Species richness, relative abundance, and habitat of reproduction of terrestrial frogs in the Triângulo Mineiro region, Cerrado biome, southeastern Brazil

Riqueza, abundância relativa e hábitat de reprodução de espécies de anuros terrestres na região do Triângulo Mineiro, bioma Cerrado, sudeste do Brasil

Species richness, relative abundance, and habitat of reproduction of terrestrial frogs in the Triângulo Mineiro region, Cerrado biome, southeastern Brazil

Riqueza, abundância relativa e hábitat de reprodução de espécies de anuros terrestres na região do Triângulo Mineiro, bioma Cerrado, sudeste do Brasil

Ariovaldo A. Giaretta^I; Marcelo Menin^II; Kátia G. Facure^I; Marcelo N. de C. Kokubum^{I, III}; Júlio C. de Oliveira Filho^I

^ILaboratório de Ecologia e Sistemática de Anuros Neotropicais, Instituto de Biologia, Universidade Federal de Uberlândia, 38400–902 Uberlândia, MG, Brasil

^IILaboratório de Zoologia, Departamento de Biologia, ICB, Universidade Federal do Amazonas, Avenida General Rodrigo Otávio Jordão Ramos 3000, 69077–000 Manaus, AM, Brasil. ([e-mail])

^IIIProgramade Pós-graduação em Ecologia, Instituto de Ciências Biológicas, Universidade de Brasília – UnB, 70910-900 Brasília, DF, Brasil

ABSTRACT

Based on field observations and pitfall sampling, we determined the species richness, relative abundance, and reproductive habitat of terrestrial frogs in three municipalities in the Triângulo Mineiro region, south Cerrado biome, in southeastern Brazil. We found thirty-two species of terrestrial frogs, belonging to the families Brachycephalidae, Bufonidae, Cycloramphidae, Dendrobatidae, Leiuperidae, Leptodactylidae and Microhylidae. Most of the species were found in open areas and reproduced in human-generated environments, such as artificial lakes (10 species) and ponds (14 species). Dominance was high, with Physalaemus cuvieri Fitzinger, 1826 (Leiuperidae) representing 48% of sampled frogs. A larger number of individuals was captured in the wet season, when most of the species were reproducing. Compared to other areas of Cerrado biome, the Triângulo Mineiro sites presented a larger number of species, which may be attributed to the larger sampled area and greater sampling effort, lower altitude and presence of human generated habitats. The richness of terrestrial frogs was also larger than that in some forested localities in southeastern Brazil, indicating that the number of species cannot be explained only by precipitation and type of vegetation cover. The greater abundance of individuals during the wet season may be related to a greater movement of adults to breeding sites and to juvenile recruitment/dispersion. The heterogeneity of environments in the Cerrado biome, including its several isolated highlands, contributes to its high (local and regional) diversity of frogs.

Keywords: Reproductive habitat, relative abundance, richness, Triângulo Mineiro, southeastern Brazil.

RESUMO

Neste estudo foram determinados a riqueza, abundância relativa e hábitat de reprodução de anuros terrestres em três municípios do Triângulo Mineiro, sul do Bioma Cerrado, sudeste do Brasil, baseados em observações de campo e armadilhas de interceptação e queda. Foram encontradas 32 espécies pertencentes às famílias Brachycephalidae, Bufonidae, Cycloramphidae, Dendrobatidae, Leiuperidae, Leptodactylidae e Microhylidae. Muitas dessas espécies foram encontradas em áreas abertas e se reproduziram em ambientes artificiais gerados por ação antrópica, tais como lagos (10 espécies) e poças (14 espécies). Physalaemus cuvieri Fitzinger, 1826 (Leiuperidae) foi a espécie dominante, representando 48% do total amostrado. Um grande número de indivíduos de diferentes espécies foi capturado na estação chuvosa, quando muitas das espécies estavam reproduzindo. As áreas amostradas na região do Triângulo Mineiro apresentaram um maior número de espécies quando comparadas com outras áreas do bioma Cerrado, o que pode ser atribuído à maior área amostrada, ao maior esforço de coleta, baixa altitude e presença de hábitats gerados por ação antrópica. A riqueza de anuros terrestres também foi maior do que àquela encontrada em localidades florestadas no sudeste do Brasil, indicando que o número de espécies não pode ser explicado somente pela precipitação e tipo de cobertura vegetal da área. A grande abundância de indivíduos durante a estação chuvosa pode estar relacionada ao maior movimento de adultos para hábitats de reprodução e ao recrutamento e dispersão de juvenis. A heterogeneidade dos ambientes no bioma Cerrado, incluindo algumas de suas áreas com maiores altitudes, contribui para a alta diversidade (local e regional) de espécies de anuros.

Palavras-chave: Hábitat de reprodução, abundância relativa, riqueza, Triângulo Mineiro, sudeste do Brasil.

