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Ecological aspects of the casque-headed frog Aparasphenodon brunoi (Anura, Hylidae) in a Restinga habitat in southeastern Brazil

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Ecological aspects of the casque-headed frog Aparasphenodon brunoi (Anura, Hylidae) in a Restinga habitat in southeastern Brazil. We describe some aspects of the ecology of Aparasphenodon brunoi, a species associated with bromeliads. We comment on the relationships of this species with bromeliad size, microhabitat use, diet and sexual dimorphism. This study was conducted on a Restinga habitat near Presidente Kennedy, state of Espírito Santo, southeastern coast of Brazil. When the animals were found inside the bromeliads, we measure bromeliad and head size of frogs. We analyzed stomach contents and determined the sex and reproductive condition. We found 17 individuals (58.6%) in bromeliad leafs, six (20.7%) in Cactaceae, three (10.3%) in liana and three (10.3%) on trunks. The correlation between head measurements and bromeliad size were high, indicating that animals apparently use bromeliads based on their size, which could be related to the minimization of water loss. The most common prey items were beetles, ants, and insect larvae, suggesting that the species is relatively generalist in prey consumption. Aparasphenodon brunoi showed significant sexual size and shape dimorphism with females having larger bodies than males (size) and females having tibia, eye diameter and SVL larger than males (shape), but larger sample size and more detailed ecological and life history data are needed to elucidate the factors that have led to sexual size dimorphism.
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Phyllomedusa- 3(1), September 2004
51
Ecological aspects of the casque-headed frog
Aparasphenodon brunoi (Anura, Hylidae) in a
Restinga habitat in southeastern Brazil
Daniel Oliveira Mesquita1, Gabriel Corrêa Costa2 and Mariana G. Zatz3
Universidade de Brasília, 70910-900, Brasília, DF, Brazil.
1Pós-graduação em Biologia Animal, Instituto de Ciências Biológicas. E-mail: danmesq@unb.br.
2Pós-graduação em Ecologia, Instituto de Ciências Biológicas. E-mail: costagc@unb.br.
3Colecão Herpetológica da UnB – CHUNB, Departamento de Zoologia, Instituto de Ciências Biológicas. E-mail:
mariana@unb.br.
Phyllomedusa 3(1):51-59, "
© 2004 Melopsittacus Publicações Científicas
ISSN 1519-1397
Received 6 March 2004.
Accepted 4 August 2004.
Distributed 30 September 2004.
Abstract
Ecological aspects of the casque-headed frog Aparasphenodon brunoi (Anura,
Hylidae) in a Restinga habitat in southeastern Brazil. We describe some aspects
of the ecology of Aparasphenodon brunoi, a species associated with bromeliads. We
comment on the relationships of this species with bromeliad size, microhabitat use,
diet and sexual dimorphism. This study was conducted on a Restinga habitat near
Presidente Kennedy, state of Espírito Santo, southeastern coast of Brazil. When the
animals were found inside the bromeliads, we measure bromeliad and head size of
frogs. We analyzed stomach contents and determined the sex and reproductive
condition. We found 17 individuals (58.6%) in bromeliad leafs, six (20.7%) in
Cactaceae, three (10.3%) in liana and three (10.3%) on trunks. The correlation between
head measurements and bromeliad size were high, indicating that animals apparently
use bromeliads based on their size, which could be related to the minimization of water
loss. The most common prey items were beetles, ants, and insect larvae, suggesting
that the species is relatively generalist in prey consumption. Aparasphenodon brunoi
showed significant sexual size and shape dimorphism with females having larger bodies
than males (size) and females having tibia, eye diameter and SVL larger than males
(shape), but larger sample size and more detailed ecological and life history data are
needed to elucidate the factors that have led to sexual size dimorphism.
Keywords: Anura, Hylidae, Aparasphenodon brunoi, casque-headed frog, diet,
microhabitat use, bromeliads, sexual dimorphism.
Introduction
Many species of invertebrates and vertebra-
tes use bromeliads for foraging, reproduction
and escaping from predators. Among vertebra-
tes, amphibians and reptiles are the most
common inhabitants. For example, the lizard
Mabuya macrorhyncha preys on animals that
live between bromeliad leaves of Neoregelia
(Vrcibradic and Rocha, 1996), and the frog
Phyllodytes luteolus carries out its entire life
cycle inside bromeliads (Teixeira et al. 1997,
Eterovick 1999).
