Seasonal and habitat structure of an anuran assemblage in a semideciduous forest area in Southeast Brazil

ELVIS A. PEREIRA MATHEUS O. NEVES JOSÉ LUIZ M.M. SUGAI RENATO N. FEIO DIEGO J. SANTANA About the authors

Abstract

In this study, we evaluated the reproductive activity and the temporal and spatial distributions of anuran assemblages in three environments within a semideciduous forest in Southeast Brazil, located at Municipality of Barão de Monte Alto, State of Minas Gerais, Brazil. The field activities were carried out during three consecutive days, monthly throughout the rainy seasons of 2013–2014 and 2014–2015. We recorded 28 anurans species, distributed in eight families. We observed the spatial-temporal distribution of some species, and their associated reproductive behaviors through exploration of vocalizations at different sites. The spatial and temporal distribution of the species seems to adapt to abiotic and biotic factors of their environment.

Key words
Anuran community; community ecology; environmental heterogeneity; niche breadth; vocalization sites

INTRODUCTION

Information about anuran habitat use and reproductive ecology allows us to interpret the relationships between these animals and abiotic and biotic factors (EterovickETEROVICK PC & SAZIMA I. 2000. Structure of an anuran community in a montane meadow in southeastern Brazil: effects of seasonality, habitat, and predation. Amphibia-Reptilia 21: 439-461. & Sazima 2004). In several vertebrate groups (e.g. birds, anurans, mammals), it has been shown that the coexistence of populations in the same area is facilitated by ecological differences (e.g. habitats, microhabitats, seasonality), due in part to interspecific behavioral interactions, involving the social organization and spatial and temporal distribution of the species in the communities (CardosoCARDOSO AJ, ANDRADE GV & HADDAD CFB. 1989. Distribuição espacial em comunidades de anfíbios (Anura) no SE do Brasil. Rev Bras Biol 49: 241-249. et al. 1989, Cardoso & HaddadCARDOSO AJ & HADDAD CFB. 1992. Diversidade e turno de vocalizações de anuros em comunidade neotropical. Acta Zool Lilloana 41: 93-105. 1992, MeninMENIN M, ROSSA-FERES DDC & GIARETTA AA. 2005. Resource use and coexistence of two syntopic hylid frogs (Anura, Hylidae). Rev Bras Zool 22: 61-72. et al. 2005, VogelVOGEL HF, ZAWADZKI H & METRI R. 2011. Coexistência entre Turdus leucomelas Vieillot, 1818 e Turdus rufiventris Vieillot, 1818 (Aves: Passeriformes) em um fragmento urbano de floresta com araucárias, Sul do Brasil. Biota Neotrop 11. et al. 2011, vanVAN BEEST FM, MCLOUGHLIN PD, VANDER WAL E & BROOK RK. 2014. Density-dependent habitat selection and partitioning between two sympatric ungulates. Oecologia 175: 1155-1165. Beest et al. 2014, CostaCOSTA GC, FRANÇA KL, OLIVEIRA-JÚNIOR TM & PICHORIM MAURO. 2016. Uso e coexistência de habitat em duas espécies intimamente relacionadas de Herpsilochmus (Aves: Thamnophilidae). Cogent Environ Sci 2: 1. doi: 10.1080 / 23311843.2016.1264126 et al. 2016, CloyedCLOYED CS & EASON PK. 2017. Niche partitioning and the role of intraspecific niche variation in structuring a guild of generalist anurans. R Soc Open Sci 4: 170060. doi: 10.1098/rsos.170060. & Eason 2017, SchirmerSCHIRMER A, HERDE A, ECCARD JA & DAMMHAHN M. 2019. Individuals in space: personality-dependent space use, movement and microhabitat use facilitate individual spatial niche specialization. Oecologia: 1-14. et al. 2019). Currently, the most functional concept of an ecological community is defined as a group of organisms that coexist in a determined habitat and also interact with one another and the surrounding environment (BegonBEGON M, HARPER JL & TOWNSEND CR. 1990. Ecology. Individuals, populations and communities. Blackwell scientific publications. Blackwell Scientific Publications, Oxford, p. 611-615. et al. 1990). The structure of adult amphibian assemblages has been studied based on habitat and microhabitat (Eterovick & Sazima 2000, Rojas-AhumadaROJAS-AHUMADA DP, LANDEIRO VL & MENIN M. 2012. Role of environmental and spatial processes in structuring anuran communities across a tropical rain forest. Austral Ecol 37: 865-873. et al. 2012), and in terms of reproductive periods (AichingerAICHINGER M. 1987. Annual activity patterns of anurans in a seasonal Neotropical environment. Oecologia 71: 583-592. 1987, SabbagSABBAG AF & ZINA J. 2011. Anurans of a riparian forest in Sao Carlos, State of São Paulo, Brazil. Biota Neotrop 11: 179-188. & Zina 2011). Intuitively, due to morphological variability associated with certain clades of amphibians (e.g. arboreal, aquatic), we assume that phylogenetic relationships have a significant effect on the structure of amphibian communities.