Most Neotropical frogs are only known taxonomically and available information on their ecology is often related to reproduction. In Brazil, frog species check lists are becoming frequent (e. g., BRANDÃO & ARAÚJO, 1998, 2001; BASTOS et al., 2003; TOLEDO et al., 2003; ETEROVICK & SAZIMA, 2004; POMBAL & GORDO, 2004; BRASILEIRO et al., 2005), but information on major ecological parameters, such as abundance, is scarce. Recent decades have been marked by debates on population decline and extinction of frog species around the world. For most species the obvious causes of the decline/extinctions are human related activities, however, the disappearance of species from preserved areas has also been reported (BLAUSTEIN & WAKE, 1990, 1995; PHILLIPS, 1990; LIPS, 1998; GARDNER, 2001; ETEROVICK et al., 2005). Today, the major problem for correctly evaluating the extent of the decline of frog populations is the lack of basic information, especially that necessary to separate natural fluctuations from actual declines (PECHMANN et al., 1991; HEYER et al., 1994; SARKAR, 1996; ALFORD & RICHARDS, 1999; MARSH, 2001).

The anurofauna of South America is the richest of the world (DUELLMAN, 1999; FROST, 2007). At present, around 110 species are known to occur in the Brazilian Cerrado (20% of Brazilian species), from which 32 (28%) are endemic (COLLI et al., 2002). The Cerrado biome, which covers about 1,780,000km², has been designated a biodiversity hotspot, with only 20% of it’s original area remaining as primary vegetation and only about 6.2% of this corresponding to protected areas (MYERS et al., 2000). About 56% of the frog species from the Cerrado are terrestrial (COLLI et al., 2002) and can be inventoried for their relative abundance by using methods such as pitfall traps. Herein we present data on richness and relative abundance of terrestrial frogs in the Cerrado of the Triângulo Mineiro, in southeastern Brazil. We also provide information on reproductive habitat of the species. Our data are particularly important because they were obtained from little studied lowland (<800m) Cerrado, which is underrepresented as conservation units and is under greater pressure due to the advance of soy, sugar cane, and cotton plantations and damming.

MATERIAL AND METHODS

The present study was based on data collected from September 1998 to December 2006 in the municipalities of Uberlândia (about 18º55’S, 48º17’W; approx. 750m altitude), Perdizes (about 19º12’S, 47º10’W; 700-1,000m altitude), and Araguari (18º33’S, 48º03’W; 700m altitude). All three localities are within the region of Triângulo Mineiro, in the state of Minas Gerais, southeastern Brazil and are crossed by the Araguari River. Uberlândia lays about 140km west of the sampled area of Perdizes and about 100km south from that of Araguari. The climate of the region has two well-defined seasons, wet/warm from September to March, and dry/mild (with occasional frosts) from April to August (ROSA et al., 1991). Monthly mean temperature ranges from 19 to 30ºC. Annual rainfall is about 1,550mm; in drier months the precipitation can be zero (GIARETTA & KOKUBUM, 2004).

At Uberlândia, the original vegetation includes lowland Cerrado environments such as streamside marshes (Mauritia flexuosa palm groves Palmae, Veredas) and riverine forests (GOODLAND & FERRI, 1979; SANO & ALMEIDA, 1998). Natural bodies of water include streams, rivers and permanent and seasonal springs; artificial bodies of water include ponds, lakes and drainage channels. In the rural areas, human activities include cattle ranching and mechanized agriculture; large portions of riverine forests have been removed for pastures and, more recently, for the construction of three new hydroelectric power stations (Miranda and Capim Branco I and II, in the Araguari River). Data on richness, reproductive habitat and period were based on weekly field trips since September 1998; data on relative abundance were based on pitfall sampling sets at two sites, Clube de Caça e Pesca and Estação Ecológica do Panga. The "Caça e Pesca" is a 300ha reserve on the outskirt of the city. The local vegetation includes typical secondary growth Cerrado, veredas and patches of exotic grass (Brachiaria sp. Poaceae and Melinis minutiflora Poaceae). The Panga is a 410ha private reserve about 35km south at the city; besides the vegetation types described for "Caça e Pesca", it also includes primary cerrado and a small segment of riverine forest (SCHIAVINI & ARAÚJO, 1989; COSTA & ARAÚJO, 2001). Continuous Cerrado environments, pastures and agricultural fields border both localities. Bodies of water include artificial lakes and ponds and veredas along permanent streamlets (about 1m wide; 0.5m deep). The degree of human disturbance is greater at "Caça e Pesca", where in the past 20 years or more some portions of the veredas were drained for agriculture. Fires were also more frequent at this site. See further details on area description and pitfall sampling method in GIARETTA & KOKUBUM (2004) and GIARETTA & MENIN (2004). At "Caça e Pesca", the pitfall traps were maintained continuously from October 1999 to November 2000; the data from Panga traps are from September 2000 to October 2001. In both localities, five arrays of traps were set, each array consisting of three buckets (about 20l; 35cm mouth diameter) in line, two meters apart, linked by a fine meshed nylon net (8m long x 0.6m high, 0.1m buried in the ground). Specimens were recovered from the buckets at least once a week. The traps were set in open formations with shrubs less than one meter tall, and next (3-10m) to water bodies such as veredas streams (n = 4), ponds (n = 4), and lakes (n = 2). The trap arrays were separated from each other by distances of 100 up to 3000m. Diversity of terrestrial frogs at both sites were estimated using Levins’ index (B) and its standardized form (B_sta) (KREBS, 1989). Micro-spatial variation ("Caça e Pesca" x Panga) in diversity was evaluated by correlating the abundance of the species throughout the Spearman rank correlation coefficient (r_s) (ZAR, 1999).

