Biota Neotropica 21(1): e20201082, 2021

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ISSN 1676-0611 (online edition)

Article
Anuran fauna of the Parque Estadual Carlos Botelho - Núcleo Sete Barras,
southeastern Brazil: species composition, use of breeding sites, and seasonal patterns
of breeding activity

Jaime Bertoluci1* , Henrique Oliveira Sawakuchi2, Carolina Ortiz1, Ricardo Augusto Brassaloti1,

José Wagner Ribeiro-Júnior3 & Shirley Famelli1

1
Universidade de São Paulo, Escola Superior de Agricultura Luiz de Queiroz, Departamento de Ciências
Biológicas, Av. Pádua Dias 11, 13418-900, Piracicaba, SP, Brasil.
2
Linköping University, Department of Thematic Studies, Environmental Change, Linköping, SE-581 83, Sweden.
3
Universidade Estadual Paulista, Instituto de Biociências, Av. 24A 1515, Rio Claro, SP, Brasil.
*Corresponding author: Jaime Bertoluci, e-mail: jaime.bertoluci@usp.br

BERTOLUCI, J., SAWAKUCHI H.O., ORTIZ, C., BRASSALOTI, R.A., RIBEIRO-JÚNIOR, J.W., FAMELLI, S.
Anuran fauna of the Parque Estadual Carlos Botelho - Núcleo Sete Barras, southeastern Brazil: species
composition, use of breeding sites, and seasonalpatterns of breeding activity. Biota Neotropica 21(1):
e20201082. https://doi.org/10.1590/1676-0611-BN-2020-1082

Abstract: The goal of this work was to study the species composition, the use of breeding sites, and the seasonal
patterns of breeding activity of the anuran fauna from Parque Estadual Carlos Botelho - Núcleo Sete Barras, state of
São Paulo, southeastern Brazil. Fieldwork was carried out from September 2005 to October 2007 through two main
methods: active visual search inside a 10 ha- permanent plot and aural and visual search in seven previously selected
aquatic breeding habitats. Species richness was related to the sampling effort by means of species accumulation curve
and through non-parametric estimators. Thirty-three species distributed in 12 families were recorded, from which 69%
are endemic to the Atlantic Forest. Trachycephalus mesophaeus represents a new record for the park. Cycloramphus
lutzorum is included as Data Deficient in the IUCN list. The species accumulation curve did not stabilize, showing
some tendency to rise. The use of breeding sites by 20 species was compared using cluster analysis, which revealed two
major groups: the first with five species (two habitat generalists and three stream specialists) and the second composed
by the other species (with different reproductive modes associated with flooded environments). The breeding period
of most species was associated to the rainy season (October to February), and only Scinax hayii showed continuous
breeding activity during the entire period of study.
Keywords: anuran amphibians; Atlantic Rainforest; diversity; breeding sites; spatial distribution; seasonal breeding
patterns.

Anurofauna do Parque Estadual Carlos Botelho – Núcleo Sete Barras, sudeste do

Brasil: composição de espécies, uso de sítios reprodutivos e padrões sazonais de
atividade reprodutiva
Resumo: O objetivo deste trabalho foi estudar a composição de espécies, o uso de habitats reprodutivos e os padrões
sazonais de atividade reprodutiva da anurofauna do Parque Estadual Carlos Botelho - Núcleo Sete Barras, estado
de São Paulo, sudeste do Brasil. O trabalho de campo foi desenvolvido de setembro de 2005 a outubro de 2007 por
meio de dois métodos principais: procura visual ativa no interior de uma parcela permanente de 10 ha e busca visual e
acústica em sete habitats aquáticos de reprodução previamente selecionados. A riqueza de espécies foi relacionada com
o esforço amostral por meio de curvas de acumulação de espécies e estimadores não-paramétricos. Foram registradas
33 espécies distribuídas em 12 famílias, 69% das quais são endêmicas da Mata Atlântica. Trachycephalus mesophaeus
representa um novo registro para o parque. Cycloramphus lutzorum está incluída como Deficiente em Dados na lista
da IUCN. A curva de acumulação de espécie não se estabilizou, mostrando alguma tendência de crescimento. A
similaridade no uso dos ambientes aquáticos por 20 espécies foi avaliada por meio de uma análise de agrupamento,
que revelou dois grupos: o primeiro com cinco espécies (duas generalistas de habitat e três especialistas de riachos)
e o segundo formado pelas demais espécies (com diferentes modos reprodutivos associados a ambientes aquáticos
lênticos). O período reprodutivo da maioria das espécies esteve associado à estação chuvosa (outubro a março), e
apenas Scinax hayii mostrou atividade reprodutiva contínua durante todo o período de estudo.
Palavras-chave: anfíbios anuros; Floresta Atlântica; diversidade; sítios reprodutivos; distribuição espacial;
padrões reprodutivos sazonais.

