Oecologia Australis 23(4):1027-1052, 2019 https://doi.org/10.4257/oeco.2019.2304.25

anuran SPECIES COMPOSITIOn FrOM CHaCO anD arEaS In CEnTraL

Cyntia Cavalcante Santos1,2*, Eric Ragalzi1, Claudio Valério-Junior1 & Ricardo Koroiva3

1 Universidade Federal de Mato Grosso do Sul, Programa de Pós-Graduação em Ecologia e Conservação, Av. Costa e Silva, s/n, Cidade Universitária, CEP 79070-900, Campo Grande, MS, Brazil.

2 Université d’Angers, UMR CNRS 6554 LETG-Angers, UFR Sciences, 2Bd Lavoisier, 49045, cedex 01, Angers, France.

3 Instituto Nacional de Pesquisas da Amazônia, Coordenação de Biodiversidade, Av. André Araújo, 2936, Petrópolis, CEP 69067-375, Manaus, AM, Brazil.

E-mails: [email protected] (*corresponding author); [email protected]; juniorvalerio19@gmail. com; [email protected] abstct: Herein, we present an updated inventory and the variations o rog communities’ composition rom ve areas o humid Chaco and Cerrado in municipality o Porto Murtinho, Mato Grosso do Sul state, Brazil. This municipality is located in an area with three : Chaco, Cerrado and . Through acoustic and visual nocturnal/diurnal and pitall evaluations rom a period o over ve years, we recorded 31 species in the Cerrado and 29 species in the humid Chaco. About 90% o the species were previously registered in the municipality o Porto Murtinho. A non-metric multidimensional analysis based on a presence/absence matrix revealed a separation in our sampling sites and communities with Cerrado and humid Chaco characteristics. This peculiarity in the species composition must be related to the transition zone, with the presence o mixed species characteristics o Cerrado and humid Chaco in both areas in the municipality o Porto Murtinho experiences a high degree o deorestation pressure, which threatens both the Cerrado and humid Chaco vegetation. This highlights the importance o knowledge actions about the richness and composition o species, corroborating ecological tools to support conservation in this region.

Keyods: Amphibia; Porto Murtinho; species inventory; transition zone.

InTrODuCTIOn heterogeneous distribution o sampling eorts or many taxonomic groups emphasizes the need to Species inventories are an important starting point conduct and update local inventories, especially or biology as these records help us understand or threatened taxa (Uetanabaro et al. 2007, Jenkins patterns and processes o biodiversity dynamics et al. 2015, Gutiérrez & Marinho-Filnho 2017). Even (Hortal et al. 2015). These catalogues o species so, studies have been discussed the problem that diversity can also indicate knowledge gaps and many areas o the world have been poorly sampled provide relevant data or conservation plans, as well regarding most taxa, generating inadequate as identiy priorities (Stohlgren et al. 1995). Despite inormation about species distributions at global, the request or global eorts to obtain inormation regional, and local levels (Wallacean shortall), about biodiversity (CBD Secretariat 1992), the and they highlight that this diversity still needs to 1028 Anuran species o the Chaco and Cerrado in central Brazil be adequately described and cataloged (Linnean MaTErIaL anD METHODS shortall) (Whittaker et al. 2005, Hortal et al. 2015). In Brazil, the Cerrado, Chaco and Caatinga Study area are part o the so-called dry diagonal o vegetal This study was conducted at ve sites located in et al. ormations (Prado & Gibbs 1993, Neves 2015). the municipality o Porto Murtinho, State o Mato These ormations present seasonally dry periods, Grosso do Sul, Brazil. Three locations presented adapted vegetation and complex distribution, Cerrado vegetation characteristics and yet ew studies have been done related to their two locations presented humid Chaco ecoregion biodiversity and conservation (Oliveira-Filho vegetation characteristics, ollowing (Dinerstein et al . 2006). At a regional level, inormation and et al. 2017) (Table 1; Figure 1). The municipality o conservation actions are needed in areas o Porto Murtinho presents large territorial extension Cerrado and Chaco, which has repeatedly been (17744.4 km²; IBGE 2017), high environmental et al. et al. stressed (Banda-R 2016, Roque 2016) heterogeneity (Pott et al. 2011) and it is considered a The Chaco presents high conservation priority transition area o the Chaco, Cerrado and Pantanal et al. due to its peculiar auna and ora (Dinerstein ecoregions (Benites et al. 2017). The climate o the 1995), while the Cerrado is one o the 35 worldwide region is Aw, according to Köoppen, with a hot and et al. biodiversity hotspots (Mittermeier 2011). The wet summer, and a dry and cool winter (Climate- high level o land-to-agriculture conversion and date 2017). At the same time, the region is conducive the poor status o land protection are the main to the development o agricultural activities, which et al. problems that these domains ace (Silva 2006). have been carried out or a long time in the region Research about the ecology o anuran and its surrounding areas, as shown by Souza et al. communities in these ormations has increased (2017). knowledge about species distribution in dierent localities (e.g., Maei et al. 2011, Santos et al. 2011, Species data Gambale et al. 2014, Pereira et al. 2016). The order Species samplings rom selected sites (Table 1) Anura is a threatened vertebrate group in the were perormed during six months and a total o worldwide (Storer 2003, Stuart 2004, Whiles et al. eight eld surveys completed in ve areas, with 2006), mainly due to habitat loss (Becker et al. 2007, our in the dry season (August 2013, September Becker & Zamudio 2011). Brazil has about 1,039 2014, August 2015 and August 2016) and our in the anuran species (Segalla et al. 2016) with knowledge rainy season (March 2014, January 2015, December gaps or the southwestern Mato Grosso do Sul state 2015 and January 2017). The sampling eort was (Souza et al. 2017). calculated as the listening hours done by each In this study, we present a survey about the researcher (total hours/campaign x 2 researchers x anuran composition in Chaco and Cerrado total number o campaigns), totaling 128 h. For the ormations in the southeast region o Porto capture eort o pitall traps, eort calculation was Murtinho, a municipality located in a Chaco, made using the amount o days per campaign times Cerrado and Pantanal transition zone o Mato the number o buckets (pitalls), totaling 704 h. Grosso do Sul, Brazil (e.g., Souza et al. 2010, Benites Capture methods were adopted using pitall et al. 2017, Dinerstein et al. 2017). We updated the traps and active search (visual and acoustic species list rom this municipality and compared encounters) (Heyer et al. 1994). To install pitalls, the species composition o our sampling sites ~20 m long trails were made within the native to studies carried out in nearby areas, aiming to vegetation, where Y- lines were then installed with understand how the anuran communities vary in ve or six 60 l buckets set with 5-m intervals. We transitions zones o these ecoregions. In addition, considered a minimum distance o 5 m rom the keeping in mind the high anthropic pressure in the edge o the orest to the beginning o each pitall vegetation environments in the municipality, we line. The acoustic method was carried out or two demonstrate the conservation status o the anuran days during each campaign (17:00 to 21:00 h) in species inventoried in this study. two existing water bodies near the Cerrado site 3 and Chaco site 2. This temporal patterning was

Oecol. Aust. 23(4): 1027–1052, 2019 Santos et al. | 1029

Tble 1. Sampling sites o anurans rom the Cerro Porã and Cangalha arms, municipality o Porto Murtinho, Mato Grosso do Sul, Brazil, and geographic coordinates (datum WGS 84).

