Anurans of Turvo State Park: Testing the Validity of Seasonal Forest As a New Biome in Brazil S

This article was downloaded by: [Mr Vinicius Matheus Caldart] On: 15 February 2012, At: 13:29 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Journal of Natural History Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tnah20 Anurans of Turvo State Park: testing the validity of Seasonal Forest as a new biome in Brazil S. Iop a , V.M. Caldart a , T.G. dos Santos b & S.Z. Cechin a a Programa de Pós Graduação em Biodiversidade Animal, Departamento de Biologia, Universidade Federal de Santa Maria. Av. Roraima s/n°, Camobi, Cep 9705-900, Santa Maria, Rio Grande do Sul, Brazil b Universidade Federal do Pampa (UNIPAMPA), Campus São Gabriel. Av. Antônio Trilha, 1847, Cep 97300-000, São Gabriel, Rio Grande do Sul, Brazil Available online: 25 Aug 2011

To cite this article: S. Iop, V.M. Caldart, T.G. dos Santos & S.Z. Cechin (2011): Anurans of Turvo State Park: testing the validity of Seasonal Forest as a new biome in Brazil, Journal of Natural History, 45:39-40, 2443-2461 To link to this article: http://dx.doi.org/10.1080/00222933.2011.596951

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.tandfonline.com/page/terms-and- conditions

This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. Journal of Natural History Vol. 45, Nos. 39–40, October 2011, 2443–2461

Anurans of Turvo State Park: testing the validity of Seasonal Forest as a new biome in Brazil S. Iopa*, V.M. Caldarta, T.G. dos Santosb and S.Z. Cechina

aPrograma de Pós Graduação em Biodiversidade Animal, Departamento de Biologia, Universidade Federal de Santa Maria. Av. Roraima s/n◦, Camobi, Cep 9705-900, Santa Maria, Rio Grande do Sul, Brazil; bUniversidade Federal do Pampa (UNIPAMPA), Campus São Gabriel. Av. Antônio Trilha, 1847, Cep 97300-000, São Gabriel, Rio Grande do Sul, Brazil

(Received 26 September 2010; ﬁnal version received 10 June 2011; printed 3 August 2011)

The composition of the anuran community of Turvo State Park was compared with that of other localities of Mesophytic semideciduous Forest, aiming to test the hypothesis that localities situated nearest the Misiones nucleus support the new phytogeographic unit, known as Tropical Seasonal Forests Region. In total 32 amphibian species were recorded in the park area and surroundings: Anura, 30 native species and one exotic; Gymnophiona, one species. The ordination among the 20 localities of Seasonal Forest showed the formation of three groups with 45% similarity: group 1, composed of localities of south-eastern and central western regions; group 2, composed of the localities of the transitional portion with the Atlantic Forest sensu stricto and group 3, composed of the southern localities. The consolidation of the second group, which includes the occurrence of endemic species, supports the proposal of a new phytogeographic unit. Keywords: community; similarity; richness; reproductive modes

Introduction Brazil has six terrestrial biomes: Amazon, Cerrado, Caatinga, Pampa, Pantanal and Atlantic Forest. The Amazon covers a total area of 4,196,943 km2, consisting of a huge rainforest continuum that is influenced by the tropics; climate is mostly hot and humid, rainfall is well distributed throughout the year. In contrast, the Cerrado biome occu- pies 2,036,448 km2 and consists mainly of savannas. The climate is tropical sub-humid hot and is characterized by two seasons, one dry and one rainy. The Caatinga occu- pies 844,453 km2 and consists mainly of savannah steppe, with a semi-arid climate. The Pampa covers 176,496 km2, consisting mainly of grasslands with rich herbaceous Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 flora and a climate without a dry season. The Pantanal covers 150,355 km2, consisting primarily of flooded savannah steppe; it has two seasons, one dry and one rainy. In the rainy season this biome is completely flooded. The Atlantic Forest has an area of 86,289 km2 and is a complex environment, composed of Seasonal Forests (inland forests that are less influenced by coastal humidity) and Tropical Rainforests (Instituto Brasileiro de Geografia e Estatística 2004; Ministério do Meio Ambiente 2011). In the past, Seasonal Forests have been categorized with Caatinga in the Seasonally Dry Tropical Forests Domain (SDTF) (Prado and Gibbs 1993; Prado 2000). This

*Corresponding author. Email:[email protected]

domain has a disjunct distribution pattern with average annual temperatures greater than 17◦C and markedly seasonal rainfall (Prado and Gibbs 1993; Pennington et al. 2000; Prado 2000). The SDTF currently occurs from south to north-east Brazil, south- east Bolivia and Paraguay and northern Argentina, but there is evidence that during the Pleistocene epoch (a cold and dry climatic period in South America) its distribution was continuous and more extensive than it is currently (Prado and Gibbs 1993; Pennington et al. 2000). However, Oliveira-Filho and Fontes (2000) claim that Seasonal Forests should be part of the Atlantic Forest domain, because, in reality, there is a broad transition between the Atlantic Forest and adjacent biomes. Based on endemic vegetation and patterns of some plant taxa, Prado and Gibbs (1993) and Prado (2000) suggest that SDTF should be part of a new phytogeographic unit (i.e. biome) known as the Tropical Seasonal Forests Region (TSFR), which has three cores: (1) Caatinga nucleus in north-eastern Brazil; (2) Misiones nucleus along the Paraguay-Parana rivers, north-eastern Argentina, eastern Paraguay and the south of the state of Mato Grosso do Sul, Brazil, and the upper valley of Uruguay between Argentina and the Brazilian states of Santa Catarina and Rio Grande do Sul; and (3) Sub-Andean Piedmont nucleus in south-western Bolivia and north-western Argentina (see map in Werneck and Colli 2006). This new phytogeographic unit has strong implications for the biogeographic endemism of birds (Prado 2000) and lizards (Werneck and Colli 2006). However, Santos et al. (2009) analysed the similarity of frogs from these forests compared with other communities of phytogeographical units using the coefﬁcient of geographic resemblance (CGR) (Duellman 1990), and con- cluded that the frogs’ composition was similar to the composition of the nearest phytogeographical unit. Seasonal Forests are the most endangered rainforest type in the world (Jansen 1997); currently only 2% of the original cover remains and this is completely frag- mented (Werneck and Colli 2006). Threats to this vegetation type include the high fertility of the soil and the gentle slope, which are conducive to agriculture and cattle ranching, as well as the great economic interest in the trees that occur there (Murphy and Lugo 1986; Prado and Gibbs 1993). In the state of Rio Grande do Sul, over 95% of the original forest has been destroyed and what remains is heavily degraded (Fontana et al. 2003), except for portions of the forest that are in protected areas, as is the case for Turvo State Park (TSP), which represents the largest remnant of Seasonal Forest in the state. Seasonal Forest degradation leads to a loss of biodiversity, the effects of which are felt at all taxonomic levels, especially for the endemic species. Because of their life history characteristics, amphibians, which undergo metamorphosis in the larval Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 stage while living in freshwater environments, are particularly vulnerable. Adult life is mainly spent in terrestrial environments, returning occasionally to aquatic conditions. The skin is highly permeable, hence physical and chemical changes in the environments may have much greater effects on the organism (Duellman and Trueb 1994; Beebee 1996). Research on the anuran community of Rio Grande do Sul is recent (Colombo et al. 2008; Both et al. 2008, 2009; Santos et al. 2008; Both 2009), which com- plicates decision-making on the conservation of frogs in the state. In view of the problem of loss of Seasonal Forest and the direct inﬂuence of this on amphibians, the present work aims to (1) describe the composition of anurans of TSP and (2) com- pare the frogs’ composition in TSP with that in other localities of Seasonal Forest, testing the hypothesis that locations near the centre of Misiones nucleus support Journal of Natural History 2445