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Bertoluci J. et al.

Introduction
rainy season (Aichinger 1987, Bertoluci 1998, Bertoluci & Rodrigues
The Atlantic Rainforest is home to 528 species of anurans, of which 2002b, Canelas & Bertoluci 2007, Narvaes et al. 2009).
about 80% are endemic (Vancine et al. 2018). This astonishing diversity The present study aimed to investigate the composition of the anuran
is commonly attributed to the highly rugged terrain and the existence of fauna of the Núcleo Sete Barras of the Parque Estadual Carlos Botelho,
geographical barriers that isolate populations and create high levels of São Paulo state, southeastern Brazil, the use of breeding sites by the
speciation and endemism; the stratified physiognomy of the vegetation, species and their seasonal patterns of breeding activity.
with a great diversity of epiphytes, together with high levels of rainfall
and humidity, result in intense partitioning of habitats and microhabitats Materials and Methods
by anurans and the evolution of specialized reproductive modes (see
Haddad & Prado 2005 and references herein). 1. Study site
In the last decades many studies were developed on anuran
amphibian communities from different physiognomies of the Atlantic The Parque Estadual Carlos Botelho (PECB) (24º00’ - 24º15’ S,
Rainforest biome (e.g, Heyer et al. 1990, Canelas & Bertoluci 2007, 47º45’ - 48º10’ W) is part of an ecological complex of the Atlantic
Araújo et al. 2010, Brassaloti et al. 2010, Forlani et al. 2010, Vilela et Rainforest in the southern part of the State of São Paulo, encompassing
al. 2011, Figueiredo et al. 2019). Population declines and even local an area of approximately 38.000 ha, with altitudes that very between
extinctions were detected in some localities, such as Santa Tereza, in 30 to 1600 m above sea level, covered by Dense Ombrophylous
Espírito Santo state (Weygoldt 1989), and Serra do Japi (Haddad & Forest (Ferraz & Varjabedian 1999) (Figure 1). According to Veloso
Sazima 1992), Estação Biológica de Boracéia (Heyer et al. 1988, 1990, et al. (1991), the vegetation at PECB may perform three different
Bertoluci & Heyer 1995, Verdade et al. 2011) and Estação Biológica physiognomic and floristic compositions: montane rainforest, sub-
do Alto da Serra de Paranapiacaba (Verdade et al. 2009), in São Paulo montane and low lands. The Núcleo Sete Barras (NSB) comprises two
state, which show the importance of ecological studies, even in well- forest formations (sub-montane and low lands) and is located in the
studied regions, such as southeastern Brazil (Haddad & Prado 2005, municipality of Sete Barras, Vale do Ribeira de Iguape, in a contact
Brito 2008, Verdade et al. 2012). zone between two geomorphological formations, Guapiara Plateau
The anuran fauna of the state of São Paulo is well known (about (low lands) and Serra de Paranapiacaba (sub-montane) (24º11’37’’ S,
230 species) and represents 27% of the Brazilian diversity and 4% of 47º55’11’’ W) (Ferraz & Varjabedian 1999).
world diversity (Rossa-Feres et al. 2011). Most species are found in The climate is Cfa of Köppen, mesothermal, subtropical, hot and
Atlantic Rainforest areas, including the Estação Biológica de Boracéia humid, with no dry season (Setzer 1946). In the study period, the mean
(66 espécies; Heyer et al. 1990; Verdade et al. 2011), the Parque Estadual annual temperature was 21.8˚ and the annual accumulated precipitation
Intervales (Bertoluci & Rodrigues 2002b; 48 species), the Estação was 1,582 mm (Bertoluci et al. 2007).
Biológica do Alto da Serra de Paranapiacaba (Verdade et al. 2009; 69
2. Data sampling and collection
species), the Parque Estadual Turístico do Alto Ribeira - PETAR (Araújo
et al. 2010; 60 species), and the Parque Natural Municipal Nascentes The anuran fauna sampling was carried out using two main methods:
de Paranapiacaba (Trevine et al. 2014; 80 species). active visual (Crump & Scott 1994) in a 2500 m transect inside a
The greatest diversity in São Paulo state was recorded in the permanent plot of 10 ha (more detail in Bertoluci et al. 2007a); and
Parque Estadual Carlos Botelho, with about 85 anuran species, which male vocal activity monitoring in seven different previously selected
is perhaps due to the abundance of water bodies and the excellent state breeding habitats (Table 1). In the plot area, we carried out two visits
of conservation of this conservation area (e.g., Guix et al. 1994, 2000, a month between September 2005 and October 2006, always two
Bertoluci et al. 2007, Forlani et al. 2010). researchers (20h/person), totalizing a sampling effort of 240h/person.
Spatial distribution and reproductive success of amphibians are The breeding habitats were visited for two consecutive nights per month
strongly dependent on the physical characteristics of reproductive between September 2005 and October 2007, totaling 52 visits in the
environments, varying in space and time. Environments with similar period. In addition, we recorded all individuals found by chance in the
abiotic factors harbor different species compositions, which indicates sampling areas. All selected reproductive habitats were located along
that there is more than one factor influencing the choice of reproductive the main track called “Trilha das Figueiras”, which is located along the
sites, such as habitat heterogeneity and degree of preservation of main road that connects the municipalities of São Miguel Arcanjo and
terrestrial habitats around aquatic breeding sites (Wells 1977, Gascon Sete Barras (Figure 1).
1991, Rudolf & Rödel 2005), which affect assemblage diversity, local Seasonal patterns of breeding activity were established by
abundance of some species and interspecific interactions (Underwood estimating the number of males (per species) calling synchronously
2000). at each aquatic site (Table 1) in the following classes of abundance:
Rainfall distribution and air temperature variation along the year (1) 1-2, (2) 3-5, (3) 6-10, (4) 11-20, (5) 21-50, (6) more than 50 males
strongly influence anuran breeding activity (Wells 2007). A higher (Bertoluci 1998, Bertoluci & Rodrigues 2002b, Canelas & Bertoluci
number of species is able to reproduce throughout the year in aseasonal 2007, Narvaes et al. 2009). The activity of species whose males did not
(Hero 1990, Gascon 1991) than in seasonal environments, where the vocalize in the selected sites was recorded in a qualitative way, and we
calling and breeding activity of most species are associated with the considered the presence in the sites of gravid females, amplectant pairs,
and egg clutches as evidences of actual reproduction, as already done