Site Ltitde Loitde Loctio

Savannah area in ecological corridor between hills Cerrado 1 (Cr1) 22°1’47.86” S 57°29’21.30” W characterized by open trees and dense tree vegetation

Steppic Savannah with Attalea phalerata (Mart. Ex Cerrado 2 (Cr2) 22°2’28.94” S 57°32’2.58” W Spreng.), in a Protect Area inside a suppression area

Portion o the study area with remnants o vegetation Cerrado 3 (Cr3) 22°0’59,38” S 57°27’9.40” W characteristic o Cerradão. Also perormed acoustic technique in a permanent water pound

Chaco 1 (Ch1) 22°6’43.87” S 57°27’55.96” W Near a Mata Ciliar o the Rio Perdido Next to a mountain chain characterized by Steppic Chaco 2 (Ch2) 22°8’7.44” S 57°33‘57.00“ W Savannah. Also perormed acoustic technique in a permanent water pound

Fie 1. Localization o sampling points or anurans o the municipality o Porto Murtinho, Mato Grosso do Sul State, Brazil. A) Map o highlighting the geopolitical division o Brazil; B) Municipality division o the Mato Grosso do Sul State, Brazil, with distribution o dierent ecoregions in the municipality o Porto Murtinho, as delineated by Dinerstein et al. (2017): yellow = humid Chaco; brow = dry Chaco; green = Pantanal; orange = Cerrado. Abbreviations correspond to sampling points and are described at Material and Methods section.

Oecol. Aust. 23(4): 1027–1052, 2019 1030 Anuran species o the Chaco and Cerrado in central Brazil established due to the behavioral variations o the Data analysis species regarding vocalization habits (Wells 1977, In order to determine i the composition o the Rodrigues et al. 2003, Prado et al. 2005, Moreira et anurans species varied among our studied areas al. 2007, Toledo et al. 2007, Uetanabaro et al. 2008). (which we consider as a “transition area” o humid During the samplings each group o pitall traps Chaco and Cerrado) and other similar studies in was visited once a day. The captured specimens ecoregions o humid Chaco, Cerrado and Pantanal (Environmental Authorization or Wildlie (Uetanabaro et al. 2007, Souza et al. 2010, Pansonato Management in situ IMASUL n° 23/104460/2013 e n° et al. 2011, Sugai et al. 2014b, Pesci et al. 2018), 61/402873/2015) were photographed and released we perormed a Non-Metric Multidimensional in capture locations ater species identication Scaling (NMDS) analysis ollowed by a pairwise by comparing their morphological characteristics comparison o Analysis o Similarity (ANOSIM) observed in the eld and revising their original or using Paleontological Statistics sotware (v. 3.18). revalidated descriptions to support the taxonomic For this analysis, our data were both evaluated as a identications (Ribeiro et al. 2005, Toledo et al. “transition zone” o humid Chaco and Cerrado and 2007, Uetanabaro et al. 2008). We ollowed Frost also as belonging to one o these ecoregions. The (2018) or the nomenclature o amphibians. previous studies were chosen because they were Aiming to improve our list o species, we carried out in landscapes with similar congurations used online databases to nd registers o anuran as the River basin (ZEE 2009) and the Apa species rom the municipality o Porto Murtinho River basin, such as vegetation ragments inserted in published articles. Specically, we used Web into regions with predominance o cattle ranching. o Science (which includes the main academic Also, authors o these studies used similar methods journals o world), Scielo (which includes the main or sample and to identiy anuran species (i.e., journals o South America) and Google Scholar. We acoustic and pitall traps). We did not consider the searched or general keywords such as “anuran”, temporal scale, since temporal variations in each “rog”, “sapo” (“rog” in Portuguese) in combination study are oten planned according to logistical with “Mato Grosso do Sul” and “Porto Murtinho”. conditions and technical and nancial resources. Uetanabaro et al. (2007), Rosset et al. (2009), Souza The NMDS was based on the presence and et al. (2010, 2017), Amaral et al. (2012), Sugai et absence matrix o anuran species and used the al. (2012), Sugai et al. (2014a) and Pansonato et Jaccard index o similarity. The order distortion in al. (2011) provided additional inormation about relation to the original data matrix was determined registers o anuran species. Considering the by stress. According to Clarke (1993), stress values opinion o experts (see Acknowledgements), we around 0.2 correspond to a regular t, while level removed our species rom the species list o Souza around 0.1 indicate a good t and a value close to et al. (2017): Boana crepitans (Wied-Neuwied 0 is an excellent t. Finally, or the eort analysis, 1924), Scinax similis (Cochran, 1952), Adenomera we constructed an accumulation curve o species martinezi (Bokermann 1956) and Leptodactylus richness (presence/absence data) based on gracilis (Duméril & Bibron 1840). According to this our survey data and estimated species richness view, the presence o these species in the state is through Chao 2 and Jackknie 1 with one thousand questionable, thus we decided to remove them in randomizations using the EstimateS 9.1.0 program order to avoid overestimation o the number o (Colwell 2013). species or Mato Grosso do Sul state. The conservation status o the species was rESuLTS classied according to the International Union or Conservation o Nature and Natural Resources Anuran composition in the municipality of Porto Red List o Threatened Species (IUCN 2018). This Murtinho study also classied species using the CITES list During the ve years o collection we ound 31 (Convention on International Trade in Endangered species in the study sites in the Cerrado and 29 Species o Wild Fauna and Flora) (CITES 2017) and species in environments with Chaco characteristics. the Brazil’s ofcial list o endangered species (Brasil In total, 32 species o anurans, distributed in 2014). ve amilies and 16 genera, were ound in both