Amphibians exhibit different strategies for occupying their environment. The occupation by species differs mainly related to vegetation structure (for species in the forest and open areas), as well as the duration of water bodies (temporary or permanent) (Díaz-PaniaguaDÍAZ-PANIAGUA C. 1990. Temporary ponds as breeding sites of amphibians at a locality in Southwestern Spain. Herpetol J 1: 447-453. 1990, Rossa-FeresROSSA-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 Zoo 18: 439-454. & Jim 2001, BertoluciBERTOLUCI J & RODRIGUES MT. 2002. Utilização de habitats reprodutivos e micro-habitats de vocalização em uma taxocenose de anuros (Amphibia) da Mata Atlântica do sudeste do Brasil. Pap Avulsos Zool 42: 287-297. & Rodrigues 2002). However, several characteristics of the habitat such as food availability, hydroperiod, availability of oviposition sites, rainfall, and refuges determine the patterns of organization of anuran assemblages (LillywhiteLILLYWHITE H, LICHT P & CHELGREN P. 1973. Role of behavioral thermoregulation in growth energetics of toad, Bufo boreas. Ecology 54: 375-383. et al. 1973, CrumpCRUMP ML. 1974. Reproductive strategies in a tropical anuran community. Miscellaneous Publication of the Museum of Natural History of University of Kansas 61: 1-68. 1974, ToftTOFT CA. 1985. Resource partitioning in amphibians and reptiles. Copeia 1985: 1-21. 1985, PulliamPULLIAM PN. 1989. Individual behaviour and the procurement of essential resources. Perspectives in Ecological Theory. In: Roughgarden J, May RM and Levin AS (Eds), Princeton University Press, Princeton, p. 25-38. 1989, BarbaultBARBAULT R. 1991. Ecological constraints and community dynamics linking community patterns to organismal ecology. The case of herpetofaunas. Acta Oecol 12: 139-163. 1991, ArzabeARZABE C. 1999. Reproductive activity patterns of anurans in two different altitudinal sites within the Brazilian Caatinga. Rev Bras Zool 16: 851-864. 1999, SkellySKELLY DK, WERNER EE & CORTWRIGHT SA. 1999. Long-term distributional dynamics of a Michigan amphibian assemblage. Ecology 80: 2326-2337. et al. 1999, EterovickETEROVICK PC & FERNANDES GW. 2001. Tadpole distribution within montane meadow streams at the Serra do Cipó, southeastern Brazil: ecological or phylogenetic constraints? J Trop Ecol 17: 683-693. & Sazima 2000, Eterovick & Fernandes 2001, PradoPRADO CPA, UETANABARO M & HADDAD CFB. 2005. Breeding activity patterns, reproductive modes, and habitat use by anurans (Amphibia) in a seasonal environment in the Pantanal, Brazil. Amphibia-Reptilia 26: 211-221. et al. 2005, Richter-BoixRICHTER-BOIX A, LLORENTE GA & MONTORI A. 2006. A comparative analysis of the adaptive developmental hypothesis in six Mediterranean anuran species along a pond permanency gradient. Evol Ecol Res 8: 1139-1154. et al. 2006).

The relationship between environmental heterogeneity and species diversity can be explained by habitat heterogeneity (SimpsonSIMPSON EH. 1949. Measurement of diversity. Nature 163: 688. 1949, MacArthurMACARTHUR RH & MACARTHUR JW. 1961. On bird species diversity. Ecology 42: 594-598. & MacArthur 1961, MacArthur & Wilson 1967). Studies about amphibians have demonstrated that complex and heterogeneous environments promote more microhabitats and ways of exploiting environmental resources, and thus, allow for a larger group of species to co-occur (PiankaPIANKA ER. 1969. Sympatry of desert lizards (Ctenotus) in Western Australia. Ecology 50: 1012-1030. 1969, DuellmanDUELLMAN WE & TRUEB L. 1986. Biology of Amphibians. New York: McGraw-Hill, 670 p. & Trueb 1986, Cardoso et al. 1989, PombalPOMBAL JUNIOR JP. 1997. Distribuição espacial e temporal de anuros (Amphibia) em uma poça permanente na Serra de Paranapiacaba, Sudeste do Brasil. Rev Bras Biol 57: 583-594. Junior. 1997, BrandãoBRANDÃO RA & ARAÚJO AFB. 1998. A herpetofauna da Estação Ecológica de Águas Emendadas. Vertebrados da Estação Ecológica de Águas Emendadas. História Natural e Ecologia em um fragmento de cerrado do Brasil Central. In: Marinho-Filho J, Rodrigues F and Guimarães M (Eds), SEMATEC/IEMA, Brasília, p. 9-21. & Araújo 1998, BernardeBERNARDE PS & ANJOS L. 1999. Distribuição espacial e temporal da anurofauna do Parque Estadual Mata dos Godoy, Londrina, Paraná, Brasil (Amphibia, Anura). Comunicações do Museu Ciências e Tecnologia da PUCRS. Série Zoologia 2: 127-140.7. & Kokubum 1999, ConteCONTE CE & MACHADO RA. 2005. Riqueza de espécies e distribuição espacial e temporal em comunidade de anfíbios anuros (Amphibia, Anura) em uma localidade do Município de Tijucas do Sul, Paraná, Brasil. Rev Bras Zool 22: 940-948. & Machado 2005, VasconcelosVASCONCELOS 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 5: 1-14. & Rossa-Feres 2005). In anurans communities, species coexistence may result in a differential use of habitats for vocalization, reproduction and larval developmental activities (Duellman & Trueb 1986, Bernarde & Anjos 1999, BastosBASTOS RP. 2007. Anfíbios do Cerrado. In Herpetologia no Brasil II. In: Nascimento LB and Oliveira ME (Eds), Sociedade Brasileira de Herpetologia. Belo Horizonte, p. 87- 100. 2007, PurrenhagePURRENHAGE JL & BOONE MD. 2009. Amphibian community response to variation in habitat structure and competitor density. Herpetologica 65: 14-30. & Boone 2009). Other influential factores include the presence of bromeliads (SchineiderSCHINEIDER JAP & TEIXEIRA RL. 2001. Relacionamento entre anfíbios anuros e bromélias da Restinga de Regência, Linhares, Espírito Santo, Brasil. Iheringia 62: 263-268. & Teixeira 2001, BastaziniBASTAZINI CM, MUNDURUCA JFV, ROCHA PLB & NAPOLI MF. 2007. Which environmental variables better explain changes in anuran community composition? A case study in the restinga of Mata de São João, Bahia, Brazil. Herpetologica 63: 459-471. et al. 2007), soil and moisture (Bernarde & Anjos 1999, ToledoTOLEDO 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 Environment 3: 136-149. et al. 2003, Bastazini et al. 2007), leaf litter, fallen logs, and temporary pools (Bernardo & Anjos 1999BERNARDE PS & KOKUBUM MNC. 1999. Anurofauna do Município de Guararapes, Estado de São Paulo, Brasil (Amphibia: Anura). Acta Biol Leopoldinense 21: 89-97., Toledo et al. 2003, Bastazini et al. 2007). Some species show plasticity in the use of spatial resources (SantosSANTOS TG, KOPP K, SPIES MR, TREVISAN R & CECHIN SZ. 2008. Temporal and spatial distribution of anurans in the Pampa Region (Santa Maria, RS). Iheringia Ser Zool 98: 244-253. et al. 2008) and variation in the availability of these resources can affect the number of species, reproductive modes, and the activity period of anurans (Duellman & Trueb 1986, KoppKOPP K, SIGNORELLI L & BASTOS RP. 2010. Temporal distribution and diversity of reproductive modes in anuran amphibians in the Emas National Park and surrounding area, State of Goiás, Brazil. Iheringia Ser Zool 100: 192-200. et al. 2010).

