ZOOLOGIA 34: e20477

ISSN 1984-4689 (online)

zoologia.pensoft.net

RESEARCH ARTICLE

Ecological and reproductive aspects of Aparasphenodon brunoi

(Anura: Hylidae) in an ombrophilous forest area of the Atlantic
Rainforest Biome, Brazil
Laura Gomez-Mesa1,2, Juliane Pereira-Ribeiro1, Atilla C. Ferreguetti1, Marlon Almeida-Santos1,
Helena G. Bergallo1, Carlos F. D. Rocha1

1
Departamento de Ecologia, Universidade do Estado do Rio de Janeiro. Rua São Francisco Xavier 524, PHLC sala 220,
Maracanã, 20550-019 Rio de Janeiro, RJ, Brazil.
2
Programa de Biología, Universidad CES-EIA, Calle 10 A, No. 22 – 04, Medellín, Colombia.
Corresponding author: Juliane Pereira-Ribeiro ([email protected])
http://zoobank.org/9DD60207-1773-4A32-A0FD-25973BCB4F61

ABSTRACT. Presented is the first information on the ecological and reproductive aspects of the treefrog, Aparasphenodon
brunoi Miranda-Ribeiro, 1920, living in ombrophilous forest areas of the Atlantic Rainforest, Brazil. We recorded the species’
daily activity and over the course of a year, population density during the year, microhabitat usage, diet, and some repro-
ductive features (quantity, diameter and mean mass of oocytes, mean reproductive effort of female). Field sampling was
conducted monthly from June 2015 to July 2016. Searches for treefrogs were systematic, using visual encounter surveys along
14 plots RAPELD long term research modules established in the forest. For each captured individual, we recorded the hour,
microhabitat used, and perch height. The diet of the population was ascertained based on 15 individuals collected outside
the study plot areas. Treefrogs used seven different types of microhabitats in the forest but the preferred microhabitats were
tree-trunks and lianas. The amount of accumulated rainfall and air temperature interacted to explain the number of A. brunoi
individuals active throughout the year. The reproductive strategy for females of this comparatively large arboreal frog in the
ombrophilous forest is to produce clutches with a large number (900.8 ± 358.1) of relatively small-sized eggs. We conclude
that in the ombrophious forest of the Vale Natural Reserve, A. brunoi is a nocturnal arboreal treefrog active throughout the
year but activity increases during the wet season as a result of increased precipitation. In the forest, treefrogs tend to perch
mainly on tree-trunks and lianas about 1 m above ground, where it feeds preferably on relatively large bodied arthropod
prey. When living in the ombrophilous forest of the Atlantic rainforest, A. brunoi may change some features of its ecology
(e.g. marked difference in the use of bromeliads) compared to when living in restinga habitats.
KEY WORDS. Casque-headed frog, ecological aspects, ecology, habitat use.

INTRODUCTION Although this species has been considered as decreasing

in population size (Rocha et al. 2004), information regarding its
Bruno’s casque-headed frog, Aparasphenodon brunoi ecology is still scarce. Along its distribution range, the relatively
Miranda-Ribeiro, 1920, is endemic to the Brazilian Atlantic low information available providing aspects on its ecology comes
Rainforest (Haddad et al. 2013), occurring from the south of from areas of restinga habitats (Teixeira et al. 2002, Mesquita et
Bahia, southward to the state of São Paulo, along the states al. 2004, Sluys et al. 2004, Wogel et al. 2006, Haddad et al. 2013),
of Espírito Santo, Minas Gerais and Rio de Janeiro, and can with no information available on the ecology of the species
be found mostly in restinga habitats of this Biome (Carvalho found within ombrophilous forest environments of the Biome.
1939, Feio et al. 1998, Argôlo 2000, Mollo Neto and Teixeira Jr The occurrence of A. brunoi in forests is comparatively
2012, Ruas et al. 2013, Haddad et al. 2013, Oliveira and Rocha less frequent, with most records being composed of lists for the
2014). Restinga is a typical environment of the Brazilian coast, studied area (e.g. Feio et al. 1998, Silva-Soares et al. 2010, Almeida
which is characterized by sand dune formations (Rizzini 1997). and Gasparini 2014). In one of the largest remnants of forests in

