Herpetology Notes, volume 12: 933-938 (2019) (published online on 24 September 2019)

Newly discovered, widely distributed, and seemingly imperiled: distribution extension of the Red-Eyed Snouted Treefrog into highly anthropic ecotones in Mato Grosso State,

Bruno F. Camera1,2,*, Tainá F. Dorado-Rodrigues2, Natália P. Smaniotto2,3, André Pansonato2, and Christine Strüssmann1,2,3

Scinax Wagler, 1830 is recognized as a very diverse bicolored iris, upper half reddish, lower half grey, and, and highly underestimated anuran group (Ferrão et al., advertisement call parameters (complete diagnosis in 2016), with more than 70 species distributed throughout Ferrão et al., 2018a). The holotype was collected at South America, ranging from eastern Mexico to Central Nascentes do Lago Jari National Park, municipality of Argentina and Uruguay (Frost, 2018). Several recent Tapauá, Amazonas State, and paratypes were recorded species descriptions (e.g., Araujo-Vieira et al., 2016; from other four municipalities in the same state: Conte et al., 2016; Ferrão et al., 2017; 2018a, b; Acosta- da Várzea, Borba, Beruri, and Manicoré (Ferrão et al., Galvis 2018; Ron et al., 2018) and range extensions 2018a). All these localities are situated along the federal (e.g., Bang and Giaretta, 2017; Dalmolin et al., 2017; highway BR-319. Running 877 km north-south from Da Silva et al., 2017; Maffei et al., 2017; Armesto et to Porto Velho — the capitals of the Brazilian al., 2018; Chávez, 2018) attest that our knowledge states of Amazonas and Rondônia, respectively, and the on the genus is still far from complete. Moreover, a two largest urban hubs in Amazonia — this highway recent molecular study evidenced that the number of links Central Amazonia to the so-called “Arc of undescribed species of from habitats along Deforestation”. In this area, situated in the eastern and sections of the Madeira River, southwestern Amazonia, southern edges of Amazonia, intensive and systematic is greatly underestimated (Ferrão et al., 2016). expansion of croplands and pasturelands have been the Scinax ruberoculatus Ferrão et al., 2018 (Red-Eyed main driving factors leading to the clearing of forests Snouted Treefrog) was recently described from Brazilian and savannahs, for the last 40 years (Fearnside and Amazonia. The species differs from its congeners by a Graça, 2006; Arvor et al., 2013; Zaiatz et al., 2018). The combination of traits, including its small size (snout consequent dramatic land use and cover changes result vent length 22.6–25.9 mm in males, 25.4–27.5 mm in massive habitat loss for several species, undoubtedly, in females), a characteristic dark brown molariform the greatest driver of local extinctions worldwide (Jantz spot from the top of the head to the scapular region, a et al., 2015). Here we report on three new records for Scinax ruberoculatus, all of them in the state of Mato Grosso, in localities situated within or near the “Arc of Deforestation”. On 12th 1 Programa de Pós-Graduação em Zoologia, Instituto de December 2003, during a herpetological Biociências, Universidade Federal de Mato Grosso, Av. inventory in the area under the influence of the small Fernando Corrêa da Costa 2367, Cuiabá, Mato Grosso hydroelectric power plant (PCH) Faxinal II, municipality 78060–900, Brazil. of Aripuanã, northwestern Mato Grosso State (10º09’42” 2 Centro de Biodiversidade, Instituto de Biociências, S, 59º26’54” W; 140 m a.s.l.; Fig. 1), a single individual Universidade Federal de Mato Grosso, Av. Fernando Corrêa of an unidentified treefrog was photographed (Fig. 2a). da Costa 2367, Cuiabá, Mato Grosso 78060–900, Brazil. After Ferrão et al. (2018a) this specimen was recognized 3 Programa de Pós-Graduação em Ecologia, Instituto de Biociências, Universidade Federal de Mato Grosso, Av. as belonging to Scinax ruberoculatus. The individual Fernando Corrêa da Costa 2367, Cuiabá, Mato Grosso was found late at night (after heavy rain which lasted 78060–900, Brazil. for about two hours, from 08:30–10:30 pm), perched * Corresponding author. E-mail: [email protected] on a shrub, on the margin of a temporary pond (Fig. 934 Bruno F. Camera et al.