Another intrinsic trait structuring an anuran community should consider phylogeny as an explanatory variable, which may reveal how related assemblages occupy different environments, and also understand why certain assemblages are similar or different (LososLOSOS JB. 1996. Phylogenetic perspectives on community ecology. Ecology 77: 1344-1354. 1996). Studies about the structure of assemblages are still mainly descriptive (WellsWELLS KD. 2007. The Ecology and Behavior of Amphibians. The University of Chicago Press, Chicago. 2007) and those that consider the effect of phylogeny are scarce, especially for amphibians (EterovickETEROVICK PC, RIEVERS CR, WACHLEVSKI M, FRANCO BP & AFONSO LG. 2010. Lack of phylogenetic signal in the variation in anuran microhabitat use in Southeastern Brazil. Evol Ecol 24: 1-24. & Fernandes 2001, Eterovick et al. 2010).

Most of the studies focusing on Neotropical anuran assemblages were carried out in the Amazon basin (e.g. Crump 1974, Aichinger 1987, Neckel-OliveiraNECKEL-OLIVEIRA S, MAGNUSSON WE, LIMA AP & ALBERNAZ ALK. 2000. Diversity and distribution of frogs in an Amazonian savanna in Brazil. Amphibia-Reptilia 21: 317-326. et al. 2000) and in the Atlantic Forest, Southeastern Brazil (e.g.Haddad & Sazima, 1992HADDAD CF & PRADO CP. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic Forest of Brazil. BioScience 55: 207-217., BertoluciBERTOLUCI J. 1998. Annual patterns of breeding activity in Atlantic Rainforest anurans. J Herpetol 32: 607-611. 1998, Bertoluci & Rodrigues 2002). Their findings show that most species reproduce during the rainy season, and a strong association between abundance and species richness with rainfall and temperature (EterovickETEROVICK PC. 2003. Distribution of anuran species among montane streams in South-Eastern Brazil. J Trop Ecol 19: 219-228. & Sazima 2000, Toledo et al. 2003, SantosSANTOS TG, VASCONCELOS TS, ROSSA-FERES DC & HADDAD CFB. 2009. Anurans of a seasonally dry tropical forest: Morro do Diabo State Park, São Paulo state, Brazil. J Nat Hist 43: 973-993. et al. 2008, Kopp et al. 2010, HartelHARTEL T, BANCILA R & COGALNICEANU D. 2011. Spatial and temporal variability of aquatic habitat use by amphibians in a hydrologically modified landscape. Freshw Biol 56: 2288-2298. et al. 2011, MaffeiMAFFEI F, UBAID FK & JIM J. 2011. Anurans in an open Cerrado area in the Municipality of Borebi, São Paulo state, Southeastern Brazil: habitat use, abundance and seasonal variation. Biota Neotrop 11: 221-233. et al. 2011). According to Santos et al. (2009), the species composition of anurans in semideciduous forest areas is more similar to those recorded in areas of Cerrado, Pantanal and even Pampa than with the communities of the ombrophilic areas of the Atlantic Forest. It is expected that studies of anuran communities in semideciduous forest will demonstrate several levels of reproductive segregation among species in the same community. The species may range from complete spatial and/or temporal sharing, to total overlapping of these factors (e.g. Bernarde & Kokubum 1999, Rossa-Feres & Jim 2001).