Oecol. Aust. 23(4): 1027–1052, 2019 Santos et al. | 1031 vegetation ormations (Table 2; Figure 2). The (N = 25) and Nobres (N = 39) in Mato Grosso State Cerrado sites showed higher species richness and (Santos et al. 2011, Silva et al. 2015), Barro Alto (N Leptodactylidae (N = 13) and Hylidae (N = 10) were = 39) in the Goiás State (Gambale et al. 2014), and the most representative amilies. About 90% o the Borebi (N = 27), São Paulo State (Maei et al. 2011). species (N = 29) we recorded had previously been All species rom our study area have previously registered in the municipality, with rst records o been recorded in Mato Grosso do Sul State (Souza Leptodactylus mystacinus, Leptodactylus syphax, et al. 2017) (Figure 4), but their occurrence was not and Boana albopunctata. Considering previous uniorm. Boana albopunctata, which we recorded studies about species occurrence in Chaco and in locations in the Chaquenha region, has only Cerrado regions in the municipality o Porto previously been recorded in the Cerrado o Mato Murtinho, 43 species had previously been listed. Grosso do Sul State. This species were previously Through the NMDS analysis (stress = 0.1329), ound in several environments, including at we were able to distinguish a pattern o species lands and ooded areas, like the collection areas composition among the ecoregions (Figure 3). The (Toledo et al. 2003, Araújo et al. 2007). On the other species compositions o our sampling sites were hand, Rhinella azarai, L. syphax, Rhinella scitula, visually much more similar to each other than to Elachistocleis motogrosso and L. mystacinus preer the other areas. Despite this hypothesis, through alluvial orest environments, with open elds close ANOSIM, we were unable to nd signicant to temporary or permanent ponds, characteristics dierences considering our areas as “transition that may be associating such species to the areas o region” (R = 0.5556, p = 0.0663) or belonging to Chaco that present great diversity o environments ecoregion classications as Cerrado and humid and climatic changes throughout the year (Zavattini Chaco (R = 0.3519, p = 0.1061). 2009, Pott et al. 2014). The estimators o species richness showed Considering our sampling, Boana punctata, that the observed richness or our sampling sites Pseudopaludicola motorzinho and Rhinella corresponded to 95.6% and 85.9% o the medium diptycha were only ound in Cerrado sites, while estimated richness by Chao 2 (S est = 33.46, SD = B. albopunctata was only ound in the humid 1.84) and Jackknie 1 (S est = 37.25, SD = 4.34), Chaco. O the 31 species registered in the Cerrado respectively (Figure 3). sites, Leptodactylus buonius had no previous Considering this and previous studies, we registers in this ecoregion in Mato Grosso do Sul registered 46 species o anurans in the municipality State according to Souza et al. (2017). However, o Porto Murtinho. None species are listed on the in that year, Faggioni et al. (2017) described the Brazilian Ministry o the Environment’s List o reproductive biology o an L. buonius population Threatened Species and CITES. Following the o this species rom a location in the municipality IUCN Red List (IUCN 2018), Lepidobatrachus asper o Porto Murtinho. In the case o the humid Chaco, is considered as “Near Threatened”, six species are R. azarai and R. scitula have previously been categorized as “Data Decient” and 39 species are registered by Narvaes & Rodrigues (2009) and categorized as “Least concern” (Table 2). Sugai et al. (2014a), respectively, but L. syphax, E. matogrosso and L. mystacinus also had not been DISCuSSIOn registered prior to this region o Mato Grosso do Sul State, according to Souza et al. (2017). In addition, The amphibian species composition ound in this two other species, Proceratophrys dibernardoi study represents approximately 20% o the total (Ferreira et al. 2016) and Ameerega berohoka number o species estimated in the Cerrado and (Sant’anna et al. 2017), were recently recorded in Brazilian Chaco (Souza et al. 2010, Valdujo et al. two sites o Mato Grosso do Sul State. Thus, such 2012) and about 40% o the species estimated in the as in other animal groups (e.g., Koroiva et al. 2017, State o Mato Grosso do Sul. To date, the number Rodrigues et al. 2018), new inventories should still o species recorded in the municipality o Porto increase the number o species recorded or both Murtinho (i.e., N = 46 species) is higher than the Cerrado and humid Chaco in the state. number o species rom other municipalities in In summary, the dierences ound between the south-central Brazil, such as Primavera do Leste species composition rom the humid Chaco and

Oecol. Aust. 23(4): 1027–1052, 2019 1032 Anuran species o the Chaco and Cerrado in central Brazil ho co to ti Po M ho oCh do to ti Po M Continuedpage... onnext ble ble 2. oCe co T mos oCh co oCh do lity / / lity rom IUCN Red List (2018). PNSB = Parque= SerradaPNSBNacional da List (2018). rom RedIUCN SM Fo MS MS ã Loc ed) ed) oCe do p m Porto Murtinho and Mato Grosso do Sul State (MS), Brazil. Conservation Ce l sC es t Cáce cient, NC = non-classi= cient,NC ho romthe municipality o oP co to Porto Murtinho, MatoGrosso do Sul, Brazil. ti Po M oCh do PnSB Ce Chaco and Cerrado s t Cxxxxxxxx x x x x x x x x x x x x LC LC LC Cxxxxxx x x x x x x x x x LC x LC LC IuCn st anurans species o e * * id fo Checklist o ernandezae ulvoguttatus mily B mily Rhinella bergi (Céspedez,2000) Rhinella diptycha (Cope, 1862) Rhinella (Gallardo, 1957) Melanophryniscus (Mertens, 1937) Melanophryniscus klappenbachi PrigioniLangone, & 2000 azarai Rhinella (Gallardo, 1965) ble ble 2. Species F T dedata DD= concern; leastthreatened; near LC = = (NT status Bodoquena.*Species recorded only the municipalityo in

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...Continued Rhinella major Rhinella (MullerHelmich, & 1936) Rhinella mirandaribeiroi (Gallardo, 1965) ocellata Rhinella (Günther, 1858) Rhinella paraguayensis Ávila, Pansonato& Strüssmann, 2010 rubescens Rhinella (A. Lutz, 1925) scitula Rhinella (Caramaschi& Niemeyer, 2003) ble ble 2. Species T

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e e e id

Barrio, y id yid * 1985 Cei, sto * Budgett,1899 ...Continued toph toph mily mily mily Ceratophrys cranwelli 1980 Lepidobatrachus asper Haddadus binotatus (Spix,1824) Odontophrynus americanus (Duméril Bibron,& 1841) Odontophrynus lavillai ble ble 2. Species F Ce F C F Odo T

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e e (Napoli (Napoli & tid (Miranda- ...Continued ob d mily Hylidmily Dendropsophus araguaya Caramaschi,1998) Dendropsophus cerradensis & Caramaschi,1998) Proceratophrys goyana Ribeiro,1937) Ameerega picta (Tschudi,1838) Ameerega braccata punctataBoana (Schneider, 1799) ranicepsBoana (Cope,1862) ble ble 2. Species F De F T