ZOOLOGIA 34: e20477 | DOI: 10.3897/zoologia.34.e20477 | September 1, 2017 1 / 8

 L. Gomez-Mesa et al.

the Atlantic Rainforest Biome, the Vale Natural Reserve (VNR) in the Natural grasslands (“Campos nativos”), which are open fields
the state of Espírito Santo in southeastern Brazil, A. brunoi was that emerge as enclaves in the forest, covered by herbaceous
reported to occur (Almeida and Gasparini 2014) but with no local and shrubby vegetation forming thickets (Fig. 1, Peixoto et al.
information regarding its ecology in this forested environment. 2008). In this study, we sampled only the ombrophilous forest
Recently, Jared et al. (2015) provided new biological in- vegetation type.
formation on this species by identifying highly toxic cutaneous Field sampling was done monthly from June 2015 through
secretions, and well-developed delivery mechanisms for both A. July 2016, including months from dry (April to September) and
brunoi and Corythomantis greeningi Boulenger, 1896. The cutane- rainy (October to March) seasons in the area. Sampling was car-
ous secretions of these species present proteolytic and fibrinolytic ried out during diurnal (11:00 am to 05:00 pm) and nocturnal
action, as well as hyaluronidase that promotes the diffusion of (06:00 pm to 11 pm) periods in order to identify activity pat-
toxins. These secretions are associated with a delivery mecha- terns of the treefrogs. Frog sampling was conducted in 14 plots
nism which consists of using bony spines, located in the skull, using the RAPELD sampling method (Magnusson et al. 2005),
that pierce the skin and inject the toxin into the predator (Jared distributed proportionally along four modules. This sampling
et al. 2015). This unique defense mechanism makes A. brunoi method consisted of permanent and standardized plots of 250
a particularly important treefrog because it has a high toxicity, m extensions each, following contour lines of the ground at a
which is 25 times higher than that found in vipers of the genus distance of 1 km between each.
Bothrops. Thus, aspects of their ecology are important for a better Treefrogs were captured on transects along plots of the
understanding of their biology in different environments. module using visual encounter and acoustic surveys (Crump
Considering the known differences in the structural hab- and Scott 1994) simultaneously by two observers. Each plot was
itat among restinga and ombrophilous forest, we would expect sampled five times but only once per month. Before sampling
that differences in aspects of the ecology of this frog could arise each plot, we measured air temperature (°C) and relative air
when living in the ombrophilous forest. In this context, we humidity (%) using a thermohygrometer. During each transect,
aimed to contribute information on such a unique species by the plot was carefully inspected by the observers, looking for
analyzing the ecological and reproductive aspects of A. brunoi treefrogs in the leaf-litter, on trees, branches, bushes, fallen logs
in the ombrophilous environment of the VNR over a one year or other microhabitats when present. We were careful to record
period. We specifically addressed the following questions: i) only active individuals (e.g. moving, foraging) to include in our
What is the daily activity of A. brunoi and what is their activity activity analysis. All individuals were found and sampled within
throughout the year? ii) Which are the preferred microhabitats five meters from the center of each side of the plot (totaling a
used by A. brunoi in the forest? iii) What is the vertical range strip of 10 m wide). For each captured individual we recorded
of A. brunoi when perching in their habitat? iv) What prey the hour, date, plot number, microhabitat used, and the height
composes the treefrog’s diet and which prey items make up the above ground (in cm) that the individual was perched when first
majority of the diet? v) What is the overall morphometrics (mean sighted. At the end of each sampling period, air temperature and
quantity, diameter, and mass) of A. brunoi oocytes? vi) What is relative humidity were measured and recorded again. Data on
the average female reproductive effort for A. brunoi? daily rainfall (in mm) in the area of the Reserve were obtained
from the meteorological station at the VNR.
MATERIAL AND METHODS We estimated treefrog density in the area (ind/ha), based
on the area of each plot (250 m extension x 10 m wide = 2500
The study was carried out in the Vale Natural Reserve m2), calculating the total searched area of plots [considering
(19°06’45”S, 40°03’03”W), located in Linhares and Jaguaré all plots transected/month x 2500 m2 extension = total area
municipality, north of Espírito Santo, Southeastern Brazil. The searched (in m2)] and divided the number of individuals of A.
reserve consists of approximately 23,500 ha and is one of the brunoi per month. Then, we calculated and compared mean
largest and most important remnants of the Atlantic Rainforest treefrog density among the months of dry and rainy seasons
Biome (MMA 2000). The regional is tropical, rainy, and warm using Student t-Test. We used Multiple Regression Analysis to
with mean annual rainfall of 1,214.6 mm and a mean annual evaluate the effects of temperature and accumulated rainfall of
temperature of 24.3 °C (Kierulff et al. 2014). The reserve is cov- the sampling days for A. brunoi density and Simple Regression
ered by a mosaic of habitats with four main vegetation types: Analysis to evaluate the effect of humidity throughout the
Ombrophilous forest (“Tabuleiro”), a dense forest with trees sampled days on A. brunoi density in the respective month of
reaching ca. 40 m height; the Sandy soil forest (“Mussununga the sampling. We obtained the accumulated temperature and
forest”), which follows the cordons of sandy soils with trees of humidity in the sampled period from the averages of the values
comparatively lower height and shrubs that allow most sunlight measured in the plots and obtained precipitation estimates of the
to reach the ground; the Permanent or Seasonally flooded forest sampled period from the sum of the accumulated precipitation
(composed locally by swamps, and lowland and riparian forests) that occurred during the sampling period. The analyses were
which are associated to water bodies that differ structurally; and conducted using the software R – 3.3.1.

