An Acad Bras Cienc (2020) 92(1): e20190458 DOI 10.1590/0001-3765202020190458 Anais da Academia Brasileira de Ciências | Annals of the Brazilian Academy of Sciences Printed ISSN 0001-3765 I Online ISSN 1678-2690 www.scielo.br/aabc | www.fb.com/aabcjournal

BIOLOGICAL SCIENCES

Seasonal and structure of an Running title: SEASONAL AND anuran assemblage in a semideciduous HABITAT STRUCTURE OF AN ANURAN ASSEMBLAGE forest area in Southeast Academy Section: BIOLOGICAL SCIENCES ELVIS A. PEREIRA, MATHEUS O. NEVES, JOSÉ LUIZ M.M. SUGAI, RENATO N. FEIO & DIEGO J. SANTANA e20190458 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, 92 State of Minas Gerais, Brazil. The fi eld activities were carried out during three consecutive (1) days, monthly throughout the rainy seasons of 2013–2014 and 2014–2015. We recorded 92(1) 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 community is defi ned as a group of organisms that coexist in a determined habitat and also Information about anuran habitat use and interact with one another and the surrounding reproductive ecology allows us to interpret environment (Begon et al. 1990). The structure of the relationships between these and adult assemblages has been studied abiotic and biotic factors (Eterovick & Sazima based on habitat and microhabitat (Eterovick & 2004). In several vertebrate groups (e.g. birds, Sazima 2000, Rojas-Ahumada et al. 2012), and anurans, mammals), it has been shown that in terms of reproductive periods (Aichinger the coexistence of populations in the same 1987, Sabbag & Zina 2011). Intuitively, due to area is facilitated by ecological differences morphological variability associated with certain (e.g. , microhabitats, seasonality), due clades of (e.g. arboreal, aquatic), we in part to interspecifi c behavioral interactions, assume that phylogenetic relationships have a involving the social organization and spatial signifi cant effect on the structure of amphibian and temporal distribution of the species in the communities. communities (Cardoso et al. 1989, Cardoso & Amphibians exhibit different strategies for Haddad 1992, Menin et al. 2005, Vogel et al. 2011, occupying their environment. The occupation van Beest et al. 2014, Costa et al. 2016, Cloyed by species differs mainly related to vegetation & Eason 2017, Schirmer et al. 2019). Currently, structure (for species in the forest and open the most functional concept of an ecological areas), as well as the duration of water bodies