the new phytogeographic unit known as TSFR, because these locations tend to be less inﬂuenced by frogs in adjacent biomes and could contain species typical of this new unit.

Materials and methods Study site This study was conducted in TSP (27◦ 07’–27◦ 16’ S, 53◦ 48’–54◦ 04’ W; 100–400 m altitude), located in the municipality of Derrubadas in the extreme north-west of the state of Rio Grande do Sul, Brazil. The park covers 17,491 ha, has a perimeter of about 90 km and is bordered by the Republic of Argentina and the Brazilian state of Santa Catarina via the Uruguay River (Secretaria Estadual do Meio Ambiente 2005). The vegetation type is mesophytic semideciduous forest, belonging to the Misiones nucleus in the TSFR domain (sensu Prado 2000), and represents the largest remain- ing area of this vegetation type in the state (Secretaria Estadual do Meio Ambiente 2005). The Brazilian portion of the area surrounding the park was converted into an intensively agricultural landscape dominated by planting of soybeans and maize without any buffer zones. On the border with Argentina, the park is bordered by the Maconá Provincial Park (about 1000 ha) and the Yabotí International Biosphere Reserve (236,613 ha), also consisting of mesophytic semideciduous forest. In fact, there is great similarity between the vertebrate fauna of the extreme north-west of Rio Grande do Sul and the Misiones region because of the environmental similarities of these two regions as well as the Uruguay River not being a major biological barrier (Gudynas 1984). The climate is characterized as subtropical sub-humid with dry summers (Maluf 2000). The average temperature of the warmest month (January) is above 22◦Cand the coldest month (July) ranges between –3 and 18◦C. The average annual rainfall is 1665 mm and the rains are well distributed throughout the year, without a dry season (Secretaria Estadual do Meio Ambiente 2005).

Sampling methods The sampling for the survey of amphibians was conducted monthly from April 2009 to March 2010. Complementary methods were used for the inventory of species: sampling sites of reproduction (Scott Jr and Woodward 1994), casual encounters (Sawaya et al. 2008), pitfall traps with drift fences (Corn 1994; Cechin and Martins 2000) and

Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 consultation of scientiﬁc collections. The sampling sites consisted of 14 breeding ponds (1 permanent, 13 tempo- rary) monitored during the months of September 2009 to March 2010. Samples were obtained along the perimeter of the ponds using visual and auditory encounters, from dusk until about midnight. The effort used to monitor the pools varied with the size and complexity of each (Scott Jr and Woodward 1994). Casual encounter records made in the period April 2009 to March 2010 in 17 other water bodies present in the park (four ponds, three swamps, eight streams and the banks of the Uruguay River) were also considered. These records consisted of occasional captures of amphibians and were collected outside the scope of the sampling methods previously described (Sawaya et al. 2008). The pitfall traps with drift fences were installed in the forest border area and inside the forest and consisted of 32 plastic 136 L capacity containers. The traps 2446 S. Iop et al.

were distributed in eight clusters arranged in a row (four in the border area and four within the forest) with four plastic containers positioned 15 m apart, connected by drift fences and about 90 cm above ground level. The minimum distance between the sets of traps was 1000 m. The traps remained open for five days monthly from April 2009 to March 2010, totalling 1440 hours per plastic container. Traps were examined every 24 h during this period. Four scientific collections were consulted in the search of records of amphibians in the region of Turvo State Park: scientific collections from Universidade Federal de Santa Maria (ZUFSM); Museu de Ciências e Tecnologia of Pontifícia Universidade Católica do Rio Grande do Sul (MCP); Universidade Federal do Rio Grande do Sul (UFRGS); Museu de Ciências Naturais of Fundação Zoobotânica do Rio Grande do Sul (MCN) (see appendix). Voucher specimens from this study were deposited in the scientific collections of the Universidade Federal de Santa Maria (ZUFSM) (license Secretaria Estadual do Meio Ambiente 2005 #302 and SISBIO/RAN #18320-1).

Statistical analyses The composition of frogs in the study area was compared with that recorded in other localities of Seasonal Forest (Tables 1 and 2; Figure 1). The comparison between communities of different localities can be affected by a difference in sampling effort, size of area sampled, characteristics and conservation status of the localities and different taxonomic concepts of the researcher (Bastos et al. 2003; Santos et al. 2009). Thus, some precautions have been taken to mitigate the potential limitations in the compar- isons: only work that had a large sampling effort (time and/or spatial) was included in the analysis; species listed as sp., gr. (species group), cf. (confer) or aff. (affinis) were excluded. The only exception to this rule was Physalaemus cf. gracilis because it is a species closely related to Physalaemus gracilis, as described by Corrizo (Lucas 2008). Lithobates catesbeianus, an exotic species, was also excluded from the analysis. The similarity between locations in relation to the composition of frogs was cal- culated using the coefficient of geographical resemblance (CGR) (Duellman 1990), where: CGR = 2NS / (NA + NB)(NS: number of species in both areas; NA: number of species in area A; NB: number of species in area B). This index is equivalent to the Sorensen, Dice and Czekanowski indexes (Wolda 1981; Krebs 1999; Magurran 2004) and ranges from 0 (maximum dissimilarity) to 1 (maximum similarity). Non- metric multidimensional scaling (NMDS) implemented in PRIMER-E 6.0 (Clarke Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 and Gorely 2006) was used to produce a two-dimensional representation of the similarity matrix. To check whether the geographical distance (measured in km) had an influence on the composition of frogs, and consequently on the outcome of the ordination, a Mantel test was performed (Manly 2000). This test correlates matrices using the statistic Z, where Z depends on the number and size of the matrices’ elements to be compared. Therefore normalization is performed to transform coefficient Z so that it ranges from +1 to –1. The significance of Z was determined by a Monte Carlo permutation test using 5000 permutations (Smouse et al. 1986). When a significant influence of geographic distance was found, a new correlation was performed using the partial Mantel test (Smouse et al. 1986) to remove this spatial effect. The Mantel test was performed in the program NTSYS PC 2.10s (Rohlf 2000). Journal of Natural History 2447