Phyllomedusa- 3(1), September 2004
52
Aparasphenodon are tree frogs
characterized by a strongly ossified skull, which
gives them the common name “casque-headed
frog” (Pombal 1993). The ossified skull appears
to have evolved independently six times in
hylids, apparently as an adaptation to similar
habitats where water is scarce (Trueb 1970).
Several genera of casque-headed frogs occur in
South America, including Osteocephalus,
Phrynohyas, Trachycephalus, Corythomantis,
Aparasphenodon and some species of Scinax
and Hyla. Aparasphenodon may be closely
related to Corythomantis (Trueb 1970). The
genus Aparasphenodon consists of three
species, ranging from southern Brazil to the
Orinoco river basin in northern Venezuela
(Argôlo 2000, Frost 2002). Aparasphenodon
brunoi Miranda-Ribeiro, 1920 occurs in coastal
areas of São Paulo, Rio de Janeiro, Espírito
Santo and Bahia states and continental areas of
the Parque Estadual do Rio Doce, in Minas
Gerais state (Feio et al. 1998, Argôlo 2000).
The species is relatively common in Restinga
habitats, which are white sand dunes partially
covered by herbaceous plants and shrubs. This
vegetation forms dispersed islands of vegetation
(Suguio and Tessler 1984), where the frog is
usually found associated to bromeliads.
Bromeliads are abundant in the Restinga and
occur on many kinds of substrates, including
soils with organic material, sandy soils, and tree
trunks (Cogliatti-Carvalho et al. 2001). The
leaves of bromeliads typically form a rosette,
within which water accumulates. The shape and
size of the bromeliads determine the amount of
water that can accumulate (Leme 1984). This
frog species is highly associated with
bromeliads and reaches 80 mm in snout vent
length (SVL) (Feio et al. 1998), but little is
known about their ecology.
Herein, we describe some aspects of the
ecology of Aparasphenodon brunoi from a
Restinga in the southern Espírito Santo state,
southeastern Brazil. We address the following
questions: (1) What are the patterns of habitat
and microhabitat use? (2) Is there a relationship
between the size of bromeliads and frog size?
(3) Is there a significant sexual dimorphism? (4)
What are the most important prey items?
Material and Methods
The study was performed in a gradient that
varies from a Restinga (21°17’59’’S,
40°57’30’’W) to a forested area within Restinga
(21°17’40’’S, 40°57’35’’W), near Presidente
Kennedy, Espírito Santo state, on the
southeastern coast of Brazil, from 20 to 27
September 2001. Aparasphenodon brunoi
(Figura 1) was collected during the day by the
Restinga shrubs and by searching bromeliads.
The forest site was visited during the day and
night. Individuals were located visually and by
their calls. Microhabitat categories, including
branch, liana, Cactaceae, trunk, bromeliad
leaves, and inside bromeliads were recorded for
29 individuals as the original position that it was
found at first sight. The height (in cm) of each
individual above the ground was recorded. All
frogs were killed in 10% alcohol solution and
preserved in 10% formalin. Specimens were
deposited in the Coleção Herpetológica da
Figure 1 - Aparasphenodon brunoi from Presidente
Kennedy (ES) (sex unknown). Photo: Adrian
A. Garda.
Mesquita et al.
Phyllomedusa- 3(1), September 2004
53
Universidade de Brasília (CHUNB 15935,
15937–15940, 24369, 24781–24800, 24909–
24945).
The following measurements were taken
only on frogs found inside the bromeliads and
of the correspondent plant which they were
associated: snout-vent length (SVL), head length
(from the tip of the snout to the commissure of
the mouth), head width (at its broadest point)
and head height (at its highest point) (N=10)
(using a Mitutoyo® digital caliper, to the nearest
0.01 mm), plant height, width between external
leaves, and diameter of the bromeliad rosette
(using a ruler and a measuring tape). Canonical
correlation analysis was used to investigate the
relationship between frog size and bromeliad
size.