10:00 pm, perched on the marginal shrubby vegetation of a temporary stream (7 m long x 2 m wide x 0.20 m deep, approximately; Fig. 2d), amidst semideciduous alluvial seasonal forest with emergent canopy (IBGE, 2018). Physalaemus cuvieri were recorded in the same site and occasion. The record of S. ruberoculatus for Diamantino extends beyond known distribution of the species by nearly 1,000 km southeastwards from the type locality (Fig. 1), to a transitional zone between southern Amazonia forests and the Cerrado savannahs from Midwestern Brazil. More recently, on 19th November 2018, a single S. ruberoculatus male was recorded (Fig. 2e) on the right margin of the Juína river, municipality of Campos de Júlio, western Mato Grosso (13°22’01” S, 59°24’07”W; 413 m a.s.l.; Fig. 1). This individual was vocalizing Figure 1. Known distribution of Scinax ruberoculatus in the perched on shrubby vegetation at 1.8 meters above the Brazilian states of Amazonas (AM) and Mato Grosso (MT). soil (Fig. 2f), amidst forested savannah, in a transitional Star: type locality (1): Nascentes do Lago Jari National Park, zone between the Cerrado and seasonal forests (IBGE, municipality of Tapauá; open circles: additional literature 2018). The specimen was collected and deposited at the records (from Ferrão et al., 2018) – Manicoré (2), Beruri (3), “Coleção Zoológica de Vertebrados da Universidade Borba (4), and Careiro da Várzea (5); closed circles: new records from the present report: Aripuanã (6), Campos de Júlio Federal de Mato Grosso”—UFMT (Cuiabá, Mato (7), and Diamantino (8). Grosso, Brazil), under the number UFMT 19331. Individuals of Boana cinerascens, Dendropsophus rubicundulus, D. cf. ozzyi, Leptodactylus rhodomystax, and Osteocephalus taurinus were recorded in the same 2b) in a clearing amidst moist broadleaf forest (open locality. ombrophylous forest sensu IBGE, 2018). This locality External characteristics (size, dorsal spot shape, and is situated on the left margin of the Aripuanã River, bicolored iris) of the specimens in the three localities downstream from the Dardanelos waterfalls, nearly 570 mentioned above match those described by Ferrão et al. km in a straight line southeast of the type locality of the (2018a) in the original description of S. ruberoculatus. species. In the forest surrounding the clearing, some of Advertisement calls were recorded of one male S. the trees presented diameter at breast height greater than ruberoculatus from Diamantino (unvouchered), using one meter and height greater than 30 m. Both understory a digital camera (Nikon COOLPIX P520) with built- and leaf-litter were scarce, and soils were hydromorphic, in microphones, and of two males from Campos de subject to waterlogging during the rainy season. Júlio, recorded on 8th February 2019, using a digital Individuals of Dendropsophus cf. sarayacuensis, D. aff. recorder (Marantz PMD 660) equipped with an external microcephalus, and Leptodactylus cf. leptodactyloides directional microphone (Yoga EM-9600). One of these were also using the temporary pond where the single specimens from Campos de Júlio was collected and individual of S. ruberoculatus was captured. Part of this deposited as a voucher at the UFMT collection (UFMT forest was cleared in 2007 during the construction of the 19338). Sound files were converted to mono WAVE hydroelectric power plant of Dardanelos, and the exact file format prior to performing any sound analysis, and site of collection now corresponds to a point along the archived in the acoustic database “Banco de Registros power plant tailrace (see data and pictures in Borgatti Bioacústicos do Laboratório de Herpetologia, Instituto et al., n.d.). de Biociências, UFMT”—LH (Cuiabá, Mato Grosso, On 19th March 2018, during a herpetological Brazil). Recordings were analysed on a personal inventory in the area to be occupied by the planned computer using Raven Pro 1.5 (Bioacoustic Research PCH Sumidouro, municipality of Diamantino, central Program 2014) with the following settings: Hamming Mato Grosso (13º52’19” S, 56º40’25” W; 355 m a.s.l.; window function; window length 256 samples; DFT Figure 1), six S. ruberoculatus males were found (Fig. size 256-point samples, brightness 50%, contrast 50%, 2c). They were vocalizing actively between 08:00– and time grid overlap 50%. The terminology in call Distribution extension of the Red-Eyed Snouted Treefrog, Brazil 935