2 / 8 ZOOLOGIA 34: e20477 | DOI: 10.3897/zoologia.34.e20477 | September 1, 2017

 Ecology of Aparasphenodon brunoi in the Atlantic Rainforest Biome

Figure 1. Location of the Vale Natural Reserve, north of Espírito Santo, southeastern Brazil, showing the vegetation types present in the
reserve and the location of the plots (black squares) and collection sites of individuals for diet analysis and reproductive aspects (stars).

We estimated the frequency of the different microhabitats to determine the sex and to analyze stomach contents under
used by the treefrog in order to identify those preferentially used. a stereomicroscope. Animal prey items were measured (to the
We measured the distribution of heights that individuals were nearest 0.1 mm) using a Vernier Caliper and categorized to the
found to identify the range and preferred height that A. brunoi taxonomic level of order (or family in the case of ants). Uniden-
perched in the forest. We found some individuals occupying the tified arthropod remains were grouped in a separate category
hole of PVC tubes (used to demarcate the plots in the forest), “unidentified arthropod remains” (U.A.R). We measured the
but we did not consider such records for microhabitat usage length (L) and width (W) of each prey item and its volume (V)
estimates because they constituted artificial microhabitats. was estimated using the ellipsoid formula: V = 4/3π (L/2) (W/2)2
We analyzed diet composition in 15 individuals collected (Dunham 1983). Diet composition was estimated in terms of
outside areas of the plots, in order to avoid interference with number (N), volume (V, in mm3) and frequency (F) of occurrence
our density estimates within plots. The frogs were euthanized (percentage of stomachs containing a particular prey category)
with a topical anesthetic gel (lidocaine 5%), fixed in 10% for- of each prey type in the stomachs. We estimated an index of
malin solution and preserved in 70% alcohol (IBAMA license relative importance (Ix) of each prey category in the diet which
46327-4). The treefrog specimens were deposited in the Museu represents the sum of percentages of the number, volume and
Nacional, Rio de Janeiro (MNRJ). We measured snout-vent frequency of each prey type: [Ix = (%N +%V +%F)] (Powell et al.
length (SVL) and jaw width (JW) of the frogs using a Vernier 1990). The effect of frog mouth width (in mm) on the volume
Caliper (to the nearest 0.1 mm) and weighed them using a Pesola (in mm3) of the largest prey consumed was estimated by simple
dynamometer (to the nearest 0.1 g). Individuals were dissected Regression Analysis.

