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Anuran diversity in an Araucaria Forest fragment and associated grassland area in a sub-tropical region in Brazil

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Considering the rapid advancement of forest fragmentation and habitat destruction, understanding species composition, richness and distribution is crucial for the development of conservation strategies. In this context, the main goal of this study is to provide an inventory of anuran species using different sampling methods (survey at breeding sites, transect sampling and pitfall traps) and to evaluate the assemblage structure of anurans in an Araucaria Forest and its associated grasslands in a subtropical region in Brazil. For the analyses, 21 breeding sites were classified into three categories: open area (OA; n=7), forest interior (FI; n=7) and forest edge (FE; n=7). A diversity profile analysis was performed to evaluate alpha diversity. ANOSIM and SIMPER analyses were carried out to verify differences regarding species composition (beta diversity) between the categories. A total of 33 species comprising nine families were recorded, representing ca. 80% of the estimated richness for the region. The greatest alpha diversity was observed in FI, whereas OA and FE did not differ in terms of diversity. Regarding beta diversity, all categories differed amongst themselves (dissimilarity 80%), which may be related to the presence of exclusive species in each category, requiring specific habitat characteristics, due to specific reproductive modes. Furthermore, many species showed high abundance due to their generalist habits. The presence of exclusive species at OA and FI reinforces the importance of preserving different habitats for the maintenance of local species richness and diversity.
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Introduction
Anuran assemblage compositions are determined
by species interactions with biotic and abiotic factors
(Eterovick and Sazima, 2000; Parris, 2004; Wells,
2007; Oda et al., 2016), as well as by historical and
evolutionary processes (Zimmerman and Simberloff,
1996; Piha et al., 2007). The availability of different
microhabitats allows for the segregation and coexistence
of species in a same habitat, as well as species
differentiation among habitats (Conte and Rossa-Feres,
2007; Santos et al., 2007; Vasconcelos et al., 2009;
Silva et al., 2011). In this sense, habitat heterogeneity
has been considered an important factor regarding
anuran assemblage structure (Cardoso et al., 1989;
Parris, 2004; Silva et al., 2012). Ecological studies seek
to understand how these interactions occur and how
they influence species richness and distribution (e.g.,
Parris, 2004; Santos et al., 2007; Ernst and Rödel, 2008;
Vasconcelos et al., 2009; Silva et al., 2012). Answering
these questions is important in the present setting, since
habitat destruction and alterations are major threats to
several species, especially anurans (Dixo and Verdade,
2006; Bishop et al., 2012). Most anurans are extremely
dependent on their habitat characteristics, due to several
factors, including permeable skin (Wells, 2007) and
reproductive modes that require specific microhabitats
(Haddad and Prado, 2005; Crump, 2015).
This study presents an evaluation of the structure of
an anuran assemblage at an Araucaria forest region and
its associated grasslands, located in the Piraí do Sul
municipality, Brazil. The study aims to (i) provide a list
of species for the region and (ii) compare the assemblage
composition of three different habitats types: open area,
forest interior and forest edge.
Material and Methods
This study was carried out at the Piraí do Sul
municipality (24.5397°S, 49.9278°W; datum SIRGAS,
Herpetology Notes, volume 11: 421-428 (2018) (published online on 09 May 2018)