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(temporary or permanent) (Díaz-Paniagua 1990, Another intrinsic trait structuring an anuran Rossa-Feres & Jim 2001, Bertoluci & Rodrigues community should consider phylogeny as an 2002). However, several characteristics of the explanatory variable, which may reveal how related habitat such as food availability, hydroperiod, assemblages occupy different environments, and availability of oviposition sites, rainfall, and also understand why certain assemblages are refuges determine the patterns of organization similar or different (Losos 1996). Studies about of anuran assemblages (Lillywhite et al. 1973, the structure of assemblages are still mainly Crump 1974, Toft 1985, Pulliam 1989, Barbault descriptive (Wells 2007) and those that consider 1991, Arzabe 1999, Skelly et al. 1999, Eterovick & the effect of phylogeny are scarce, especially for Sazima 2000, Eterovick & Fernandes 2001, Prado amphibians (Eterovick & Fernandes 2001, Eterovick et al. 2005, Richter-Boix et al. 2006). et al. 2010). The relationship between environmental Most of the studies focusing on Neotropical heterogeneity and species diversity can be anuran assemblages were carried out in the explained by habitat heterogeneity (Simpson Amazon basin (e.g. Crump 1974, Aichinger 1987, 1949, MacArthur & MacArthur 1961, MacArthur Neckel-Oliveira et al. 2000) and in the Atlantic & Wilson 1967). Studies about amphibians have Forest, Southeastern Brazil (e.g. Haddad & demonstrated that complex and heterogeneous Sazima, 1992, Bertoluci 1998, Bertoluci & environments promote more microhabitats and Rodrigues 2002). Their findings show that most ways of exploiting environmental resources, species reproduce during the rainy season, and and thus, allow for a larger group of species a strong association between abundance and to co-occur (Pianka 1969, Duellman & Trueb species richness with rainfall and temperature 1986, Cardoso et al. 1989, Pombal Junior. 1997, (Eterovick & Sazima 2000, Toledo et al. 2003, Brandão & Araújo 1998, Bernarde & Kokubum Santos et al. 2008, Kopp et al. 2010, Hartel et al. 1999, Conte & Machado 2005, Vasconcelos & 2011, Maffei et al. 2011). According to Santos et Rossa-Feres 2005). In anurans communities, al. (2009), the species composition of anurans species coexistence may result in a differential in semideciduous forest areas is more similar use of habitats for vocalization, reproduction to those recorded in areas of Cerrado, Pantanal and larval developmental activities (Duellman & and even Pampa than with the communities of Trueb 1986, Bernarde & Anjos 1999, Bastos 2007, the ombrophilic areas of the Atlantic Forest. It is Purrenhage & Boone 2009). Other influential expected that studies of anuran communities in factores include the presence of bromeliads semideciduous forest will demonstrate several (Schineider & Teixeira 2001, Bastazini et al. levels of reproductive segregation among 2007), soil and moisture (Bernarde & Anjos 1999, species in the same community. The species may Toledo et al. 2003, Bastazini et al. 2007), leaf litter, range from complete spatial and/or temporal fallen logs, and temporary pools (Bernardo & sharing, to total overlapping of these factors Anjos 1999, Toledo et al. 2003, Bastazini et al. (e.g. Bernarde & Kokubum 1999, Rossa-Feres & 2007). Some species show plasticity in the use Jim 2001). of spatial resources (Santos et al. 2008) and The general objective of this study was to variation in the availability of these resources describe the spatial-temporal distributions of can affect the number of species, reproductive anurans in a semideciduous forest area, located modes, and the activity period of anurans in the Municipality of Barão de Monte Alto, (Duellman & Trueb 1986, Kopp et al. 2010). State of Minas Gerais, Brazil. More specifically,

An Acad Bras Cienc (2020) 92(1) e20190458 2 | 17 ELVIS A. PEREIRA et al. SEASONAL AND HABITAT STRUCTURE OF AN ANURAN ASSEMBLAGE we first described the reproductive period WGS84), State of Minas Gerais. The climate of the and activity of the species during two rainy region is classified as Aw (sensu Köppen 1918), seasons, as well as their spatial distribution with a dry season that coincides with winter, considering reproductive site characteristics. and the maximum observed precipitation for We also tested the hypothesis that phylogenetic the driest month of this season is less than 60 distances, reproductive mode, and reproductive mm (Kottek et al. 2006). The local vegetation period explain differences in reproductive site is characterized as Seasonal semi-deciduous characteristics of anurans. Forest of lowlands between 132 and 700 m elevation (Veloso et al. 1991). Mean annual rainfall is about 1.287 mm and the mean annual MATERIALS AND METHODS temperature is 22.6°C. We monitored three Study area habitats: a temporary stream and marsh (Area The study was carried out in the Municipality A) in a forested area, a temporary marsh and of Barão de Monte Alto (21°14’42”S, 42°14’16”W, 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.

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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.

Elevation Environment Coordinates Description (m) 50m permanent marsh in a secondary forest area surrounded by trees and bushes on the banks and permanent 21° 32’ 39” S 2 1 Area A 390 m anthropogenic pond with approximately 1.100m of water 42° 27’ 55” W surface, with secondary forest fragment and pasture on the banks.

21° 27’ 59” S 200m a temporary stream within semideciduous forest with 2 Area B 560 m 42° 23’50” W sandy/rocky bed and riparian forest preserved.

150m2 temporary marsh surrounded by pastures and 4.000m2 21° 32’42” S 3 Area C 360 m permanent pond stretch with secondary forest fragment and 42° 29’ 00” W pasture on the banks.