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Biota Neotrop., 21(1): e20201082, 2021 3

Anuran assemblage of an Atlantic forest site

Figure 1. Geographical location of the study area showing the location of the sampled breeding sites (●).

Table 1. Physical characteristics of the seven water bodies studied in the Núcleo Sete Barras, Parque Estadual Carlos Botelho, southeastern
Brazil. Legend: VAR – arboreal vegetation; VAT – understory bush vegetation; VHR – herbaceous vegetation (Poaceae); VHA – aquatic
herbaceous vegetation. *Transect 100 m.

Sites Geographic coordinates Altitude (m) Hydroperiod Type Substrate Vegetation type

L1 24º11’36” S, 47º55’43” W 241 Semipermanent Pond Argiloso VAR, VAT

L2 24º12’13” S, 47º55’56” W 52 Semipermanent Pond Muddy VAR, VAT, VHA
L3 24º12’08” S, 47º56’30” W 44 Permanent Pond Muddy VAR, VAT, VHA
L4 24º12’21” S, 47º57’16” W 48 Permanent Pond Muddy VAR, VAT, VHA
L5 24º11’37” S, 47º55’11” W 65 Permanent Reservoir Argiloso VAT, VHR
R1 24º11’35” S, 47º55’11” W 53 Permanent Stream* Rocky VAR, VAT
R2 24º11’39” S, 47º55’55” W 48 Temporary Stream* Muddy VAR, VAT, VHA

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Bertoluci J. et al.