Table 1. Community of amphibians in areas of Seasonal Forest compared with the records found in Turvo State Park, Derrubadas, Rio Grande do Sul. ∗Areas modiﬁed. SF = Seasonal Forest, MOF = Mixed Ombrophilous Forest, C = Cerrado, DOF = Dense Ombrophilous Forest.

Locality Abbreviation Vegetation

Distrito de Itapé (Zina et al. 2007)∗ DI SF, C Estação Ecológica de Caetetus (Bertoluci et al. 2007) EEC SF Floresta Estadual Edmundo Navarro de Andrade FEENA SF (Toledo et al. 2003) Floresta Nacional de Chapecó (Lucas and Fortes 2008)∗ FNC SF, MOF Guararapes (Bernarde and Kokubum 1999)∗ GUA SF, C Icém (Silva and Rossa-Feres 2007)∗ ICE SF, C Londrina, Paraná (Bernarde and Aanjos 1999; Machado LON SF et al. 1999; Machado and Bernarde 2006)∗ Mata de Santa Genebra (Zina et al. 2007)∗ MSG SF Nova Itapirema (Vasconcelos and Rossa-Feres 2005) NI SF, C Parque Estadual do Rio Guarani (Bernarde and PERG SF Machado 2001) Parque Estadual Morro do Diabo (Santos et al. 2009) PEMD SF, C Parque Nacional da Serra da Bodoquema (Uetanabaro PNSB SF et al. 2007) Quarta Colônia (Cechin et al. 2002)∗ QC SF Reserva Legal Mata São José (Zina et al. 2007)∗ RLMSJ SF Rio Tibaji (Médio) (Machado and Bernarde 2003; RTM SF, MOF Machado 2004)∗ Santa Fé do Sul (Santos et al. 2007)∗ SFS SF Serra do Japi (Ribeiro et al. 2005) SJ SF, DOF Tapiraí e Piedade (Condez et al. 2009) TP SF, DOF Usina Hidrelétrica de Quebra Queixo (Hartmann et al. UHQQ SF, MOF 2008)

For this, a hypothesis matrix was set up, to represent the consistency of the groups shown in the NMDS, and was given the values of 0 and 1. The value 0 represented pairs of locations that were placed in different groups in the NMDS and the value 1 represented a pair of locations within the same group in the NMDS. Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012

Results In total, 32 amphibian species were recorded in the TSP area, belonging to two orders: 31 species of the order Anura (30 native and one exotic), belonging to nine fami- lies, Bufonidae (4), Centrolenidae (1), Cycloramphidae (4), Hylidae (11), Hylodidae (1), Leiuperidae (3), Leptodactylidae (5), Microhylidae (1) and Ranidae (1); and one species belonging to the order Gymnophiona (Caeciliidae) (Table 3). The known geographic distributions of four frog species were extended through the ﬁrst record of these for the state of Rio Grande do Sul: Crossodactylus schmidti and Proceratophrys avelinoi (Caldart et al. 2010), Hypsiboas curupi (Iop et al. 2009), and Rhinella ornata. 2448 S. Iop et al. Locality × ×× × ×× ×××××××××××× × Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 × × ×× × ×××××××××××× ×× ×× × ×× × ×× × TSP UHQQ FNC LON QC PERG PEMD GUA SFS NI RLMSJ EEC DI MSG RTM FEENA PNSB ICE SJ TP Spix, (Lutz, Spix, Table 2. Community of amphibians recorded in 20 areas of Seasonal Forest. For abbreviations see Table 1. (Steindachner, 1864) atroluteus (Miranda-Ribeiro, 1920) devincenzii Klappenbach, 1968 (Hensel, 1867) 1934) 1824 (Müller, 1924) 1824 (Werner, 1894) Taxon Brachycephalidae Ischnocnema guentheri Bufonidae Melonophryniscus Melanophryniscus Rhinella arenarum Rhinella henseli Rhinella icterica Centrolenidae Vitreorana uranoscopa Rhinella ornata Rhinella schineideri Journal of Natural History 2449 ) Continued ( ××× ×× × × × ×× × × ×× ××××××××××××× Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 ××××× × × ×× × ×× ×××××××××× × × × × × × ×× ×××××××× ×× ××× ×××××××× ×× ××××× ××××××××××× (Duméril (Peters, (Schmidt, (Spix, 1824) macroglossa (Duméril and Bibron, 1841) americanus and Bibron, 1841) Mercadal de Barrio and Barrio, 1993 bigibbosa 1872) (Lutz, 1950) (Napoli and Caramaschi, 2000) (Peters, 1872) (Peters, 1872) sanborni 1944) (Boulenger, 1889) Craugastoridae Haddadus binotatus Cycloramphidae Limnomedusa Odontophrynus Proceratophrys avelinoi Proceratophrys Hylidae Aplastodiscus perviridis Dendropsophus elianeae Dendropsophus microps Dendropsophus minutus Dendropsophus Dendropsophus nanus 2450 S. Iop et al. Locality × × ×× ×× ××××××× × ××× ×× ×× × ×× ×××× × × ××× Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 ×× ×× ×× ××××× × ×× × × ×× ×× ×× × × × TSP UHQQ FNC LON QC PERG PEMD GUA SFS NI RLMSJ EEC DI MSG RTM FEENA PNSB ICE SJ TP (Spix, Pombal rubicundulus (Reinhardt and Lütken, 1862) albopunctatus 1824) (Garcia, Faivovich and Haddad 2007) (Wied-Newied, 1821) (Duméril and Bibron, 1841) (Braum and Braum, 1977) and Haddad, 1992 (Burmeiser, 1856) (Cope, 1862) tetraploidea Table 2. (Continued). Taxon Dendropsophus Hypsiboas Hypsiboas curupi Hypsiboas faber Hypsiboas pulchellus Hypsiboas leptolineatus Hypsiboas prasinus Hypsiboas raniceps Phyllomedusa Journal of Natural History 2451 ) Continued ( × ×× × × × ××××× × ×× × × Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 × ×× ×××××××× × ×××× ×××××××× ×× ××××× × ×× × ×× ×××××××× × ××× ×××××××× ×× ××××× ×× ×× × × × × (Cope, (Laurenti, venulosus 1768) Gallardo, 1961 biligonigerus 1860) Bokermann, 1962 Fitzinger, 1826 Günther, 1858 (Faivovich, 2005) (Boulenger, 1888) (Peters, 1871) (Lutz, 1925) Pombal, Haddad and Kasahara 1995 (Lutz, 1925) Trachycephalus Hylodidae Crossodactylus schmidti Leiuperidae Physalaemus Physalaemus centralis Physalaemus cuvieri Pseudis minuta Scinax aromothyella Scinax catharinae Scinax granulatus Scinax fuscovarius Scinax perereca Scinax squalirostris 2452 S. Iop et al. Locality ×× ××××××××××× ×× × Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 ×× × ××× ×× × × ×××××××× × ×××××× × ××××× ×× × ×××××× ×× × ××× ××××× × × × TSP UHQQ FNC LON QC PERG PEMD GUA SFS NI RLMSJ EEC DI MSG RTM FEENA PNSB ICE SJ TP (Spix, Ahl, 1936 (Hensel, falcipes 1867) (Schneider, 1799) (Duméril and Bibron, 1841) labyrinthicus mystacinus (Brumeister, 1861) 1824) plaumanni (Valenciennes, 1838) Table 2. (Continued). Taxon Pseudopaludicola Leptodactylidae Leptodactylus fuscus Leptodactylus gracilis Leptodactylus Leptodactylus Leptodactylus Microhylidae Elachistocleis bicolor Journal of Natural History 2453