For Perdizes, species list and habitat information were based on (1) the examination of specimens collected at the Galheiro Reserve (Estação Ecológica de Galheiro; 2,840ha) during a survey performed prior to the construction of Nova Ponte Hydroelectric power station, (2) collections made by the employees of the CompanhiaEnergética de Minas Gerais (CEMIG), and (3) our own data, collected 1-2 nights (2-3 persons) per month between 2002 and 2005. The vegetation at Galheiro Reserve includes several Cerrado physiognomies, including forests and small fractions of rock montane fields (CARDOSO et al., 2002), veredas being rare there. This reserve is surrounded by cattle ranches, agricultural fields and the hydroelectric reservoir of Nova Ponte (Araguari River). We have no data on abundance at this locality.

In Araguari, fieldwork was conducted at a single site (7 days, about 100 hour/man), during December (2005 and 2006). Considering the small sampling period, for Araguari we just present its exclusive species. The sampled environments were the slopes of the Paranaíba River, where narrow strips (up to 30m wide) of forest remain and cover the rocky beds of seasonal streamlets and rain drainage grooves. Cattle are raised between these forest remnants.

Juveniles of two closely related species (Physalaemus cuvieri Fitzinger, 1826 and P. centralis Bokermann, 1962) were hard to be told apart one each other (often P. cuvieri present red coloration on flanks and hidden parts of legs). Because adults of P. centralis were rarely heard in field and captured in traps (see results), juveniles that could not be clearly attributed to this species were grouped with P. cuvieri.

We searched for a correlation (Spearman r _s) between frog movement (species abundance in the pitfalls) and the length of reproductive season (number of calling months). This analysis was restricted to the "common species", those with at least ten individuals collected in pitfalls during any month (considering the pooled sample of the two sampling sites). Body size is thought to have important ecological implications related to energetic requirements (KNOUFT, 2002) and it is expected to be negatively related with abundance (DINIZ-FILHO et al., 2004); we tested this assumption by rank correlating (ZAR, 1999) our data on abundance with those of size (adult males) of each species.

Voucher specimens were deposited in the frog collection at the Museu de Biodiversidade do Cerrado, at the Universidade Federal de Uberlândia (AAG–UFU): (2155; 2194; 2275; 2289; 2308; 2333; 2338; 2340; 2343; 2400; 2423; 2442; 2445; 2456; 2499; 2500; 2577; 2604; 2622; 2624; 2689; 2691; 2692; 2693; 2856; 2871; 3055; 3096; 3097; 3107; 3848; 4096).

RESULTS

Thirty-two species of terrestrial frogs, belonging to Brachycephalidae, Bufonidae, Cycloramphidae, Dendrobatidae, Leiuperidae, Leptodactylidae, and Microhylidae were found in our samplings in the region of the Triângulo Mineiro (Tab. I) (see AMPHIBIAWEB, 2004, for color pictures of some species).

Most species were from open areas and breed in human generated environments, such as lakes (10 species) and ponds (14 species) (Tab. I); no species could be regarded as strictly forest dweller. Species found in both forests and open areas were Barycholos ternetzi (Miranda-Ribeiro, 1937), Leptodactylus mystaceus (Spix, 1824), L. syphax Bokermann, 1969, and Odontophrynus cultripes Reinhardt & Lütken, 1862.

Thirty species were found in Uberlândia (Tab. I); eighteen species were found in Galheiro reserve, with one (L. cunicularius Sazima & Bokermann, 1978) being exclusive in relation to Uberlândia. Species from Uberlândia that were not found at Galheiro were Rhinella granulosa (Spix, 1824), L. furnarius Sazima & Bokermann, 1978, L. mystaceus, L. podicipinus (Cope, 1862), Leptodactylus sertanejo Sazima & Bokermann, 1978, P. centralis, all four Pseudopaludicola species, and Dermatonotus muelleri (Boettger, 1885). One species, Leptodactylus cf. chaquensis Cei, 1950, was found only in Araguari.

A total of 2,114 frogs were collected in the pitfalls at both sites in Uberlândia, 1,126 in "Caça e Pesca" and 988 in Panga (Tab. II), the difference in abundance being significant (χ² = 8.88, df = 1, p < 0.005). Twenty pitfall-trapped species were common to both localities; four were exclusively from "Caça e Pesca" (Leptodactylus sertanejo, Pseudopaludicola saltica (Cope, 1887), P. mystacalis (Cope, 1887) and Rhinella cf. veredas (Brandão, Maciel & Sebben, 2007)) and two exclusively from Panga (Ischnocnema penaxavantinho (Giaretta, Toffoli & Oliveira, 2007) and P. ternetzi Miranda-Ribeiro, 1937) (Tab. II). Dominance was higher at Panga (χ² = 65.9, df = 1, p < 0.001), with P. cuvieri consisting of 57% of the sampled frogs; 40% at "Caça e Pesca". Based on pitfalls, richness (16-17 spp., Tab. II) and species rank abundances (r_s = 0.38, p = 0.05, n = 20 spp.) were similar at both sites, but species diversity was higher at "Caça e Pesca" (Tab. II). Frog species from Uberlândia not represented in pitfalls were: B. ternetzi, R. schneideri (Werner, 1894), Dermatonotus muelleri, L. mystaceus, L. podicipinus, Odontophrynus cultripes, and Pseudopaludicola aff. canga Giaretta & Kokubum, 2003; R. schneideri, O. cultripes, and Pseudopaludicola aff. canga were present at "Caça e Pesca"; L. mystaceus just was found at Panga.