2. Use of breeding sites

by Bertoluci (1998), Bertoluci and Rodrigues (2002b), and Canelas &
Bertoluci (2007). Twenty species were recorded in the seven breeding sites we
Some individuals were collected and submitted to a saturate monitored (Table 3). The number of species in the sites varied from
atmosphere of CO2 (resolution Nº 714 of 20 June 2002 of CFMV), fixed four to 12. Site L1 showed the highest number of species (12),
in formal 10% and preserved in alcohol 70% (under license IBAMA followed by Site L2 (11). The lowest number of species was found
n° 430/05). Voucher specimens were deposited in the herpetological in Site R2 (4), the only temporary site studied. Fritziana fissilis,
collection of Escola Superior de Agricultura Luiz de Queiroz, Dendrophryniscus brevipollicatus and Physalaemus spiniger were
Universidade de São Paulo (Appendix I). recorded in the surroundings of water bodies. Cluster analysis identified
two major groups: (I) formed by Rhinella ornata and R. icterica (Ia) and
3. Data analysis
Cycloramphus lutzorum, Vitreorana uranoscopa and Bokermannohyla
The species richness registered in relation to the sampling effort was hylax (Ib); (II) formed by the four species of Dendropsophus (IIa) and
assessed by the species accumulation curve (sensu Colwell et al. 2004), other species (IIb) (Figure 5).
calculated through the exact method (Kindt 2004) using the function
3. Seasonal breeding patterns
“specaccum”. To estimate the richness we used the function “specpool”
and “poolaccum” and the non-parametric estimators Bootstrap and Table 4 summarizes the annual breeding patterns of the 20 anuran
Jacknife I (Santos 2003) with 10,000 randomizations with sample species whose males vocalized in the seven aquatic sites showed in
reposition, “vegan” package (Oksanen et al. 2011), developed for R Table 3. Classes shown here are the highest classes of the number of
environment (R Development Core Team 2012). A matrix with monthly calling males recorded each month considering all monitoring sessions
occurrence was used for all species registered in the reproductive and all sites. Evidences of actual reproduction (amplectant pairs,
habitats and chance encounters. oviposition behavior or egg clusters) are indicated. Anurans called
To evaluate the similarity in the use of the breeding sites, we in almost every month of the two-years period, with higher number
considered only species that show reproductive activity in the selected of active species (more than 10) being recorded in the rainy seasons
aquatic sites between September 2006 and October 2007. Based on the (October to February) of both years. Only Scinax hayii displayed a
breeding sites use, species were classified as habitat generalists and continuous breeding pattern, with males calling in 22 of the 24 samples.
specialists. Dissimilarity between species pairs was also calculated by
the complement of the Jaccard index (DJ = 1– J), and this triangular Discussion
matrix was submitted to a cluster analysis by the UPGMA method (e.g.,
Sneath & Sokal 1973), which calculates the coefficient of cofenetic 1. Species composition
correlation (r), indicating the degree of representativeness of the
similarity matrix in the dendrogram, so that values ​​of r ≥ 0.8 allow to The species composition at the NSB is typical of Neotropical
consider that the dendrogram adequately represents the dissimilarity sites, with high representativeness of Hylidae (Duellman 1999). In
matrix (Rohlf 2000). For this analysis we use the “hclust” function, addition, 69% of the species are endemic to the Atlantic Rainforest;
applying the “average” method, also from the “vegan” package the high degree of endemism is also typical of this biome (Vancine et
(Oksanen et al. 2011), developed for the R-environment (R Development al. 2018), however the geomorphological characteristics of NSB, with
Core Team 2012). altitudes close to the sea level, rising in a gradient that reaches 1,000
m in altitude, influenced the composition of the anuran fauna, which is
Results composed by species typical of the low Atlantic Rainforest (Rhinella
hoogmoedi, Ololygon argyreornata and O. littoralis) (Pombal & Gordo
1. Species composition 1991, Caramaschi & Pombal 2006, Bertoluci et al. 2007) alongside of
species restricted to the hillside forest (e.g., Ischnocnema aff. guentheri)
During the study period we recorded to the NSB 33 species (Bertoluci et al. 2007).
distributed in 12 families: Brachycephalidae (1 species), Bufonidae The estimated richness values theoretically
​​ indicate the possibility
(4), Centrolenidae (1), Craugastoridae (1), Cycloramphidae (1), of increasing at least three species in the sampling survey, which can be
Hemiphractidae (1), Hylidae (15), Hylodidae (1), Leptodactylidae observed when considering the high ß diversity of anuran fauna found
(5), Microhylidae (1), Odontophrynidae (1), and Phyllomedusidae (1) in PECB in its different phytophysiognomies or even in an altitudinal
(Table 2, Figure 2). Trachycephalus mesophaeus represents a new record gradient (e.g. Guix et al. 1994, Guix et al. 2000, Bertoluci et al. 2007,
to the area. The species accumulation curve did not show stabilization Moraes et al. 2007, Forlani et al. 2010).
(Figure 3), with certain trend towards ascension, which is evident by The anuran fauna of different portions of PECB was described in
the high confidence interval. The Jackknife estimator I, based in the four other studies (Guix et al., 1994; Guix et al., 2000; Bertoluci et al.,
rare species occurrence, showed higher value in the last month of our 2007; Forlani et al., 2010). The compilation of these lists by Forlani et
sampling (SJ = 35.88 ± 1.665 standard error), and the Bootstrap estimator, al. (2010) resulted in a richness of 85 species for the entire park. We
considering the full data set (repeated sampling with reposition), for 10000 add here one species to that list, Trachycephalus mesophaeus, maybe
randomization, was SB = 34.34 ± 1.004 (Figure 4). due to our higher sampling effort compared to those of the studies cited