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 L. Gomez-Mesa et al.

For each gravid female, we recorded the mass of each ova- between the months of dry season (x = 1.79 + 1.90 ind/ha) and
ry using an electronic scale (precision of 0.001 g), counted the months of rainy season (x = 8.06 + 2.81 ind/ha) (t-test = 5.247,
total number of mature oocytes in both ovaries and measured t = <0.001, n = 12). The relationship between the accumulated
the diameter of ten ovarian oocytes from each individual female rainfall of the sampling period in each month (p = 0.01) and tem-
using digital calipers (to the nearest 0.1 mm). We estimated female perature (p = 0.04) was significantly related with corresponding
reproductive effort by dividing the total mass (g) of eggs by the density of individuals active in that particular month (Multiple
total female body mass (g) including egg mass (Prado et al. 2000). Regression Analysis; F2-9 = 10.328; R2 = 0.695; p = 0.005; n = 12;
We did not perform a regression analyses between female body Density = -15.156+0.115*Rainfall+0.636*Temperature) (Figs 2, 3).
size (SVL mm) and the respective number of oocytes due to the In contrast, the accumulated humidity of the sampling period in
small sample size of gravid females (N = 4). We calculated an egg each month was not significantly related to the corresponding
diameter effort index and a number of oocytes effort index by density of active individuals in that particular month (F1-10 =
dividing the mean egg diameter and the mean number of oocytes, 0.083; R2 = 0.008; p = 0.77; n = 12).
respectively, by the mean SVL. The results are represented as the In relation to daily activity, the first individuals were found
mean ± SD and the range of data, the smallest and the largest num- active at dusk, from 06:00 pm, period at which we registered
ber. Voucher specimens of A. brunoi are deposited in the Museu the highest number of individuals. Then, the number of active
Nacional do Rio de Janeiro (MNRJ) under the voucher numbers individuals decreased steadily till 22:00. Before 06:00 pm and
Linhares, MNRJ 91008, 91009, 91010, 91011, 91012, 91013, after 10:00 pm no individuals of A. brunoi were found (Fig. 4).
91014, 91015, 91016, 91017, 91018, 91019, 91020, 91021, 91022. In relation to use of the microhabitat, A. brunoi (n = 51)
used seven different types of microhabitats in the forest, tree-
RESULTS trunks (51%; n = 26) and lianas (23.5%; n = 12) being the most
frequent microhabitats used (Fig. 5, Suppl. material 1: Table S1).
We recorded a total of 77 individuals of A. brunoi, all of Individuals were found perched from 10 to 500 cm above the
them by visual encounters, in the ombrophilous forest. Treefrogs ground with a median perch height of 40 cm (first quartile = 20
occurred in all months throughout the study, except July and cm, third quartile = 100 cm, n = 77).
September 2015, when no individuals were found. The abun- We analyzed the stomach content of 15 A. brunoi indi-
dance of individuals varied consistently throughout the year, viduals (8 males and 7 females) (x = 54,4 ± 6,8; 46.0–66.0 mm
with most individuals active during the rainy season (October SVL; 5.5–46.0 g) and, of these, three stomachs were empty.
to March) (n = 62; 80.6% of all individuals recorded) compared Aparasphenodon brunoi consumed nine different types of prey in
with that in the dry season (April to September) (N = 15; 19.4%). its diet (Table 1). The most representative were Orthoptera (20%)
The estimated density of A. brunoi for the area varied markedly and Acari (16%). However, Phasmatodea dominated in volume

2 3
Figures 2–3. Results of Multiple Regression Analysis between (2) the accumulated rainfall of the sampling period in each month (June 2015
– July 2016) and (3) temperature with corresponding density of active individuals of Aparasphenodon brunoi in the Vale Natural Reserve,
municipality of Linhares, Espírito Santo, Southeastern Brazil (Density = -15.156+0.115*Rainfall+0.636*Temperature).