Fieldwork site microhabitats: exposed roots, rock, leaf Field studies about temporal and spatial litter, cattail leaf, ground, partially submerged, distributions of anurans were carried out during and grass, for use in the descriptive part and three consecutive days, monthly throughout to acquire the spatial measurements of the the rainy seasons of 2013–2014 and 2014–2015 species. From the data obtained from these (October to March), monitoring one area per seven microhabitats, we defined four other night. We performed the fieldwork between types of microhabitats (height above water and 18:00 h and 23:30 h, with a total of 88 observation distance from water, microhabitat (separated hours, and a sampling effort of 196h/person. into fifteen new categories): ground, rock; The same person counted and carried out the ground and rock; ground, rock and root; ground measurements with the individuals. Monthly and partially submerged; root; leaf litter; ground climatic data of mean temperature and and grass; partially submerged; leaf litter and accumulated rainfall were obtained from the grass; leaf litter and cattail; partially submerged Automatic Weather Station of Muriaé, located and grass; grass; grass and cattail; cattail; and approximately 19 km in a straight line from the extract (separated into 2 categories): herbaceous study area. At the beginning of each collection, or arboreal) to test the hypotheses. For species we also measured air and water temperature of that were actively calling during the same night each environment with a Digital Thermometer and in the same habitat, we estimated the Western with Clock for Internal and External number of calling males and assigned them Environments (Internal Temperature: -10°C to to the following abundance classes: (1) 1–2; +50°C, External Temperature: -50°C to +70°C, (2) 3–10; (3) 11–50 and (4) more than 50 calling Accuracy: ±1°C, Clock Accuracy: ±1 minute/ individuals. We recorded the calls with the Sony month). IC Recorder to help with species identification We performed active searches for anurans and deposited the sound files in the Fonoteca in the field, registering species found, along with Mapinguari da Universidade Federal de Mato data on microhabitat that they used as calling Grosso do Sul. An estimated number of calling sites. We established seven possible calling individuals is widely used for anurans (Heyer et al. 1994) and assessed as efficient, provided that

An Acad Bras Cienc (2020) 92(1) e20190458 4 | 17 ELVIS A. PEREIRA et al. SEASONAL AND HABITAT STRUCTURE OF AN ANURAN ASSEMBLAGE estimates are always done by the same observer Wiens (2011) and reduced the tree to only one (Shirose et al. 1997). species per genus that was included in our Based on calling activity periods during sampling, using the function drop.tip () and the months of monitoring, we defined five created a matrix of phylogenetic distances among different reproductive patterns (adapted from each genus. From this distance, we ordered Canelas & Bertoluci 2007): (1) species that call genera based on phylogenetic relatedness in the beginning of the rainy season; (2) species reproductive modes following Haddad et al. that call in the middle of the rainy season; (3) (2013) and reproductive period determined species that call at the end of the rainy season; during this study. Due to correlations among (4) species that call throughout the entire some of these explanatory variables, we applied rainy season; (5) species that call only in the a Variation Partitioning method (Borcard et al. beginning and end of the rainy season. The 1992) using partial regression, which results vertical and horizontal distribution of species in percentages of variation explained only was studied by characterizing the calling sites, by each explanatory variable and shared by and measuring the height and distance (through them. The variation partitioning results were a tape measure) that animals were located represented in a Venn diagram. We also verified in the microenvironment in relation to the the relationship between rainfall and number of nearest body of water. We also noted age and species in calling sites using a linear regression reproductive data, such as young individuals, with a Poisson distribution. ovigerous females, froglets, couples in amplexus, The significance level used to explain the and tadpoles. spatial organization of the composition of All voucher specimens were collected with species in the habitats was P < 0.05. For this, the a license from the Instituto Chico Mendes de data were analyzed using the statistical software Conservação da Biodiversidade (ICMBio n° R version 3.1.3. (R Core Team 2015), using the 40744–1 e 40744–2), and were housed in the “cluster” package (Maechler et al. 2015) to create herpetological collection of the Museu de the Gower distance matrix among the species Zoologia João Moojen, Universidade Federal de based on the environmental measurements: Viçosa (MZUFV). we used the “ape” package (Paradis et al. 2004) to create the phylogenetic distance matrices Statistical analysis among genera, and finally the “vegan” package We used four characteristics to describe (Oksanen et al. 2015) to create the NMDS and the reproductive sites of species: height variation partitioning. and distance from water; microhabitat, and extract. We organized each individual based on reproductive site characteristics using Non- RESULTS metric Multidimensional Scaling (NMDS) (Manly In the three monitored habitats in the study 1994), combining the two rainy periods (October area, we found 28 species of anurans belonging to March, 2013-14 and 2014-15). Thus, we defined to the families Bufonidae (1), Brachycephalidae the response variable as the axis of the NMDS (1), Craugastoridae (1), Cycloramphydae (1), in one dimension, which recovered 92% of the (15), Microhylidae (1), 2 variance of the original distances (r = 0.929). We (6), Odontophrynidae (1), and Ranidae (1). Area used the phylogenetic tree based on Pyron &