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Anuran assemblage of an Atlantic forest site

Table 2. Anuran species recorded in the Núcleo Sete Barras, Parque Estadual Carlos Botelho, southeastern Brazil, between September 2005
and October 2007.
Brachycephalidae Ischnocnema aff. guentheri (Steindachner, 1864)
Bufonidae Dendrophryniscus brevipollicatus Jiménez de la Espada, 1870 1871 “1870”
Rhinella hoogmoedi Caramaschi & Pombal, 2006
Rhinella icterica (Spix, 1824)
Rhinella ornata (Spix, 1824)
Centrolenidae Vitreorana uranoscopa (Müller, 1924)
Craugastoridae Haddadus binotatus (Spix, 1824)
Cycloramphidae Cycloramphus lutzorum Heyer, 1983
Hemiphractidae Fritziana fissilis (Miranda Ribeiro, 1920)
Hylidae Boana albomarginata (Spix, 1824)
Boana bischoffi (Boulenger, 1887)
Boana faber (Wied-Neuwied, 1821)
Boana semilineata (Spix, 1824)
Bokermannohyla hylax (Heyer, 1985)
Dendropsophus berthalutzae (Bokermann, 1962)
Dendropsophus elegans (Wied-Neuwied, 1824)
Dendropsophus minutus (Peters, 1872)
Dendropsophus seniculus (Cope, 1868)
Ololygon argyreornata (Miranda-Ribeiro, 1926)
Ololygon littoralis (Pombal & Gordo, 1991)
Ololygon rizibilis (Bokermann, 1964)
Scinax aff. alter (B. Lutz, 1973)
Scinax hayii (Barbour, 1909)
Trachycephalus mesophaeus (Hensel, 1867)
Hylodidae Hylodes cf. phyllodes
Leptodactylidae Adenomera marmorata Steindachner, 1867
Leptodactylus latrans (Steffen, 1815)
Leptodactylus notoaktites Heyer, 1978
Physalaemus olfersii (Lichtenstein & Martens, 1856)
Physalaemus spiniger (Miranda-Ribeiro, 1926)
Microhylidae Myersiella microps (Duméril & Bibron, 1841)
Odontophrynidae Proceratophrys boiei (Wied-Neuwied, 1825)
Phyllomedusidae Phyllomedusa distincta A. Lutz in B. Lutz, 1950

