Herpetology Notes, volume 10: 703-707 (2017) (published online on 08 December 2017)

Range extension of the poorly know tree frog Dendropsophus haraldschultzi (Bokermann, 1962) (Amphibia, Anura, Hylidae): first records for two Brazilian Amazon states

Alexandre F. R. Missassi1,*, Carlos E. Costa-Campos2, Jucivaldo D. Lima3 and Carolina Lambertini4

The small to medium-sized hylid frog species of the the head (Bokermann, 1962; Rodrigues and Duellman, genus Dendropsophus Fitzinger, 1843, comprises a 1994) (Fig. 1). specious clade within the subfamily Dendropsophinae Despite its wide distribution, D. haraldschultzi is Fitzinger, 1843, with two morphological and one poorly known and recorded from only a few localities chromossomical synapomorphies (sensu Duellman et along the Amazon Rainforest (e.g., Lynch and Mayorga, al., 2016). Broadly distributed through the Neotropics, 2011; Waldez et al., 2013; Gagliardi-Urrutia et al., 2015), Dendropsophus contains 98 primarily arboreal species, with dispersed records available in the literature. In this occurring in open and forested areas from Nuclear paper, we provide a review of the known distribution of Central America to northern Argentina and Uruguay D. haraldschultzi, and introduce new records, broadly (Duellman et al., 2016; Frost, 2016). extending its range throughout the Brazilian Amazon Within this diverse anuran clade, Dendropsophus Basin. haraldschultzi (Bokermann, 1962) was described from The new records were based on thirty one specimens Santa Rita do Weill, São Paulo de Olivença, Amazonas from recent field samplings and museum specimens. The state, Brazil. Originally named Hyla haraldschultzi, it specimens are housed at the Herpetological Collection was later transferred to the genus Dendropsophus by of the Universidade Federal do Amapá (CECCAMPOS), Faivovich et al. (2005). Dendropsophus haraldschultzi Herpetological Collection of the Museu Paraense can be diagnosed from other congeners by its small body Emílio Goeldi “Osvaldo Rodrigues da Cunha” (MPEG) size (18 to 25 mm), a light brown dorsum with small and Museum of Zoology from Universidade Estadual dark dots, the presence of a lightly marked medial line de Campinas “Adão José Cardoso” (ZUEC) (acronyms with adjacent longitudinal brown stripes, and the skin of follow Sabaj Pérez 2016, except for CECCAMPOS). the body having series of glands more conspicuous in The specimen’s identification followed the original description (Bokermann, 1962). We performed a literature review focusing on the species distribution records. GPS coordinates for the museum specimens were obtained and, when necessary, we refined 1 Laboratório de Herpetologia, Departamento de Zoologia, literature available records using Google Earth (Google, Museu Paraense Emílio Goeldi, Avenida Perimetral, 1901, 2005). Finally, we made a distribution map covering all 66077-830, Belém, Pará, Brazil available and including our new records for the species, 2 Universidade Federal do Amapá, Departamento de Ciências Biológicas e da Saúde, Laboratório de Herpetologia, Campus using the software QGIS 2.18.0. Marco Zero, Rodovia JK, Km 02, 68903-419, Macapá, On the night of April 14, 2014 at Ilha de Santana, Amapá, Brazil Santana municipality, southern Amapá state, Brazil, 3 Instituto de Pesquisas Científicas e Tecnológicas do Estado do three male adults and two females were collected Amapá, Núcleo de Biodiversidade, Zoologia (Herpetofauna), during a nocturnal active search in a transition area 68912-250, Macapá, Amapá, Brazil between Amazon Rainforest and Savanna (0.080000o S, 4 Laboratório de História Natural de Anfíbios Brasileiros o (LaHNAB), Departamento de Biologia Animal, Instituto de -51.182222 W, datum: WGS84). The individuals were Biologia, Universidade Estadual de Campinas, UNICAMP, found perched on herbaceous and shrub vegetation, with 13083-862, Campinas, São Paulo, Brazil males of Adenomera hylaedactyla (Cope, 1868), Boana * Corresponding author e-mail: [email protected] boans (Linnaeus, 1758), B. punctata (Schneider, 1799), 704 Alexandre F. R. Missassi et al.