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 Ecology of Aparasphenodon brunoi in the Atlantic Rainforest Biome

4 5
Figures 4–5. Activity and microhabitat use of Aparasphenodon brunoi: (4) Number of individuals of A. brunoi (N = 77) recorded between
11:00 am and 11:00 pm in transects in the Vale Natural Reserve (VNR), municipality of Linhares, Espírito Santo, Southeastern Brazil).
(5) Use of natural microhabitats by individuals of A. brunoi (N = 51) in the VNR. (H) On herbaceous plant, (TF) on a fallen tree trunk, (L)
on liana, (TT) on a tree trunk, (TR) on a tree root, (PL) on a palm leaf, or in a (HTT) hollow in a tree trunk.

Table 1. Diet of Aparasphenodon brunoi at the Vale Natural Reserve, 1.34 ± 0.38 mm3. The average total oocyte mass was 1.8 ± 0.7
north of Espírito Santo, Brazil. Number (N), volume (V mm3), fre- g (0.8–2.4_ g; n = 4) (Suppl. material 2: Table S2). The average
quency (F) and Importance index (lx) of prey categories. U.A.R = female reproductive effort was 7.0 ± 2.0% (4–9%, n = 4). The
unidentified arthropod remains. eggs diameter effort index was 2% and the number of oocytes
effort index was 1.4 oocytes/mm.
Gut Contents N (%) V (%) F (%) Ix
Arachnida
DISCUSSION
Aranae 2 (8) 314.3 (5.48) 1 (6.67) 20.15
Acari 4 (16) 0.06 (0.001) 3 (20) 36.00 Our data indicated that A. brunoi is an essentially noc-
Insecta turnal treefrog species as most anurans (Duellman and Trueb
Orthoptera 5 (20) 1008.57 (31.51) 3 (20) 71,51 1994), which is active in the first hours of the night. The species
Phasmatodea 1 (4) 1822.21 (31.75) 1 (6.67) 42.42 is active throughout the year but with a higher intensity from
Isoptera 1 (4) 0.30 (0.01) 1 (6.67) 10.68 November to March, coinciding with the rainy season in the
Lepidoptera 1 (4) 1117.61 (19.47) 1 (6.67) 30.14 area. The density of individuals during the wet season was con-
Hymenoptera (ants) 1 (4) 0.20 (0.004) 1 (6.67) 10.67 siderably higher (4.7 times higher) than that recorded during
Coleoptera 1 (4) 157.72 (2.57) 1 (6.67) 13.24 the dry season. In fact, the only months which we did not find
Larvae 2 (8) 245.04 (4.27) 2 (13.33) 25.6 active individuals (July and September) were months of the dry
Plant Remains 7 (28) 53.12 (0.93) 7 (46.67) 75.6 season in the area. A. brunoi activity (80.6%) occurred mostly
U.A.R – 220.293 (3.84) – – during the wet season. Also, the amount of rainfall accumulated
Total 25 (100) 5739.42 (100) 21 – during sampling period interacted with temperature to explain
the number of individuals of A. brunoi active throughout the
year. All these data together reinforce that annual activity of A.
(31.7%) followed by Orthoptera (31.5%), and Orthoptera (20%) brunoi predominates during the wet season in the ombrophi-
and Acari were the most frequent, with the same percentage lous forest. Although in the Restinga environment of Praia da
(20%) and Larvae represented 13.3% of frequency (Table 1). Neves (Espírito Santo state) Teixeira et al. (2002) recorded some
In relation to the index of relative importance (Ix), Orthoptera individuals of this species in some months of both dry and wet
dominated (71.51%) followed by Phasmatodea (42.42%). The seasons. At the restinga of Barra de Maricá (Rio de Janeiro state)
relationship between mean prey volume and treefrog JW was activity of this treefrog was restricted to months of the rainy
significantly related (F1-13 = 8.388; R2 = 0.392; p = 0.012; n = 15). season (Britto-Pereira et al. 1988). This tendency of increased
The mean number of oocytes (± 1 SD) per female was activity during the rainy season in the restinga environment
900.8 ± 358.1 (535–1338; n = 4), with 455.8 ± 218.4 oocytes may result from the fact that this season provides more source
in the left ovary (183–641) and 445 ± 182.5 oocytes in the of humidity to A. brunoi. The importance of humidity to favor
right ovary (320–715; n = 4). The mean oocyte diameter was activity in many frog species is well known and mostly results
1.36 ± 0.13 mm (1.22–1.52 mm; n = 40) and mean volume was from their permeable skin (and associated risks of desiccation)

