and Salvinia auriculata Aubl Adult males were found calling perched on Thalia (Salviniaceae) (Fig. 2 C, D, E, F). Spawn comprised of a geniculata L. (Marantaceae), Luziola spruceana Benth single gelatinous translucent mass deposited in floating
Table 3. Calling timings for Sphaenorhynchus carneus and sympatric anuran species in the floodplain of the district of Ariri, municipality of Macapá, state of Amapá. * Anuran species of that use the same vocalization site of Sphaenorhynchus carneus.
+RXU 6SHFLHV 6SKDHQRUK\QFKXVFDUQHXV 6FLQD[JDUEHL 3VHXGLVSDUDGR[D /\VDSVXVEROLYLDQXV 6SKDHQRUK\QFKXVODFWHXV %RDQDUDQLFHSV 3VHXGRSDOXGLFRODEROLYLDQD 6FLQD[UXEHU 'HQGURSVRSKXVFIZDOIRUGL /HSWRGDFW\OXVDIISRGLFLSLQXV /HSWRGDFW\OXVIXVFXV /HSWRGDFW\OXVPDFURVWHUQXP Natural history notes of Sphaenorhynchus carneus in the eastern Brazilian Amazon 617
Figure 2. Calling (A – B) and oviposition (C) sites, gravid female (D), and egg-masses (E – F) of Sphaenorhynchus carneus from floodplain of the district of Ariri, municipality of Macapá, state of Amapá. Adult male of Sphaenorhynchus carneus calling perched on (A) Luziola spruceana Benth (Poaceae) (specimen CECC 1946) and (B) aquatic macrophyte Nymphoides indica (L.) (specimen CECC 1958). (C) Site of oviposition. (D) Gravid female (SVL 16.5 mm; CECC 1984). (E anG F) Egg-masses in different stages of development, located on the emergent vegetation Nymphoides indica (L.) Kuntze (Menyanthaceae).
aquatic macrophytes and we recorded spawns in June Discussion and August 2015 and April to May 2016 (Table 4). The Sphaenorhynchus carneus fed on a low variety of number of eggs per clutch ranged from 157 to 291 eggs invertebrates. The species mainly preys upon ants, (199.7 ± 38.7 eggs, n = 8), positively related to SVL (R2 which suggests that S. carneus uses the active foraging = 0.16, p < 0.05) and the diameter of the eggs ranged strategy. Our results corroborate that S. carneus is an from 0.94 to 1.52 mm (1.21 ± 0.14 mm, n = 30). ant specialist anuran (sensu Toft, 1980, 1981), as has 618 Juliana Gonçalves Corrêa et al.
Table 4. Records of the reproductive period of influence of rainfall seasonality reproductive activity, as Sphaenorhynchus carneus in the floodplain of the district has been widely reported for anurans in the Neotropical Ariri, municipality of Macapá, state of Amapá. Filled cells region (Hödl, 1990). However, in the dry season, when (grey) indicate presence. rainfall was low and the floodplain area was completely
dry, we did not record any individuals vocalising or )LHOG $GXOWPDOHV *UDYLGIHPDOHV $PSOH[XV 6SDZQV engaging in reproduction. At the beginning of the -XQ rainy season, two males were recorded and spawning -XO began at the study site, indicating that the reproductive $XJ 6HS season had begun for the species and emphasising the 2FW rainy influence as an important factor in reproductive 1RY periodicity. 'HF In the study area, species sympatric with S. carneus -DQ also show seasonal influence on reproductive activity. )HE In the rainy season, the only species phylogenetically 0DU close to S. carneus that use emergent plants and aquatic $SU 0D\ macrophyte was S. lacteus (Daudin, 1800), which has similar vertical and horizontal distribution. These records may be indicating a competition for calling perches or a competition over food. In the dry season, three species were calling at the study site, Boana raniceps been suggested by Duellman (1978) and Rodriguez (Cope, 1862), Leptodactylus mascrosternum Miranda- and Duellman (1994). The dominant presence of Ribeiro, 1926 and Pseudopaludicola boliviana Parker, ants in the diet composition was mentioned to other 1927. These species use the temporary puddles of water six species of the tribe Sphaenorhynchini: Gabohyla caused by trampling of buffaloes as vocalisation and pauloalvini (Bokermann, 1973), S. dorisae (Goin, reproduction sites (E. Campos, pers. comm.). 