Herpetology Notes, volume 12: 491-499 (2019) (published online on 19 May 2019)
Species composition and reproductive modes of anurans from the southwestern state of Goiás, Brazil
Seixas Rezende Oliveira1,2, Carolina Emília dos Santos¹, Antonio Olímpio de Souza¹, Matheus Souza Lima- Ribeiro3, Kauê Vergilio2, Marlon Zórtea2, Diego Afonso Silva2, Fabiano Rodrigues de Melo2,4, Frederico Augusto Guimarães Guilherme5, Wilian Vaz-Silva6, and Alessandro Ribeiro de Morais7
Abstract. The Brazilian Cerrado biome is a biodiversity hotspot under gradual transformation by human activity, such as monocultures of cash crops and cattle ranching. While the Cerrado contains a considerable diversity of animals, its anuran fauna is still relatively poorly studied, even though 210 amphibian species are known to occur in this biome. Here, we survey the anuran fauna in the central Brazil, providing data on species richness and composition, reproductive modes, and conservation status. We conducted the surveys in southwestern Goiás state between 2009 and 2012, with a 10-day field trip for every three months. Sampling consisted of three complementary approaches: pitfall traps, active searches at breeding sites, and auditory censuses. Additionally, published studies that provide species lists for southwestern Goiás were also considered, and the reproductive modes of the species were defined. We report 45 anuran species from six families and 16 genera, as well as nine reproductive modes from 88 sampling points in the studied region. Six of the 45 species are new recordings in the region, amplifying the information available on its anuran fauna. The species richness of the studied region is the equivalent of 6% of the total anuran diversity found in Brazil, and 22% of that of the Cerrado biome. Nine of the 45 recorded species are endemic to Cerrado, and three of these had not been recorded previously in southwestern Goiás. None of the reported species are listed as endangered, one is Data Deficient (DD), and all the others are Least Concern (LC). Most species presented reproductive mode in which exotrophic eggs and tadpoles are deposited in lentic bodies of water. The low diversity of reproductive modes found in the region appears to be related to the reduced heterogeneity of microhabitats. The knowledge of the zoogeographic patterns and the natural history of the anuran species are important contributions of this study that subsidize actions related to conservation policies for species in the Cerrado biome.
Keywords: Cerrado, Endemism, Red List, Inventory
Introduction 1 Programa de Pós-Graduação em Biodiversidade e Conservação, Instituto Federal Goiano, Campus Rio Verde, The Cerrado is the second largest Brazilian biome, 75901-970, Cx Postal 66, Rio Verde, GO, Brazil. covering approximately 21% of the country (Borlaug, 2 Laboratório de Biodiversidade Animal, Instituto de 2002), and is composed of a phytophysiognomic Biociências, Campus Jataí, Universidade Federal de Goiás, mosaic, with more than 20 distinct types of vegetation, 75801-615, Jataí, Goiás, Brazil. including forests, savannahs, and grasslands (Ribeiro 3 PaleoMACROecology Lab., Instituto de Biociências, Campus & Walter, 1998). In addition to its enormous area, Jataí, Universidade Federal de Goiás, 75801-615, Jataí, heterogeneous vegetation cover, and animal diversity, Goiás, Brazil. 4 Depto. de Eng. Florestal, Universidade Federal de Viçosa, the Cerrado is traversed by the three principal river Viçosa, MG,36570-900, Brazil. basins of South America, the Amazon, Plate, and São 5 Universidade Federal de Goiás, Regional Jataí, Instituto de Francisco basins (Adámoli et al., 1986). The Cerrado Biociências, Herbário Jataiense, BR 364/ Km 192, Jataí, GO, has been widely impacted by the expansion of cattle 75801-615, Brazil. ranches and crops. In many areas, the natural vegetation 6 Escola de Ciências Agrárias e Biológicas, Centro de Estudos has been replaced by monocultures of cash crops such as e Pesquisas Biológicas, e Programa de Pós-Graduação sugarcane, maize, and soybean, extensive areas covered em Ciências Ambientais e Saúde, Pontifícia Universidade Católica de Goiás – PUC