above, raising the overall richness of PECB to 86 species. This richness lutzorum is considered Data Deficient with decreasing populations by
corresponds to 37% of the anuran known for the state of São Paulo IUCN (2019); major threats to this frog are residential and commercial
(Rossa-Feres et al. 2011). As expected the composition of the anuran development, agriculture and aquaculture, and biological resource use.
fauna of NSB is similar to those of other localities of southeastern Brazil
2. Breeding site utilization
covered by the Dense Ombrophilous Forest of São Paulo state (Bertoluci
et al. 2007), like the Estação Biológica de Boracéia (Heyer et al., 1990; Species that used the monitored reproductive habitats did not
Bertoluci et al., 2005), the Parque Estadual Intervales (Bertoluci, 1998), distribute homogeneously among sites. Rhinella ornata, R. icterica and
and the Reserva Biológica do Alto da Serra de Paranapiacaba (Verdade Ololygon littoralis were classified as habitat generalists (they used all
et al. 2009). The different physiognomies of the Atlantic Forest, the habitat types); the pattern of habitat use of these species has already
large altitudinal gradient (Guix et al. 1994, 2000) and the good state of been observed in other taxocenoses (e.g., Izecksohn & Carvalho-e-Silva
conservation of PECB areas, and habitat heterogeneity (e.g., Silva et al. 2001, Bertoluci & Rodrigues 2002c, Narvaes et al. 2009).
2011 and references therein) are also relevant factors in the interpretation Vitreorana uranoscopa, Cycloramphus lutzorum and
of this high richness. Bokermannohyla hylax were considered stream specialists. Vitreorana
Although none of the species recorded in the present study were uranoscopa lays eggs on leaves of the marginal vegetation suspended
included in the Brazilian red list of endangered fauna, Cycloramphus over streams, where eggs fall and tadpoles complete development to

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Bertoluci J. et al.

Figure 2. Anuran species recorded in the Núcleo Sete Barras (PECB): (a) Ischnocnema aff. guentheri, (b) Dendrophryniscus brevipollicatus,
(c) Rhinella icterica, (d) Rhinella ornata, (e) Haddadus binotatus, (f) Cycloramphus lutzorum, (g) Proceratophrys boiei, amplectant pair,
(h) Hylodes cf. phyllodes, (i) Physalaemus spiniger, (j) Adenomera marmorata, (k) spawn of A. marmorata, (l) Myersiella microps, (m)
Bokermannohyla hylax, (n) Dendropsophus elegans, (o) Dendropsophus seniculus, (p) Boana albomarginata, (q) Boana bischoffi, (r)
fighting males of Boana faber, (s) Boana semilineata, (t) Phyllomedusa distincta, (u) Scinax aff. alter, (v) Scinax hayii, amplectant pair,
(w) Ololygon littoralis, (x) Trachycephalus mesophaeus.

metamorphosis (Heyer 1985a, 1990). Cycloramphus species lay their slope, altering the original structure of the habitat. Changes caused by
eggs on rocks and in wet rock crevices, with semi-terrestrial tadpoles anthropogenic disturbances modify the local structure of the forest,
living at the water-land interface, microhabitats commonly found on the form new microhabitats and make different resources available, which
banks of rocky streams (Haddad & Prado 2005), as sampled in PECB. influences community structure (Connell & Slatyer 1977, Pickett &
Bokermannohyla hylax is a typical species of dense ombrophilous forest White 1985, Tocher et al. 2001).
streams (Heyer 1985b; Bertoluci 2002; Bertoluci et al. 2003). Males Species of the genus Rhinella were considered habitat generalists,
vocalize from the vegetation on the edge of forest streams, tadpoles seek showing the primitive reproductive mode for the group, which favors the
shelter under rocks, dead leaves or burrow into the mud (Bertoluci et exploration of different habitat types (Haddad & Prado 2005). Subgroup
al. 2003). The presence of this species in Site L1 (classified as a pond) Ib of the dendrogram includes only species with specialized reproductive
is probably due to the interruption of the stream course by the road modes associated with streams (Heyer et al. 1990, Bertoluci et al. 2004,

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Anuran assemblage of an Atlantic forest site