Anuran diversity in an Araucaria Forest fragment and
associated grassland area in a sub-tropical region in Brazil
Nathalie Edina Foerster1,* and Carlos Eduardo Conte,2,3
1 Autonomous researcher: Major França Gomes, 673, CEP
80310-000, Curitiba, Paraná, Brazil
2 Instituto Neotropical: Pesquisa e Conservação (INPCON).
Avenida Coronel Francisco Heráclito dos Santos, 100, CEP
81531-980, Curitiba, Paraná, Brazil
3 Criadouro Onça Pintada. Estrada do Pocinho, s/n, Campina
Grande do Sul, CEP 83420-000, Paraná, Brazil
* Corresponding author. E-mail: nathalie.foerster@gmail.com
Abstract. Considering the rapid advancement of forest fragmentation and habitat destruction, understanding species
composition, richness and distribution is crucial for the development of conservation strategies. In this context, the main goal
of this study is to provide an inventory of anuran species using different sampling methods (survey at breeding sites, transect
sampling and pitfall traps) and to evaluate the assemblage structure of anurans in an Araucaria Forest and its associated
grasslands in a subtropical region in Brazil. For the analyses, 21 breeding sites were classified into three categories: open
area (OA; n=7), forest interior (FI; n=7) and forest edge (FE; n=7). A diversity profile analysis was performed to evaluate
alpha diversity. ANOSIM and SIMPER analyses were carried out to verify differences regarding species composition (beta
diversity) between the categories. A total of 33 species comprising nine families were recorded, representing ca. 80% of the
estimated richness for the region. The greatest alpha diversity was observed in FI, whereas OA and FE did not differ in terms of
diversity. Regarding beta diversity, all categories differed amongst themselves (dissimilarity 80%), which may be related to the
presence of exclusive species in each category, requiring specific habitat characteristics, due to specific reproductive modes.
Furthermore, many species showed high abundance due to their generalist habits. The presence of exclusive species at OA and
FI reinforces the importance of preserving different habitats for the maintenance of local species richness and diversity.
Keywords: Anura; assemblage structure; Campos Gerais; Mixed Ombrophilous Forest; Piraí do Sul
Nathalie Edina Foerster & Carlos Eduardo Conte
422
2000) (SISBIO license n°26992-1), in a region known
as Campos Gerais, in the state of Paraná, Brazil, in two
areas: 1) Floresta Nacional de Piraí do Sul (FNPS) and
2) Piraí da Serra (Figure 1).
The FNPS (24.5667°S, 49.9167°W) is located
between the first and second Paraná plateau, comprising
152 ha. The area presents a slightly undulating relief,
with altitudes ranging between 900 and 1248m above
sea level (asl). The dominant vegetation types are Pinus,
Araucaria and Imbuia (Ocotea), and Araucaria forest in
different successional stages where selective logging
has transpired (Moro et al., 2009). Different vegetation
types, such as Pinus, Eucalyptus and crops, as well as
different-sized Araucaria forest fragments, occur in the
surrounding areas of the FNPS (ICMBio, 2011).
The Piraí da Serra area (24.4667°S, 50.0167°W) is
located in the Environmental Protection Area (APA)
of the Devonian Escarpment, with an elevation of
around 1000 m asl comprising 51.20 ha (SEMA, 2004)
at approximately 15 km from the FNPS. The region is
formed by approximately 37% grassy-woody steppe,
18% Araucaria Forest, 45% fast-growing exotic species
monocultures (Pinus and Eucalyptus) and crops (Veloso
et al., 1991; Bilenca and Miñarro, 2004; SEMA, 2004).
The Campos Gerais climate, according to Köppen, is
Cfb (humid subtropical), with mild summers. Maximum
average temperatures in the hottest months are below
22˚C, and during the coldest months are below 18˚C,
with frequent frost (Moro et al., 2009).
Diversity data was obtained monthly at 24 sites,
from October 2012 to March 2013. Three sites were
composed of transects locates in the forest interior, 20
sites were breeding habitats (six puddles, nine swamps,
five lakes, one artificial tank and three 120-meter
transects in streams) at FNPS and its surrounding areas,
and one site was a stream transect in Piraí da Serra (Table
1). The habitats sampling sequence of each campaign
was altered to minimize possible variations in species
activities (sensu Conte and Rossa-Feres, 2006).
The applied sampling methods were: 1) breeding site
sampling (Scott Jr. and Woodward, 1994), in which the
perimeter of each water body and stream were slowly
traversed, counting individuals from different species
and calling males during one hour per site per campaign,
totalling 150 hours for all habitats; and 2) transects
inside the forest, slowly traversed, counting individuals
from different species and calling males, with an effort
of one hour per transect per campaign, totalling 18
Figure 1. Map of Brazil, state of Paraná and satellite images of the sampled areas in the municipality of Piraí do Sul: A- Piraí da
Serra; B- Floresta Nacional de Piraí do Sul and surrounding areas. Asterisks indicate the locations of the habitats sampled in the
study area; more than one habitat can be located at the same asterisk point at the map. The red asterisks indicate the locations at
the Floresta Nacional de Piraí do Sul. Satellite image: Google Earth©.
hours for all transects, jointly. Pitfall traps were used as
the inventory method (Corn, 1994). Five sites with three
trap lines were sampled. Each line was composed by
four 60-liter buckets, located 10 meters apart from each
other, connected by drift fences, set in a way to induce
individual capture. The buckets remained open for five
consecutive nights per campaign, totalling an effort of
60 buckets per night per campaign. Samplings using
pitfall traps were carried out bimonthly from November
2012 to September 2013. Only species richness data
was collected using this method. Data obtained in this
manner was not used for the diversity analyses.