For the analysis of feeding habits we
removed the stomachs (N=63) and identified
prey items to order. We recorded the length and
width (to the nearest 0.01 mm) of intact prey
with Mitutoyo® digital calipers, and estimated
prey volume (V) as an ellipsoid:
,
223
42
π= lw
V
where w is prey width and l is prey length.
We calculated the numeric and volumetric
percentages of each prey category for individual
frogs and for pooled stomachs. To investigate
the relationship between prey size and frog head
measurements, we used a canonical correlation
analysis with two sets of variables: maximum
prey length and width vs. frog head width,
height, and length.
We determined sex and reproductive condi-
tion of each frog using direct observation of
gonads. The females were considered repro-
ductive when their ovaries were extremely
convoluted and enlarged. We considered as
reproductive males, individuals that have
completely evident vocal sac. We recorded for
all individuals, collected inside and outside of
bromeliads and previously deposited in CHUNB
(N=63), the following morphometric variables:
SVL, head width, height, and length; tibia,
forearm and foot length; and tympanum and eye
diameter. We considered the SVL of the smaller
reproductive male and female as the SVL of
sexual maturity; all individuals with SVL equal
or superior to that ones were considered adults.
We log-transformed (base 10) all morpho-
metric variables prior to analyses to meet the
requirements of normality (Zar 1998). To
partition the total morphometric variation
between size and shape variation, we defined
body size as an isometric size variable (Rohlf
and Bookstein 1987) following the procedure
described by Somers (1986). We calculated an
isometric eigenvector defined a priori with
values equal to p-0.5, where p is the number of
variables (Jolicoeur 1963). Next, we obtained
scores from this eigenvector, hereafter called
body size, by post-multiplying the n by p matrix
of log-transformed data, where n is the number
of observations, by the p by 1 isometric
eigenvector. To remove the effects of body size
from the log-transformed variables, we used
residuals of regression between body size and
each shape variable. To test the null hypothesis
of no difference between sexes, we conducted
separate analyses of variance on body size
(ANOVA) and the shape variables (MANOVA)
of adult individuals.
We carried out statistical analyses using
SYSTAT 9.0 for Windows with a significance
level of 5% to reject null hypotheses.
Throughout the text, means appear ± 1 SD. All
measures are in mm.
Results
We collected, during the night, a total of 29
active individuals, being 17 (58.6%) in
bromeliad leaves, six (20.7%) in cactaceae,
three (10.3%) in lianas and three (10.3%) in
trunks (Figure 2). The animals were at mean
height of 65.7 cm (25-210 cm). During the day,
the individuals were found only inside the
bromeliads (N=10). In this period their activity
Ecology of the casque-headed frog Aparasphenodon brunoi (Anura, Hylidae)
Phyllomedusa- 3(1), September 2004
54
was restricted to emitting call from the interior
of bromeliads.
The correlation between the measures of the
body and the measures of the bromeliads were
high. The first and second canonic variables of
the body measures show that the three measures
have equal influence in the composition of the
canonic variable. The first canonic variable of
the bromeliad measurements gave more
emphasis in the bromeliad width and height. The
first canonical correlation was 0.972, having
statistical significance (p=0.022), showing
association between the body measures of
Aparasphenodon brunoi and the bromeliad
measurements (Table 1).
We analyzed 85 stomachs and 26% (22)
were empty. We found 10 prey categories, being
more frequent beetles (56.1%) and ants (16.8%).
Considering the number of items per stomach,
the diet consisted mainly of beetles (44.0%) and
ants (17.1%). By volume, beetles were the most
important prey item (60.5%), followed by insect
larvae (16.5%) and ants (16.1%) (Table 2). The
Figure 2 - Frequency distribution of Aparasphenodon
brunoi according to microhabitat categories.
Sample sizes are indicated at the top of the
bars.
Standardized canonical coefficients for the body measurements
First canonical variable Second canonical variable
Snout-vent length 0.837 0.529
Head height 0.814 0.340
Head length 0.887 0.427
Standardized canonical coefficients for the bromeliad measurements
First canonical variable Second canonical variable
Bromeliad height 0.950 0.234
Bromeliad width 0.964 0.232
Cup diameter 0.643 0.734
Canonical variables Canonical correlation F p
I 0.972 3.94 0.022
II 0.684 1.22 0.361
Table 1 - Canonical correlation among bromeliad and body measurements of Aparasphenodon brunoi (N=10).
results based on pooled stomach were similar.