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B showed the greatest richness with 21 species labyrinthicus, and spixi. Only present, of these, 11 are hylids. Areas A and C, Ischnocnema sp. occurred exclusively in Area C however, showed a richness of 20 species each, (Table II). but in Area A there were 14 hylids and in Area C In both rainy seasons sampled, the only 11 (Table II). Table III (a, b and c) shows the reproductive activity of the species, characterized results of the spatial-temporal distribution of by the presence of calling males, was not species found over the six months of sampling associated with the highest rainfall, (Z=0.775, of the rainy season (2013–14 and 2014–15). P=0.438) (Figure 2). Considering the overall In the months of February and March, we analysis (sum of the periods 2013–14 and 2014– found the fewest number of species (14) with 15) the peaks of abundance of calling males, calling activity, and in December we registered with more than 50 individuals vocalizing, were the highest number of calling species (20). Only recorded at the beginning (October 2013) and three species did not fit into the established end (March 2015) of the rainy season (Tables IIIa, reproductive patterns due to absence of calling b and c). observations (Adenomera marmorata), or Through regressions of all these explanatory because it had incipient vocalization activity variables with species scores, only reproductive (Elachistocleis cesarii and fuscovarius). modes (0.02%), genus (0.06%), and reproductive With environmental occupation, we found period (0.16%) were significant. However, there six species (22%) using just one single type of was no significant interaction among these microhabitat as a calling site, whereas 10 (37%) three variables, but reproductive mode and species used two and/or three microhabitats, genus shared 0.08% of the variables (Figure 3). and only one species (3.7%) used four We also removed from the phylogenetic tree microhabitats (Pithecopus rohdei). The grass of Pyron (Pyron & Wiens 2011) only the families microhabitat was utilized most (21 species: 77%), and genera included in the sample design, we whereas rock microhabitat was utilized least defined the scores and based on this tree, we (one species: miliaris). Of the seven made a patristic distance matrix between each microhabitats defined in this study, Area A was family and gender. From this distance we order the only one that contained all of the different families and genera based on phylogenetic types of calling sites (Table IIIa). proximity. The influence of historical factors Of the registered species, five (17.8%) was significant, the phylogeny explained part occurred exclusively in Area A: of the variation in the use of micro-habitat by pseudomeridianus, Elachistocleis cesarii, the species, being basically related to the basal Adenomera marmorata, Proceratophrys boiei, separation between Hylidae and other terrestrial and Leptodactylus catesbeianus. On the other families. hand, Area B had only three (10.7%) exclusive species: Ischnocnema sp., Leptodactylus

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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.

Environments Taxa RM Area A Area B Area C Bufonidae Rhinella ornata (Spix 1824) X X X 1 Brachycephalidae Ischnocnema sp. - - X 23 Craugastoridae Haddadus binotatus (Spix 1824) X X X 23 Thoropa miliaris (Spix 1824) X X X 19 Hylidae Dendropsophus bipunctatus (Spix 1824) X - - 1 Dendropsophus branneri (Cochran 1948) X X X 1 Dendropsophus decipiens (Lutz 1925) X - X 24 Dendropsophus elegans (Wied-Neuwied 1824) X X X 1 Dendropsophus minutus (Peters 1872) X X X 1 Dendropsophus pseudomeridianus (Cruz, Caramaschi & Dias 2000) - X - 1 albomarginata (Spix 1824) X - X 1 Boana albopunctata (Spix 1824) X X X 1 Boana faber (Wied-Neuwied 1821) X X X 4 Boana pardalis (Spix 1824) X X X 4 Boana polytaenia (Cope 1870 “1869”) X X X 1 Boana semilineata (Spix 1824) X X X 1 Scinax crospedospilus (Lutz 1925) X - X 1 Scinax fuscovarius (Lutz 1925) X X - 1 Microhylidae Elachistocleis cesarii (Schneider 1799) - X - 1 Leptodactylidae Adenomera marmorata Steindachner 1867 - X - 32 Leptodactylus fuscus (Schneider 1799) X - X 30 Leptodactylus labyrinthicus (Spix 1824) - - X 11 Leptodactylus latrans (Steffen 1815) X X X 11 Leptodactylus spixi Heyer 1983 - X X 30 Physalaemus cuvieri Fitzinger 1826 X X X 11 Odontophrynidae Proceratophrys boiei (Wied-Neuwied 1825) - X - 2