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Napoli & (Peters, (Boulenger, ...Continued (Napoli & Dendropsophus nanus 1889) Dendropsophus rubicundulus (Reinhardtand Lütken, 1862) Dendropsophus ( elianeae Caramaschi,2000) Dendropsophus jimi Caramaschi,1999) Dendropsophus melanargyreus (Cope,1887) Dendropsophus microcephalus (Cope,1886) Dendropsophus minutus 1872) ble ble 2. Species T

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(Spix, (Schmidt, ...Continued Dendropsophus sanborni 1944) albopunctata Boana (Spix,1824) af.Boana geographica 1824) caingua Boana (Carrizo, 1991) crepitansBoana (Wied-Neuwied, 1924) lundiiBoana (Burmeister,1856) Lysapsuslimellum Cope,1862 Osteocephalus taurinus Steindachner, 1862 ble ble 2. Species T

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uscovarius ...Continued uscomarginatus Scinax (Lutz,1925) Scinax nasicus (Cope, 1862) Scinax ruber (Laurenti, 1768) Scinax squalirostris (Lutz,1925) Pseudisparadoxa (Linnaeus, 1758) Pseudisplatensis Gallardo,1961 Scinax acuminatus (Cope,1862) Scinax constrictus Lima, Bastos& Giaretta, 2005 Scinax (Lutz,1925) ble ble 2. Species T

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Boulenger, * ctylid ...Continued onius mily mily Adenomeradiptyx (Boettger,1885) Adenomera hylaedactyla 1868) Leptodactylus bu Boulenger, 1894 Trachycephalus typhonius (Linnaeus, 1758) Phyllomedusa sauvagii 1882 Pithecopus azureus (Cope,1862) ble ble 2. Species F Phyllomed F Leptod T

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uscus (Spix, en, en, Cei, 1950 Sazima & Jiménez (Ste Sazima& ...Continued urnarius Leptodactylus Bokermann,1978 Leptodactylus (Schneider,1799) Leptodactylus jolyi Bokermann, 1978 Leptodactylus labyrinthicus 1824) Leptodactylus latinasus de Espada, la 1875 Leptodactylus latrans 1815) Leptodactylus chaquensis Leptodactylus elenae Heyer,1978 ble ble 2. Species T

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(Cope, (Spix,

Bokermann, ...Continued Leptodactylus syphax 1969 Physalaemus albonotatus (Steindachner, 1864) Physalaemus biligonigerus 1861 “1860”) Physalaemus centralis Bokermann, 1962 Leptodactylus mystaceus 1824) Leptodactylus mystacinus (Burmeister,1861) Leptodactylus podicipinus 1862) ble ble 2. Species T

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Miranda- ...Continued Pseudopaludicola motorzinho Pansonato, Veiga- Menoncello, Mudrek,Jansen, Recco-Pimentel, Martins & Strüssmann,2016 Pseudopaludicola ternetzi Ribeiro,1937 Physalaemuscuvieri Fitzinger,1826 Physalaemus marmoratus (Reinhardt & Lütken, 1862) Physalaemus nattereri (Steindachner,1863) ble ble 2. Species T

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e

ohylid (Boettger, Caramaschi ...Continued er & er Vaira, 2013 mily Micmily Chiasmocleis albopunctata (Boettger,1885) Chiasmocleis mehelyi 1997 and Cruz, Dermatonotus muelleri 1885) Elachistocleis bicolor (Guérin-Menéville, 1838) Elachistocleiscesarii (Miranda Ribeiro (1920)) Elachistocleisharoi Pereyra,Akmentins, Lau ble ble 2. Species F T

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Fie 2. Species accumulation curve comparing the number o observed species (Sobs, squares) and the estimated richness o anuran species or our sampling sites in the municipality o Porto Murtinho, Mato Grosso do Sul, Brazil. The estimates were calculated with the estimator Chao 2 and Jackknie 1. Black diamonds = number o species observed (est); Black square= Chao 2 richness estimator; Light grey circles = Jackknie 1 richness estimator.

Fie 3. Nonmetric multidimensional scaling o the selected studies or species composition o anurans o the municipality o Porto Murtinho, Mato Grosso do Sul State, Brazil and comparison with dierent areas o the diagonal o dry vegetal ormations.

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Fie 4. Species registered in the study area in the municipality o Porto Murtinho, Mato Grosso do Sul, Brazil. a) Boana raniceps, b) Dendropsophus nanus, c) Chiasmocleis albopunctata, d) Melanophryniscus ulvoguttatus, e) Leptodactylus buonius, ) Leptodactylus mystacinus, g) Leptodactylus chaquensis, h) Physalaemus nattereri, i) Adenomera diptix, j) Rhinella scitula, k) Phyllomedusa sauvagii, l) Pithecopus azureus. Photos by Cyntia C. Santos and Berinaldo Bueno

Cerrado and other areas with the same ormations that are connected to each other, such as at (Uetanabaro et al. 2007, Souza et al. 2010, Sugai lands and natural springs between limestone, et al. 2014a) must be related to the preerences natural and temporary water bodies and swamps between the type o environment where the or permanent dams, in addition to alluvial orests species were ound. Considering that this study and the riparian orests o the Perdido River, area is in the Chaco and Cerrado transition zone, present a complex and permissible environment the presence o dierent phytophysiognomies or a wide variety o species. As stated by Zanella