Goiás. Av. Engler, s/n, Bloco L, in the invasive molasses grass (Melinis minutiflora), Setor Jardim Mariliza, 74.885-460, Goiânia, GO, Brazil. and plantations of eucalypts (Eucalyptus spp.). The 7 Instituto Federal Goiano, Campus Rio Verde, Caixa Postal 66, Cerrado biome is considered to be one of the world’s 35 75.901-970 Rio Verde, Goiás, Brazil. global biodiversity hotspots, regions characterized by * Corresponding author: [email protected] 492 Seixas Rezende Oliveira et al. high concentrations of endemic species, combined with of water being searched for 60 minutes. All individuals extensive and increasing habitat loss (Mittermeier et al., observed were registered and their vocalizations 2011). Despite the considerable diversity of animals were recorded for posterior identification. Voucher found in Cerrado, its anuran fauna is still poorly known, specimens were deposited in the zoological collection although 210 amphibian species have been recorded to of the Jataí campus of the Federal University of Goiás. date in this biome (Valdujo et al., 2012). These animals The nomenclatural status present in Frost (2018) was are found in almost all types of terrestrial environment, adopted in this study. Species were also identified by where they often play an important role in the local consulting specialists, whenever necessary. Previous trophic web (Wells, 2007). published lists of species from southwestern Goiás (Vaz- In this study, we performed an inventory of the Silva et al., 2007; Kopp et al., 2010; Morais et al., 2011; anurans from the southwestern of Goiás state, in order Oliveira et al., 2015) were also consulted, to complete to contribute with the filling of data gaps of the Cerrado the inventory. The compilation of these data provided a anurofauna. We recorded the occurrence of anuran complete picture of the anuran fauna of the study area, species, their reproductive modes and conservation although some species with uncertain classifications status. that could not be conferred (e.g., Scinax sp., Scinax gr. ruber, Elachistocleis cf. ovalis, and Pseudopaludicola Material and Methods aff. falcipes) were excluded from the list. Next, the reproductive mode was determined for each The present study focused on southwestern of State of anuran species based on Haddad and Prado (2005), Goiás, central Brazil. This region covers a total area of Vieira et al. (2009), Kopp et al. (2010), and Vasconcelos 56,111.526 km² and cattle ranching is the predominant et al. (2010). The conservation status of each species was land use (Martins et al., 2016). Ranching has expanded also determined, based on the lists of the International progressively in recent years, and now dominates the Union for Conservation of Nature (IUCN, 2018) and the local economy. The whole region is inserted within the Brazilian government (MMA, 2014). The endemism of Cerrado biome, and has a tropical savannah climate each species in the Cerrado was also recorded, based on (Aw) (Köppen, 1948), with a dry season that extends Valdujo et al. (2012). from May to September, and a rainy season that occurs Finally, to test if the diversity of reproductive modes between October and April (Cardoso et al., 2014). The is determined by taxonomical richness, the number anuran fauna of southwestern Goiás State was surveyed of reproductive modes was correlated against species between 2009 and 2012, with 10-day field trips being richness taking into account the family taxonomical conducted every three months, resulting in a total level. sampling effort of 160 field days. A total of 28 points were sampled in the municipalities of Aparecida do Rio Results and Discussion Doce (-18.2974°S,-51.1462W), Aporé (-18.7900°S, - 52.0639W), and Jataí (-17.8791°S, -51.7207W). Based on the field surveys conducted during the In the field, the amphibian species were sampled using present study, a total of 44 anuran species (Fig. 1-2) complementary techniques, including pitfall traps, were sampled at 88 localities (Fig. 3) in southwestern active searches at breeding sites (Scott and Woodward, Goiás State. In addition to presenting a comprehensive 1994), and auditory censuses. Each