Total abundance at each site was considered as the sum
of abundances of all sampled months. This estimate was
used to avoid population underestimations, considering
the observation made by Nomura et al. (2012) when
evaluating a compilation of studies that indicated
differences in capture and recapture results. These
results demonstrate that, despite differences between
species, the number of individuals present in more than
one breeding event tends to be lower than the number of
individuals present at only a single breeding event.
The first-order Jackknife estimator extrapolation
method was applied to evaluate species richness
estimates of the study area and sampling efforts, where
random samples were added to the species accumulation
curve until an asymptote was obtained (Colwell et
al., 2004). The analyses were carried out using the
EstimateS version 9.0.0 software (Colwell, 2013).
The 21 breeding habitats, with the exception of the
forest transects, were classified into three categories
for the diversity analyses: seven in the forest interior
(FI), comprising two swamps, two ponds, three
streams and one artificial tank; seven at the forest
Anuran diversity in an Araucaria Forest fragment in Brazil 423
Table 1. Characterization of the sampled habitats in Piraí do Sul municipality, from October 2012 to March 2013 according to
the matrices in which they were inserted: Open area: swamps (SO1, SO2), lakes (LO1, LO2), ponds (PO1, PO2), stream (STO1);
Forest edge: swamps (SE1, SE2), lakes (LE1), ponds (PE1-PE4); Forest interior: swamps (SF1, SF2), lakes (LF1, LF2); streams
(STF1, STF2); artificial tank (ATF), Transections (TF1, TF2, TF3). Vegetation in the breeding habitat: % Interior = percentage of
vegetation inside the breeding habitat, % Marginal= percentage of vegetation on the edge of breeding habitat. Type of vegetation:
He = herbaceous, Sr = shrub, Ab = arboreal, Pt = pteridophyta, Aq = aquatic, Tb = Typha sp., Gr = gramineae, Br = Bryophyte. *
= Not applicable.
Breeding habitat vegetation
Habitat % Interior % Marginal Vegetation type Maximum
depth (m)
SO1 60 80 Sr, He, Gr,Aq 1,30
SO2 100 100 Sr, Ab, Hb, Gr 0,40
SE1 55 60 Sr, Ab, He, Pt, Gr, Aq 0,80
SE2 60 65 Sr, Ab, He, Gr 0,25
SF1 100 100 Sr ,Ab, He, Gr, Pt, Aq 0,40
SF2 100 100 Sr, Ab, He, Gr, Pt, Aq 4,00
LO1 10 75 Sr, He, Gr, Aq 5,40
LO2 50 90 Sr, He, Tb, Aq 3,60
LE1 30 75 Sr, Ab, He, Aq, Gr 3,40
LF1 5 100 Sr, Ab, He, Tb, Aq, Gr 6,00
LF2 40 100 Sr, Ab, He, Aq, Gr 4,40
PO1 5 60 Sr, He, Aq, Gr 1,15
PO2 1 30 Br, Gr 1,00
PE1 5 75 Sr, Ab, He 3,00
PE2 98 25 Sr, Ab, He, Gr 0,25
PE3 80 25 Sr, Ab, He 0,40
PE4 2 30 Sr, Ab, He, Gr 1,50
STO1 0 100 Sr, He, Gr, Br 2,00
STF1 0 95 Sr, Ab, He, Gr, Pt 0,30
STF2 0 100 Sr, Ab, He, Pt 0,40
ATF 90 100 Sr, Ab, He, Aq, Gr 0,45
TF1 * 100 Sr, Ab, He, Gr, Pt *
TF2 * 100 Sr, Ab, He, Pt *
TF3 * 100 Sr, Ab, He, Pt *
edge (FE), composed of five swamps, one pond and
four puddles; and seven in an open area (OA), namely
two swamps, two ponds, two puddles and one stream
(Table 1). A Diversity Profile analysis was performed
to verify differences regarding alpha diversity between
categories applying the Rénvi index, in which α=0 is
the total number of species, where α=1 gives a greater
weight to richness according to the Shannon Index, and
α>2 attributes weight to equitability according to the
Simpson Index. As different α values were observed,
there was no problem in applying the diversity and
interpretation indexes, since each of these indices
attributes different weights to rare species (Mendes et al.,
2008). This analysis generates curves that graphically
represent which habitats are more diverse. However, if
the curves connect at a certain point, it is not possible to
define which one is more diverse, and, in this case, they
cannot be compared (Tóthmérész, 1995). The analyses
and curves were plotted and evaluated using the Past
version 2.17c software package (Hammer et al., 2001).