Figure 1. Dorsal, ventral and dorsolateral view of Dendropsophus haraldschultzi (ZUEC 23177, field number MCP 59) from Lontra da Pedreira locality, Amapá state, Brazil. Note in dorsal view, the presence of a series of glands conspicuous in the head. Scale bar: 5 mm.

B. lanciformis (Cope, 1871) and Scinax boesemani unpublished localities: Tabatinga, Uarini and Maraã (Goin, 1966) calling at the same pond (Fig. 2). municipalities in Amazonas state; Casinha, Oriximiná In the nights of March, 2 to 4, 2016, seven male adults municipality, Pará state; and Ariri, Macapá municipality, and one female were collected in a similar transition area Amapá state. We include these new records in our new as cited above (0.304306º N, -50.872556º” W, datum: distribution map for this species. WGS84), at Lontra da Pedreira, Macapá municipality, Both collected individuals and preserved specimens southern Amapá state, Brazil. The specimens were represent the first record of D. haraldschultzi for Pará collected in a pond beside the road, with males and Amapá states (Tab. 1), and seven new records for calling on grasses and shrub vegetation approximately the species in Brazilian Amazon Basin (Appendix, Fig. 1m above water level. Males of the species Boana 3). Our records extends its distribution approximately punctata (Schneider, 1799), B. multifasciata (Günther, at 1086 km northeast from Lago Januari, Amazonas 1859), Dendropsophus leucophyllatus (Bereis, state (Hödl, 1977), being Lontra da Pedreira locality in 1783), Scarthyla goionorum (Bokermann, 1962), Amapá state the eastern distribution limit known for the Leptodactylus macrosternum Miranda-Ribeiro, 1926, species, approximately 2094 km from the type locality L. petersii (Steindachner, 1864) and Sphaenorhyncus (Bokermann, 1962) (Tab. 1, Fig. 3). lacteus (Daudin, 1800), were also calling at the same Based on examined literature, D. haraldscultzi occurs pond. in Colombia, Peru and Brazil (Fig. 3). Near to Leticia Furthermore, while examining preserved specimens municipality, Colombia, the species was found in at MPEG, we found eighteen specimens from five lowland and várzea forests (Lynch, 2005). Additional

Table 1. New records of Dendropsophus haraldschultzi from Pará and Amapá states, Brazil. The symbol (*) represents 1approximations, Table 1. New records while of the Dendropsophus other coordinates haraldschultzi represent from Paráthe andexact Amapá collecting states, Brazil. point. The The symbol altitude (*) represents corresponds approximations, to meters while above the other sea coordinates represent the 2level. exact The collecting range extension point. The altitudeis presented corresponds by the to metersdistance above from sea thelevel. type The localityrange extension and from is presented previous by therecords distance (Hödl from the1977) type separated locality and by from previous records (Hödl a bar. The SVL (snout-vent length) is the range in size of collected specimens. 3 1977) separated by a bar. The SVL (snout-vent length) is the range in size of collected specimens.

Municipality Locality Coordinates Altitude Range extension Specimens SVL (mm) (m asl) (Km) Oriximiná/PA Casinha 01º45’42.59”S, 055º51’49.00”W(*) - 1509 / 484 2 ƃ 18.7 – 20.3 Santana/AP Ilha de Santana 00o04’48.00”S, 051o10’56.00”W 14 2045 / 1040 3 ƃ / 2 Ƃ 20.1 – 23.7 Macapá/AP Ariri 00º17’57.50”N, 051º07’47.60”W 16 2068 / 1057 1 ƃ / 2 Ƃ 15.6 – 23.2 Macapá/AP Lontra da Pedreira 00º18’15.5” N, 050º52’21.20” W 20 2094 / 1086 7 ƃ / 1 Ƃ 18.6 –23.1 Dendropsophus haraldschultzi in two Brazilian Amazon states 705

Figure 2. Two individuals of Dendropsophus haraldschultzi (CECCAMPOS 00464 and CECCAMPOS 00092, respectively) from Ilha de Santana locality, Amapá state, Brazil.