Figure 1. Map of South America highlighting the geopolitical division of Brazil. States of Rio Grande do Sul, (RS), Santa Catarina (SC), Paraná (PR), São Paulo (SP) and Mato Grosso do Sul (MS) are represented in grey. The 19 locations of Seasonal Forest (grey points) and TSP anuran communities (black point) are shown. For abbreviations see Table 1.

There were eight reproductive modes (sensu Haddad and Prado 2005) among the 30 native species of frogs occurring in TSP (Table 3). Eggs and exotrophic tadpoles in lentic water bodies (mode 1) was the most commonly found (n = 14 species, 46%). Eggs and exotrophic tadpoles in lotic water bodies (mode 2) was the second most found among the species (n = 5 species, 16%), followed by eggs in foam nests ﬂoating in lentic water bodies (mode 11) and foam nests with eggs and early larval stages in nests built underground (mode 30) (n = 4 species, 13% each). Of the other modes, eggs and early larval stages in burrows built underwater, exotrophic tadpoles in lotic Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 water bodies (mode 3); eggs and early larval stages in natural pools or constructed after ﬂooding, exotrophic tadpoles in lentic or lotic water bodies (mode 4); arboreal eggs which hatch into exotrophic tadpoles falling into lentic water bodies (mode 24); and arboreal eggs which hatch into exotrophic tadpoles falling into lotic water bodies (mode 25), were used by only one species each (n = 1 species, 3% each). Ordination analysis among Seasonal Forest locations showed the formation of three groups with 45% similarity: group 1 consisted of the localities of south-eastern and central west Brazil, group 2 consisted of the localities in the transition zone to the Atlantic Forest sensu stricto, and group 3 consisted of the localities in the south (Figure 2). 2454 S. Iop et al.

Table 3. Amphibian species recorded in Turvo State Park in the period April 2009 to March 2010. RM = reproductive mode sensu Haddad and Prado (2005), from personal observations and literature data (Achaval and Olmos 2003; Pombal and Haddad 2005; Santos et al. 2008, 2009). ∗Exotic species.

Order/Family Species RM

Anura Bufonidae Melanophryniscus atroluteus (Miranda-Ribeiro, 1920) 1 Melanophryniscus devincenzii Klappenbach, 1968 2 Rhinella icterica Spix, 1824 1 Rhinella ornata Spix, 1824 1 Centrolenidae Vitreorana uranoscopa (Müller, 1924) 25 Cycloramphidae Limnomedusa macroglossa (Duméril and Bibron, 1841) 2 Odontophrynus americanus (Duméril and Bibron, 1841) 1 Proceratophrys avelinoi Mercadal de Barrio and Barrio, 1993 2 Proceratophrys bigibbosa (Peters, 1872) 2 Hylidae Dendropsophus microps (Peters, 1872) 1 Dendropsophus minutus (Peters, 1872) 1 Dendropsophus sanborni (Schmidt, 1944) 1 Hypsiboas curupi (Garcia, Faivovich and Haddad, 2007) 2 Hypsiboas faber (Wied-Newied, 1821) 4 Phyllomedusa tetraploidea Pombal and Haddad, 1992 24 Pseudis minuta Günther, 1858 1 Scinax aromothyella Faivovich, 2005 1 Scinax fuscovarius (Lutz, 1925) 1 Scinax granulatus (Peters, 1871) 1 Scinax perereca Pombal, Haddad and Kasahara, 1995 1 Hylodidae Crossodactylus schmidti Gallardo, 1961 3 Leiuperidae Physalaemus biligonigerus (Cope, 1861) 11 Physalaemus cuvieri Fitzinger, 1826 11 Physalaemus cf. gracilis 11 Leptodactylidae Leptodactylus fuscus (Schneider, 1799) 30

Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 Leptodactylus aff. latinasus 30 Leptodactylus latrans (Linnaeus, 1758) 11 Leptodactylus mystacinus (Brumeister, 1861) 30 Leptodactylus plaumanni Ahl, 1936 30 Microhylidae Elachistocleis bicolor (Valenciennes and Guérin-Méneville, 1838) 1 Ranidae Lithobates catesbeianus (Shaw, 1802)∗ 1 Gymnophiona Caeciliidae Siphonops paulensis Boettger, 1892 Journal of Natural History 2455

Figure 2. Ordination analysis of Seasonal Forest anuran communities using the index of geographic similarity coefﬁcient (CGR) and non-metric multidimensional scaling (NMDS). For abbreviations see Table 1. 1 = group formed by the sites in the mid-west and south-eastern Brazil, 2 = group formed by sites in the Atlantic Forest, 3 = group formed by sites in southern Brazil.