A similarity analysis (ANOSIM) was conducted
to evaluate differences in beta diversity among the
categories, measuring the difference between two or
more groups from a certain distance (Clarke, 1993). A
similarity percentage analysis (SIMPER) was used to
evaluate species relative contribution for the dissimilarity
in each category (Clark, 1993). Due to the high
values for species richness, species that cumulatively
contributed up to 90% were considered. The applied
distance measurement for these analyses was the Bray-
Curtis Index that evaluates the dominance and rarity
between species by applying richness and abundance
data (Krebs, 1999). The analyses were carried out using
the Past version 2.17c software package (Hammer et al.,
2001).
Results
Thirty three anuran species were recorded at Piraí do
Sul, distributed throughout 17 genera and nine families,
namely (Table 2): Brachycephalidae (1), Bufonidae
(2), Centrolenidae (1), Hylidae (19), Hylodidae
(1), Leptodacylidae (5), Michohylidae (1), and
Odontophrynidae (2), Phyllomedusidae (1). According
to the data generated by the richness estimation
method, the registered richness corresponds to 80%
of the theoretical richness (N=40, Figure 2). Twenty-
eight of the 33 species were recorded by the breeding
site sampling method (Table 2), seven by transection
inside the forest, two exclusively by the pitfall trap
method (Chiasmocleis leucosticta and Odontophrynus
americanus), and three by the sampling habitats method
[Bokermannohyla circumdata, Scinax sp. (gr. ruber)
and Crossodactylus sp.]
No significant difference between OA and FE was
observed when evaluating diversity profiles, whereas
FI displayed a significantly higher alpha diversity in
relation to the other categories (Figure 3). Regarding
beta diversity, all categories differed amongst themselves
(r = 0.199, p = 0.006), with an 80% species composition
dissimilarity among categories. Of the 27 species
considered in this study, only 14 contributed with
90.51% for this inter-categories differentiation (Table
Nathalie Edina Foerster & Carlos Eduardo Conte
424
Figure 2. Observed richness during the six months of sampling,
from October 2012 to March 2013 (●) and expected richness
with additional samples to reach the estimated number of
species (○), at Piraí do Sul, Paraná, Brazil.
Figure 3. Amphibian Diversity Profile among treatments
(OA- open area; FE- forest edge; FI- forest interior) sampled
at Piraí do Sul from October 2012 to March 2013. The curves
are generated by different α values given by different diversity
indices, so the generated curves represent which are the most
diverse (alpha diversity) habitats.
3), identified as the species displaying the greatest
abundance (Table 2).
Discussion
The species richness recorded herein represents 23%
of the richness reported for the state of Paraná and
25.6% for Araucaria Forest (AF) (Conte, 2010; Conte et
al., 2010). This is similar to other studies conducted in
AF areas, such as at the Fazenda Experimental Gralha
Azul, in the Fazenda Rio Grande municipality (n = 32;
Conte and Rossa-Feres, 2007) and Floresta Nacional
Chapecó (n = 29; Lucas and Fortes, 2008), and higher
when compared to the Parque Municipal São Luís de
Tolosa, located in the Rio Negro (n = 24; Santos and
Anuran diversity in an Araucaria Forest fragment in Brazil 425
Table 2. Anuran species composition and abundance and method by which they were sampled during the sampling period from
October 2012 to March 2013 at the Piraí do Sul municipality, and the respective treatments in which they were recorded. Forest
edge (FE); Open area (OA); Forest interior (FI); Sampling method: breeding site visual encounter survey (BS); Transects in forest
interior (TF); Pitfall traps (PT); * Species recorded outside the breeding habitats sampled; Note: species collected in pitfall traps
and recorded outside the sampled habitats do not have abundance data.