In both localities, a larger number of individuals were observed in the wet season (Fig. 1) when most of the species were reproducing (Tab. III). Species calling during both dry and wet seasons were R. schneideri, Rhinella cf. veredas, L. furnarius (GIARETTA & KOKUBUM, 2004), O. cultripes, Proceratophrys aff. goyana (Miranda-Ribeiro, 1937) and Pseudopaludicola aff. canga. In both localities, the peaks in frog abundance corresponding to the second rainy season (reproductive season of most species) were of the same magnitude of that of the previous year (Fig. 1). Abundance was not correlated with body size of the species (r _s = 0.095, p > 0.50, n = 20 spp.).

Eleven species can be regarded as common (Tab. III). The months of the beginning (October and November) and final (March) of the wet season presented the greatest overlap (70-100%) of frog movement and reproduction.

DISCUSSION

Climatic factors directly affect the beginning and duration of the reproductive season of frogs (GOTTSBERGER & GRUBER, 2004) and in tropical regions with seasonal climate, most of the frog species reproduce during the rainy season (e. g., AICHINGER, 1987; ROSSA-FERES & JIM, 1994), which holds true for the Cerrado species as well (present work).

Reproductive adaptations to seasonal (xeric) environments, such as breeding activity concentrated in the rainy season (ARZABE, 1999), short reproductive cycle, and burrowing behavior (DUELLMAN, 1999) are expected for the frogs of Cerrado. In Uberlândia, frogs were more abundant during wet months, which can be attributed to a greater movement rate of adults around breeding sites and juvenile recruitment/dispersion (GIARETTA & KOKUBUM, 2004; GIARETTA & MENIN, 2004).

Although the rank of abundance was relatively similar in our both sampled sites, the "Caça e Pesca" (the most disturbed site) presented a higher species diversity and abundance. This can be attributed to species underrepresented at Panga, such as R. granulosa (Spix, 1824), L. ocellatus (Linnaeus, 1758), L. labyrinthicus (Spix, 1824), and P. marmoratus (Reinhardt & Lütken, 1862), which reproduce mainly in human generated bodies of water (e. g. lakes and ponds) (FRANÇA et al., 2004; GIARETTA & MENIN, 2004; SILVA et al., 2005) which are less common there. The even smaller number of species at Galheiro could also be related to the scarcity of adequate breeding areas such as ponds and veredas as well, and to its higher altitude. The small sample effort expended at Araguari precludes more detailed comparisons with the others localities.

High values of dominance, such as those found for P. cuvieri at Uberlândia are typical of seasonally stressed environments, as found in other frog species communities (GIARETTA et al., 1997, 1999). Our results did not support the expected inverse correlation between specific abundance and body size (DINIZ-FILHO et al., 2004). For the frog species studied we expect that other factors such as fecundity, capabilities of movement, hydric regulation and predator avoidance may play a role in the determination of the local abundance.

Within the Cerrado Biome, few localities can be regarded as well studied in terms of frog species composition and most of these localities are reserves above 1,000m altitude. There were 14 species of terrestrial frogs at Estação Ecológica de Águas Emendadas (800-1,250m altitude) (BRANDÃO & ARAÚJO, 1998), and 15 at Parque Nacional da Serra da Canastra (900-1,350m) (HADDAD et al., 1988), Floresta Nacional de Silvânia (900m) (DINIZ-FILHO et al., 2004) and Morrinhos (720m) (BORGES & JULIANO, 2007). Restricting comparisons to similar sized sampled areas, Uberlândia presented a richness of terrestrial frogs similar to that of Brasília (1,170m, 25 spp.) (BRANDÃO & ARAÚJO, 2001), and Serra do Cipó (650-1,800m, 25 spp.) (ETEROVICK & SAZIMA, 2004). Differences among localities may in part also be attributed to the sampling effort, and to the degree of human disturbance, since around human settlements the presence of ponds and lakes may allow greater population densities of those species that otherwise would occur in undetectable densities. The expected decrease in species richness of frogs with increasing altitude (FAUTH et al., 1989; GIARETTA et al., 1999) may also play a role within the Cerrado biome. Keeping in mind the problems regarding taxonomic resolution, the estimated number of shared species (terrestrial frogs) between the Triângulo Mineiro and other localities varied from 11 (Serra da Canastra, HADDAD et al., 1988) to 15 (Brasília). These low percentages of shared species (34-47%) may result from the heterogeneity of habitats found in the Cerrado biome, which represents a mosaic of different vegetation types, including gallery forests, veredas, mesophytic forests, dry forests, and altitudinal fields, among others (CAVALCANTI & JOLY, 2002; OLIVEIRA-FILHO & RATTER, 2002), with several isolated highlands (Serra da Canastra and Serra do Cipó). This heterogeneity and discontinuity of habitats helps to explain the existence of species with discontinuous distributions (e. g. Ameerega flavopicta (Lutz, 1925), L. syphax and L. cunicularius) and the species turnover (beta-diversity) among montane localities (Serra da Canastra and Serra do Cipó) and even within the Triângulo Mineiro (present study). The regional heterogeneity found in Cerrado biome is thought to have little effect upon the composition of the herpetofauna, since lizards present a higher turnover in South American forest habitats (COLLI et al., 2002). This statement apparently does not hold for frogs, because their ecological needs (HADDAD & SAWAYA, 2000; TOLEDO et al., 2003, present study) are substantially different from those of lizards which are less dependent on humidity for dispersion and reproduction.