pitfall trap was inventory of the anuran species of this region, six species made of four 60-liter buckets, buried in the ground and (Boana goiana (B. Lutz, 1968), Scinax constrictus interlinked by a plastic mesh, 50 cm high and 35 m in (Lima, Bastos and Giaretta, 2004), Baricholos ternetzi length. The buckets were distributed in a Y configuration (Miranda-Ribeiro, 1937), Pseudopaludicola mystacalis (Cechin and Martins, 2000), at a distance of 10 m from (Cope 1887), Odontophrynus cultripes (Reinhardt and each other. These traps were installed in a number of Lütken, 1861”1862”), Proceratophrys dibernadoi different phytophysiognomies and were activated only (Brandão et al., 2013) were recorded in southwestern for periods of fieldwork, when they were checked every Goiás for the first time, expanding the known anuran 24 hours. diversity of the region. Active searches at breeding sites were conducted These 44 species are distributed in six families and at specific sampling points, such as streams, lakes, 16 genera. The Hylidae and Leptodactylidae were the reservoirs, and other bodies of water. Searches were richest families (18 species each), followed by the conducted between 18:00 h and 24:00 h, with each body Bufonidae and Odontophrynidae (three species each), Species composition and reproductive modes of anurans from Goiás, Brazil 493
Figure 1. Anurans registered in southwestern of Goiás, Brazil. A) Leptodactylus labyrinthicus; B) Rhinella diptycha; C) Boana albopunctata; D) Leptodactylus syphax; E) Boana raniceps; F) Scinax aff. x-signatus; G) Barycholos ternetzi; H) Leptodactylus mystacinus; I) Boana lundii ; J) Dendropsophus rubicundulus; K) Proceratophrys dibernadoi; L) Leptodactylus fuscus; M) Adenomera aff. hylaedactyla; N) Dendropsophus minutus; O) Chiasmocleis albopunctata. 494 Seixas Rezende Oliveira et al.
Figure 2. Anurans registered in southwestern of Goiás, Brazil. A) Scinax fuscomarginatus; B) Dendropsophus cruzi; C) Dendropsophus melanargyreus; D) Physalaemus nattereri; E) Trachycephalus typhonius; F) Dendropsophus jimi; G) Pithecopus hypochondrialis; H) Leptodactylus furnarius; J) Rhinella mirandaribeiroi.
the Microhylidae (two species), and the Craugastoridae biome (Colli et al., 2002; Brasileiro et al., 2005; Kopp (one species). A total of nine reproductive modes were et al., 2010; Santoro and Brandão, 2014; Oliveira et al., recorded for the 44 species (Table 1). We observe that 2015), as well as the Pantanal (Prado et al., 2005) and the families with the highest number of species have a the Atlantic Forest (Haddad & Prado, 2005). higher number of reproductive modes (Fig. 4). None Nine of the 44 anuran species recorded in the present of the species are listed as endangered by either the study are endemic to the Cerrado (Table 2), and three IUCN (2017) or MMA (2014), although one species of these species had not been recorded previously in (Pithecopus hypochondrialis) is classified as data southwestern Goiás State (Vaz-Silva et al., 2007; Kopp deficient (DD). et al., 2010; Morais et al., 2011; Oliveira et al., 2015). The anuran species richness recorded in southwestern Barycholos ternetzi and Odontophrynus cultripes are Goiás State is equivalent to 6% of the total amphibian typical of the biome (Valdujo et al., 2012) and may be diversity found in Brazil (Segalla et al., 2016), and 22% found in other parts of the Cerrado (Morais et al., 2012). of that confirmed for the Cerrado biome (Valdujo et al., However, Proceratophrys dibernadoi is known only 2012). In Brazil, the Hylidae and the Leptodactylidae from southwestern Goiás State and neighboring areas of are the richest families (Segalla et al., 2016), and this Mato Grosso State (Frost, 2017). predominance is upheld throughout most of the Cerrado Species composition and reproductive modes of anurans from Goiás, Brazil 495
Figure 3. Anuran sampling areas in southwestern Goiás state, central Brazil.
Table 1. Reproductive modes recorded for the anuran species registered in southwestern of Goiás state, central Brazil. Table 1: Reproductive modes recorded for the anuran species registered in southwestern of Goiás state, central Brazil.