The general objective of this study was to describe the spatial-temporal distributions of anurans in a semideciduous forest area, located in the Municipality of Barão de Monte Alto, State of Minas Gerais, Brazil. More specifically, we first described the reproductive period and activity of the species during two rainy seasons, as well as their spatial distribution considering reproductive site characteristics. We also tested the hypothesis that phylogenetic distances, reproductive mode, and reproductive period explain differences in reproductive site characteristics of anurans.

MATERIALS AND METHODS

Study area

The study was carried out in the Municipality of Barão de Monte Alto (21°14’42”S, 42°14’16”W, WGS84), State of Minas Gerais. The climate of the region is classified as Aw (sensuKöppenKÖPPEN WP. 1918. Klassification der Klimate nach Temperatur, Niederschlag und Jahreslauf. Petermanns Mitteilungen 64: 193-203. 1918), with a dry season that coincides with winter, and the maximum observed precipitation for the driest month of this season is less than 60 mm (KottekKOTTEK M, GRIESER J, BECK C, RUDOLF B & RUBEL F. 2006. World Map of the Köppen-Geiger climate classification updated. Meteorol Z 15: 259-263. et al. 2006). The local vegetation is characterized as Seasonal semi-deciduous Forest of lowlands between 132 and 700 m elevation (VelosoVELOSO HP, RANGEL FILHO ALR & LIMA JCA. 1991. Classificação da vegetação brasileira adaptada a um sistema universal. IBGE: Departamento de Recursos Naturais e Estudos Ambientais, Rio de Janeiro. et al. 1991). Mean annual rainfall is about 1.287 mm and the mean annual temperature is 22.6°C. We monitored three habitats: a temporary stream and marsh (Area A) in a forested area, a temporary marsh and pond (Area B), and a marsh and permanent pond (Area C) (Figure 1; Table I).

Figure 1
Location of the Municipality of Barão de Monte Alto, State of Minas Gerais, Brazil. Points: (1) Area A, (2) Area B and (3) Area C.
Table I
Environments monitored during rainy seasons 2013–2014 and 2014–2015 (October to March, respectively) in the Municipality of Barão de Monte Alto, State of Minas Gerais, Brazil.

Fieldwork

Field studies about temporal and spatial distributions of anurans were carried out during three consecutive days, monthly throughout the rainy seasons of 2013–2014 and 2014–2015 (October to March), monitoring one area per night. We performed the fieldwork between 18:00 h and 23:30 h, with a total of 88 observation hours, and a sampling effort of 196h/person. The same person counted and carried out the measurements with the individuals. Monthly climatic data of mean temperature and accumulated rainfall were obtained from the Automatic Weather Station of Muriaé, located approximately 19 km in a straight line from the study area. At the beginning of each collection, we also measured air and water temperature of each environment with a Digital Thermometer Western with Clock for Internal and External Environments (Internal Temperature: -10°C to +50°C, External Temperature: -50°C to +70°C, Accuracy: ±1°C, Clock Accuracy: ±1 minute/month).

We performed active searches for anurans in the field, registering species found, along with data on microhabitat that they used as calling sites. We established seven possible calling site microhabitats: exposed roots, rock, leaf litter, cattail leaf, ground, partially submerged, and grass, for use in the descriptive part and to acquire the spatial measurements of the species. From the data obtained from these seven microhabitats, we defined four other types of microhabitats (height above water and distance from water, microhabitat (separated into fifteen new categories): ground, rock; ground and rock; ground, rock and root; ground and partially submerged; root; leaf litter; ground and grass; partially submerged; leaf litter and grass; leaf litter and cattail; partially submerged and grass; grass; grass and cattail; cattail; and extract (separated into 2 categories): herbaceous or arboreal) to test the hypotheses. For species that were actively calling during the same night and in the same habitat, we estimated the number of calling males and assigned them to the following abundance classes: (1) 1–2; (2) 3–10; (3) 11–50 and (4) more than 50 calling individuals. We recorded the calls with the Sony IC Recorder to help with species identification and deposited the sound files in the Fonoteca Mapinguari da Universidade Federal de Mato Grosso do Sul. An estimated number of calling individuals is widely used for anurans (HeyerHEYER WR, DONNELLY MA, MCDIARMID RW, HAYEK LC & FOSTER MS. 1994. Measuring and monitoring biological diversity. Standard methods for Amphibians. Smithsonian Institution Press, Washington. et al. 1994) and assessed as efficient, provided that estimates are always done by the same observer (ShiroseSHIROSE LJ, BISHOP CA, GREEN DM, MACDONALD CJ, BROOKS RJ & HELFERTY NJ. 1997. Validation tests of an amphibian call count survey technique in Ontario, Canada. Herpetologica 53: 312-320. et al. 1997).

