Oecologia Australis 23(4):1027-1052, 2019 https://doi.org/10.4257/oeco.2019.2304.25
anuran SPECIES COMPOSITIOn FrOM CHaCO anD CErraDO arEaS In CEnTraL BrazIL
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] abst ct: 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 ecoregions: Chaco, Cerrado and Pantanal. Through acoustic and visual nocturnal/diurnal and pit all 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 de orestation 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.
Key o ds: Amphibia; Porto Murtinho; species inventory; transition zone.
InTrODuCTIOn heterogeneous distribution o sampling e orts 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 identi y priorities (Stohlgren et al. 1995). Despite in ormation about species distributions at global, the request or global e orts to obtain in ormation regional, and local levels (Wallacean short all), 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 short all) (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 ecoregion 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, in ormation 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 di erent localities (e.g., Ma ei 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 per ormed during six months and a total o worldwide (Stor er 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 e ort 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 e ort o pit all traps, e ort 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 (pit alls), totaling 704 h. Grosso do Sul, Brazil (e.g., Souza et al. 2010, Benites Capture methods were adopted using pit all 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 pit alls, 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 pit all 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
T ble 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 L tit de Lo it de Loc tio
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 per ormed 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 per ormed acoustic technique in a permanent water pound
Fi e 1. Localization o sampling points or anurans o the municipality o Porto Murtinho, Mato Grosso do Sul State, Brazil. A) Map o South America highlighting the geopolitical division o Brazil; B) Municipality division o the Mato Grosso do Sul State, Brazil, with distribution o di erent 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 pit all 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 Wildli e (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 per ormed a Non-Metric Multidimensional in capture locations a ter species identi cation 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 so tware (v. 3.18). revalidated descriptions to support the taxonomic For this analysis, our data were both evaluated as a identi cations (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 con gurations used online databases to nd registers o anuran as the Paraguay River basin (ZEE 2009) and the Apa species rom the municipality o Porto Murtinho River basin, such as vegetation ragments inserted in published articles. Speci cally, 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 identi y anuran species (i.e., journals o South America) and Google Scholar. We acoustic and pit all 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 o ten 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 in ormation 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 e ort 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 Jackkni e 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 classi ed 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 classi ed 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 (Ma ei 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 uni orm. 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 pre er the other areas. Despite this hypothesis, through alluvial orest environments, with open elds close ANOSIM, we were unable to nd signi cant to temporary or permanent ponds, characteristics di erences 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 classi cations 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 Jackkni e 1 (S est = 37.25, SD = 4.34), Chaco. O the 31 species registered in the Cerrado respectively (Figure 3). sites, Leptodactylus bu onius 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. bu onius 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 De cient” 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 di erences ound between the south-central Brazil, such as Primavera do Leste species composition rom the humid Chaco and
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