It has been suggested that the great anuran diversity, as that observed in the Amazonia (CRUMP, 1974) and in the Atlantic Forest (DUELLMAN, 1988, 1999; HEYER et al., 1990), may be explained by their high levels of precipitation and the extensive forest cover and the topographic heterogeneity (DUELLMAN, 1999). However, the number of terrestrial frogs found in the Triângulo Mineiro was similar (Boracéia, São Paulo, ca. 29 spp; HEYER et al., 1990) or even larger (GIARETTA et al., 1997, 1999) than forested localities in southeastern Brazil. Our results call attention to the possibility that the distinguishable rich terrestrial frog fauna of the Atlantic Forest (e. g. Boracéia, HEYER et al., 1990) is due to a disproportional contribution of its riparian species.

The Leptodactylid and Leiuperidae frogs represent a large portion of the frog fauna of American tropics (DUELLMAN, 1988). In the region of Triângulo Mineiro, as well as in other localities from the Cerrado biome, they are ubiquitously represented, mainly by the foam nesting species of Physalaemus and Leptodactylus. Examples of widely distributed species within the Cerrado are L. furnarius, L. fuscus (Schneider, 1799), L. labyrinthicus, L. ocellatus, L. syphax, P. centralis, P. cuvieri and P. saltica. Leptodactylus cunicularius was known from relatively higher elevations (HADDAD et al., 1988; CARDOSO & HADDAD, 1992), and its presence in Galheiro indicates an influence of the surrounding highlands in this locality, as also indicated by the presence of Scinax canastrensis (Cardoso & Haddad, 1982) (Hylidae) (OLIVEIRA FILHO & KOKUBUM, 2003) in the same area.

In southeastern Brazil there are approximately 20 Ischnocnema species (FROST, 2007; HEINICKE et al., 2007), of which 19 are forest dwellers. The number of Brachycephalidae species in open areas, which includes most of the Cerrado physiognomies, may be constrained by their terrestrial reproductive mode, which relies on consistently high humidity (LYNCH & DUELLMAN, 1997).

In spite of the intense human-generated environmental disturbance, with just 15% of its original natural areas remaining (CAVALCANTI & JOLY, 2002), the Triângulo Mineiro region still presents a rich frog fauna, what can be attributed to the relatively recent history (< 60 years) of major human disturbances, such as intensive agriculture and damming. A supposed natural resistance of the frogs of Cerrado, which evolved in a seasonally dry environment subject to natural disturbances such as fires, could also have played a role in their persistence. At present most of the terrestrial frog species from lowland Cerrado are found in open plant formation and in human generated areas and may not be threatened by moderated habitat alteration such as free ranging cattle farming. In fact, from the sixteen recognized threatened species of anurans in Brazil (MINISTÉRIO DO MEIO AMBIENTE, 2003), just one is a Cerrado species. Special attention on conservation may be paid to those species that were not represented in pitfall sampling, (e. g. L. mystaceus and those non-terrestrial frogs (Hylidae) restricted to forest), which may have small and fragmented local populations and are restricted to particular habitats, thus being more susceptible to changes in the environment. We emphasize that a very different situation is expected if extensive agriculture (with complete removal of natural vegetation) is implemented, which may fill water bodies with earth and contaminate them with chemicals and fertilizers. At present days, sugar cane and soybean plantations are the worse threats.

The data on Cerrado herpetofauna is still scarce (HEYER, 1988) and large areas of this biome never were surveyed (COLLI et al., 2002). The present taxonomic resolution is far from satisfactory and this may hinder detailed comparisons among areas as well. Because of the rapid degradation of the Cerrado biome in recent years, and the insufficient data on its fauna, extensive censuses in different localities are still necessary for the establishment of priority and political areas of conservation. Our data on richness and abundance can be useful to future species monitoring. Considering its biological diversity, as illustrated here for terrestrial frogs, and rate of destruction, those lowland (< 800m alt.) Cerrado environments deserve implementation of conservation programs. Establishment of major reserves should include as much the diversity of the Cerrado physiognomies (especially forests) as possible, but effective protection of the small water courses and its surrounding habitats would have a great positive impact on the preservation of the diversity of frog species in the Cerrado.