Based on calling activity periods during the months of monitoring, we defined five different reproductive patterns (adapted from CanelasCANELAS MAS & BERTOLUCI J. 2007. Anurans of the Serra do Caraça, Southeastern Brazil: species composition and phenological patterns of calling activity. Iheringia-Sér Zool 97: 21-26. & Bertoluci 2007): (1) species that call in the beginning of the rainy season; (2) species that call in the middle of the rainy season; (3) species that call at the end of the rainy season; (4) species that call throughout the entire rainy season; (5) species that call only in the beginning and end of the rainy season. The vertical and horizontal distribution of species was studied by characterizing the calling sites, and measuring the height and distance (through a tape measure) that animals were located in the microenvironment in relation to the nearest body of water. We also noted age and reproductive data, such as young individuals, ovigerous females, froglets, couples in amplexus, and tadpoles.

All voucher specimens were collected with a license from the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio n° 40744–1 e 40744–2), and were housed in the herpetological collection of the Museu de Zoologia João Moojen, Universidade Federal de Viçosa (MZUFV).

Statistical analysis

We used four characteristics to describe the reproductive sites of species: height and distance from water; microhabitat, and extract. We organized each individual based on reproductive site characteristics using Non-metric Multidimensional Scaling (NMDS) (ManlyMANLY BFG. 1994. A Primer of Multivariate Statistics. Chapman and Hall, London. 1994), combining the two rainy periods (October to March, 2013-14 and 2014-15). Thus, we defined the response variable as the axis of the NMDS in one dimension, which recovered 92% of the variance of the original distances (r2 = 0.929). We used the phylogenetic tree based on PyronPYRON RA & WIENS JJ. 2011. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phylogenet Evol 61: 543-583. & Wiens (2011) and reduced the tree to only one species per genus that was included in our sampling, using the function drop.tip () and created a matrix of phylogenetic distances among each genus. From this distance, we ordered genera based on phylogenetic relatedness reproductive modes following HaddadHADDAD CFB, TOLEDO LF, PRADO CPA, LOEBMANN D, GASPARINI JL & SAZIMA I. 2013. Guia dos anfíbios da Mata Atlântica – diversidade e biologia. Anolis Books, São Paulo, 542 p. et al. (2013) and reproductive period determined during this study. Due to correlations among some of these explanatory variables, we applied a Variation Partitioning method (BorcardBORCARD D, LEGENDRE P & DRAPEAU P. 1992. Partialling out the spatial component of ecological variation. Ecology 73: 1045-1055. et al. 1992) using partial regression, which results in percentages of variation explained only by each explanatory variable and shared by them. The variation partitioning results were represented in a Venn diagram. We also verified the relationship between rainfall and number of species in calling sites using a linear regression with a Poisson distribution.

The significance level used to explain the spatial organization of the composition of species in the habitats was P < 0.05. For this, the data were analyzed using the statistical software R version 3.1.3. (R Core Team 2015), using the “cluster” package (MaechlerMAECHLER M, ROUSSEEUW P, STRUYF A, HUBERT M & HORNIK K. 2015. Cluster: cluster analysis basics and extensions. R package. Available from: https://cran.r-project.org/web/packages/cluster/index.html.
https://cran.r-project.org/web/packages/...
et al. 2015) to create the Gower distance matrix among the species based on the environmental measurements: we used the “ape” package (ParadisPARADIS E, CLAUDE J & STRIMMER K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290. et al. 2004) to create the phylogenetic distance matrices among genera, and finally the “vegan” package (OksanenOKSANEN JF, BLANCHET G, KINDT R, LEGENDRE P, MINCHIN PR, O’HARA RB & WAGNER H. 2015. Vegan: community ecology, R package. Available from: http://CRAN.R-project.org/package=vegan.
http://CRAN.R-project.org/package=vegan....
et al. 2015) to create the NMDS and variation partitioning.

RESULTS

In the three monitored habitats in the study area, we found 28 species of anurans belonging to the families Bufonidae (1), Brachycephalidae (1), Craugastoridae (1), Cycloramphydae (1), Hylidae (15), Microhylidae (1), Leptodactylidae (6), Odontophrynidae (1), and Ranidae (1). Area B showed the greatest richness with 21 species present, of these, 11 are hylids. Areas A and C, however, showed a richness of 20 species each, but in Area A there were 14 hylids and in Area C only 11 (Table II). Table III (a, b and c) shows the results of the spatial-temporal distribution of species found over the six months of sampling of the rainy season (2013–14 and 2014–15).

Table II
List of anurans species and habitats where they occur in the Municipality of Barão de Monte Alto, State of Minas Gerais, Brazil: Area A, Area B and Area C. RM – Reproductive Modes (According to Haddad & Prado 2005). (-) – No species.
Table III
Areas in the Municipality of Barão de Monte Alto, State of Minas Gerais, Brazil. Male classes in vocalization activity: - 1-2; - 3-10; - 11-50 and - over 50. S: Found only individuals that were not vocalizing; Ov: ovate; Ju: juvenile; Fg: froglet. AE (Arboreal Extract): H: herbaceous; Sh: shrubby. MV (Microenvionment Vocalization): Lt: litter; Gn: ground; Gr: grass; C: cattail; Ro: rock; Rt: root, PS: partially submerged. Months of the rainy season (2013–14 and 2014–15).

In the months of February and March, we found the fewest number of species (14) with calling activity, and in December we registered the highest number of calling species (20). Only three species did not fit into the established reproductive patterns due to absence of calling observations (Adenomera marmorata), or because it had incipient vocalization activity (Elachistocleis cesarii and Scinax fuscovarius).