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Table II. Continuation

Environments Taxa RM Area A Area B Area C Phyllomedusidae Pithecopus rohdei (Mertens 1926) X X - 24 Ranidae Lithobates catesbeianus (Shaw 1802) - X - - Total 20 21 20

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).

(a) Species Oct Nov Dec Jan Feb Mar AE MV D. bipunctatus Sh, H C, Gr D. branneri Ju H Gr, C D. decipiens S H Gr, C D. elegans Ju S, Ju H C, Gr D. minutus H Gr, C B. albomarginata Sh, H Gr, C B. albopunctata S H Gr, C H. binotatus H Gn B. faber Ju H Gr, PS B. pardalis H C, Gr B. polytaenia H Gr, C B. semilineata S, Ju Ju Fg, Ju H C, Gr L. fuscus H Gn L. latrans S, Ju S, Ju S S, Ju S S, Ju H Gn, Gr P. curvieri H PS P. rohdei Ju H Gn, Gr (a) Species Oct Nov Dec Jan Feb Mar AE MV R. ornata H Gn S. crospedospilus Sh, H Gr S. fuscovarius H Gr T. miliaris S H Gn N° species vocalizing 11 12 10 10 07 10 N° species registered 13 13 11 11 09 11

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Table III. Continuation

(b) Species Oct Nov Dec Jan Feb Mar AE MV A. marmorata S H Lt D. branneri H C, Gr D. elegans H C, Gr D. minutus H C, Gr D. pseudomeridianus H Gr E. cesarii H Gn B. albopunctata Ju H C, Gr H. binotatus S H Gn B. faber S Sh, H PS, Gr B. pardalis Ju H C, Gn, Gr B. polytaenia S, Ju H C, Gr B. semilineata Fg S, Fg Fg Fg H C, Gn, Gr L. latrans S S Ju S H Gn, Gr, PS P. boiei S S S, Ju, Fg S H Rt, Gn, Lt P. cuvieri J, Fg H PS P. rohdei S H Lt, C, Gn, Gr R. ornata S S H Gn, Gr S. fuscovarius S S S Sh, H C, Gn, Gr T. miliaris S S S S H Rt, Ro, Gn N° species vocalizing 10 11 12 10 10 10 N° species registered 12 12 15 12 13 10

(c) Species Oct Nov Dec Jan Feb Mar AE MV D. branneri Ju H C, Gr D. decipiens Ov H Gr D. elegans Ov Ju, Ov Ju, Ov Fg Ju, O Fg H C, Gr D. minutus Ov Ju, Ov, Fg H C, Gr (c) Species Oct Nov Dec Jan Feb Mar AE MV B. albomarginata Sh, H Gr, C B. albopunctata H Gr, C H. binotatus S S S H Gn B. faber H PS, Gr, Gn B. pardalis Fg H Gr B. polytaenia H C B. semilineata Ju, Fg Fg Ju, Fg H Gr

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Table III. Continuation

Ischnocnema sp. Sh Gr L. fuscus Ju S H Gn, Gr L. labyrinthicus H PS, Gn, Gr L. latrans S Ju S S S H Gn, Gr, PS L. spixi H Gn P. cuvieri S S H Gn, PS, Gr R. ornata H Gn S. crospedospilus S S S Sh, H Gn, Gr, C T. miliaris S H Gn N° species vocalizing 11 12 13 13 10 08 N° species registered 13 12 14 13 13 10

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).