The Mantel test revealed that geographically closer communities of frogs are also more similar in composition (r = 0.56, p < 0.01). However, when removing the effect of geographical distance by the Mantel test, the groups represented in the NMDS are still consistent (r = 0.74, p < 0.01).

Discussion The community of anurans of TSP can be characterized as a mixture of species with distributions associated with the Atlantic Forest sensu stricto (Vitreorana ura- Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 noscopa) (Frost 2010); species with distribution restricted to southern Brazil and the neighbouring countries of Argentina, Paraguay and Uruguay (Elachistocleis bicolor, Leptodactylus plaumanni, Limnomedusa macroglossa, Melanophryniscus atroluteus, M. devincenzii, Physalaemus biligonigerus, Pseudis minuta, Scinax aromothyella and S. granulatus) (Frost 2010); and species widely distributed throughout South America (Dendropsophus minutus, D. sanborni, Hypsiboas faber, Leptodactylus fuscus, L. latrans, L. mystacinus, Odontophrynus americanus, Physalaemus cuvieri, Rhinella icterica, R. ornata and Scinax fuscovarius) (Frost 2010). The high diversiﬁcation of reproductive modes reported for amphibians in the humid Atlantic Forest is positively related to the availability of moist microhabitats and the rugged relief (Haddad and Prado 2005). According to Vasconcelos et al. 2456 S. Iop et al.

(2010), the lesser diversification of reproductive modes registered in localities of the Cerrado and Seasonal Forests is related to the high concentration of annual rainfall in these locations. Thus, it is expected that anuran communities in seasonally dry areas display a low number of reproductive modes. TSP, despite being located in a Seasonal Forest, experiences a homogeneous distribution of rainfall, which results in a high diversification of reproductive modes since areas under little seasonal variation of rain, for example, favour the occurrence of terrestrial and semi-terrestrial reproductive modes (e.g. modes 17–23) (Duellman 1988; Hödl 1990). The results obtained in this study indicate a low diversity of reproductive modes and the prevalence of widespread non-terrestrial modes (modes 1 and 2) that are resistant to desiccation (modes 11 and 30), and are consistent with findings in seasonally dry locations (Hödl 1990; Prado et al. 2005; Vasconcelos and Rossa-Feres 2005; Santos et al. 2007, 2009). In this case, this feature may be related to historical factors related to the unique climate of SDTF. In fact, the expansion of SDTF in South America took place under the cold and dry climate of the Pleistocene epoch (Prado and Gibbs 1993; Pennington et al. 2000) and so the climate seasonality may have historically limited the diversification of anuran reproductive modes in this vegetation type. Of the 30 native species recorded in TSP, Crossodactylus schmidti, Dendropsophus microps, Proceratophrys bigibbosa, Rhinella ornata, and Vitreorana uranoscopa can be regarded as dependent on forested habitats (Gallardo 1961; Kwet and Faivovich 2001; Garcia and Vinciprova 2003; Ribeiro et al. 2005; Santos et al. 2009). Such species are often considered specialists in limpid streams inside the forest and therefore are considered bioindicators of this habitat type (Gallardo 1961; Gudynas and Gehrau 1981; Kwet and Faivovich 2001; Garcia and Vinciprova 2003; Santos et al. 2008). In fact, most of the species listed in the literature as bioindicators of this habitat type occurred in a well-preserved area of the park (i.e. associated with streams inside the forest). The similarity analysis and hypothesis tests showed that anuran communities of Seasonal Forests yielded three consistent groups. Group 1 consists of locations in south-eastern and central west Brazil, and includes a number of locations and similar climatic and physiognomic conditions: the region’s climate type is tropical, hot and humid (Aw of the Köppen–Geiger classification; Peel et al. 2007), with two well- defined seasons, a dry season (between April and September) and a rainy season (from October to March), the beginning of which is unpredictable (Rossa-Feres and Jim 2001). The locations included in this group suffer the influence of frogs found in the Cerrado, owing to its geographical proximity to this biome (Bernarde and Kokubum 1999; Vasconcelos and Rossa-Feres 2005; Zina et al. 2007; Santos et al. 2009), and gen- Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 erally experienced strong agricultural conversion processes (Santos et al. 2007; Zina et al. 2007). The high similarities among the communities of frogs in these locations have been reported in other studies (Bertoluci et al. 2007; Zina et al. 2007; Araújo et al. 2009; Santos et al. 2009), which suggest that the composition of the seasonal forest fauna is more similar to that recorded in areas of Cerrado, Pantanal and Pampa than that in the Atlantic Forest sensu stricto. The second group is formed by the localities of Seasonal Forests in the transition zone to the Atlantic Forest sensu stricto in the south-east (SJ and TP). The climate of the SJ locality is characterized as humid temperate with warm summers (Cfa; Peel et al. 2007), while the TP location is subject to both the humid temperate climate with warm summers (Cfa) and the humid temperate climate with temperate summers Journal of Natural History 2457

(Cfb; Peel et al. 2007; Condez et al. 2009). The similarity of the communities of frogs from areas of transition with the Atlantic Forest sensu stricto was also highlighted by Bertoluci et al. (2007), Zina et al. (2007) and Santos et al. (2009). Group 3 is formed by the localities of southern Brazil, with a predominance of subtropical climate characterized by homogeneity in rainfall (i.e. without a dry season) and a seasonal climate governed by a circannual variation in temperature and photoperiod (Both et al. 2008; Santos et al. 2008; Canavero et al. 2009). At least three frog species commonly recorded in the localities that make up this group can be regarded as endemic to Misiones nucleus Seasonal Forests: Crossodactylus schmidti, Hypsiboas curupi and Proceratophrys avelinoi. The existence of species of unique frogs in Seasonal Forests supports the proposal of Prado (2000): a new phytogeographic unit (biome). Similar results were previously reported for birds (Prado 2000) and lizards (Werneck and Colli 2006), but not for amphibians (Santos et al. 2009). In fact, the database used by Santos et al (2009) consisted mainly of locations representing Seasonal Forests in the peripheral region of the Misiones nucleus, with more inﬂuence on the anuran composition of the Cerrado. The inclusion of a greater number of southern towns, situated closer to the centre of the Misiones nucleus, appears to have facilitated the detec- tion of this new pattern reported here, which includes species endemic to the Tropical Seasonal Forests. In this context, the importance of effective conservation/protection of fragments that represent the TSFR at the centre of Misiones nucleus is emphasized.