With environmental occupation, we found six species (22%) using just one single type of microhabitat as a calling site, whereas 10 (37%) species used two and/or three microhabitats, and only one species (3.7%) used four microhabitats (Pithecopus rohdei). The grass microhabitat was utilized most (21 species: 77%), whereas rock microhabitat was utilized least (one species: Thoropa miliaris). Of the seven microhabitats defined in this study, Area A was the only one that contained all of the different types of calling sites (Table IIIa).

Of the registered species, five (17.8%) occurred exclusively in Area A: Dendropsophus pseudomeridianus, Elachistocleis cesarii, Adenomera marmorata, Proceratophrys boiei, and Leptodactylus catesbeianus. On the other hand, Area B had only three (10.7%) exclusive species: Ischnocnema sp., Leptodactylus labyrinthicus, and Leptodactylus spixi. Only Ischnocnema sp. occurred exclusively in Area C (Table II).

In both rainy seasons sampled, the reproductive activity of the species, characterized by the presence of calling males, was not associated with the highest rainfall, (Z=0.775, P=0.438) (Figure 2). Considering the overall analysis (sum of the periods 2013–14 and 2014–15) the peaks of abundance of calling males, with more than 50 individuals vocalizing, were recorded at the beginning (October 2013) and end (March 2015) of the rainy season (Tables IIIa, b and c).

Figure 2
Linear regression comparing the richness of anurans in breeding activity with rainfall in the rainy season (October to March) between 2013–14 and 2014–15. Black dots (each point represents one month of study).

Through regressions of all these explanatory variables with species scores, only reproductive modes (0.02%), genus (0.06%), and reproductive period (0.16%) were significant. However, there was no significant interaction among these three variables, but reproductive mode and genus shared 0.08% of the variables (Figure 3). We also removed from the phylogenetic tree of Pyron (Pyron & Wiens 2011) only the families and genera included in the sample design, we defined the scores and based on this tree, we made a patristic distance matrix between each family and gender. From this distance we order families and genera based on phylogenetic proximity. The influence of historical factors was significant, the phylogeny explained part of the variation in the use of micro-habitat by the species, being basically related to the basal separation between Hylidae and other terrestrial families.

Figure 3
Venn diagram representing the percentages of each significant explanatory variable and the correlation between them based on the spatial organization of species composition in habitats in the Municipality of Barão de Monte Alto, State of Minas Gerais, Brazil.

DISCUSSION

We found 28 species of anurans, distributed in 14 genera and 10 families: Bufonidae (1), Brachycephalidae (1), Craugastoridae (1), Cycloramphydae (1), Hylidae (14), Microhylidae (1), Leptodactylidae (6), Odontophrynidae (1), Phyllomedusidae (1) and Ranidae (1) (Table II). The assemblage of anurans studied is predominated by Hylids (sensu Pyron & Wiens 2011), the same pattern was found in various studies in the neotropical region (e.g. GottsbergerGOTTSBERGER B & GRUBER E. 2004. Temporal partitioning of reproductive activity in a Neotropical anuran community. J Trop Ecol 20: 271-280. & Gruber 2004, AbrunhosaABRUNHOSA PA, WOGEL H & POMBAL JUNIOR JP. 2006. Anuran temporal occupancy in a temporary pond from the Atlantic Rain Forest, South-Eastern Brazil. Herpetol J 16: 115-122. et al. 2006, JuncáJUNCÁ FA. 2006. Diversidade e uso de hábitat por anfíbios anuros em duas localidades de Mata Atlântica, no norte do estado da Bahia. Biota Neotrop 6: 1-17. 2006, Canelas & Bertoluci 2007, MoreiraMOREIRA LFB, MACHADO IF, LACE ARGM & MALTCHIK LG. 2007. Calling period and reproductive modes in an anuran community of a temporary pond in Southern Brazil. S Am J Herpetol 2: 129-135. et al. 2007, SantanaSANTANA DJ, SÃO PEDRO VA, HOTE PS, ROBERTI HM, SANTA’ANNA AC, FIGUEIREDO-DE-ANDRADE CA & FEIO RN. 2010. Anurans in the Region of the High Muriaé River, State of Minas Gerais, Brazil. Herpetol. Notes 3: 1-10. et al. 2010, PereiraPEREIRA EA, NEVES MO, HOTE PS, SANTANA DJ & FEIO RN. 2016. Anurans of the Municipality of Barão de Monte Alto, Minas Gerais, Brazil. Check List 12: 1-13. et al. 2016). The sampled localities do not have a strong seasonality of climatic variables (precipitation, temperature) due to the small amplitude of thermal variation during the study months. This may explain why the reproductive season of the species is not concentrated during the two rainy seasons. Some variables were more important than others and among the most important, habitat heterogeneity, reproductive period, reproductive mode, and phylogenetic distance had a greater influence on the species, as was observed in the overlap in the vocalization period of several species in the same environment. Because most of the variables are synchronized, the interactions of these external factors are often more important than a single environmental factor. The analyzed variables are discussed below.