Acknowledgments. Financial support by CNPq and FAPEMIG, and a fellowship (AAG) by CNPq. Companhia Energética do Estado de Minas Gerais (CEMIG) financially supported works at the Galheiro Reserve. F. G. Lemos, D. T. Ribeiro, and R. C. Costa helped in the field work. J. A. F. Diniz Filho critically read the draft. Adir Lemos allowed works at his property in Araguari. W. Quatman reviewed the English. The employees of the CEMIG kindly helped us during the field works. IBAMA provided collect permission (#84/2002/MG; process # 02015.008064/02–51).

Recebido em fevereiro de 2006. Aceito em outubro de 2007.

• AICHINGER, M. 1987. Annual activity patterns of anurans in a seasonal Neotropical environment. Oecologia 71:583-592.
• ALFORD, R. A. & RICHARDS, S. J. 1999. Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 30:133-165.
• AMPHIBIAWEB: INFORMATION ON AMPHIBIAN BIOLOGY AND CONSERVATION. 2004. Berkeley, California: AmphibiaWeb Available at: http://www.amphibiaweb.org/ Acessed on: 05.07.2007.
  » link
• ARZABE, C. 1999. Reproductive activity patterns of anurans in two different altitudinal sites within the Brazilian Caatinga. Revista Brasileira de Zoologia 16(3):851-864.
• BASTOS, R. P.; MOTTA, J. A. O.; LIMA, L. P. & GUIMARÃES, L. D. 2003. Anfíbios da Floresta Nacional de Silvania, Estado de Goiás Goiânia. 82p.
• BLAUSTEIN, A. R. & WAKE, D. B. 1990. Declining Amphibian populations: A global phenomenon? Trends in Ecology and Evolution 5(7):203-204.
• ___. 1995. The puzzle of declining amphibian populations. Scientific American 1995:56-61.
• BORGES, F. J. A. & JULIANO, R. F. 2007. Distribuição espacial e temporal de uma comunidade e anuros do município de Morrinhos, Goiás, Brasil (Amphibia, Anura). Neotropical Biology and Conservation 2(1):21-27.
• BRANDÃO, R. A. & ARAÚJO, A. F. B. 1998. A herpetofauna da Estação Ecológica de Águas Emendadas. In: MARINHO FILHO, J.; RODRIGUES, F. & GUIMARÃES, M. eds. Vertebrados da Estação Ecológica de Águas Emendadas: história natural e ecologia em um fragmento de cerrado do Brasil Central Brasília, Secretaria de Meio Ambiente Ciência e Tecnologia do Distrito Federal. p.9-21.
• ___. 2001. A herpetofauna associada às matas de galeria no Distrito Federal. In: RIBEIRO, J. F.; FONSECA, C. E. L. & SOUSASILVA, J. C. eds. Cerrado: caracterização e recuperação de Matas de Galeria Planaltina, Embrapa Cerrados. p.561-604.
• BRASILEIRO, C. A.; SAWAYA, R. J.; KIEFER, M. C. & MARTINS, M. 2005. Anfíbios de um fragmento de Cerrado aberto do sudeste do Brasil. Biota Neotropica 5:1-17.
• CARDOSO, A. J. & HADDAD, C. F. B. 1992. Diversidade e turno de vocalização de anuros em comunidade tropical. Acta Zoologica Lilloana 41:93-105.
• CARDOSO, E.; MORENO, M. I. C. & GUIMARÃES, A. J. M. 2002. Estudo fitossociológico em área de Cerrado sensu stricto na Estação de Pesquisa e Desenvolvimento Ambiental Galheiro Perdizes, MG. Revista Caminhos de Geografia 3:30-43.
• CAVALCANTI, R. B. & JOLY, C. A. 2002. Biodiversity and conservation priorities in the Cerrado region. In: OLIVERA, P. S. & MARQUIS, R. J. eds. The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna New York, Columbia University. p.351-367.
• COLLI, G. R.; BASTOS, R. P. & ARAÚJO, A. F. B. 2002. The character and dynamics of the Cerrado herpetofauna. In: OLIVERA, P. S. & MARQUIS, R. J. eds. The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna New York, Columbia University. p.223-241.
• COSTA, A. A. & ARAÚJO, G. M. 2001. Comparação da vegetação arbórea de cerradão e cerrado na Reserva do Panga, Uberlândia, Minas Gerais. Acta Botanica Brasilica 15:63-72.
• COSTA, R. C.; FACURE, K. G.; & GIARETTA, A. A. 2006. Courtship, vocalizations, and tadpole description of Epipedobates flavopictus (Anura, Dendrobatidae) in southern Goiás, Brazil. Biota Neotropica 6 Available at: <http://www.biotaneotropica.org>. Acessed on: 05.07.2007.
• CRUMP, M. L. 1974. Reproductive strategy in a tropical anuran community. Miscellaneous Publications of the Museum of Natural History, University of Kansas 61:1-68.