Acknowledgements The authors are grateful to the director and staff of TSP and Marcia Regina Spies for autho- rizing the use of program PRIMER-E. S.I. and V.M.C. are grateful to CAPES for the master’s degree fellowships granted, and S.Z.C. is grateful to CNPq for the research fellowship (process n. 303359/2009-9).

References Achaval F, Olmos A. 2003. Anfíbios y Reptiles del Uruguay. Montevideo (Uruguay): Graphis. Araújo CO, Condez TH, Sawaya RJS. 2009. Anfíbios Anuros do Parque Estadual das Furnas do Bom Jesus, sudeste do Brasil, e suas relações com outras taxocenoses no Brasil. Biota Neotrop [Internet]. [cited 15 August 2008];9(2):1–22. Available from: http://www.biotaneotropica.org.br/v9n2/en/abstract?article+bn01309022009 Bastos RP, Motta JAO, Lima LP, Guimarães LD. 2003. Anfíbios da Floresta Nacional de Silvânia, estado de Goiás. 1st ed. Goiânia (Brazil): Stylo Gráﬁca e Editora. Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 Beebee TJC. 1996. Ecology and conservation of amphibians. London (England): Chapman and Hall. Bernarde OS, Anjos L. 1999. Distribuição espacial e temporal da anurofauna no Parque Estadual Mata dos Godoy, Londrina, Paraná Brasil (Amphibia: Anura). Comun Mus Ciênc Tecnol PUCRS. 12:127–140. Bernarde OS, Kokubum MNC. 1999. Anurofauna do Município de Guararapes, Estado de São Paulo, Brasil (Amphibia, Anura). Acta Biol Leopold. 21:89–97. Bernarde OS, Machado RA. 2001. Riqueza de espécies, ambientes de reprodução e temporada de vocalização da anurofauna em Três Barras do Paraná, Brasil (Amphibia: Anura). Cuad Herpetolog. 14(2):93–104. Bertoluci J, Brassaloti RA, Júnior JWR, Vilela VMFN, Sawakuchi HO. 2007. Species composition and similarities among anuran assemblages of forests in south-eastern Brazil. Sci Agric. 64(4):364–374. 2458 S. Iop et al.

Both C. 2009. Riqueza, composição de guildas e padrões de co-ocorrência de comunidades de girinos em poças no sul do Brasil [dissertation]. [Porto Alegre (Brazil)]: Universidade Federal do Rio Grande do Sul. Both C, Kaefer IL, Santos TG, Cechin STZ. 2008. An austral anuran assemblage in the Neotropics: seasonal occurrence correlated with photoperiod. J Nat Hist. 42:205–222. Both C, Solé M, Santos TG, Cechin SZ. 2009. The role of spatial and temporal descriptors for Neotropical tadpole communities in southern Brazil. Hydrobiologia. 124(1):125–138. Caldart VM, Iop S, Santos TG, Cechin SZ. 2010. Extension of the geographical distribution of two anuran species for Rio Grande do Sul state, Brazil, with comments on natural history. Biota Neotrop [Internet]. [cited 20 February 2011];10(3):143–147. Available from: http://www.biotaneotropica.org.br/v10n3/en/abstract?article+bn02610032010 Canavero A, Arim M, Brazeiro A. 2009. Geographic variations of seasonality and coexistence in communities: the role of diversity and climate. Austral Ecol. 34:741–750. Cechin SZ, Martins M. 2000. Eficiência de armadilhas de queda (pitfall traps) em amostragens de anfíbios e répteis no Brasil. Rev Bras Zool. 17(3):729–749. Cechin SZ, Giasson LO, Hartmann MA, Santos TG, Boelter R. 2002. Anfíbios. In: José Itaqui, editor. Quarta Colônia: Inventários Técnicos – Fauna e Flora. 1st ed. Santa Maria (Brazil): Condesus/Quarta Colônia. Clarke KR, Gorley RN. 2006. Software PRIMER v6. PRIMER-E, Plymouth, UK. Colombo P, Kindel A, Vinciprova G, Krause L. 2008. Composição e ameaças à conservação dos anfíbios anuros do Parque Estadual de Itapeva, município de Torres, Rio Grande do Sul, Brasil. Biota Neotrop [Internet]. [cited 12 July 2010];8(3):229–240. Available from: http://www.biotaneotropica.org.br/v8n3/en/abstract?inventory+bn01208032008 Condez TH, Sawaya RJ, Dixo M. 2009. Herpetofauna dos remanescentes de Mata Atlântica da região de Tapiraí e Piedade, SP, sudeste do Brasil. Biota Neotrop [Internet]. [cited 26 January 2010];9(1):157–185. Available from: http://www.biotaneotropica. org.br/v9n1/pt/abstract?inventory+bn01809012009 Corn PS. 1994. Straight-line drift fences and pitfall traps. In: Heyer WR, Donnelly MA, McDiarmid RW, Hayek LAC, Foster MS, editors. Measuring and monitoring biological diversity – standard methods for amphibians. 1st ed. Washington DC: Smithsonian Institution Press. p. 109–117. Duellman WE. 1988. Pattern of species diversity in anuran amphibians in the American tropics. Ann Mo Bot Gard. 75:79–104. Duellman WE. 1990. Herpetofaunas in neotropical rainforests: comparative composition, history, and resource use. In: Gentry AH, editor. Four Neotropical Rainforests. 1st ed. New Haven (CT): Yale University Press. p. 455–505. Duellman WE, Trueb L. 1994. Biology of Amphibians. London: McGraw-Hill. Fontana SC, Bencke GA, Reis RE. 2003. Livro vermelho da fauna ameaçada de extinção no Rio Grande do Sul. Porto Alegre (Brazil): Editora Universitária da PUCRS (EDIPUCRS). Frost DR. 2010. Amphibian species of the world: an online reference [Internet]. Version 5.4. Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 New York: American Museum of Natural History; [cited 20 July 2010]. Available from: http://research.amnh.org/vz/herpetology/amphibia/AmericanMuseumofNaturalHistory Gallardo JM. 1961. Anfibios anuros de Misiones con la descripción de una nueva espécie de Crossodactylus. Neotropica. 7:33–38. Garcia CS, Vinciprova G. 2003. Anfíbios. In: Fontana CS, Bencke GAA, Reis RE, editors. Livro vermelho da fauna ameaçada de extinção no Rio Grande do Sul. Porto Alegre (Brazil): Editora Universitária da PUCRS (EDIPUCRS). Gudynas E. 1984. Sobre el Rio Uruguay como barrera biogeografica para anfibios, y la signif- icancia de la presencia de Leptodactylus chaquensis Cei 1950 (Anura, Leptodactylidae) en el Uruguay. Bol Soc Zool Urug. 2:78–89. Gudynas E, Gehrau A. 1981. Notas sobre la distribuición y ecología de Limnomedusa macroglossa (Duméril and Bibron, 1841) en Uruguay (Anura, Leptodactylidae). Iheringia (Zool). 60:81–99. Journal of Natural History 2459