Table 2. Anuran species composition and abundance and method by which they were sampled during the sampling period from October 2012 to March 2013 at
the Piraí do Sul municipality, and the respective treatments in which they were recorded. Forest edge (FE); Open area (OA); Forest interior (FI); Sampling
method: breeding site visual encounter survey (BS); Transects in forest interior (TF); Pitfall traps (PT); * Species recorded outside the breeding habitats sampled;
Note: species collected in pitfall traps and recorded outside the sampled habitats do not have abundance data.
Taxa FE OA FI BS TF PT
Brachycephalidae
Ischnocnema henselii (Peters1872) 8 X X X
Bufonidae
Rhinella abei (Baldissera-Jr, Caramaschi and Haddad 2004) 1 X X
Rhinella icterica (Spix 1824) X
Centrolenidae
Vitreorana uranoscopa (Müller 1924) 13 X
Odontophrynidae
Odontophrynus americanus (Duméril and Bibron, 1841) X
Proceratophrys boiei (Wied-Neuwied, 1825) 9 19 X X X
Hylidae
Aplastodiscus perviridis A. Lutz in B. Lutz 1950 34 4 31 X X
Boana. sp (gr. pulchellus) 2 X
Aplastodiscus albosignatus (A.Lutz and B. Lutz 1938) 4 7 34 X
Boana albopunctata (Spix 1824) 95 337 146 X
Boana bischoffi (Boulenger 1887) 150 73 222 X X
Boana faber (Wied-Neuwied 1821) 18 7 5 X
Boana jaguariaivensis Caramaschi, Cruz and Segalla, 2010 306 X
Boana prasina (Burmeister, 1856) 5 64 27 X X
Bokermannohyla circumdata (Cope 1871) *
Dendropsophus microps (Peter 1872) 19 48 55 X X
Dendropsophus minutes (Peters1872) 117 466 230 X
Dendropsophus sanborni (Schmidt 1944) 137 430 49 X
Ololygon aromothyella Faivovich, 2005 2 X
Ololygon rizibilis (Bokermann, 1964) 10 32 X X
Scinax fuscovarius (A. Lutz, 1925) 8 8 65 X
Scinax sp.(gr. ruber)*
Scinax squalirostris (A. Lutz, 1925) 10 X
Sphaenorhynchus caramaschii Toledo, Garcia, Lingnau and Haddad, 2007 99 3 201 X
Hylodidae
Crossodactylus sp.*
Leptodactylidae
Physalaemus cuvieri Fitzinger, 1826 46 102 55 X X
Physalaemus aff. gracilis 31 78 17 X X
Physalaemus lateristriga (Steindachner, 1864) 21 X
Leptodactylus cf. latrans (Steffen, 1815) 19 33 9 X
Leptodactylus notoaktites Heyer, 1978 1 8 X
Microhylidae
Chiasmocleis leucosticta (Boulenger, 1888) X
Phyllomedusidae
Phyllomedusa tetraploidea Pombal and Haddad, 1992 2 4 14 X
Conte, 2014) and Campo Largo (n = 21; Trevisan and
Hiert, 2016) municipalities. The observed richness can
be considered high and is probably due to the high
number of sampled habitats and the great difference in
landscape composition, as well as the environmental
heterogeneity of these environments. Santos and Conte
(2014) observed that a higher number of species are
registered when a greater scope of site types is sampled
in an AF area (e.g., puddles, lakes, and streams). This is
due to the breeding requirements for each species, that
may require specific conditions in each habitat (e.g.,
different microhabitats and humidity for calling activity,
among others), inserted in different matrices (Gonçalves
et al., 2015). Ischnocnema henselii and Vitreorana
uranoscopa are the most demanding species concerning
habitat quality among forest-dependent anuran species.
Vitreorana uranoscopa was recorded only in one stream
within the forest, because of its reproductive mode,
dependent upon lotic habitats like streams (Heyer, 1985;
Haddad and Prado, 2005). The reproductive mode of
Ischnocnema henselii consists of laying eggs in litter.