Reproductive Description Number of Mode species 1 Eggs and exotrophic tadpoles in lentic bodies of water 27 4 Eggs and early larval stages in natural or constructed pools; following flooding, 1 exotrophic tadpoles in lentic or lotic bodies of water 11 Eggs in foam nest floating on lentic bodies of water; exotrophic tadpoles in lentic 6 bodies of water 13 Eggs in foam nests floating on the water accumulated in constructed pools; 2 extrophic tadpoles in lentic bodies of water 23 Direct development of terrestrial eggs 1 24 Eggs hatching into exotrophic tadpoles that drop into lentic bodies of water 1 30 Foam nest with eggs and early larval stages in constructed subterranean nests, 4 following flooding, exotrophic tadpoles in lentic bodies of water 32 Foam nest in constructed subterranean chambers, endotrophic tadpoles complete 3 development in the nest
496 Seixas Rezende Oliveira et al.
Figure 4. Relationship between species richness and diversity of reproductive modes by family.
Table 2. Anuran species recorded, reproductive modes, and endemism in the Cerrado.
Family/species Present Vaz-Silva Kopp et Morais et Oliveira et Reproductive Endemic study et al. 2007 al. 2010 al. 2011 al. 2015 mode to Cerrado Family Bufonidae Rhinella mirandaribeiroi (Gallardo, 1965) X X X 1 Rhinella diptycha (Cope , 1862) X X X X X 1 Rhinella ocellata (Günther, 1859) X 1 X Family Hylidae Dendropsophus cruzi (Pombal & Bastos, 1998) X X X X 1 X Dendropsophus jimi (Napoli & Caramaschi, 1999) X X X X 1 Dendropsophus minutus (Peters, 1872) X X X X X 1 Dendropsophus nanus (Boulenger, 1989) X X X 1 Dendropsophus rubicundulus (Reinhardt & X X X 1 Lütken, 1862) Dendropsophus melanargyreus (Jim & X X X X 1 Caramaschi, 1980) Boana albopunctata (Spix, 1824) X X X X 1 Boana goiana (B. Lutz, 1968) X 1 X Boana lundii (Burmeister, 1856) X X X 4 Boana paranaiba (Günther, 1859 1858 ) X X X 1 Boana raniceps Cope, 1862 X X X X 1 Pithecopus hypochondrialis (Cope, 1862) X X 24 Scinax constrictus Lima, Bastos & Giaretta, 2004 X X 1 X Scinax fuscovarius (Lutz, 1925) X X X X 1 Scinax fuscomarginatus (A. Lutz, 1925) X X X X X 1 Scinax aff. x-signatus (Spix, 1824) X X 1 Trachycephalus typhonius (Linnaeus, 1758) X X 1 Pseudis bolbodactyla Lutz, 1925 X X X 1 Family Leptodactylidae Adenomera aff. hylaedactyla (Cope, 1868) X X X 32 Adenomera martinezi Bokermann, 1956 X 32 X Adenomera marmorata (Steindachner, 1867) X X 32 Species composition and reproductive modes of anurans from Goiás, Brazil 497
Table 2. Continued.