Haddad CFB, Prado CPA. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic Forest of Brazil. BioScience. 55(3):207–217. Hartmann MT, Hartmann PA, Giasson LOM. 2008. Anfíbíos. In: Cherem JJ, Kammers M, editors. A fauna das áreas de influência da Usina Hidrelétria Quebra Queixo. Erechim (Brazil): Habilis. Hödl W. 1990. Reproductive diversity in Amazonian lowland frogs. Fortschr Zool. 38:41–60. Iop S, Caldart VM, Rocha MC, Paim PM, Cechin SZ. 2009. Amphibia, Anura, Hylidae, Hypsiboas curupi Garcia, Faivovich and Haddad, 2007: first record for the state of Rio Grande do Sul, Brazil. Check List. 5(4):860–862. Jansen DH. 1997. Florestas tropicais secas. In: Wilson EO, editor. Biodiversidade. Rio de Janeiro (Brazil): Editora Nova Fronteira. p.166–176. Krebs CJ. 1999. Ecological methodology. Menlo Park (CA): Addison Wesley Educational. Kwet A, Faivovich J. 2001. Proceratophrys bigibbosa species group (Anura: Leptodactylidae), with description of a new species. Copeia. 1:203–215. Lucas EM. 2008. Diversidade e conservação de anfíbios anuros no estado de Santa Catarina, sul do Brasil [thesis]. [São Paulo (Brazil)]: Universidade de São Paulo. Lucas EM, Fortes VB. 2008. Frog diversity in the Floresta Nacional de Chapecó, Atlantic Forest of southern Brazil. Biota Neotrop [Internet]. [cited 20 January 2010];8(3):51–61. Available from: http://www.biotaneotropica.org.br/v8n3/pt/abstract?article+bn00508032008 Machado RA. 2004. Ecologia de assembléias de anfíbios anuros no município de Telêmaco Borba, Paraná, sul do Brasil [thesis]. [Curitiba (Brazil)]: Universidade Federal do Paraná. Machado RA, Bernarde OS, Morato SAA, Anjos L. 1999. Análise comparada da riqueza de anuros entre duas áreas com diferentes estados de conservação no Município de Londrina, Paraná, Brasil (Amphibia: Anura). Rev Bras Zool. 16(4):997–1004. Machado RA, Bernarde PS. 2003. Anurofauna da bacia do Rio Tibagi. In: Moacir EM, Bianchini E, Shibatta AO, Pimenta JA, editors. A Bacia do Rio Tibagi. Londrina (Brazil): MC-Gráfica. p. 297–306. Machado RA, Bernarde PS. 2006. Anfíbios anuros do Parque Estadual Mata do Godoy. In: Torezan JMD, editor. Ecologia do Parque Estadual Mata do Godoy. Londrina (Brazil): Itedes. Magurran AE. 2004. Measuring biological diversity. Oxford: Blackwell. Maluf JRT. 2000. Nova classificação climática do Estado do Rio Grande do Sul. Rev Bras Agrometeorol. 8:141–150. Manly BFG. 2000. Multivariate statistical methods – a primer. 2nd ed. Boca Raton (FL): Chapman and Hall. Ministério do Meio Ambiente (MMA). 2011. Biomas [Internet]. [cited 21 February 2011]. Available from: http://www.mma.gov.br/sitio/index.php?ido=conteudo.monta& idEstrutura=72&idMenu=2351. Murphy PG, Lugo AE. 1986. Ecology of tropical dry forest. Ann Rev Ecol Syst. 17:67–88. Oliveira-Filho AT, Fontes MAL. 2000. Patterns of floristic differentiation among Atlantic Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 Forests in south-eastern Brazil and the influence of climate. Biotropica. 32(4b):793–810. Peel MC, Finlayson BL, McMahon TA. 2007. Updated world map of the Köppen–Geiger climate classification. Hydrol Earth Syst Sci. 11:1633–1644. Pennington RT, Prado DE, Pendry CA. 2000. Neotropical seasonally dry forests and Quaternary vegetation changes. J Biogeogr. 27:261–273. Pombal JP Jr, Haddad CFB. 2005. Estratégias e modos reprodutivos de anuros (Amphibia) em uma poça permanente na Serra de Paranapiacaba, Sudeste do Brasil. Pap Avulsos Zool. 45(15):201–213. Prado CPA, Uetanabaro M, Haddad CFB. 2005. Breeding activity patterns, reproductive modes and habitat use by anurans (Amphibia) in a seasonal environment in the Pantanal, Brasil. Amphib Reptil. 26:211–221. Prado DE. 2000. Seasonally dry forests of tropical South America: from forgotten ecosystems to a new phytogeographic unit. Edinb J Bot. 57(3):437–461. 2460 S. Iop et al.