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(2011), the evolutionary history o the Caatinga, severe vegetation loss (Harris et al. 2006) in Cerrado and Chaco could be independent, since recent years deserves greater concern and action the endemic patterns or each o these regions have because o the wide diversity o anuran species specic characteristics (Morrone 2014). However, (Rosset et al. 2009, Souza et al. 2010, 2017, Sugai in transition zones, multiple actors can cause et al. 2013). The municipality o Porto Murtinho the dierentiation o community composition is the only place in Brazil where Odontophrynus (Kark et al. 2007, Vasconcelos et al. 2010, Sabbag & lavillai (Rosset et al. 2009) and L. asper (Sugai et Zina 2011) we hypothesized that anuran species al. 2013) occur, the latter being recorded as “near richness and the number o reproductive modes threatened” by the IUCN (2018) in Mato Grosso rom dierent Brazilian localities vary according do Sul State. Thus, the anuran composition and to climatic and altitudinal variables. Published the great landscape complexity o the Chaco and data were compiled rom 36 Brazilian localities and Cerrado environments evidence the importance climatic and altitudinal data were extracted rom o increasing studies about the ecology o an available database. In addition to ecological communities and natural history o species, such and historical processes (Moritz et al. 2000), as those that make up the municipality o Porto today we discuss how the scale inuences these Murtinho, since they are necessary and important aspects and changes the species responses (Willis or conservation o organisms and or sensitive & Whittaker 2002, Kark & van Rensburg 2006). regions with high levels o anthropogenic threats. Obviously, water availability is still considered a key actor or maintaining rogs since these taxa aCKnOwLEDgMEnTS are totally dependent on this resource or their survival (Duellman & Trueb 1994, Pough et al. We thank Mahil Agropecuária and Città 2015), but, intrinsic characteristics o each species Planejamento Urbano e Ambiental or supporting might outweigh the delimitation in previously this work. We thank also three anonymous established ecoregions. reerees and the herpetology expert, Diego José As highlighted by Morais et al. (2013), there Santana, or their very useul suggestions and are still ew studies about the natural history and comments. We thank Berinaldo Bueno or his distribution range o many anuran species. About photos o Leptodactylus buonius, Phyllomedusa 15% o the species ound in the municipality o sauvagii and Pithecopus azureus. CCS, CVJ, RK and Porto Murtinho has not previously been classied ERS were nanced in part by the Coordenação de on the endangered species lists, especially classed Apereiçoamento de Pessoal de Nível Superior as “Data Decient”. Species inventories could ll - Brasil (CAPES) – Finance Code 001. CCS such knowledge gaps and improve insight on the received nanced in part also a FUNDECT-MS actual risk situation o species in Mato Grosso do and Capes/Coecub (Project n°875/2017 Process Sul State, particularly regarding knowledge about n°88887.143361/2017-00). R.K. was supported geographic distribution. In addition, recently, the by PNPD/CAPES Program Fellowship and high level o environmental diversity, ecological FIXAM-I/FAPEAM (Ed. n°005/2018 Process n° peculiarities, and the presence o endemic 062.01503/2018) postdoctoral scholarship. species have raised the interest o researchers in the municipality o Porto Murtinho, which rEFErEnCES have improved the knowledge o taxonomically undersampled groups and attracting new Amaral, I. B., Landgre-Filho, P., Souza, F. L., & researchers and opportunities to this municipality Uetanabaro, M. 2012. Melanophryniscus (e.g. Gomes & Araujo 2015, Gomes et al. 2016, klappenbachi distribution. Herpetological Benites et al. 2017). Review, 43, 98. Newly named one o the top priority Araújo, F. R. R. C., Bocchiglieri, A., & Holmes, R. conservation areas by the Brazilian Ministry M. 2007. Ecological aspects o the Hypsiboas o the Environment, the municipality o Porto albopunctatus (Anura, Hylidae) in central Brazil. Murtinho is greatly important or biodiversity Neotropical Biology and Conservation, 2(3), conservation (Brasil 2016). The municipality’s 165–168.

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Banda-R, K., Delgado-Salinas, A., Dexter, K. G., rom https://www.cbd.int/doc/legal/cbd-en. Linares-Palomino, R., Oliveira-Filho, A., Prado, pd D., Pullan, M., Quintana, C., Riina, R., Rodriguez CITES - Convenção sobre o Comércio Internacional M., G. M., Weintritt, J., Acevedo-Rodriguez, das Espécies da Fauna e da Flora Silvestres P., Adarve, J., Alvarez, E., Aranguren B., A., Ameaçadas de Extinção. 2017. Appendix I, II Arteaga, J. C., Aymard, G., Castano, A., Ceballos- and III valid rom 4 October 2017. Retrieved Mago, N., Cogollo, A., Cuadros, H., Delgado, F., on November 1st, 2017, rom https://cites. Devia, W., Duenas, H., Fajardo, L., Fernandez, org/sites/deault/iles/eng/app/2017/E- A., Fernandez, M. A., Franklin, J., Freid, E. Appendices-2017-10-04.pd H., Galetti, L. A., Gonto, R., Gonzalez-M., R., Clarke, K. R. 1993. Non-parametric multivariate Graveson, R., Helmer, E. H., Idarraga, A., Lopez, analyses o changes in community structure. R., Marcano-Vega, H., Martinez, O. G., Maturo, Austral Ecology, 18(1), 117–143. DOI: 10.1111/ H. M., McDonald, M., McLaren, K., Melo, O., j.1442-9993.1993.tb00438.x Mijares, F., Mogni, V., Molina, D., Moreno, N. d. P., Climate-date. 2017. Dados climáticos para cidades Nassar, J. M., Neves, D. M., Oakley, L. J., Oatham, mundiais. Retrieved on January 1st, 2017, rom M., Olvera-Luna, A. R., Pezzini, F. F., Dominguez, https://pt.climate-data.org/location/43479/ O. J. R., Rios, M. E., Rivera, O., Rodriguez, N., Colwell, R. K. 2013. EstimateS: Statistical estimation Rojas, A., Sarkinen, T., Sanchez, R., Smith, M., o species richness and shared species rom Vargas, C., Villanueva, B., & Pennington, R. T. samples. Version 9. User’s Guide and application. 2016. Plant diversity patterns in neotropical Dinerstein, E., Olson, D., Joshi, A., Vynne, C., dry orests and their conservation implications. Burgess, N. D., Wikramanayake, E., Hahn, N., Science, 353(6306), 1383–1387. DOI: 10.1126/ Palminteri, S., Hedao, P., Noss, R., Hansen, science.aa5080 M., Locke, H., Ellis, E. C., Jones, B., Barber, C. Becker, C. G., Fonseca, C. R, Haddad, C. F. B., V., Hayes, R., Kormos, C., Martin, V., Crist, E., Batista, R. F., & Prado, P. I. 2007. Habitat split and Sechrest, W., Price, L., Baillie, J. E. M., Weeden, the global decline o amphibians. Science 318, D., Suckling, K., Davis, C., Sizer, N., Moore, R., 1775-1777. DOI 10.1126/Science.1149374 Thau, D., Birch, T., Potapov, P., Turubanova, S., Becker, C. G., & Zamudio, K. R. 2011. Tropical Tyukavina, A., de Souza, N., Pintea, L., Brito, amphibian populations experience higher J. C., Llewellyn, O. A., Miller, A. G., Patzelt, A., disease risk in natural habitats. Proceedings Ghazanar, S. A., Timberlake, J., Klöser, H., o the National Academy o Sciences, 108(24), Shennan-Farpón, Y., Kindt, R., Lillesø, J.-P. B., van 9893–9898. DOI: 10.1073/pnas.1014497108 Breugel, P., Graudal, L., Voge, M., Al-Shammari, Benites, M., Mamede, S., Carvalho, G., & Alho, C. K. F., & Saleem, M. 2017. An ecoregion-based J. 2017. Assessment o avian occurrence in the approach to protecting hal the terrestrial realm. Brazilian Chaco. International Journal o Avian Bioscience, 67(6), 534–545. DOI: 10.1093/biosci/ & Wildlie Biology, 2(4), 26. DOI: 10.15406/ bix014 ijawb.2017.02.00026 Dinerstein, E., Olson, D. M., Graham, D. J., Webster, Brasil. 2014. Portaria na 444, de 17 de dezembro A. L., Primm, S. A., Bookbinder, M. P., & Ledec, G. de 2014: Atualização da lista nacional ocial de 1995. una evaluacion del estado de conservacion espécies da auna ameaçadas de extinção. pp. de las eco-regiones terrestres de America 121-126. Brasilia, DF. Latina y el Caribe. Washington, D.C.: Banco Brasil. 2016. Áreas prioritárias para conservação, Internacional de Reconstrucción y Fomento/ uso sustentável e repartição dos beneícios da Banco Mundial: p. 135. biodiversidade. Retrieved on November 23rd, Duellman, W. E., & Trueb, L. 1994. Biology o 2016, rom http://www.mma.gov.br/images/ amphibians. Baltimore: The Johns Hopkins arquivo/80049/Areas Prioritarias/Cerrado University Press: p. 670. e Pantanal/FICHA%0AS Areas Prioritarias Faggioni, G. P., Souza, F. L., Uetanabaro, M., Cerrado e Pantanal_2 atualizacao 22ago16.pd Landgre-Filho, P., & Prado, C. P. A. 2017. Diet o CBD Secretariat. 1992. Convention on Biological Leptodactylus buonius Boulenger, 1894, in the Diversity. Retrieved on September 25th, 2017, brazilian Chaco. Herpetozoa, 30(1/2), 72–76.