• DINIZ-FILHO, J. A. F.; BINI, L. M.; BASTOS, R. P.; VIEIRA, C. M.; SOUZA, M. C.; MOTTA, L. A. O.; POMBAL JR., J. P. & PEIXOTO, J. C. 2004. Anurans from a local assemblage in Central Brazil: linking local processes with macroecological patterns. Brazilian Journal of Biology 64(1):41-52.
• DUELLMAN, W. E. 1988. Patterns of species diversity in anuran amphibians in the American Tropics. Annals of the Missouri Botanical Garden 75:79-104.
• ___. 1999. Distribution patterns of amphibians in South America. In: DUELLMAN, W. E. ed. Patterns of distribution of amphibians: a global perspective Baltimore, The Johns Hopkins University. p.255-328.
• ETEROVICK, P. C. & SAZIMA, I. 2004. Anfíbios da Serra do Cipó, Minas Gerais Amphibians from the Serra do Cipó, Minas Gerais Belo Horizonte, PUC Minas. 150p.
• ETEROVICK, P. C.; CARNAVAL, A. C. O. Q.; BORGES-NOJOSA, D. M.; SILVANO, D. L.; SEGALLA, M. V. & SAZIMA, I. 2005. Amphibian declines in Brazil: an overview. Biotropica 37(2):166-179.
• FAUTH, J. E.; CROTHER, B. I. & SLOWINSKI, J. B. 1989. Elevational patterns of species richness, evenness, and abundance of the Costa Rican leaf-litter herpetofauna. Biotropica 21(2):178-185.
• FRANÇA, L. F.; FACURE, K. G. & GIARETTA, A. A. 2004. Trophic and spatial niches of two large-sized species of Leptodactylus (Anura) in Southeastern Brazil. Studies on Neotropical Fauna and Envirnment 39(3):243-248.
• FROST, D. R. 2007. Amphibian Species of the World: an Online Reference Version 5.0. American Museum of Natural History, New York, USA. Available at: http:// research.amnh.org/herpetology/amphibia/index.php Acessed on: 05.07.2007.
• GARDNER, T. A. 2001. Declining amphibian populations: a global phenomemom in conservation biiology. Animal Biodiversity and Conservation 24(2):25-43.
• GIARETTA, A. A. & FACURE, K. G. 2006. Terrestrial and communal nesting in Eupemphix nattereri (Anura, Leiuperidae): Interactions with predators and pond structure. Journal of Natural History 40:2577-2587.
• GIARETTA, A. A & KOKUBUM, M. N. C. 2004. Reproductive ecology of Leptodactylus furnarius Sazima & Bokermann, 1978 a frog that lay eggs in underground chambers (Anura, Leptodactylidae). Herpetozoa 16(3/4):115-126.
• GIARETTA, A. A. & MENIN, M. 2004. Reproduction, phenology and mortality sources of a species of Physalaemus (Anura: Leptodactylidae). Journal of Natural History 38:1711-1722.
• GIARETTA, A. A.; FACURE, K. G.; SAWAYA, R. J.; MEYER, J. H. M. & CHEMIN, N. 1999. Diversity and abundance of litter frogs of a montane forest in southeastern Brazil: seasonal and altitudinal changes. Biotropica 31(4):669-674.
• GIARETTA, A. A.; SAWAYA, R. J.; MACHADO, G.; ARAÚJO, M. S.; FACURE, K. G.; MEDEIROS, H. F. & NUNES, R. 1997. Diversity and abundance of litter frogs at altitudinal sites at Serra do Japi, Southeastern Brazil. Revista Brasileira de Zoologia 14(2):341-346.
• GOODLAND, R. & FERRI, G. M. 1979. Ecologia do Cerrado São Paulo, Livraria Itatiaia & Universidade de São Paulo. 193p.
• GOTTSBERGER, B. & GRUBER, E. 2004. Temporal partitioning of reproductive activity in a neotropical anuran community. Journal of Tropical Ecology 20(3):271-280.
• HADDAD, C. F. B. & SAWAYA, R. J. 2000. Reproductive modes of Atlantic forest hylid frogs: A general overview and the description of a new mode. Biotropica 32(4b):862-871.
• HADDAD, C. F. B.; ANDRADE, G. V. & CARDOSO, A. J. 1988. Anfíbios anuros no Parque Nacional da Serra da Canastra, Estado de Minas Gerais. Brasil Florestal 64:9-20.
• HEINICKE, M. P.; DUELLMAN, W. E. & HEDGES, S. B. 2007. Major Caribbean and Central American frog faunas originated by ancient oceanic dispersal. Proceedings of the National Academy of Science 104(24):10092-10097.
• HEYER, W. R. 1988. On Frog Distribution Patterns East of Andes. In: VANZOLINI, P. E. & HEYER, W. R. eds. Proceedings of a Workshop on Neotropical Distribution Pattern Rio de Janeiro, Academia Brasileira de Ciências. p.245-273.
• HEYER, W. R.; DONNELLY, M. A.; MCDIARMID, R. W.; HAYEK, L. C. & FOSTER, M. S. 1994. Measuring and monitoring biological diversity: standard methods for amphibians Washington, Smithsonian Institution. 364p.