Prado DE, Gibbs PE. 1993. Patterns of species distributions in the dry seasonal forests of South America. Ann Mo Bot Gard. 80:902–927. Ribeiro RS, Egito GTBT, Haddad CFB. 2005. Chave de identiﬁcação: anfíbios anuros da vertente de Jundiaí da Serra do Japi, estado de São Paulo. Biota Neotrop [Internet]. [cited 20 January 2010];5(2):1–15. Available from: http://www.biotaneotropica.org.br/ v5n2/pt/abstract?identiﬁcation-key+bn03005022005 Rohlf FJ. 2000. NTSYSpc 2.10s: numerical taxonomic and multivariate analysis System. Setauket (NY): Exeter Software. Rossa-Feres DC, Jim J. 2001. Similaridade no sítio de vocalização em uma comunidade de anfíbios anuros na região noroeste do Estado de São Paulo, Brasil. Rev Bras Zool. 18(2):439–454. Santos TG, Kopp K, Spies MR, Trevisan R, Cechin SZ. 2008. Distribuição temporal e espacial de anuros em área de Pampa, Santa Maria, RS. Iheringia (Zool). 98:244–253. Santos TG, Rossa-Feres DC, Casatti L. 2007. Diversidade e distribuição espaço-temporal de anuros em região com pronunciada estação seca no sudeste do Brasil. Iheringia (Zool). 97(1):37–49. Santos TG, Vasconcelos TS, Rossa-Feres DC, Hadad CFB. 2009. Anurans of a seasonally dry tropical forest: Morro do Diabo State Park, São Paulo state, Brazil. J Nat Hist. 43:973–993. Sawaya RJ, Marques OAV, Martins M. 2008. Composição e história natural das ser- pentes de Cerrado de Itirapina, São Paulo, sudeste do Brasil. Biota Neotrop [Internet]. [cited 20 January 2010];8(2):127–149. Available from: http://www.biotaneotropica.org. br/v8n2/en/abstract?article+bn01308022008 Scott NJ Jr, Woodward BD. 1994. Surveys at breeding sites. In: Heyer WR, Donnelly MA, McDiarmid RW, Hayek LAC, Foster MS, editors. Measuring and Monitoring Biological Diversity – Standard Methods for Amphibians. Washington DC: Smithsonian Institution Press. p. 84–92. SEMA (Secretaria Estadual do Meio Ambiente). 2005. Plano de Manejo do Parque Estadual do Turvo. Porto Alegre (Brazil): Estado do Rio Grande do Sul. 348 p. Silva FR, Rossa-Feres DC. 2007. Uso de fragmentos por anuros (Amphibia) de área aberta na região noroeste do Estado de São Paulo. Biota Neotrop [Internet]. [cited 20 January 2010];7(2):141–148. Available from: http://www.biotaneotropica.org.br/v7n2/ pt/abstract?article+bn03707022007 Smouse PE, Long JC, Sokal RR. 1986. Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool. 35(4):627–632. Toledo LF, Zina J, Haddad CFB. 2003. Distribuição Espacial e Temporal de uma Comunidade de anfíbios Anuros do Município de Rio Claro, São Paulo, Brasil. Holos Environ. 3(2):136–149. Uetanabaro M, Souza FL, Filho PL, Beda AF, Brandão RA. 2007. Anfíbios e répteis do Parque Nacional da Serra da Bodoquena, Mato Grosso do Sul, Brasil. Biota Neotrop [Internet]. [cited 20 January 2010];7(3):279–289. Available from: http://www.biotaneotropica. Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012 org.br/v7n3/pt/abstract?article+bn01207032007 Vasconcelos TS, Rossa-Feres DC. 2005. Diversidade, distribuição espacial e temporal de anfíbios anuros (Amphibia, Anura) na região noroeste do estado de São Paulo, Brasil. Biota Neotrop [Internet]. [cited 20 January 2010];5(2):1–14. Available from: http://www.biotaneotropica.org.br/v5n2/pt/abstract?article+BN01705022005 Vasconcelos TS, Santos TG, Haddad CFB, Rossa-Feres DC. 2010. Climatic variables and altitude as predictors of anuran species richness and number of reproductive modes in Brazil. J Trop Ecol. 26:423–432. Werneck FP, Colli GR. 2006. The lizard assemblage from Seasonally Dry Tropical Forest enclaves in the Cerrado biome, Brazil, and its association with the Pleistocenic Arc. J Biogeogr. 33:1983–1992. Wolda H. 1981. Similarity indices, sample size and diversity. Oecologia. 50:296–302. Journal of Natural History 2461

Zina J, Enneses J, Pinheiro SCP, Haddad CFB, Toledo LF. 2007. Taxocenose de anuros de uma mata semidecídua do interior do Estado de São Paulo e comparações com outras taxocenoses do Estado, sudeste do Brasil. Biota Neotrop [Internet]. [cited 20 January 2010];7(2):49–57. Available from: http://www.biotaneotropica.org.br/v7n2/ pt/abstract?article+bn006070

Appendix Rhinella icterica: MCP 3160, 4550; MCN 188, 868; UFRGS 2226. Rhinella ornata: MCN 197; UFRGS 2182–2185. Melanophryniscus atroluteus: MCP 3158. Limnomedusa macroglossa: UFRGS 2162, 2163, 2177, 2180, 2181, 2224, 2225; ZUFSM 3339. Odontophrynus americanus: MCP 1576; UFRGS 2204. Dendropsophus microps: MCN 1106, 1116. Dendropsophus minutus: MCP 1590, 3165–3171, 4544, 4545; UFRGS 2170, 2209, 2210, 2211, 2214. Dendropsophus sanborni: MCP 4553. Hypsiboas faber: MCP 2492, 3161. Hypsiboas curupi: UFRGS 2230–2237. Phyllomedusa tetraploidea: MCP 2575; UFRGS 2198–2201. Pseudis minuta: MCP 3159. Scinax aromothyella: MCP 4552; UFRGS 2168, 2169, 2186, 2215–2217. Scinax fuscovarius: MCP 1567, 1571, 1574, 1575, 2516, 2524, 3406, 3466, 4551. Scinax perereca: MCP 2515, 2523, 2525, 3460; UFRGS 2171–2179. Physalaemus cuvieri: MCP 3163, 4548, 4549; UFRGS 2206. Physalaemus cf. gracilis: MCP 2510, 3164, 4377; UFRGS 2084–2089, 2205. Leptodactylus fuscus: MCP 1585, 2572, 3162, 4539–4542; UFRGS 2203. Leptodactylus aff. latinasus: MCP 1581, 1582; UFRGS 2164, 2166, 2167, 2207, 2227, 2228; UFRGS 2164–2167. Leptodactylus latrans: MCP 1586, 2571; UFRGS 2165. Leptodactylus mystacinus: MCP 1583, 2574, 4372, 4543; UFRGS 2202. Elachistocleis bicolor: MCP 1595, 2444, 2445, 2447, 3148, 3481; UFRGS 2208. Lithobates catesbeianus: MCP 2557, 4535–4538. Siphonops paulensis: MCP 1134; UFRGS 2229. Downloaded by [Mr Vinicius Matheus Caldart] at 13:29 15 February 2012