1957), S. lacteus, S. planicola (Lutz and Lutz, 1938), S. prasinus Bokermann, 1973, and S. surdus (Cochran, Calling sites of S. carneus are similar to those described 1953) (Duellman, 1978; Rodriguez and Duellman, for Central Amazonia (Hödl, 1977), being composed 1994; Parmalee, 1999; Faivovich et al., 2005, Teixeira mainly of macrophytes (Salvinia spp., Salviniaceae), and Ferreira, 2010; Araujo-Vieira et al., 2019). This vegetation commonly associated with lowland areas of specialist feeding behaviour, commonly named as the Amazon. The reproductive mode is number 1 (sensu mymercophagy, is considered a putative synapomorphy Haddad and Prado, 2005): eggs deposition occurs on of the tribe Sphaenorhynchini (Faivovich et al., 2005; emergent vegetation in the lentic water and exotrophic Araujo-Vieira et al., 2019). Myrmicinae ants dominated tadpoles, similar to that of most other members of the the diet of S. carneus, which can be explained by genus (Crump, 1974; Toledo et al., 2007; Araujo-Vieira the higher diversity of genera and uses of substrates et al., 2015). However, Bokermann (1973) observed (arboreal, terrestrial, and some deeply associated that S. carneus also lays clutches on leaves overhanging with plants) of this taxon when compared to other ant water similar to Gabohyla pauloalvini. Sphaenorhynchus subfamilies (Fernández and Sharkey, 2006). Among carneus is a species that exhibits daytime and night- Myrmicinae, Solenopsis was the most abundant genus time activity, with increased activity at the end of the recorded in the diet of S. carneus. According Fernández day and, therefore, it is considered predominantly and Sharkey (2006) and Baccaro et al. (2015), Solenopsis crepuscular (Suárez-Mayorga and Lynch, 2001). This is one the most locally diverse genus in the Neotropics typical activity pattern has been observed for other and abundant in different habitats. congeners in different habitats in Brazil (Araujo-Vieira The studied floodplain area shows strong rainfall et al., 2015; Roberto et al., 2017; Volkmer et al., 2017). seasonality. Although we have not tested it, we observed The protection of these areas is of vital importance for that the number of individuals recorded could be related the conservation of the local anurofauna, considering to rainfall variations and possibly to the river flooding. the descriptions and the extension of the distribution We recorded data over two years, in each of which S. of anurans in the region (e.g., Corrêa et al., 2015). carneus showed reproductive activity over an extended Natural history studies have clarified various aspects of period (sensu Wells, 1977), associated with a strong species biology, filling knowledge gaps and providing Natural history notes of Sphaenorhynchus carneus in the eastern Brazilian Amazon 619 information that can potentially be applied in various Duellman, W.E. (1978): The biology of an equatorial herpetofauna branches of biology. The continuation of this study in Amazonian Equador. University of Kansas, Museum of should provide a basis for further researches with anuran Natural History Miscellaneous Publications 65: 1–352. Duellman, W.E., Trueb, L. (1994): Biology of Amphibians. amphibians in eastern Amazonia. Baltimore, The Johns Hopkins University Press. Faivovich, J., Haddad, C.F.B., Garcia, P.C.O., Frost, D.R., Acknowledgments. We are grateful to Katyuscia Araujo-Vieira Campbell, J.A., Wheeler, W.C. (2005): Systematic review of for the valuable