Numerically, beetles were most important
(38.1%), followed by ants (27.4%), and
volumetrically, beetles were dominant (54.0%),
followed by insect larvae (20.0%) (Table 2).
Mesquita et al.
Phyllomedusa- 3(1), September 2004
55
Occurrence Stomach Means Pooled Stomachs
Prey categories f f% N %N Vol. (mm
3
) %Volume N %N Vol. (mm
3
) %Vol.
Aranae 1 2.44 0.02 ± 0.16 2.5 ± 15.81 819.36 ± 5246.49 4.17 ± 20.41 1 1.19 33593.91 7.79
Coleoptera 23 56.10 0.78 ± 0.88 43.96 ± 43.12 5680 ± 8982.79 60.48 ± 44.40 32 38.10 232915.50 54.03
Formicidae 11 16.83 0.561 ± 1.76 17.08 ± 31.01 798.95 ± 2566.64 16.12 ± 31.70 23 27.38 32756.85 7.60
Gastropoda 2 4.88 0.05 ± 0.22 1.88 ± 8.75 1105.20 ± 7076.72 2.75 ± 13.50 2 2.38 45313.10 10.51
Orthoptera 5 12.20 0.15 ± 0.42 7.44 ± 23.53 ––6 7.14 ––
Isoptera 3 7.32 0.195 ± 0.95 4.64 ± 17.16 ––8 9.52 ––
Insect larvae 4 9.76 0.10 ± 0.30 7.50 ± 24.15 2109.00 ± 8998.80 16.48 ± 37.64 4 4.76 86468.96 20.06
Non identified 6 14.63 0.15 ± 0.36 12.50 ± 31.52 ––6 9.52 ––
Plant material 1 2.44 0.02 ± 0.16 1.25 ± 7.91 ––1 1.19 ––
Insect egg 1 2.44 0.02 ± 0.16 1.25 ± 7.91 ––1 1.19 ––
Table 2. Diet composition of Aparasphenodon brunoi (N= 63).
Table 3. Canonical correlation among prey and head measurements of Aparasphenodon brunoi (N=26).
Standardized canonical coefficients for the head measurements
First canonical variable Second canonical variable
Head width 0.003 0.154
Head length 0.099 0.186
Standardized canonical coefficients for the prey measurements
First canonical variable Second canonical variable
Maximum prey width 0.077 0.038
Maximum prey length 0.020 0.077
Canonical variables Canonical correlation F p
I 0.330 0.70 0.594
II 0.094 0.21 0.654
The correlation between the head measure-
ments and the prey measurements were low. The
first canonical variable of the head measure-
ments showed that both measures have equal
influence on the composition of the canonical
variable while the second variable showed a
contrast between the head width and height. The
first canonical variable of the measurements of
the prey represents a contrast between the
maximum width and weight of the prey. The
first canonical correlation was 0.330 but it has
no statistical significance, showing no asso-
ciation between head and prey measurements
(Table 3).
Ecology of the casque-headed frog Aparasphenodon brunoi (Anura, Hylidae)
Phyllomedusa- 3(1), September 2004
56
The smallest adult female measured 56.32
mm SVL, whereas the smallest adult male was
48.88 mm. The largest male measured 62.42 mm
and the largest female measured 81.24 mm. We
found significant differences between sexes in
body size (ANOVA F1,25= 9.743; p=0.005). In
addition, we found significant differences
between the sexes in shape variables (MANOVA
Wilks Lambda = 0.444; p=0.032). To determine
which of the shape variables contributed most
to sexual dimorphism, we performed a stepwise
discriminant analysis (Tabachnick and Fidell
1996). Three shape variables were selected as
the most powerful discriminators of the two
sexes, correctly classifying 78% of individuals
(Table 4). Tibia length was the first variable
selected, correctly classifying 74% of indivi-
duals, followed by eye and tympanum diameter.