Oecol. Aust. 23(4): 1027–1052, 2019 Santos et al. | 1049

Ferreira, C. M. M., Sugai, J. L. M. M., Souza, F. L., 2017. Resolução no 2, de 29 de junho de 2017. p. Andrade, S. P., Vaz-Silva, W., Bastos, R. P., & 96. Morais, A. R. 2016. The advertisement call and IUCN - International Union or Conservation o geographic distribution o Proceratophrys Nature. 2018. IUCN Red List o Threatened dibernardoi Brandão, Caramaschi, Vaz-Silva species. Retrieved on October, 23, 2018 rom & Campos 2013 (Anura, Odontophrynidae). http://www.iucnredlist.org Zootaxa, 4205(5), 480. DOI: 10.11646/ Jenkins, C. N., Alves, M. A. S., Uezu, A., & Vale, zootaxa.4205.5.6 M. M. 2015. Patterns o vertebrate diversity Frost, D. R. 2018. Amphibian species o the world: and protection in Brazil. PLOS ONE, 10(12), an online reerence. Version 6.0. Retrieved e0145064. DOI: 10.1371/journal.pone.0145064 on October 23, 2018, rom http://research. Kark, S., Allnutt, T. F., Levin, N., Manne, L. L., & amnh.org/herpetology/amphibia/index.html. Williams, P. H. 2007. The role o transitional American Museum o Natural History, New York, areas as avian biodiversity centres. Global USA. Ecology and Biogeography, 16(2), 187–196. DOI: Gambale, P. G., Woitovicz-Cardoso, M., Vieira, R. 10.1111/j.1466-8238.2006.00274.x R., Batista, V. G., Ramos, J., & Bastos, R. P. 2014. Kark, S., & van Rensburg, B. J. 2006. Ecotones: Composição e riqueza de aníbios anuros em marginal or central areas o transition? Israel remanescentes de Cerrado do Brasil Central. Journal o Ecology & Evolution, 52(1), 29–53. Iheringia - Série Zoologia, 104(1), 50–58. DOI: DOI: 10.1560/IJEE.52.1.29 10.1590/1678-4766201410415058 Koroiva, R., Rodrigues, M. E., Valente-Neto, F., & Gomes, V. G. N., & Araujo, A. C. 2015. Cacti species Roque, F. O. 2017. Odonates rom Bodoquena rom the Brazilian Chaco: oral and ruit traits. Plateau: checklist and in ormation about Gaia Scientia, 9(2), 1–8. endangered species. Biota Neotropica, 16(3), Gomes, V. G. N., Koroiva, R., & Araujo, A. C. 2016. e20160310. DOI: 10.1590/1676-0611-BN-2016- Vertebrate orivory on the short-columnar 0310 cactus Echinopsis rhodotricha K. Schum. in the Maei, F., Ubaid, F. K., & Jim, J. 2011. Anuroauna Brazilian Chaco. Plant Ecology, 217(12), 1481– em área de cerrado aberto no município de 1487. DOI: 10.1007/s11258-016-0659-9 Borebi, estado de São Paulo, Sudeste do Brasil: Gutiérrez, E., & Marinho-Filnho, J. 2017. The uso do habitat, abundância e variação sazonal. mammalian aunas endemic to the Cerrado Biota Neotropica, 11(2), 221–233. DOI: 10.1590/ and the Caatinga. ZooKeys, 644, 105–157. DOI: S1676-06032011000200023 10.3897/zookeys.644.10827 Mittermeier, R. A., Turner, W. R., Larsen, F. W., Harris, M. B., Arcângelo, C., Pinto, E. C. T., Camargo, Brooks, T. M., & Gascon, C. 2011. Global G., Ramos-Neto, M. B., & Silva, S. M. 2006. biodiversity conservation: The critical role Estimativa da perda de cobertura vegetal o hotspots. Biodiversity Hotspots. pp. 3–22. original na Bacia do Alto Paraguai e Pantanal Berlin, Heidelberg: Springer Berlin Heidelberg. brasileiro: ameaças e perspectivas. Natureza e DOI. 10.1007/978-3-642-20992-5_1. Conservação, 4(2), 50–66. Morais, A. R., Siqueira, M. N., Lemes, P., Maciel, N. Heyer, W. R., Donnelly, M. A., McDiarmid, R. W., M., De Marco, P., & Brito, D. 2013. Unraveling the Hayek, L.-A. C., & Foster, M. S. 1994. Measuring conservation status o Data Decient species. and monitoring biological diversity - Standard Biological Conservation, 166, 98–102. DOI: methods or amphibians. Washington: 10.1016/j.biocon.2013.06.010 Smithsonian Books: p. 384. Moreira, L. F. B., Machado, I. F., Lace, A. R. G. M., & Hortal, J., Bello, F., Diniz-Filho, J. A. F., Lewinsohn, Maltchik, L. 2007. Calling period and reproductive T. M., Lobo, J. M., & Ladle, R. J. 2015. Seven modes in anuran community o a temporary shortalls that beset large-scale knowledge pond in southern Brazil. South American Journal o biodiversity. Annual Review o Ecology, o Herpetology, 2(2), 129–135. DOI:10.2994/1808- Evolution, and Systematics, 46(1), 523–549. DOI: 9798(2007)2[129:CPARMI]2.0.CO;2 10.1146/annurev-ecolsys-112414-054400 Moritz, C., Patton, J. L., Schneider, C. J., & Smith, T. IBGE - Instituto Brasileiro de Geograa e Estatística. B. 2000. Diversication o rainorest aunas: An