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 L. Gomez-Mesa et al.

and the need of humidity for reproduction (Duellman and Trueb tors which do not chew their prey and are limited by gape size
1994). This may be the reason that in restinga habitats, an envi- (Lima and Moreira 1993, Maia-Carneiro et al. 2013). The low
ronment characterized by low availability of free water and high amount of plant matter in the frog’s diet probably corresponds
temperatures (Silva et al. 2011), A. brunoi tend to live relatively to plant parts ingested during attempts to capture prey, as has
restricted to bromeliads using the water stored inside the tank been suggested also for the diet of many other frog species (e.g.
of these plants as source of moisture (Britto-Pereira et al. 1988, Martins et al. 2010, Machado et al. 2016).
Teixeira et al. 2002). In restinga habitats, during diurnal period Reproductive data showed that ovigerous females of A.
(the hottest one), individuals of A. brunoi remain inside the brunoi produce on average about 900 oocytes per reproductive
tank of bromeliads whereas nocturnally they remain frequently event with a reproductive effort of about 7%. This relatively
outside these plants, on leaves of bromeliads and some other high number of oocytes produced by reproductive event may be
plants and trunks (Sazima and Cardoso 1980, Schineider and related to the relatively large body size of this arboreal treefrog.
Teixeira 2001, Mesquita et al. 2004, Sluys et al. 2004). Conversely, The diameter of each egg was relatively small (x = 1.36 ± 0.13
in the ombrophilous forest of the VNR, our data indicated that mm) when compared to the diameters of the eggs of other
A. brunoi used seven different types of microhabitats where it treefrogs, such as Hypsiboas faber (1.92 ± 0.15 mm), Aplastodiscus
perches preferentially about 1 m above ground, the preferred eugenioi (2.31 ± 0.22 mm) and Phasmahyla gutatta (2.40 ± 0.25
microhabitats for this species in the forest were tree trunks and mm) (Hartmann et al. 2010), and may result from a trade-off
lianas and coincidently, not bromeliads. We believe that the between number and size of oocytes produced in which females
increased moisture and milder environmental temperatures of produce large clutches with smaller eggs, a reproductive strategy
the ombrophilous forest favors a wider range of microhabitats for female A. brunoi in the ombrophilous forest (an interesting
and allows the frogs to remain active throughout the year. Inter- issue to compare to populations in restinga environments).
estingly, from the 77 A. brunoi individuals recorded during our We conclude that A. brunoi is a nocturnal arboreal treefrog,
study, not a single frog was associated with bromeliads, although active throughout the year but having increased activity during the
these plants are frequent and abundant in the VNR, especially in wet season, resulting from the large amount of rain. In the forest,
the non-forest vegetation types (Siqueira et al. 2014, pers. obs. of the treefrog tend to perch mainly on tree-trunks and lianas about
authors). This is suggestive that the observed differences in the 1 m above ground (instead of using predominantly bromeliads as