comments on this manuscript and pre-peer the frog family Hylidae, with special reference to Hylinae: review. We thank Raimundo N. P. Souto (ArthroLab/UNIFAP) Phylogenetic analysis and taxonomic revision. Bulletin of the for helping in the identification of prey items. Collection American Museum of Natural History 294: 1–240. permits (#45990-1) were provided by Instituto Chico Mendes Fernández, F., Sharkey, M.J. (2006): Introducción a los Hymenoptera de Conservação da Biodiversidade (ICMBio/SISBIO). We also de la Región Neotropical. Bogotá, Sociedad Colombiana de thank the Herpetology Notes editor and the anonymous referees Entomologia y Universidad Nacional de Colômbia. for the constructive feedback and revisions on our manuscript. Frost, D.R. (2020): Amphibian Species of the World: An Online Reference. Version 6.0. American Museum of Natural History, References New York, USA. Available at http://research.amnh.org/vz/ herpetology/amphibia/. Accessed on 20 March 2020. Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.L.M., Haddad, C.F.B., Prado, C.P.A. (2005): Reproductive modes in Sparovek, G. (2013): Köppen’s climate classification map for frogs and their unexpected diversity in the Atlantic Forest of Brazil. Meteorologische Zeitschrift 22: 711–728. Brazil. BioScience 55: 207–217. Araujo-Vieira, K., Lacerda, J.V.A., Pezzuti, T.L., Leite, F.S.F., Hartmann, M.T., Hartmann, P.A., Haddad, C.F.B. (2010): Assis, C.L., Cruz, C.A.G. (2015): A new species of Hatchet- Reproductive modes and fecundity of an assemblage of anuran faced Treefrog Sphaenorhynchus Tschudi (Anura: Hylidae) amphibians in the Atlantic rainforest, Brazil. Iheringia 100: from Quadrilátero Ferrífero, Minas Gerais, southeastern Brazil. 207–215. Zootaxa 4059: 096–114. Hödl, W. (1977): Call differences and calling site segregation in Araujo-Vieira, K., Blotto, B.L., Caramaschi, U., Haddad, C.F.B., anuran species from central Amazonian floating meadows. Faivovich, J., Grant, T. (2019): A total evidence analysis of Oecologia 28: 351–363. the phylogeny of hatchet-faced treefrogs (Anura: Hylidae: Hödl, W. (1990): Reproductive diversity in Amazonian lowland Sphaenorhynchus). Cladistics 35: 469–486. frogs. Fortschritte der Zoologie 38: 41–60. Araujo-Vieira, K., Luna, M.C., Caramaschi, U., Haddad, C.F.B. Leivas, P.T., Mayer, T.B., Fávaro, L.F. (2018): The reproductive (2020): A new genus of lime treefrogs (Anura: Hylidae: biology of Dendropsophus minutus (Amphibia: Anura) in South Sphaenorhynchini). Zoologischer Anzeiger 286: 81–89. of Brazil. Herpetology Notes 11: 395–403. Azevedo-Ramos, C., Coloma, L.A., Ron, S. (2004): Parmelee, J.R. (1999): Trophic ecology of a tropical anuran Sphaenorhynchus carneus. The IUCN Red List of Threatened assemblage. Scientific Papers, University of Kansas, Natural Species. IUCN Red List of Threatened Species. Available at History Museum 11: 1–59. https://www.iucnredlist.org/en. Accessed on 09 April 2020. Pinkas, L., Oliphant, M.S., Inverson, I.L.K. (1971): Food habits Baccaro, F.B., Feitosa, R.M., Fernandez, F., Fernandes, I.O., Izzo, of albacore, bluefin tuna, and bonito in Californian waters. T.J., Souza, J.L.P., Solar, R. (2015): Guia para os gêneros de Fisheries Bulletin 152: 11–105. formigas do Brasil. Manaus, Editora INPA. Rafael, J., Melo, G., De Carvalho, C., Casari, S., Constantino, R. Bokermann, W.C.A. (1973): Duas novas espécies de (2012): Insetos do Brasil: Diversidade e Taxonomia. Ribeirão “Sphaenorhynchus” da Bahia (Anura, Hylidae). Revista Preto, Holos Editora. Brasileira de Biologia 33: 589–594. Ramalho, W.P., Andrade, M.S., Matos, L.R.A., Vieira, L.J.S. (2016): Colli, G.R., Araújo, A.F.B., Da Silveira, R., Roma, F. (1992): Niche Amphibians of várzea environments and floating meadows of partitioning and morphology of two syntopic Tropidurus (Sauria: the oxbow lakes of the Middle Purus River, Amazonas, Brazil. Tropiduridae) in Mato Grosso, Brazil. Journal of Herpetology Biota Neotropica 16: 1–15. 