Family/species Present Vaz-Silva Kopp et Morais et Oliveira et Reproductive Endemic study et al. 2007 al. 2010 al. 2011 al. 2015 mode to Cerrado Leptodactylus furnarius Sazima& Bokermann, 1978 X X X 30 Leptodactylus fuscus (Schneider, 1799) X X X X X 30 Leptodactylus labyrinthicus (Spix, 1824) X X X 13 Leptodactylus latrans (Steffen, 1815) X X X X 11 Leptodactylus mystacinus (Burmeister, 1861) X X X 30 Leptodactylus podicipinus (Cope, 1862) X X X X 13 Leptodactylus sertanejo Giareta & Costa, 2007 X 30 Leptodactylus syphax Bokermann, 1969 X X 11 Pseudopaludicola falcipes (Hensel, 1867) X X X 1 Pseudopaludicola mystacalis(Cope 1887) X 1 Pseudopaludicola saltica (Cope, 1887) X X X 1 X Physalaemus centralis Bokermann, 1962 X X X X X 11 Physalaemus cuvieri Fitzinger, 1826 X X X X X 11 Physalaemus marmoratus (Reinhardt &Lütken, X X X 11 1862 “1861”) Physalaemus nattereri (Steindachner, 1863) X X X X X 11 Family Craugastoridae Barycholos ternetzi (Miranda –Ribeiro,1937) X 23 X Family Microhylidae Chiasmocleis albopunctata (Boettger, 1885) X X X 1 Elachistocleis cesarii (Miranda-Ribeiro, 1920) X X X 1 Family Odontophrynidae Odontophrynus cultripes Reinhardt & Lütken, X 1 X 1861"1862" Proceratophrys dibernadoi Brandão, Caramaschi, X 1 X Vaz-Silva & Campos, 2013
Endemic species make up 51.6% of the anuran fauna of environments sampled in the present study (Table known to occur in the Cerrado, although this scenario 2), only two new reproductive modes (23 and 24) may shift as new species are discovered and existing were recorded for southwestern Goiás State. In fact, taxonomic arrangements are revised (Valdujo et al., previous studies in highly seasonal environments, such 2012). Furthermore, new surveys in areas already as southwestern Goiás itself (Kopp et al., 2010) and the sampled may often result in the detection of amphibian Pantanal (Prado et al., 2005), have tended to record a species not observed previously (Verdade et al., 2012). reduced diversity of reproductive modes. Reproductive mode 1 (extrophic eggs and tadpoles in The homogeneity of reproductive modes are usually lentic bodies of water) was the most common in the attributed to the reduced heterogeneity of microhabitats anuran species of southwestern Goiás State (Tables 1 (Prado et al., 2005; Kopp et al., 2010). The environments and 2). The anuran families with more species tended sampled in the present study are not as heterogeneous as to present a greater number of reproductive modes. For forest habitats (see Kopp et al, 2010), and the climate example, three modes were recorded in the Hylidae, of southwestern Goiás State is characterized by extreme and five in the Leptodactylidae. Similar trends have seasonal fluctuations. Vasconcelos et al. (2010) showed been recorded in the Atlantic Forest (Haddad and that anuran reproductive modes in areas with highly Prado, 2005) and Pantanal (Prado et al., 2005). The seasonal climates tend to be associated with the annual reproductive modes recorded in the present study rains. In the present study, in fact, only modes 23 and included those related to bodies of water (modes 1 and 32 were not associated directly with the presence of 11), the vegetation (mode 24), and the soil (modes 4, sources of water. 13, 23, 30, and 32) (see Table 1). Despite the diversity 498 Seixas Rezende Oliveira et al.
The knowledge of aspects of the natural history of Parque Nacional de Emas e entorno, estado de Goiás, Brasil. the anuran species is primordial for the understanding Iheringia Série Zoologia 100: 192–200. of the ecological interactions and important for the Köppen, W. (1948): Climatologia: con un estudio de los climas de la tierra, Primera Edición. México D. F, Fondo de Cultura establishment of conservation policies. Basic data on Economica. natural history are unknown for many Cerrado species. Martins, A.P., Scopel, I., Souza, M.S., Peixinho, D.M. (2016): Uso Therefore, this paper expands the basic knowledge da terra e cobertura vegetal de 1985 a 2015 no Sudoeste de Goiás of anuran species in a region that historically suffers e relações com o meio físico. In: Reconfiguração do Cerrado - anthropic pressure due to the expansion of agricultural Uso, conflitos e impactos ambientais, p. 11–34. Peixinho, D.M., activities that results in the loss of biodiversity. Sousa M.S., Eds., Goiânia, Brazil, Gráfica UFG. MMA. (2014): Lista Nacional Oficial de Espécies da Fauna Acknowledgments. FAGG, SRO and ARM are grateful to the Ameaçadas de Extinção. Portaria Nº 444. de 17 de dezembro Fundação de Amparo à Pesquisa do Estado de Goiás (CNPq/ de 2014. Available at:
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Accepted by Javier Cortés Suárez