use of bromeliads as microhabitats among forested and restinga in restingas), where it feeds preferably on relatively large bodied
environments may be associated with the role of these plants arthropod prey. The reproductive strategy for females of this
as a source of moisture for these treefrogs in restinga habitats, comparatively large arboreal treefrog in the ombrophilous forest
a question that remains to be investigated. is to produce a large amount of relatively small-sized eggs. When
Our data indicated that in the ombrophilous forest A. living in the ombrophilous forest A. brunoi may change some
brunoi is an arthropod predator, with Orthoptera, Phasmato- features of its ecology (e.g. marked difference in the use of bro-
dea, and Lepidoptera being the most important prey items in meliads) compared to when living in restinga habitats. Our study
its diet. In restinga areas, a diet composed by arthropods with is the first to gather information on the ecology of this treefrog
consumption of Insecta, Arachnida and Myriapoda has aslo been in ombrophilous forest of the Atlantic Rainforest Biome of Brazil.
reported (Teixeira et al. 2002, Mesquita et al. 2004, Sluys et al.
2004). The relatively wide array of prey types consumed indicates ACKNOWLEDGMENTS
that A. brunoi is not a selective species and the consumption of
relatively active prey can indicate ambush foraging behavior This study is part of the results of the “PPBio Mata Atl­
in this species. This can be advantageous to some species that ântica”, a program of the Ministry of Science, Technology and
have low foraging velocity and thus, a comparatively lower Innovation (MCTI). The authors benefitted from grants provided
intensity than active foraging species (Strussman et al. 1984). to HGB (process 307715/2009-4 and 457458/2012-7) and to
The inclusion of some relatively large preys as Orthoptera, CFDR (304791/2010-5, 470265/2010-8 and 302974/2015-6)
Phasmatodea and Lepidoptera in the diet can be suggestive of from Conselho Nacional de Desenvolvimento Científico e
a specific energetic need by this treefrog. Probably the relative Tecnológico (CNPq) and through “Cientistas do Nosso Estado”
preference of arthropods of a relatively large size may be related Program from FAPERJ to CFDR (processes E-26/102.765.2012 and
to the energetic balance of this relatively large-bodied arboreal E-26/202.920.2015) and to HGB (process E-26/103.016.2011).
treefrog (costs and benefits of ingesting large prey). This idea LGM thanks to the program “Becas Iberoamérica, Estudiantes
is also supported by our data that shows that about 40% of de Grado. Santander Universidades”. JPR and ACF received
the variation in prey volume (size) ingested was explained by fellowships for master and PhD respectively from Coordenação
frog mouth size, an indicative that as the treefrog increases in de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). The
size tend to prey on larger prey (volumes), probably to keep a ICMBio provided the permit for the development of the study
positive energy balance. Also, a positive relationship between (46327-3) and the Vale Natural Reserve the permit to research
frog mouth size and ingested prey size is expected for preda- in the Reserve.