(Haddad & Prado 2005). Leptodactylus latrans builds floating foam

nests in permanent or semipermanent environments (Vaz-Ferreira &
Gerhau 1975) and P. distincta lays eggs on leaves hanging over water
in permanent aquatic environments (Woehl & Woehl 2000). The most
intimate grouping between O. rizibilis and L. latrans may be due to
the use of semi-permanent environments, suitable for their specialized
reproductive mode. The second branch is formed by all Boana species,
among which only Boana faber has a specialized reproductive mode
(eggs in nests dug in mud in the banks of lentic water bodies; Martins
& Haddad 1988), despite being habitat generalist.
The high degree of overlap in the use of reproductive habitats
corroborates the well-established idea that suitable water bodies for
reproduction behave as limiting factors for anurans (e.g., Bertoluci &
Figure 3. Species accumulation curve between September 2005 and October Rodrigues 2002c). However habitat heterogeneity permits anurans use
2007. specific microhabitats as calling, oviposition and developmental sites
with low or no overlap, influencing anuran richness and the composition
Haddad & Prado 2005). Group II includes only species that breed in of the assemblages (e.g., Bertoluci & Rodrigues 2002c, Vasconcelos
lentic water bodies, all of the family Hylidae, except Leptodactylus & Rossa-Feres 2008, Vasconcelos et al. 2009, Figueiredo et al. 2019).
latrans (Leptodactylidae). In subgroup IIa are Dendropsophus species,
3. Seasonal patterns of breeding activity
typical of lagoons (e.g., Bertoluci & Rodrigues 2002c, Narvaes et al.
2009) and with generalized reproductive mode (e.g., Haddad & Prado The breeding activity of anurans at PECB-NSB was closely related
2005). In subgroup IIb there are two smaller branches; the former to the rainy season. This general pattern is commonly found in seasonal
includes all species of Scinaxinae (Scinax and Ololygon), as well as tropical areas of both Amazonia (Toft & Duellman 1979, Aichinger,
Leptodactylus latrans and Phyllomedusa distincta, pond-associated 1987, Hero, 1990, Gascon 1991, Duellman, 1995) and southeastern
species. Among the species of Scinax all have generalized reproductive Brazil (Bertoluci 1998, Eterovick & Sazima 2000, Bertoluci &
mode except Ololygon rizibilis, which produces an aquatic foam nest Rodrigues 2002b, Canelas & Bertoluci 2007, Narvaes et al. 2009). Only

Figure 4. Richness estimators (A) Bootstrap (SB = 32.53) and (B) Jacknife I (SJ = 35.88 ± 1.665 standard error) built from 10,000 randomizations, during 26
months (September 2005 to October 2007).

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Bertoluci J. et al.

Table 3. Distribution of 20 anuran species in seven aquatic breeding sites of the Núcleo Sete Barras, Parque Estadual Carlos Botelho,
southeastern Brazil.
Species L1 L2 L3 L4 L5 R1 R2
Rhinella ornata ● ● ● ● ● ● ●
Boana albomarginata ● ● ● ● ●
Boana semilineata ● ● ● ● ●
Ololygon littoralis ● ● ● ● ● ●
Dendropsophus berthalutzae ● ● ● ●
Phyllomedusa distincta ● ● ●
Scinax hayii ● ● ●
Boana bischoffi ● ● ●
Bokermannohyla hylax ● ● ●
Rhinella icterica ● ● ●
Dendropsophus minutus ● ●
Dendropsophus seniculus ● ●
Leptodactylus latrans ● ●
Dendropsophus elegans ● ●
Vitreorana uranoscopa ● ●
Boana faber ● ●
Ololygon rizibilis ●
Ololygon argyreornata ●
Scinax aff. alter ●
Cycloramphus lutzorum ●
Total 12 11 8 9 9 5 4

Figure 5. Cluster analyses of 20 anuran species based on their occurrence in seven breeding sites of the Núcleo Sete Barras-Parque Estadual Carlos Botelho (SP). (1)
Rhinella ornata, (2) R. icterica, (3) Cycloramphus lutzorum, (4) Vitreorana uranoscopa, (5) Bokermannohyla hylax, (6) Dendropsophus seniculus, (7) D. minutus,
(8) D. elegans, (9) D. berthalutzae, (10) Leptodactylus latrans, (11) Ololygon rizibilis, (12) O. littoralis, (13) O. argyreornata, (14) Scinax alter, (15) S. hayii, (16)
Phyllomedusa distincta, (17) Boana semilineata, (18) B. albomarginata, (19) B. faber, (20) B. bischoffi.