These eggs exhibit direct development, requiring forest
environments that can provide an adequate amount of
litter and humidity (Haddad and Prado, 2005). Boana
jaguariaivensis, is noteworthy among species with
habitat specificities in the open area, since it present a
displays mode linked to streams on outcrops in native
grassland fields (Caramaschi et al., 2010). These
specifications mostly linked to reproductive modes
restrict species to certain breeding sites, leading to
difference between habitat compositions.
The breeding site sampling method was very effective
for recording species. However, the other methods
were also important, allowing for encounters with
exclusive species, such as Chiasmocleis leucosticta
and Odontophrynus americanus, recorded only by
pitfall traps. These species present fossorial, cryptic and
explosive breeding habits. Furthermore, a record for C.
leucosticta in the study area is of remarkable importance,
since this is the most western record of this species for
the state of Paraná (Segalla and Langone, 2004; Conte,
2010; Crivellari et al., 2011). The importance of using
different methods has been pointed out by other studies,
such as the one carried out by Silva (2010), in which the
author evaluates different studies that applied adult and
tadpole sampling techniques, and reported that species
richness in all studies would be reduced if only one
method were to be applied, instead of more.
The FI category displayed a greater alpha diversity
in relation to OA, with higher equitability among
species, which can be related to the high forest habitat
heterogeneity (Eterovick, 2003; Santos et al., 2007;
Vasconcelos et al., 2009; Ramos and Santos, 2006). The
generalist or specialist character of a species may reflect
in their presence or absence in a certain environment
(Wells, 2007). Forest environments present vertical
stratification, allowing species to segregate and coexist
in this habitat (Silvano et al., 2003; Silva et al., 2012).
Nathalie Edina Foerster & Carlos Eduardo Conte
426
Table 3. Percentage of dissimilarity contribution for the 14 species that contributed most to the difference on species composition
between the sampled habitats in Piraí do Sul municipality from October 2012 to March 2013 categorized accordingly to the
treatments: forest interior (FI); forest edge (FE); open area (OA). Dissimilarity %: percentage of species individually to the
difference; Accumulated %: the sum of percentage contribution between the previous species to the differentiation. Average
abundance: the proportion of abundance of each species between treatments.
Open areas present lower stratification, excluding
species that undergo direct development, due to lower
litter moisture and less shading. Because of this, the OA
habitats presented a higher amount of habitat-generalist
species (Oda et al., 2016).
A high differentiation among species composition
(beta diversity) was observed, since each category
recorded exclusive species and differences regarding
species abundance. Dendropsophus minutus, D.
sanborni, and Boana albopunctata are generalist species
regarding habitat and microhabitat use (Giovanelli,
2004; IUCN, 2016) and, in spite of being present in all
the categories, were much more abundant in OA. These
species are typical of open areas and are favoured by the
deforestation of areas originally covered by the Atlantic
Rainforest (Conte and Rossa-Feres, 2006). This is due
to the fact that these species present a more generalized
reproductive mode (mode 1), which consists in laying
eggs in still water, with little specificity regarding
breeding habitats (Haddad, 1998; Haddad and Prado,
2005).
Forest fragments in the Campos Gerais region are
naturally scarce (Moro and Milan, 2016), and the
historical and current deforestation increases in the
region justify the existence of the conservation unit
studied herein. Although it is small, the FNPS can serve
as both a shelter and corridor area for different species.
Furthermore, no prior information relative to species
composition before the disturbances and alterations on
region landscape is available. Exclusive species were
recorded at OA and FI, with forest habitat-dependent
reproductive modes. Thus, this research demonstrates
the relevance of both forest and open areas for the
preservation of local species.
Acknowledgments. We thank Grupo O Boticário de Proteção
à Natureza and Instituto Neotropical: Pesquisa e Conservação
for their financial support, CNPq and CAPES for the scholarship
awarded to N.E.F (Masters) and to C.E.C. (PRODOC No 18-
32/2010). We also thank the staff of FNPS for all the support and
housing. Thanks to the group of the Amphibian’s Laboratory of
UFPR for all the help during the fieldwork and suggestions.
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Accepted by Gabriela Bittencourt-Silva
Nathalie Edina Foerster & Carlos Eduardo Conte
428
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