Figure 3. Geographic distribution of Dendropsophus haraldschultzi, encompassing literature data (white squares), type locality (white star) and new reports (black dots). Legend: 1 – Tarapacá municipality, Amazonas departament, Colombia; 2 – Lago Tarapoto, Puerto Narino municipality, Amazonas departament, Colombia; 3 – Lago Yahuarcaca, Leticia municipality, Amazonas departament, Colombia; 4 – Leticia – Tarapacá, Amazonas departament, Colombia; 5 – Iquitos region, Loreto departament, Peru; 6 – Pacaya-Samiria National Reserve, Loreto departament, Peru; 7 – Nueva Esperanza locality, Ucayali river, Loreto departament, Peru; 8 – Santa Rita do Weill district, Amazonas state, Brazil (type locality); 9 – São Paulo de Olivença municipality, Amazonas state, Brazil; 10 – Tabatinga municipality, Amazonas state, Brazil (new); 11 - Est. Eco. Mamirauá (new); 12 – Lago Maraã, Comunidade Nova Canaã, Reserva Amanã, Amazonas state, Brazil (new); 13 – lower Purus River Basin, RDS Piagaçu-Purus, Amazonas state, Brazil; 14 – near Manaus municipality, southwestern end of Lago Januari, Amazonas state, Brazil; 15 – Casinha locality, Lago Sapucá, Oriximiná municipality, Pará state, Brazil (new); 16 – Ilha de Santana locality, Santana municipality, Amapá state, Brazil (new); 17 – Ariri locality, Macapá municipality, Amapá state, Brazil (new); 18 – Lontra da Pedreira locality, Macapá municipality, Amapá state, Brazil (new) (Bokermann, 1962; Hödl, 1977; Rodriguez and Duellman, 1994; Lynch, 2005; Lynch and Mayorga, 2011; Upton et al., 2011; Waldez et al., 2013; Gagliardi-Urrutia et al., 2015 Upton 2015). 706 Alexandre F. R. Missassi et al. records for Colombia include Amazonas and Puerto sampling efforts are needed to uncover the anuran Nariño localities, and the authors presented a taxonomic diversity. key and illustration for identification of the tadpoles The Amazon Basin harbours the most amphibian from the eastern lowlands of the country (Lynch and species in South America, but gaps in the knowledge of Mayorga, 2011), which was unknown for the species biology, species composition/richness and geographic (Rodrigues and Duellman, 1994). distribution need to be elucidated (Duellman, 1999). In Peru, D. haraldschultzi can be found in the Iquitos Thus, our review on the distribution of D. haraldschultzi region. In a study performed there, the authors presented represents a first step and important source of data for diagnostic characters and data from natural history conservation strategies. (Rodriguez and Duellman, 1994). The species was also found in Nueva Esperanza, a locality within the Tapiche Acknowledgements. We thank S. L. Gama, E. Galeno, D. Silva, and Blanco rivers, tributaries of the Ucayali river, located K. Corrêa, D. Pelaes and A. Santiago for field assistance. L. F. in southern Loreto, Peru (Gagliardi-Urrutia et al., 2015), Toledo and M. S. Hoogmoed confirmed species identification and provided personal data from sampled localities. A. L. C. Prudente and is abundant in the Pacaya-Samiria National Reserve, provided the access to MPEG collection. J. L. Lee provided an area bordered by Marañon River and Ucayali River, valuable comments and English review. This work was funded within the upper northeast Amazonian forest of Peru by Coordination for the Improvement of Higher Education (Upton et al., 2011; Upton, 2015). Personnel (CAPES) and the National Council of Technological In Brazil, D. haraldschultzi was known only from the and Scientific Development (PROTAX 440413/2015-0, CNPq type locality (see Bokermann, 1962) and two localities 405285/2013-2). in Amazonas state: near Manaus, within the várzea forests of Solimões River at the southwestern end of the References Lago Janauari (-3.216667º S, -60.033333º W) (Hödl, Bokermann, W. C. A. (1962): Cuatro nuevos hylidos del Brasil. 