Oecol. Aust. 23(4): 1027–1052, 2019 1050 Anuran species o the Chaco and Cerrado in central Brazil

integrated molecular approach. Annual Review Prado, C. A., Uetanabaro, M., & Haddad, C. F. o Ecology and Systematics, 31(1), 533–563. DOI: 2005. Breeding activity patterns, reproductive 10.1146/annurev.ecolsys.31.1.533 modes, and habitat use by anurans (Amphibia) Morrone, J. J. 2014. Biogeographical regionalisation in a seasonal environment in the Pantanal, o the Neotropical region. Zootaxa, 3782, 1–110. Brazil. Amphibia-Reptilia, 26(2), 211–221. DOI: 10.11646/zootaxa.3782.1.1 Prado, D. E., & Gibbs, P. E. 1993. Patterns o Narvaes, P., & Rodrigues, M. T. 2009. Taxonomic species distributions in the dry seasonal revision o Rhinella granulosa species group orests o South America. Annals o the (Amphibia, Anura, Buonidae), with a description Missouri Botanical Garden, 80(4), 902–927. o a new species. Arquivos de Zoologia, 40(1), DOI: 10.2307/2399937 1–73. Ribeiro, R. S., Egito, G. T. B. T., & Haddad, C. F. B. Neves, D. M., Dexter, K. G., Pennington, R. T., Bueno, 2005. Chave de identicação: aníbios anuros M. L., & Oliveira Filho, A. T. 2015. Environmental da vertente de Jundiaí da Serra do Japi, Estado and historical controls o oristic composition de São Paulo. Biota Neotropica, 5(2), 235–247. across the South American Dry Diagonal. Journal DOI: 10.1590/S1676-06032005000300017 o Biogeography, 42(8), 1566–1576. DOI: 10.1111/ Rodrigues, D. J., Lopes, F. S., & Uetanabaro, M. jbi.12529 2003. Padrão reprodutivo de Elachistocleis Oliveira-Filho, A. T., Jarenkow, J. A., & Rodal, M. J. bicolor (Anura, Microhylidae) na Serra da N. 2006. Floristic relationships o seasonally dry Bodoquena, Mato Grosso do Sul, Brasil. orests o eastern south America based on tree Iheringia. Série Zoologia, 93(4), 365–371. DOI: species distribution patterns. In: R. T. Pennington, 10.1590/S0073-47212003000400003 G. P. Lewis, & J. A. Ratter (Eds.), Neotropical Rodrigues, M. E., Moura, E. B., Koroiva, R., Savannas and Seasonally Dry Forests. pp. 159– Borges, A. C. P., & Roque, F. O. 2018. Survey 192. Boca Raton, USA: CRC Press. o dragonies (Odonata) in palm swamps o Pansonato, A., Mott, T., & Strüssmann, C. 2011. Anuran Cerrado hotspot. Entomological News, 128(1), amphibians’ diversity in a northwestern area o 24–38. DOI: 10.3157/021.128.0104 the Brazilian Pantanal. Biota Neotropica, 11(4), Roque, F. O., Ochoa-Quintero, J., Ribeiro, D. B., 77–86. DOI: 10.1590/s1676-06032011000400008 Sugai, L. S. M., Costa-Pereira, R., Lourival, R., Pereira, E. A., Neves, M. O., Hote, P. S., Santana, D. & Bino, G. 2016. Upland habitat loss as a threat J., & Feio, R. N. 2016. Anurans o the municipality to Pantanal wetlands. Conservation Biology, o Barão de Monte Alto, state o Minas Gerais, 30(5), 1131–1134. DOI: 10.1111/cobi.12713 southeastern Brazil. Check List, 12(5), 1977. DOI: Rosset, S. D., Baldo, D., & Haddad, C. F. B. 10.15560/12.5.1977 2009. Amphibia, Anura, Cycloramphidae, Pesci, G. P., Sánchez, J. M., Muñiz Leao, S., & Odontophrynus lavillai: First record or Brazil Pelegrin, N. 2018. Reptiles y anbios de una and geographic distribution map. Check List, localidad del Chaco Húmedo en Formosa, 5(1), 32–34. DOI: 10.15560/5.1.32 . Cuadernos de Herpetología, 32(1), Sabbag, A. F., & Zina, J. 2011. Anurans o a riparian 47–54. DOI: 10.31017/CdH.2018.(2017-05) orest in Sao Carlos, state o Sao Paulo, Brazil. Pott, A., Damasceno-Junior, G. A., & da Silva, M. Biota Neotropica, 11(3), 179–188. DOI: 10.1590/ P. 2014. Características da Bacia Hidrográca S1676-06032011000300015 do Rio Miranda. Revista GeoPantanal, 9(16), Sant’anna, A. C., Rocha, S. B., Akieda, P. S., Galvão, 125–140. C., & Neves, M. O. 2017. Distribution extension Pott, A., Oliveira, A., Damasceno-Junior, G., & Silva, o Ameerega berohoka Vaz-Silva and Maciel, J. 2011. Plant diversity o the Pantanal wetland. 2011 (Amphibia, Anura, Dendrobatidae): a Brazilian Journal o Biology, 71(1), 265–273. new state record in the Central-West Region o DOI: 10.1590/S1519-69842011000200005 Brazil. Herpetology Notes, 10, 41–43. Pough, F. H., Andrews, R. M., Crump, M. L., Santos, M. M., Ávila, R. W., & Kawashita-Ribeiro, Savitzky, A. H., Wells, K. D., & Brandley, M. C. R. A. 2011. Checklist o the amphibians and 2015. Herpetology. 4 ed. Sunderland: Sinauer reptiles in Nobres municipality, Mato Grosso Associates: p. 591. state, central Brazil. Herpetology Notes, 4, 455–