Figure 2. Live adult male specimens (left column) and breeding habitats (right column) of Scinax ruberoculatus from three localities in the State of Mato Grosso, Brazil: Aripuanã (A, B), Diamantino (C, D), and Campos de Júlio (E, F).

descriptions is in accordance to Köhler et al. (2017), 2018a). Each call consisted of a single pulsed note, following the call-centred approach. To produce composed of 13–18 pulses. Call duration varied from spectrograms and waveforms, we used the R package 0.21–0.28 s, and inter-call intervals varied from 1.1–2.7 “Seewave” (Sueur et al., 2008) and tuneR (Ligges s. The dominant frequency varied from 1894.9–1981.1 et al., 2007), with the following settings: FFT size of Hz and the bandwidth varied from 1394.8 Hz to 4458.3 512 points, Hamming window function, and 90% of Hz. The calls were emitted at a rate of 22.2–54.5 calls overlap. per minute. The acoustic parameters of the calls recorded in The advertisement calls recorded at Campos de Júlio Diamantino are also consistent with those described (Fig. 3) consisted of single pulsed notes composed of and featured in the original description (Ferrão et al., 10–13 pulses. Call duration varied from 0.15–0.19 s, 936 Bruno F. Camera et al.

Figure 3. Oscillogram and audiospectrogram (DFT size = 512 samples) of the advertisement call of Scinax ruberoculatus from the State of Mato Grosso, Brazil: (A) voucher call LH 1030, recorded on 19th March 2018, 21:00h, municipality of Diamantino; (B) voucher call LH 980, from specimen UFMT 19338, recorded on 8th February 2019, 21:20h, air temperature 24.5ºC, municipality of Campos de Júlio.