Figure 3. Venn diagram representing the percentages of each signifi cant 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.

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DISCUSSION thermal variation during the study months (23 to 26.5°C), which may explain why temperature had We found 28 species of anurans, distributed no apparent effect on the reproductive activity in 14 genera and 10 families: Bufonidae (1), on anurans. However, this is not commonly Brachycephalidae (1), Craugastoridae (1), found in studies of amphibian communities, Cycloramphydae (1), Hylidae (14), Microhylidae which generally show correlations between (1), Leptodactylidae (6), Odontophrynidae reproductive activity and environmental (1), Phyllomedusidae (1) and Ranidae (1) temperature (e.g. Vasconcelos & Rossa-Feres (Table II). The assemblage of anurans studied 2005, Conte & Rossa-Feres 2006). Other studies is predominated by Hylids (sensu Pyron & have shown that the reproductive activity of Wiens 2011), the same pattern was found in only a few species within an assemblage is various studies in the neotropical region (e.g. influenced by temperature, and also depends on Gottsberger & Gruber 2004, Abrunhosa et al. their reproductive mode (Gottsberger & Gruber 2006, Juncá 2006, Canelas & Bertoluci 2007, 2004, Moreira et al. 2007). Moreira et al. 2007, Santana et al. 2010, Pereira Area C can be considered the most et al. 2016). The sampled localities do not heterogeneous, as it is located in a transition have a strong seasonality of climatic variables from pasture and secondary forest. The positive (precipitation, temperature) due to the small association between richness of anurans and amplitude of thermal variation during the study habitat heterogeneity is compatible with various months. This may explain why the reproductive studies that relate richness of different season of the species is not concentrated groups with area and habitat heterogeneity during the two rainy seasons. Some variables (Ricklefs & Lovette 1999, Vallan 2000, Báldi were more important than others and among 2008, Silva et al. 2011, Souza et al. 2014, Araújo the most important, habitat heterogeneity, et al. 2018). The most accepted explanation reproductive period, reproductive mode, and for this association (Tews et al. 2004) is the phylogenetic distance had a greater influence habitat heterogeneity hypothesis (Simpson on the species, as was observed in the overlap 1949). It assumes that more structurally in the vocalization period of several species in complex environments hold more niches and the same environment. Because most of the have various forms of environmental resource variables are synchronized, the interactions of exploitation, thus increasing species diversity these external factors are often more important (Campos & Vaz-Silva 2010). than a single environmental factor. The analyzed However, this hypothesis does not conform variables are discussed below. exactly to the results of this research, because In tropical regions rainfall seems to be the the vertical stratification, one component of principal factor regulating the reproductive environmental heterogeneity, promoted greater activities of anurans (Heyer 1973), because hylid richness, thus allowing more species it determines the availability and duration of to co-exist given there was greater resource reproductive sites (Gottsberger & Gruber 2004). availability (Colli et al. 2002, Nogueira et al. In this study, the linear regression showed there 2009). On one hand, this explains the higher was no relationship between the presence of number of hylids (14) in Area A, but does not actively calling species and temperature (Figure explain why Area C, which is also located in a 2). The study site showed a small range of forested area, does not have an equally rich