Oecol. Aust. 23(4): 1027–1052, 2019 Santos et al. | 1051

461. Sugai, J. L. M. M., Souza, F. L., Filho, P. L., & Sczesny- Segalla, M. V., Caramaschi, U., Cruz, C. A. G., Grant, Moraes, E. A. 2014a. Rhinella scitula (Caramaschi T., Haddad, C. F. B., Garcia, P. C. A., Berneck, B. V. & Niemeyer, 2003) (Amphibia: Anura: M., & Langone, J. A. 2016. Brazilian amphibians: Buonidae): New distribution records. Check List o species. Herpetologia Brasileira, 5(2), List, 10(3), 694–696. DOI: 10.15560/10.3.694 34–46. Sugai, J. L. M. M., Souza, F. L., Uetanabaro, M., Silva, M. C., Oliveira, R. H., Morais, D. H., Kawashita- & Filho, P. L. 2012. Geographic distribution: Ribeiro, R. A., Brito, E. S., Robson, & Ávila, W., Rhinella azarai (Azara’s granulated toad). Claudio, M., & Silva, D. 2015. Amphibians and Herpetological Review, 43, 441. reptiles o a Cerrado area in Primavera do Sugai, J. L. M. M., Terra, J. de S., & Ferreira, V. L. Leste Municipality, Mato Grosso State, Central 2014b. Anurans o a threatened savanna area Brazil. Salamandra, 51(2), 187–194. in western Brazil. Biota Neotropica, 14(1), Silva, J. F., Farinas, M. R., Felli, J. M., & Klink, C. e20134058. DOI: 10.1590/S1676-06034058 A. 2006. Spatial heterogeneity, land use and Toledo, L. F., Giovanelli, J. G. R., Giasson, L. O. M., conservation in the cerrado region o Brazil. Prado, C. P. A., Guimarães, L. D., Bastos, R. P., Journal o Biogeography, 33(3), 536–548. DOI: & Haddad, C. F. B. 2007. Guia interativo dos 10.1111/j.1365-2699.2005.01422.x aníbios anuros do Cerrado, Campos Rupestres Souza, F. L., Prado, C. P. A., Sugai, J. L. M. M., e Pantanal. São Paulo: Neotropica. Ferreira, V. L., Aoki, C., Landgre-Filho, P., Toledo, L. F., Zina, J., & Haddad, C. F. B. 2003. Strüssmann, C., Ávila, R. W., Rodrigues, D. J., Distribuição espacial e temporal de uma Albuquerque, N. R., Terra, J., Uetanabaro, M., comunidade de aníbios anuros do município Béda, A. F., Piatti, L., Kawashita-Ribeiro, R. A., de Rio Claro, São Paulo, Brasil. Holos Delatorre, M., Faggioni, G. P., Demczuk, S. D. Environment, 3(2), 136–149. DOI: 10.14295/ B., & Duleba, S. 2017. Diversidade de aníbios do holos.v3i2.1126 Estado de Mato Grosso do Sul, Brasil. Iheringia. Uetanabaro, M., Prado, C. P. A., Rodrigues, D. J., Série Zoologia, 107. DOI: 10.1590/1678- Gordo, M., & Campos, Z. 2008. Guia de campo 4766e2017152 dos anuros do Pantanal e Planaltos de entorno. Souza, F. L., Uetanabaro, M., Landgre-Filho, P., Campo Grande: Ed. UFMS: p. 196. Piatti, L., & Prado, C. P. A. 2010. Herpetoauna, Uetanabaro, M., Souza, F. L., Landgre-Filho, P., municipality o Porto Murtinho, Chaco region, Beda, A. F., & Brandão, R. A. 2007. Aníbios state o Mato Grosso do Sul, Brazil. Check List, e répteis do Parque Nacional da Serra da 6(3), 470–475. DOI: 10.15560/6.3.470 Bodoquena, Mato Grosso do Sul, Brasil. Biota Stohlgren, T. J., Quinn, J. F., Ruggiero, M., & Neotropica, 7(3), 279–289. Waggoner, G. S. 1995. Status o biotic inventories Valdujo, P. H., Silvano, D. L., Colli, G., & Martins, in US national parks. Biological Conservation, M. 2012. Anuran species composition and 71(1), 97–106. DOI: 10.1016/0006-3207(94)00026- distribution patterns in brazilian cerrado, M a neotropical hotspot. South American Storer, A. 2003. Amphibian declines: uture Journal o Herpetology, 7(2), 63–78. DOI: directions. Diversity and Distributions, 9(2), 10.2994/057.007.0209 151–163. DOI: 10.1046/j.1472-4642.2003.00014.x Vasconcelos, T. S., Santos, T. G., Haddad, C. F. B., & Stuart, S. N. 2004. Status and trends o amphibian Rossa-Feres, D.C. 2010. Climatic variables and declines and extinctions worldwide. altitude as predictors o anuran species richness Science, 306(5702), 1783–1786. DOI: 10.1126/ and number o reproductive modes in Brazil. science.1103538 Journal o Tropical Ecology, 26(04), 423–432. Sugai, J. L. M. M., Faggioni, G. P., Piatti, L., Lemos, DOI: 10.1017/S0266467410000167 A. A., Souza, F. L., & Prado, C. P. A. 2013. Wells, K. D. 1977. The social behaviour o anuran Lepidobatrachus asper Budgett,1899 (Amphibia: amphibians. Animal Behaviour, 25, 666–693. Anura: Ceratophryidae): new country record, DOI: 10.1016/0003-3472(77)90118-X distribution map and natural history notes. Whiles, M. R., Lips, K. R., Pringle, C. M., Kilham, Check List, 9(1), 133. DOI: 10.15560/9.1.133 S. S., Bixby, R. J., Brenes, R., Connelly, S.,

Oecol. Aust. 23(4): 1027–1052, 2019 1052 Anuran species o the Chaco and Cerrado in central Brazil

Colon-Gaud, J. C., Hunte-Brown, M., Huryn, A. D., Montgomery, C., & Peterson, S. 2006. The eects o amphibian population declines on the structure and unction o Neotropical stream ecosystems. Frontiers in Ecology and the Environment, 4(1), 27–34. DOI:0/1540- 9295(2006)004[0027:TEOAPD]2.0.CO Whittaker, R. J., Araújo, M. B., Jepson, P., Ladle, R. J., Watson, J. E. M., & Willis, K. J. 2005. Conservation Biogeography: assessment and prospect. Diversity and Distributions, 11(1), 3–23. DOI: 10.1111/j.1366-9516.2005.00143.x Willis, K. J., & Whittaker, R. J. 2002. ECOLOGY: Enhanced: Species diversity- scale matters. Science, 295(5558), 1245–1248. DOI: 10.1126/ science.1067335 Zanella, F. C. V. 2011. Evolução da biota da diagonal de ormações abertas secas da América do Sul. In: C. J. B. Carvalho & E. A. B. Almeida (Eds.), Biogeograa da América do Sul: padrões e processos. pp. 198–220. São Paulo: Roca. Zavattini, J. A. 2009. As chuvas e as massas de ar no estado de Mato Grosso do Sul: estudo geográco com vista à regionalização climática. São Paulo: Ed. UNESP: p. 212. ZEE. 2009. Zoneamento ecológico econômico de Mato Grosso do Sul. Retrieved on November 23rd, 2016, rom https://sogi8.sogi.com.br/ Arquivo/Modulo113.MRID109/Registro32633/ lei no 3.839, de 28-12-2009.pd

Submitted: 15 May 2018 Accepted: 25 February 2019 Published online: 16 December 2019 Associate Editors: Camila Aoki, Gudryan J. Barônio & Arnildo Pott

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