In tropical regions rainfall seems to be the principal factor regulating the reproductive activities of anurans (HeyerHEYER WR. 1973. Ecological interactions of frog larvae at a seasonal tropical location in Thailand. J Herpetol 7: 337-361. 1973), because it determines the availability and duration of reproductive sites (Gottsberger & Gruber 2004). In this study, the linear regression showed there was no relationship between the presence of actively calling species and temperature (Figure 2). The study site showed a small range of thermal variation during the study months (23 to 26.5°C), which may explain why temperature had no apparent effect on the reproductive activity on anurans. However, this is not commonly found in studies of amphibian communities, which generally show correlations between reproductive activity and environmental temperature (e.g. Vasconcelos & Rossa-Feres 2005, ConteCONTE CE & ROSSA-FERES DC. 2006. Diversidade e ocorrência temporal da anurofauna (Amphibia, Anura) em São José dos Pinhais, Paraná, sul do Brasil. Rev Bras Zool 23: 162-175. & Rossa-Feres 2006). Other studies have shown that the reproductive activity of only a few species within an assemblage is influenced by temperature, and also depends on their reproductive mode (Gottsberger & Gruber 2004, Moreira et al. 2007).

Area C can be considered the most heterogeneous, as it is located in a transition from pasture and secondary forest. The positive association between richness of anurans and habitat heterogeneity is compatible with various studies that relate richness of different animal groups with area and habitat heterogeneity (RicklefsRICKLEFS RE & LOVETTE IJ. 1999. The roles of island area per se and habitat diversity in the species -area relationships of four Lesser Antillean faunal groups. J Anim Ecol 68: 1142-1160. & Lovette 1999, VallanVALLAN D. 2000. Influence of forest fragmentation on amphibian diversity in the nature reserve of Ambohitantely, highland Madagascar. Biol Conserv 96: 31-43. 2000, BáldiBÁLDI A. 2008. Habitat heterogeneity overrides the species-area relationship. J Biogeogr 35: 675-681. 2008, SilvaSILVA RA, MARTINS IA & ROSSA-FERES DDC. 2011. Environmental heterogeneity: Anuran diversity in homogeneous environments. Zoologia 28. et al. 2011, SouzaSOUZA FL, MARTINS FI & RAIZER J. 2014. Habitat heterogeneity and anuran community of an agroecosystem in the Pantanal of Brazil. Phyllomedusa: J Herpetol 13: 41-50. et al. 2014, AraújoARAÚJO KC, GUZZI A & ÁVILA RW. 2018. Influence of habitat heterogeneity on anuran diversity in Restinga landscapes of the Parnaíba River delta, Northeastern Brazil. ZooKeys 757: 69. et al. 2018). The most accepted explanation for this association (TewsTEWS J, BROSE U, GRIMM V, TIELBORGER K, WICHMANN MC, SCHWAGER M & JELTSCH F. 2004. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31: 79-92. et al. 2004) is the habitat heterogeneity hypothesis (Simpson 1949). It assumes that more structurally complex environments hold more niches and have various forms of environmental resource exploitation, thus increasing species diversity (CamposCAMPOS FS & VAZ-SILVA W. 2010. Distribuição espacial e temporal da anurofauna em diferentes ambientes no Município de Hidrolândia, GO, Brasil Central. Neotrop Biol Conserv 5: 179-187. & Vaz-Silva 2010).

However, this hypothesis does not conform exactly to the results of this research, because the vertical stratification, one component of environmental heterogeneity, promoted greater hylid richness, thus allowing more species to co-exist given there was greater resource availability (ColliCOLLI GR, BASTOS RP & ARAÚJO AFB. 2002. The character and dynamics of the Cerrado herpetofauna. The Cerrados of 32 Brazil: Ecology and Natural History of a Neotropical Savanna. In: Oliveira PS and Marquis RJ (Eds), Columbia University Press, New York, p. 223-241. et al. 2002, NogueiraNOGUEIRA C, COLLI GR & MARTINS M. 2009. Local richness and distribution of the lizard fauna in natural habitat mosaics of the Brazilian Cerrado. Austral Ecol 34: 83-96. et al. 2009). On one hand, this explains the higher number of hylids (14) in Area A, but does not explain why Area C, which is also located in a forested area, does not have an equally rich hylid fauna. Maybe the higher richness of hylids in Area A could be best explained by the intermediate disturbance hypothesis (ConnellCONNELL JH. 1978. Diversity of tropical rainforests and coral reefs. Science 199: 1304-1310. 1978). Area A is the environment that suffered the greatest and most frequent anthropogenic interference; it was used for logging Eucalyptus plantations and raising cattle. With a moderate level of disturbance, the assemblage comprises a mosaic of habitats, favoring the occurrence of high species diversity (HustonHUSTON MA. 1994. Biological diversity - the coexistence of species on changing landscapes. Cambridge University Press, New York. 1994, PiankaPIANKA ER. 1994. Evol Ecol Harper Collins College Publishers, New York. 1994, RicklefsRICKLEFS RE. 2003. A economia da natureza. 5th Edition. Guanabara Koogan, Rio de Janeiro. 2003). Changes in plant community and soil can also be instrumental in structuring the assemblage of anurans (Bastazini et al. 2007).