An Acad Bras Cienc (2020) 92(1) e20190458 11 | 17 ELVIS A. PEREIRA et al. SEASONAL AND HABITAT STRUCTURE OF AN ANURAN ASSEMBLAGE hylid fauna. Maybe the higher richness of Of the species that were not possible to hylids in Area A could be best explained by the establish a temporal calling pattern, such as intermediate disturbance hypothesis (Connell Thoropa miliaris, it is possible that they have 1978). Area A is the environment that suffered an explosive reproductive pattern, and their the greatest and most frequent anthropogenic calling nights may have not coincided with our interference; it was used for logging Eucalyptus collection nights in the field (Toledo et al. 2003). plantations and raising cattle. With a moderate This may be the case for Elachistocleis cesarii level of disturbance, the assemblage comprises and Proceratophrys boiei, which also have a mosaic of habitats, favoring the occurrence of explosive patterns of reproduction (Bertoluci high species diversity (Huston 1994, Pianka 1994, 1998, Canelas & Bertoluci 2007). Ricklefs 2003). Changes in plant community and The phylogenetic signal related to the soil can also be instrumental in structuring the use of microhabitat of species reflects old assemblage of anurans (Bastazini et al. 2007). evolutionary relationships, which are related Temporal differences in reproductive to the separation between terrestrial and seasons can be an important factor in the arboreal species during the Cretaceous period, reproductive isolation of species that share the approximately 100 million years ago (Duellman same habitat (Bertoluci & Rodrigues 2002). We & Trueb 1986, Igawa et al. 2008, Báez et al. 2009). observed overlap in calling periods of many Within each of these clades, other factors are species in the same habitat (Tables IIIa, b and c). related to the use of micro-habitat among the This overlap is possible because species exploit species involved, such as selective pressures different microhabitats, which is an important of the past causing recent niche displacement factor for reproductive isolation (Cardoso et al. or evolutionary divergence (Zimmerman & 1989, Pombal Junior 1997, Toledo et al. 2003), Simberloff 1996, Eterovick et al. 2010). Although and reduces the occurrence of interspecific relatively small, the phylogenetic signal is territorial disputes. This is the case for Boana fundamental in explaining the evaluated niche albopunctata and B. faber, which call during the variation. Because, traits exhibited by species same period, but almost always occupy different may be influenced to various degrees by their microhabitats. However, Dendropsophus phylogenetic history, as well as contemporary branneri, D. elegans, and D. minutus co-occur selective pressures. Species in a given clade in all of the habitats and have overlapping may show high similarity for traits with strong calling periods. Nevertheless, Dendropsophus phylogenetic signal, whereas labile traits may elegans was found calling in higher strata differ even in closely related species that have and sometimes in large sized trees, whereas diversified into different ecological niches D. branneri and D. minutus shared shrubs of (Richardson 2001). aquatic vegetation. In cases of temporal and In most habitats, the abiotic structure of the spatial overlap, reproductive isolation can occur environment determines the community and due to acoustic divergence (Pombal Junior 1997, influences the distributions and interactions of Bernarde & Machado 2001, Toledo et al. 2003). animal species (Bell et al. 1991, Tews et al. 2004). Eterovick (2003) pointed out the call behavioral When we evaluated which variables best explain flexibility and interactions with physical and the anuran species composition among the biotic variables as one of the determining areas, we observed that part of the explanation factors of reproductive patterns in anurans. for reproductive mode or for genus was due