1977), and in both lowland forest areas (terra firme) Neotropica, 8: 81–92. and forest areas subject to periodic inundation (várzea) Duellman, W. E. (1999): Distribuition patterns of amphibians in in the lower Purus River Basin, Piagaçu-Purus Reserve South America. In: Duellman, W. E. (ed.) Patterns of distribution (Waldez et al., 2013), with the largest sampling know to of Amphibians. The Johns Hopkins University Press, Baltimore and London, 255–327. the left margin of Amazonas River (Fig. 3). Duellman, W. E., Marion, A. B. and Hedges, S. B. (2016): At Lontra da Pedreira, Amapá state, D. haraldschultzi Phylogenetics, classification, and biogeography of the treefrogs individuals were found in a pond beside the road, few (Amphibia: Anura: Arboranae). Zootaxa, 4104: 001–109. kilometres from várzea forest. According to Rodrigues Faivovich, J., Haddad, C. F. B., Garcia, P. C. A., Frost, D. R., and Duellman (1994), males and females can be found Campbell, J. A. and Wheeler., W. C. (2005): Systematic review near open ponds and permanent large streams. Lynch of the frog family Hylidae, with special reference to the Hylinae: (2005) and Waldez et al. (2013) also found individuals Phylogenetic Analysis and Taxonomic Revision. Bulletin of the American Museum of Natural History, 294: 1–240. in lowland forest areas, and várzea forests. In the Frost, D. R. (2016). Amphibian Species of the World: an Online Guiana Shield, the Essequibo - Branco Rivers form a Reference. Version 6.0. American Museum of Natural History. probable biogeographic barrier to forest-inhabiting Available at: http://research.amnh.org/vz/herpetology/amphibia. frogs, and distinct anuran fauna can be found on the Last accessed on Oct 01, 2016. shield’s east and west sides (Hoogmoed, 1979). Given Gagliardi-Urrutia, G., Iglesias, M. O. and Venegas, P. J. (2015): that our collection data reveals that D. haraldschultzi, Amphibias and reptiles. in Pitman, N., Vriensendorp, C., Chávez, occurs near várzea and lowland forests, we hypothesize L. R., Wachter, T., Reyes, D. A., del Campo, Á., Gagliard- Urrutia, G., González, D. R., Trevejo, L., González, D. R. and that this species is restricted from the east side of the Heilpern, S. (eds.). Perú: Tapiche-Blanco. Rapid Biological and Guiana Shield and does not pass the Essequibo - Branco Social Inventories Report 27. The Field Museum, Chicago. River barrier. Hoogmoed, M. S. (1979): The herpetofauna of the Guianan region. Our new records show that the distribution of D. In: Duellman, W. E. (ed.) The South American herpetofauna: haraldschultzi is wider than previously recorded in its origin, evolution, and dispersal. Museum of Natural History, Brazil, until now restricted to Amazonas state (Hödl, University of Kansas, Kansas. 1977; Frost, 2016). The first specimens recorded from Hödl, W. (1977): Call diferences and calling site segregation in anuran species from Central Amazonian Floating Meadows. Pará and Amapá states were collected near from areas Oecologia, 28: 351–363. of anthropogenic occupation, at the left margin from Lynch, J. D. and Suárez-Mayorga, A. M. (2011): Clave ilustrada de Amazonas River. Such a discovery reveals how much los renacuajos em las tierras bajas al oriente de los Andes, com remains to be known in these region, and greater énfasis em Hylidae. Caldasia, 33: 235–270. Dendropsophus haraldschultzi in two Brazilian Amazon states 707

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Accepted by Robson Ávila