Temporal differences in reproductive seasons can be an important factor in the reproductive isolation of species that share the same habitat (Bertoluci & Rodrigues 2002). We observed overlap in calling periods of many species in the same habitat (Tables IIIa, b and c). This overlap is possible because species exploit different microhabitats, which is an important factor for reproductive isolation (Cardoso et al. 1989, Pombal Junior 1997, Toledo et al. 2003), and reduces the occurrence of interspecific territorial disputes. This is the case for Boana albopunctata and B. faber, which call during the same period, but almost always occupy different microhabitats. However, Dendropsophus branneri, D. elegans, and D. minutus co-occur in all of the habitats and have overlapping calling periods. Nevertheless, Dendropsophus elegans was found calling in higher strata and sometimes in large sized trees, whereas D. branneri and D. minutus shared shrubs of aquatic vegetation. In cases of temporal and spatial overlap, reproductive isolation can occur due to acoustic divergence (Pombal Junior 1997, Bernarde & Machado 2001BERNARDE PS & MACHADO RA. 2001. Riqueza de espécies, ambientes de reprodução e temporada de vocalização da anurofauna em Três Barras do Paraná, Brasil (Amphibia: Anura). Cuad Herpetol 14: 93-194., Toledo et al. 2003). Eterovick (2003) pointed out the call behavioral flexibility and interactions with physical and biotic variables as one of the determining factors of reproductive patterns in anurans.

Of the species that were not possible to establish a temporal calling pattern, such as Thoropa miliaris, it is possible that they have an explosive reproductive pattern, and their calling nights may have not coincided with our collection nights in the field (Toledo et al. 2003). This may be the case for Elachistocleis cesarii and Proceratophrys boiei, which also have explosive patterns of reproduction (Bertoluci 1998, Canelas & Bertoluci 2007).

The phylogenetic signal related to the use of microhabitat of species reflects old evolutionary relationships, which are related to the separation between terrestrial and arboreal species during the Cretaceous period, approximately 100 million years ago (Duellman & Trueb 1986, IgawaIGAWA T, KURABAYASHI A, USUKI C, FUJII T & SUMIDA M. 2008. Complete mitochondrial genomes of three Neobatrachian anurans: a case study of divergence time estimation using different data and calibration settings. Gene 407: 116-129. et al. 2008, BáezBÁEZ AM, MOURA GJB & GOMEZ RO. 2009. Anurans from the Lower Cretaceous Crato Formation of Northeastern Brazil: implications for the early divergence of neobatrachians. Cretac Res 30: 829-846. et al. 2009). Within each of these clades, other factors are related to the use of micro-habitat among the species involved, such as selective pressures of the past causing recent niche displacement or evolutionary divergence (ZimmermanZIMMERMAN BL & SIMBERLOFF D. 1996. An historical interpretation of habitat uses by frogs in a Central Amazonian Forest. J Biogeogr 23: 27-46. & Simberloff 1996, Eterovick et al. 2010). Although relatively small, the phylogenetic signal is fundamental in explaining the evaluated niche variation. Because, traits exhibited by species may be influenced to various degrees by their phylogenetic history, as well as contemporary selective pressures. Species in a given clade may show high similarity for traits with strong phylogenetic signal, whereas labile traits may differ even in closely related species that have diversified into different ecological niches (RichardsonRICHARDSON JML. 2001. The relative roles of adaptation and phylogeny in determination of larval traits indiversifying anuran lineages. Am Nat 157: 282-299. 2001).

In most habitats, the abiotic structure of the environment determines the community and influences the distributions and interactions of animal species (BellBELL SS, MCCOY ED & MUSHINSKY HR. 1991. Habitat structure the physical arrangement of objects in space. London: Chapman and Hall. et al. 1991, Tews et al. 2004). When we evaluated which variables best explain the anuran species composition among the areas, we observed that part of the explanation for reproductive mode or for genus was due to the correlation between the two (0.08). On the scale of this study, the reproductive modes are probably phylogenetically conserved. The presence of a phylogenetic signal indicates that phylogeny represents a fraction of the variation in the use of habitat for each species. It represents an important vertical segregation in forming patterns of diversity and local distribution of anurans. However, according to our results the factor that best explained the differences in individual habitats was the reproductive period (0.16) (Figure 3). Because the species may differ in their annual reproductive periods (WellsWELLS KD. 1977. The courtship of frogs. The reproductive biology of amphibians. In: Taylor DH and Guttman SI (Eds), Plenum, New York, 475 p. 1977), daily periods of calling activity, acoustic parameters of their advertisement calls, and time sharing of resources are important mechanisms of reproductive isolation (Wells 1977). A phylogenetically pooled community contains species that are, on average, more related than expected by chance (WebbWEBB CO. 2000. Exploring the phylogenetic structure of ecological communities: An example for rain forest trees. Am Nat 156: 145-155. 2000, Webb et al. 2002). The results of this study demonstrate that the occupation of breeding sites does not occur randomly, but occurs through the selection of preferred habitats for individual species. The habitat level can be related to phylogenetic niche conservation, which is maintained during the process of Atlantic Forest occupation by the group studied.

ACKNOWLEGMENTS

We would like to thank everyone who helped us during the fieldwork. All residents of Barão de Monte Alto. EAP thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for financial support and the Instituto Chico Mendes de Conservação da Biodiversidade – ICMBio for collecting license.

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Publication Dates

  • Publication in this collection
    11 May 2020
  • Date of issue
    2020

History

  • Received
    10 May 2019
  • Accepted
    15 Aug 2019
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