An Acad Bras Cienc (2020) 92(1) e20190458 12 | 17 ELVIS A. PEREIRA et al. SEASONAL AND HABITAT STRUCTURE OF AN ANURAN ASSEMBLAGE to the correlation between the two (0.08). On AICHINGER M. 1987. Annual activity patterns of anurans the scale of this study, the reproductive modes in a seasonal Neotropical environment. Oecologia 71: 583-592. are probably phylogenetically conserved. The ARAÚJO KC, GUZZI A & ÁVILA RW. 2018. Influence of habitat presence of a phylogenetic signal indicates that heterogeneity on anuran diversity in Restinga landscapes phylogeny represents a fraction of the variation in of the Parnaíba River delta, Northeastern Brazil. ZooKeys the use of habitat for each species. It represents 757: 69. an important vertical segregation in forming ARZABE C. 1999. Reproductive activity patterns of anurans patterns of diversity and local distribution of in two different altitudinal sites within the Brazilian anurans. However, according to our results the Caatinga. Rev Bras Zool 16: 851-864. factor that best explained the differences in BÁEZ AM, MOURA GJB & GOMEZ RO. 2009. Anurans from the individual habitats was the reproductive period Lower Cretaceous Crato Formation of Northeastern Brazil: implications for the early divergence of neobatrachians. (0.16) (Figure 3). Because the species may differ Cretac Res 30: 829-846. in their annual reproductive periods (Wells BÁLDI A. 2008. Habitat heterogeneity overrides the 1977), daily periods of calling activity, acoustic species-area relationship. J Biogeogr 35: 675-681. parameters of their advertisement calls, and time BARBAULT R. 1991. Ecological constraints and community sharing of resources are important mechanisms dynamics linking community patterns to organismal of reproductive isolation (Wells 1977). A ecology. The case of herpetofaunas. Acta Oecol 12: phylogenetically pooled community contains 139-163. species that are, on average, more related than BASTAZINI CM, MUNDURUCA JFV, ROCHA PLB & NAPOLI MF. 2007. expected by chance (Webb 2000, Webb et al. Which environmental variables better explain changes in anuran community composition? A case study in the 2002). The results of this study demonstrate that restinga of Mata de São João, Bahia, Brazil. Herpetologica the occupation of breeding sites does not occur 63: 459-471. randomly, but occurs through the selection of BASTOS RP. 2007. Anfíbios do Cerrado. In Herpetologia preferred habitats for individual species. The no Brasil II. In: Nascimento LB and Oliveira ME (Eds), habitat level can be related to phylogenetic Sociedade Brasileira de Herpetologia. Belo Horizonte, p. 87- 100. niche conservation, which is maintained during the process of Atlantic Forest occupation by the BEGON M, HARPER JL & TOWNSEND CR. 1990. Ecology. Individuals, populations and communities. Blackwell group studied. scientific publications. Blackwell Scientific Publications, Oxford, p. 611-615. Acknowledgments BELL SS, MCCOY ED & MUSHINSKY HR. 1991. Habitat structure We would like to thank everyone who helped us the physical arrangement of objects in space. London: during the fieldwork. All residents of Barão de Monte Chapman and Hall. Alto. EAP thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for financial support BERNARDE PS & ANJOS L. 1999. Distribuição espacial e and the Instituto Chico Mendes de Conservação da temporal da anurofauna do Parque Estadual Mata dos Godoy, Londrina, Paraná, Brasil (Amphibia, Anura). Biodiversidade – ICMBio for collecting license. Comunicações do Museu Ciências e Tecnologia da PUCRS. Série Zoologia 2: 127-140.7. REFERENCES BERNARDE PS & KOKUBUM MNC. 1999. Anurofauna do Município de Guararapes, Estado de São Paulo, Brasil ABRUNHOSA PA, WOGEL H & POMBAL JUNIOR JP. 2006. Anuran (Amphibia: Anura). Acta Biol Leopoldinense 21: 89-97. temporal occupancy in a temporary pond from the BERNARDE PS & MACHADO RA. 2001. Riqueza de espécies, Atlantic Rain Forest, South-Eastern Brazil. Herpetol J 16: ambientes de reprodução e temporada de vocalização 115-122.

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ZIMMERMAN BL & SIMBERLOFF D. 1996. An historical Correspondence to: Elvis Almeida Pereira interpretation of habitat uses by frogs in a Central E-mail: [email protected] Amazonian Forest. J Biogeogr 23: 27-46. Authors Contributions Elvis Almeida Pereira conceived and designed the experiments, How to cite performed the experiments, analyzed the data, prepared PEREIRA EA, NEVES MO, SUGAI JLMM, FEIO RN & SANTANA DJ. 2020. figures and/or tables, authored or reviewed drafts of the Seasonal and habitat structure of an anuran assemblage. An Acad Bras paper, approved the final draft. Matheus de Oliveira Neves Cienc 92: e20190458. DOI 10.1590/0001-3765202020190458. performed the experiments, authored or reviewed drafts of the paper, approved the final draft. José Luíz Massao Moreira Sugai analyzed the data and approved the final draft. Diego José Manuscript received on May 10, 2019; Santana conceived and designed the experiments, performed accepted for publication on August 15, 2019 the experiments, analyzed the data, contributed analysis tools, authored or reviewed drafts of the paper, approved the final ELVIS A. PEREIRA1,2,3 draft. Renato Neves Feio authored or reviewed drafts of the https://orcid.org/0000-0002-8810-7878 paper, approved the final draft. MATHEUS O. NEVES2,4 https://orcid.org/0000-0002-6848-2099

JOSÉ LUIZ M.M. SUGAI5 https://orcid.org/0000-0003-1480-4053

RENATO N. FEIO6 https://orcid.org/0000-0002-3607-2896

DIEGO J. SANTANA2,5 http://orcid.org/0000-0002-8789-3061

An Acad Bras Cienc (2020) 92(1) e20190458 17 | 17