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 Table 4. Seasonal calling and breeding patterns of 20 anuran species in seven aquatic breeding sites of Parque Estadual Carlos Botelho – Núcleo Sete Barras, southeastern Brazil, between
September 2005 and September 2007. Classes for the number of synchronously calling males: (1) 1-2, (2) 3-5, (3) 6-10, (4) 11-20, (5) 21-50, and (6) more than 50; V, abundance of calling
males not estimated; * evidence of actual reproduction (amplexes or egg clusters); + presence of individuals without breeding activity.
2005 2006 2007
Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep
Scinax hayii v v 6 6 3 2 2 5 2 5 6 5 6 1 2 5 4 3 1 5* 6 5
Rhinella icterica + v 2 1 + + * 1 1 2 3 1 + 3 2* + 1 2* 1 3
Boana faber 6* 6* 5* 6* 4* 2 2* 1 4 2* 1
Biota Neotrop., 21(1): e20201082, 2021

Dendropsophus
elegans v* 6 5 5 4 6 5 3 2 2
Ololygon

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littoralis 2 2 1 v 2 + 2 2 1 1 4* 2 4 + + 2 2 1 4 6* 6
Rhinella ornata v v 4 2 + 1 5 5 v + 1 1 * 4 3* 3
Bokermannohyla
hylax v 2 1 2 2 + 2 4 2 4 2 1 4 + 3 2
Boana
albomarginata 1 1 1 3 1 4 + + 2
Scinax aff. alter v* 6* 4 * 2* 1 3 4 * 1 * + 4
Boana bischoffi + 1 4 2 5 5 4 5* 3 2 3 2 2 2 1 3
Boana
semilineata 1 + + + 2 2 + 2 4 1 2 2 3 3 1 4 5 4*
Dendropsophus
minutus 2 v 3 1 1 1 1 3 4 1 1 2 2
Phyllomedusa
distincta 3 2 2 2 1 1 + 1
Anuran assemblage of an Atlantic forest site

Ololygon
rizibilis 2 1
Cycloramphus
lutzorum + + + +
Dendropsophus
seniculus 3
Dendropsophus
bertalutzae 6* 3 2 5 6 6 5
Ololygon
argyreornata 2
Leptodactylus
latrans + 1
Vitreorana
uranoscopa *
Total number of
species 2 10 11 10 13 11 4 2 0 7 4 9 9 11 14 14 13 10 6 6 7 7 8 8 15
9

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 10 Biota Neotrop., 21(1): e20201082, 2021

Bertoluci J. et al.

Conflicts of interest
Scinax hayii showed calling activity almost throughout the entire period
of study (22/24 months), a continuous breeding pattern already observed The authors declare that they have no conflict of interest related to
in the populations of the Estação Biológica de Boracéia (Ombrophylous the publication of this manuscript.
forest; Bertoluci & Rodrigues 2002b) and Estação Ecológica Juréia-
Itatins (Restinga forest; Narvaes et al. 2009), both sites located is São Ethics
Paulo state, southeastern Brazil. A breeding pattern associate to the
rainy season was showed by S. hayii in the Parque Estadual Intervales Permits necessary to this study in the time it was developed were
(Ombrophylous forest, Bertoluci 1998), also in São Paulo state. These collection license from IBAMA and license to study in conservation
differences seems to be related to the different climate regimes of these units (COTEC). We had these two licenses.
localities. A high proportion of continuous breeders is characteristic of
aseasonal environments (e.g. Crump 1974). Data availability
We conclude claiming attention to the importance of preserving all
types of habitats and microhabitats in the entire altitudinal gradient of Results from this study should be stored in the Sistema de
PECB as a strategy for the conservation of frogs of southeastern Brazil, Informação Ambiental do Programa Biota/Fapesp/SinBiota, since it
one of the richest regions of the world. was part of Programa Biota SP.

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