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 Ecology of Aparasphenodon brunoi in the Atlantic Rainforest Biome

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 L. Gomez-Mesa et al.

Ruas DS, Mendes CVM, Del-Grande ML, Solé M (2013) Aparasphe- Supplementary material 1
nodon brunoi Miranda-Ribeiro, 1920 (Anura: Hylidae): Distribu- Table S1. Summary of observations of Aparasphenodon
tion extension and geographic distribution map for Bahia state, brunoi in Vale Natural Reserve, municipality of Linhares, state
Brazil. Check List 9: 858–859. https://doi.org/10.15560/9.4.858 of Espírito Santo, Southeastern Brazil.
Sazima I, Cardoso AJ (1980) Notas sobre a distribuição de Cory- Authors: Laura Gomez-Mesa, Juliane Pereira-Ribeiro, Atilla
thomantis greeningi Boulenger, 1896 e Aparasphenodon brunoi C. Ferreguetti, Marlon Almeida-Santos, Helena G. Bergal-
Miranda-Ribeiro, 1920 (Amphibia, Hylidae). Iheringia, Série lo, Carlos F.D. Rocha
Zoologia, 55: 3–7. Data type: (measurement/occurence/multimedia/etc.)
Schineider JAP, Teixeira RL (2001) Relacionamento entre anfíbios Copyright notice: This dataset is made available under the
anuros e bromélias da restinga de Regência, Linhares, Espírito Open Database License (http://opendatacommons.org/licenses/
Santo, Brasil. Iheringia, Série Zoologia, 91: 41–48. https://doi. odbl/1.0/). The Open Database License (ODbL) is a license agree-
ment intended to allow users to freely share, modify, and use this
org/10.1590/S0073-47212001000200005
Dataset while maintaining this same freedom for others, provided
Silva HRD, Carvalho ALGD, Bittencourt-Silva GB (2011) Se- that the original source and author(s) are credited.
lecting a Hiding Place: Anuran Diversity and the use of
Link: https://doi.org/10.3897/subtbiol.34.20477.suppl1
Bromeliads in a Threatened Coastal Sand Dune Habitat in
Brazil. Biotropica 43: 218–227. https://doi.org/10.1111/j.
1744-7429.2010.00656.x
Supplementary material 2
Silva-Soares T, Hepp F, Costa PN, Luna-Dias C, Gomes MR, Car- Table S2. Data of Aparasphenodon brunoi individuals col-
valho-e-Silva AMPT, Carvalho-e-Silva SP (2010) Anfíbios anu- lected outside plot areas for diet and reproductive aspects
ros da RPPN Campo Escoteiro Geraldo Hugo Nunes, Muni- analysis.
cípio de Guapimirim, Rio de Janeiro, Sudeste do Brasil. Biota Authors: Laura Gomez-Mesa, Juliane Pereira-Ribeiro, Atilla
Neotropica 10: 225–233. https://doi.org/10.1590/S1676- C. Ferreguetti, Marlon Almeida-Santos, Helena G. Bergal-
06032010000200025 lo, Carlos F.D. Rocha
Sluys MV, Rocha CFD, Hatano FH, Boquimpani-Freitas L, Marra RV Data type: (measurement/occurence/multimedia/etc.)
(2004) Anfíbios da restinga de Jurubatiba: composição e his- Copyright notice: This dataset is made available under the
Open Database License (http://opendatacommons.org/licenses/
tória natural. In: Pesquisas de longa duração na Restinga de
odbl/1.0/). The Open Database License (ODbL) is a license agree-
Jurubatiba: ecologia, história natural e conservação. RiMa, São ment intended to allow users to freely share, modify, and use this
Carlos, 165–178. Dataset while maintaining this same freedom for others, provided
Siqueira GS, Kierulff MCM, Alves-Araújo A (2014) Florística das that the original source and author(s) are credited.
plantas vasculares da Reserva Natural Vale, Linhares, Espírito Link: https://doi.org/10.3897/subtbiol.34.20477.suppl1
Santo, Brasil. Ciência e Ambiente 49: 67–129.
Strussman C, Vale MBR, Meneghini MH, Magnusson WE (1984)
Diet and foraging mode of Bufo marinus and Leptodactylus Submitted: 23 November 2016
ocellatus. Journal of Herpetology 18: 138–146. https://doi. Received in revised form: 27 March 2017
org/10.2307/1563741 Accepted: 11 May 2017
Teixeira RL, Schineider JAP, Almeida GI (2002) The occurrence of Editorial responsibility: Felipe Grazziotin
amphibians in bromeliads from a Southeastern Brazilian rest-
inga habitat, with special reference to Aparasphenodon brunoi
(Anura, Hylidae). Brazilian Journal of Biology 62: 263–268. Author Contributions: LGM, JPR and ACF collected the data; LGM,
https://doi.org/10.1590/S1519-69842002000200010 JPR and MAS did the analysis of diet and reproductive aspects; HGB
Wogel H, Weber LN, Abrunhosa PA (2006) The tadpole of the casque- helped with the statistical analysis; CFDR and all authors participated
headed frog, Aparasphenodon brunoi Miranda-Ribeiro (Anura: in the writing and review of the manuscript.
Hylidae). South American Journal of Herpetology 1: 54–60. https:// Competing Interests: The authors have declared that no competing
doi.org/10.2994/1808-9798(2006)1[54:TTOTCF]2.0.CO;2 interests exist.

8 / 8 ZOOLOGIA 34: e20477 | DOI: 10.3897/zoologia.34.e20477 | September 1, 2017