To determine whether important variables were
excluded from the analysis due to inter-
correlation with tibia length, we excluded tibia
length and repeated the analysis. Eye diameter
was then selected first, correctly classifying 70%
of the individuals, followed by SVL and
tympanum diameter. We repeated the analysis
once more with the exclusion of tibia length and
eye diameter and this time only SVL was
selected. These results indicate that besides tibia
length, eye and tympanum diameter, SVL is also
important in stating differences between the
sexes, with females having tibia, eye diameter
and SVL larger than males (Table 5).
Discussion
Aparasphenodon brunoi shows higher
Step Variable entered R2Wilks Lambda p < Error-rate
1 Adjusted tibia length 0.13 0.87 0.06 0.26
2 Adjusted eye diameter 0.22 0.68 0.009 0.29
3 Adjusted tympanum 0.16 0.57 0.004 0.22
Table 4 - Stepwise discriminant analysis of shape variables of Aparasphenodon brunoi. Error-rate indicates posterior
probability error-rate estimates based on cross-validation.
activity during the night, being easily found in
the Restinga Forest, outside the bromeliads.
However, in most cases, they were found within
the bromeliad leaves. Like most vertebrates,
anuran diurnal activities are highly affected by
requirements of food, mate, and shelter to avoid
predation and maintain ideal physiological
conditions, because they have a very permeable
skin, being highly susceptible to water loss by
evaporation (Hodgkison and Hero 2001).
Therefore, most anurans are typically nocturnal
(Duellman and Trueb 1994). In the case of A.
brunoi, since bromeliads retains a large amount
of water and the air humidity in the forest is
usually stable and high, these animals can show
diurnal activity, even in the sun (Silva et al.
1988). Although unusual, diurnal activities have
been reported in many anurans species, such as
Litoria nannotis (Hodgkison and Hero 2001),
dendrobatids (Zug et al. 2001), some
leptodactylids (Kwet and Di-Bernardo 1999,
Zug et al. 2001), and others (Duellman and
Trueb 1994). In this study, we observed diurnal
activity in A. brunoi in moisture days, when we
noticed some individuals calling from inside
bromeliads. However, no individual was
observed outside the bromeliads during the day.
We found a significant correlation between
frog head and bromeliad size. It has been
showed that the phragmatic behavior in A.
brunoi effectively reduces evaporative water
loss (Andrade and Abe 1997). Our data suggest
that these animals are selecting bromeliads
based on size, which could be an effort to
minimize water loss. The annual precipitation in
Restinga is high, varying from 1100 to 1500 mm
Mesquita et al.
Phyllomedusa- 3(1), September 2004
57
(Louro and Santiago 1984), but the high
permeability of sandy soils reduces the water
availability. In addition, the shape of bromeliads
promotes the accumulation of water and the
head adjustment in the bromeliad rosette is
important to maintain ideal physiological
conditions.
Some groups of amphibians are considered
dietary specialists, for example ants are the
primary diet item of dendrobatids (Toft 1995).
However, this is not the case for other groups.
For example, Rana nigromaculata (Ranidae) is
generalist and eats a high variety of prey items
dependent more so with availability than
selectivity (Hirai and Matsui 1999). Rana
catesbeiana and R. clamitans, in Michigan, also
show a highly diverse diet, eating mainly
coleopterans, hemipterans and spiders (Werner
et al. 1995). In Argentina, the diet of Pseudis
paradoxa and Lysapsus limellus (Hylidae,
Pseudinae) primarily consists of other
amphibians, beetles, mosquitoes and
Osteichthyes fishes, respectively (Duré and Kehr
2001). In a study in the Restinga of Jurubatiba,
Rio de Janeiro state, southeastern Brazil,
Aparasphenodon brunoi ate mainly beetles (Van
Sluys et al. 2004). In a study in the same area,
based on the diets of 21 individuals, A. brunoi
ate mainly ants, cockroaches and grasshoppers
(Teixeira et al. 2002). Our study shows that A.
brunoi has a very diverse diet, eating mainly
beetles, insect larvae and ants. Based on
proportion of prey use, this species could be
considered a generalist; however data on
arthropod availability in the study area and the
relationship between availability and prey
Ecology of the casque-headed frog Aparasphenodon brunoi (Anura, Hylidae)
Table 5 - Summary statistics of morphometric characters of adult Aparasphenodon brunoi. Values indicate mean ± 1
standard deviation. Size-adjusted values (see text) are in parentheses. Values are in mm.