• HEYER, W. R.; RAND, A. S.; CRUZ, C. A. G.; PEIXOTO, O. L. & NELSON, C. E. 1990. Frogs of Boracéia.Arquivos de Zoologia 31(4):231-410.
• KNOUFT, J. H. 2002. Regional analysis of body size and population density in stream fish assemblages: testing predictions of the energetic equivalence rule. Canadian Journal of Fisheries and Aquatic Sciences 59:1350-1360.
• KOKUBUM, M. N. C. & GIARETTA, A. A. 2005. Reproductive ecology and behaviour of a species of Adenomera (Anura, Leptodactylinae) with endotrophic tadpoles: systematic implications. Journal of Natural History 39:1745-1758.
• KREBS, C. J. 1989. Ecological Methodology New York, Harper and Row. 654p.
• LIPS, K. R. 1998. Decline of a tropical montane amphibian fauna. Conservation Biology 12:106-117.
• LYNCH, J. D. & DUELLMAN, W. E. 1997. Frogs of the genus Eleutherodactylus (Leptodactylidae) in Western Ecuador: systematics, ecology, and biogeography. The University of Kansas Natural History Museum, Special Publication 23:1-236.
• MARSH, D. M. 2001. Fluctuations in amphibian populations: a meta-analysis. Biological Conservation 101:327-335.
• MENIN, M. & GIARETTA, A. A. 2003. Predation on foam nests of leptodactylid frogs (Anura, Leptodactylidae) by larvae of Beckeriella niger (Diptera, Ephidridae). Journal of Zoology 261:239-243.
• MINISTÉRIO DO MEIO AMBIENTE. 2003. Instrução Normativa n. 3 de 27 de maio de 2003: Lista Nacional das Espécies da Fauna Brasileira Ameaçadas de Extinção. Diário Oficial da União, 28/05/2003, Seção 1:88-97.
• MYERS, N.; MITTERMEIER, R. A.; MITTERMEIER, C. G.; FONSECA, G. A. B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858.
• OLIVEIRA-FILHO, A. T. & RATTER, J. A. 2002. Vegetation physiognomies and woody flora of the Cerrado Biome. In: OLIVEIRA, P. S. & MARQUIS, R. J. eds. The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna New York, Columbia University. p.91-120.
• OLIVEIRA FILHO, J. C. & GIARETTA, A. A. 2006. Tadpole and advertisement call of Chiasmocleis albopunctata (Anura, Microhylidae) from Brazil. Zootaxa 1353:63-68.
• OLIVEIRA FILHO, J. C. & KOKUBUM, M. N. C. 2003. Scinax canastrensis Geographical Distribution. Herpetological Review 34(2):163.
• PECHMANN, J. H. K.; SCOTT, D. E.; SEMLITSCH, R. D.; CALDWELL, J. P.; VITT, L. J. & GIBBONS, J. W. 1991. Declining amphibian populations: the problem of separating human impacts from natural fluctuations. Science 253:891-895.
• PHILLIPS, K. 1990. Where have all the frogs and toads gone? BioScience 40:422-424.
• POMBAL JR., J. P. & GORDO, M. 2004. Anfíbios Anuros da Juréia. In: MARQUES, O. A. V. & DULEBA, W. eds. Ambiente, Flora e Fauna da Estação Ecológica da JuréiaItatins Ribeirão Preto, Holos. p.243-256.
• ROSA, R.; LIMA, S. C. C. & ASSUNÇÃO, W. L. 1991. Abordagem preliminar das condições climáticas de Uberlândia (MG). Sociedade e Natureza 3:91-108.
• ROSSA-FERES, D. C. & JIM J. 1994. Distribuição sazonal em comunidades de anfíbios anuros na região de Botucatu, São Paulo. Revista Brasileira de Biologia 54(2):323-334.
• SANO, S. N. & ALMEIDA, S. P. 1998. Cerrado: ambiente e flora Planaltina, Embrapa. 556p.
• SARKAR, S. 1996. Ecological theory and anuran declines. BioScience 46(3):199-207.
• SCHIAVINI, I. & ARAUJO, G. M. 1989. Considerações sobre a Vegetação da Reserva Ecológica do Panga. Sociedade e Natureza 1:61-66.
• SILVA, W.R.; GIARETTA, A. A. & FACURE, K. G. 2005. On the natural history of the pepper frog Leptodactylus labyrinthicus (Anura, Leptodactylidae). Journal of Natural History 39:555-566.
• TOLEDO, L. F.; RAMOS, J. Z. P. & HADDAD, C. F. B. 2003. Distribuição Espacial e Temporal de uma Comunidade de Anfíbios Anuros do Município de Rio Claro, São Paulo, Brasil. Holos Environment 3(2):136-149.
• ZAR, J. 1999. Biostatistical Analysis Fourth edition. New Jersey, Prentice Hall. 663p.

Publication Dates

• Publication in this collection
  05 Aug 2008
• Date of issue
  June 2008

History

• Accepted
  Oct 2007
• Received
  Feb 2006