26: 66–69. Roberto, I.J., Araujo-Vieira, K., de Carvalho-e-Silva, S.P., Ávila, Corrêa, J.G., Souza, J.C., França, P.F., Costa-Campos, C.E. (2015): R.W. (2017): A new species of Sphaenorhynchus (Anura: Sphaenorhynchus carneus (Cope, 1868) (Amphibia: Anura: Hylidae) from Northeastern Brazil. Herpetologica 73: 148–161. Hylidae): distribution extension, geographic distribution map Rodriguez, L.O., Duellman, W.E. (1994): Guide to the Frogs of the and new state record. Check List 11: 1725. Iquitos Region, Amazonian Peru. Lawrence, Kansas. Asociación Crump, M.L. (1974): Reproductive strategies in a tropical anuran de Ecología y Conservación, Amazon Center for Environmental community. Miscellaneous Publication Museum of Natural Education and Research, and Natural History Museum, The History University of Kansas 61: 1–65. University of Kansas. Crump, M.L., Scott-Jr., N.J. (1994): Visual encounter surveys. Silva, L.M.A., Lima, J.F., Tavares-Dias, M. (2016): Ictiofauna como In Measuring and Monitoring Biological Diversity Standard indicadora da qualidade ambiental do Rio Matapi, Afluente Methods for Amphibians, p. 84–92. Heyer, W.R., Donnelly, do Rio Amazonas no estado do Amapá (Brasil). Boletim de M.A., McDiarmid, R.W., Hayek, L.A.C., Foster, M.S., Eds., Pesquisa e Desenvolvimento Macapá, Embrapa Amapá. Washington, USA, Smithsonian Institution Press. Suárez-Mayorga, A.M., Lynch, J.D. (2001): Los renacuajos 620 Juliana Gonçalves Corrêa et al.
colombianos de Sphaenorhynchus (Hylidae): descripciones, Toledo, L.F., Llusia, D., Vieira, C.A., Corbo, M., Márquez, R. anotaciones sistemáticas y ecológicas. Revista de la Academia (2014): Neither convergence nor divergence in the advertisement Colombiana de Ciencias Exactas, Físicas y Naturales 25: 411– call of sympatric congeneric Neotropical treefrogs. Bioacoustics 419. 24: 31–47. SYSTAT (2007): SYSTAT 12 for Windows. Statistics, Version 12. Verdade, V.K., Valdujo, P.H., Carnaval, A.C., Schiesari, L., San Jose, California, USA. Toledo, L.F., Mott, T., et al. (2012): A leap further: the Brazilian Teixeira, L.R., Ferreira, R. (2010): Diet and fecundity of Amphibian Conservation Action Plan. Alytes 29: 28–43. Sphaenorynchus planicola (Anura, Hylidae) from a coastal Vitt, L.J., Caldwell, J.P. (2014): Herpetology. An introductory lagoon in Southeastern Brazil. Revista Española de Herpetologia biology of amphibians and reptiles. Amsterdam, Elservier. 24: 19–25. Volkmer, G., da Fonte, L.F.M., Brum, F.T., Verrastro, L. (2017): Toft, C.A. (1980): Seasonal variation in populations of panamanian Quando e onde vocaliza Sphaenorhynchus surdus (Anura: litter frogs and their prey: A comparison of wetter and drier sites. Hylidae) no sul do Brasil? Iheringia, Série Zoologia 107: Oecologia 47: 34–38. e2017029. Toft, C.A. (1981): Feeding ecology of Panamanian litter anurans: Wells, K.D. (1977): The social behaviour of anuran amphibians. Patterns in diet and foraging mode. Journal of Herpetology 15: Animal Behaviour 25: 666–693. 139–144. Wells, K.D. (2007): The ecology and behavior of amphibians. Toledo, L.F. (2005): Predation of juvenile and adult anurans Chicago, The University of Chicago Press. by invertebrates: Current knowledge and perspectives. Herpetological Review 36: 395–400. Toledo, L.F., Garcia, P.C.A., Lingnau, R., Haddad, C.F.B. (2007): A new species of Sphaenorhynchus (Anura; Hylidae) from Brazil. Zootaxa 1658: 57–68.
Accepted by Fábio Hepp