and inter-call intervals varied from 0.7–1.5 s. The The expansion of the agriculture frontier and road dominant frequency varied from 1808.8–1894.9 Hz, building are extensive and consistent factors leading and the bandwidth varied from 1323.8–5047.1 Hz. to deforestation in the Amazonia (Pfaff et al., 2018). The calls were emitted at a rate of 47.4–68.2 calls per Soils with medium to high clay content, suitable for minute. When compared with the acoustical traits of cultivating several crops and for establishing large- S. ruberoculatus provided by Ferrão et al. (2018a), scale pasturelands, predominate in northern and central our results revealed a minor variation and allow for regions of Mato Grosso (Camargo, 2011), largely confirming the presence of the species in the State of coincident with the “Arch of Deforestation” (Fearnside, Mato Grosso. 2017). This has concentrated about 80% of deforestation Ferrão et al. (2018a) reported that S. ruberoculatus only in the Amazon in the last decades (Fearnside, 2017). In reproduces in ponds that are not connected to lotic water spite of the fact that advance of the agricultural frontier bodies, as observed for the single individual found in now threatens the last continuous, northernmost areas of Aripuanã. However, all six males from Diamantino were the Cerrado (a region known as MATOPIBA, see Lima found calling from the margin of a slow-flowing stream. et al., 2019), many of the abandoned former pastures and Ferrão et al. (2018a) also posed that both the occurrence agricultural areas in southern Amazonia are degraded and abundance of S. ruberoculatus were positively and in need of ecosystem restoration (Rezende and affected by the silt content in the soil, which ultimately Vieira, 2019). results in higher water retention (Ferrão et al., 2018a). Besides that, Brazilian energy matrix still is — and Large-scale soil information provided in Camargo will continue to be, in the next decade, at least — based (2011) shows that soils are predominantly podzolic, in hydropower, and many of the hydroelectric power medium-textured, clayey, and on undulated topography plants already in operation, under construction, or even in Aripuanã. In Diamantino there is a predominance planned are located in the mid-northern portion of the of latosols, also clay-rich, on flat topography, while state of Mato Grosso (Dias et al., 2018; ANEEL, 2019). in Campos de Julio there is a predominance of sandy Hydroelectric plants are known to affect negatively the quartz soils, occasionally intermingled with slightly local biodiversity due to fragmentation, degradation, clayed latosols, on flat to slightly undulated topography or habitat loss (Lees et al., 2016). All known records (Camargo, 2011). of S. ruberoculatus in Mato Grosso, were obtained Distribution extension of the Red-Eyed Snouted Treefrog, Brazil 937 during faunal inventories and/or monitoring associated Grosso, Brazil, using remote sensing data. GeoJournal 78: with the environmental licensing of hydroelectric 833–850. plants. Remarkably, in one of the cases, at Aripuanã, Borgatti, L., Miranda, P.D., Neto, J.P., Cunha, M. F. (2019): The Dardanelos hydroelectric development on the Aripuanã River. In: the exact site where we found the single individual of Main Brazilian Dams III: Design Construction and Performance, S. ruberoculatus was completely destroyed during the p. 119–135 Piasentin, C., Ed., Brazilian Committee on Dams, construction of the plant. [s.l.]. Available at: http://www.cbdb.org.br/documentos/mbdiii/ Although we expect that populations of S. dardanelos.pdf. Accessed on 28 March 2019. ruberoculatus do occur in several other localities in Bang, D.L., Giaretta, A.A. (2017): Filling a gap in the distribution mid-northern Mato Grosso, this entire portion of the of Scinax rostratus (Peters, 1863) (Anura, ) in northern state is facing the multiplication and/or enlargement of Brazil, with further data on its advertisement call. Check List urban settlements, besides large scale agriculture and 13: 2150. Barrio-Amorós, C.L., Orellana, A., Chacón, A. (2004): A new power projects. Therefore, we argue that many of the S. species of Scinax (Anura: Hylidae) from Andes of . ruberoculatus known populations probably already are Journal of Herpetology 38: 105–112. or will be threatened by habitat loss in a near future. Camargo, L. (2011): Atlas de Mato Grosso: abordagem Scinax ruberoculatus was not yet evaluated by the socioeconômico-ecológica. Cuiabá, BRA, Entrelinhas. International Union for Conservation of Nature— Chávez, G. (2018): Geographic distribution of Scinax onca IUCN, and its status is presently being evaluated by (Anura: Hylidae) and the first record of its occurrence in Peru. the Brazilian government, for the first time (ICMBio, Phyllomedusa 17: 279–283. 2018). Our records contribute to the knowledge of the Conte, C.E., Araujo-Vieira, K., Crivellari, L.B., Berneck, B von M. (2016): A new species of Scinax Wagler (Anura: Hylidae) from geographical distribution and provide additional data Paraná, southern Brazil. Zootaxa 4193: 245–265. to better assess the conservation status of this species. Da Silva, I.R.S., Santana, D.O., Rocha, S.M., Faria, R.G. (2017): Moreover, this report shows the importance of faunal New records for Scinax fuscomarginatus Lutz, 1925 (Anura: inventories for a better understanding of the composition, Hylidae) from Sergipe, Brazil. 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Accepted by Michael Jowers