Males (N=14)
3.535 ± 0.078
55.239 ± 3.794
(-0.010 ± 0.018)
24.388 ± 1.225
(-0.005 ± 0.014)
32.971 ± 1.832
(0.011 ± 0.013)
19.841 ± 1.125
(-0.011 ± 0.019)
18.221 ± 1.168
(-0.000 ± 0.017)
4.135 ± 1.532
(-0.019 ± 0.096)
6.393 ± 0.323
(-0.002 ± 0.025)
24.680 ± 1.428
(-0.002 ± 0.019)
Females (N=14)
3.663 ± 0.125
65.176 ± 8.244
(0.015 ± 0.054)
28.459 ± 2.725
(0.016 ± 0.038)
35.635 ± 9.627
(-0.041 ± 0.232)
24.843 ± 9.382
(-0.014 ± 0.084)
20.938 ± 2.158
(-0.010 ± 0.045)
4.078 ± 0.281
(-0.006 ± 0.035)
6.736 ± 0.490
(-0.019 ± 0.024)
28.446 ± 2.723
(0.009 ± 0.041)
Character
Body size
Snout-vent length
Tibia length
Foot length
Head length
Head width
Tympanum diameter
Eye diameter
Forearm length
Phyllomedusa- 3(1), September 2004
58
selectivity are needed to support this statement.
Still, it will be necessary more samples throughout
the year to avoid the seasonality effects.
Several authors have indicated that
relationships between prey and head
measurements could be related to resource
partitioning between sexes and/or species
(Magnusson and Silva 1993, Van Sluys et al.
2001). Teixeira et al. (2002) did not find any
correlation between prey and body size,
however they did not use any statistical test to
support this evidence. In our study, based on a
canonical correlation, no significant relationship
between prey and head measurements was found
in Aparasphenodon brunoi. These relationships
are likely more related with resource
partitioning among species in an assemblage
rather than due to size variation within the same
species (Magnusson and Silva 1993).
Three main hypotheses have been proposed
to explain the existence of sexual dimorphism
in frogs. Several studies have found that when
females are larger than males there is a
significant relationship between female SVL and
clutch size (Kuramoto 1978, Kaplan 1980,
Duellman and Trueb 1994). We found statistical
differences in body size between sexes in A.
brunoi, with the females being larger than
males; however, we did not collect clutch size
data for A. brunoi, and we are thus unable to
access this hypothesis.
Another hypothesis to explain sexual
dimorphism could be related to male-male
competition for mates, with larger males
benefiting with this kind of dimorphism
(Duellman and Trueb 1994). Alternatively,
sexual size dimorphism can be a mechanism for
reducing intersexual competition for food
resources (Magnusson and Silva 1993, Van
Sluys et al. 2001), where the difference in the
head size between sexes leads to a difference in
prey size consumed by each sex. However the
canonical correlation between head and prey
size was not significant. Furthermore, this
pattern could be due to resource sharing among
species of an assemblage rather than difference
between sexes (Magnusson and Silva 1993). In
our study area, there are four other species that
use bromeliads in their life cycle (Hyla
albomarginata, Scinax altera, S. cuspidatus and
Trachycephalus nigromaculatus) (Teixeira et al.
2002), which could interact with and influence
A. brunoi ecology.
Teixeira et al. (2002) stated that sexual size
dimorphism occurred in A. brunoi with females
being larger than males; however their statistical
tests do not support this affirmation. Based on
univariate and multivariate analyses of variance
on a set of morphometric variables we found
sexual dimorphism in A. brunoi. Nevertheless,
a study including a larger sample size and more
detailed ecological and life history data are
needed to elucidate the factors that have led to
sexual size dimorphism.
Acknowledgements
We thank Alexandre Bamberg Araújo,
Mirella A. Kacinskis and Mariana F. P. de
Araújo for help with the fieldwork; Antônio
Sebben, Reuber A. Brandão, Janalee P.
Caldwell, Adrian A. Garda, Donald B. Shepard
and Alison M. Gainsbury for insightful
comments on a previous version of the
manuscript and for help in English. This work
was supported by a doctorates fellowship from
Coordenação de Aperfeiçoamento de Pessoal de
Nível Superior CAPES to DOM and by a
masters fellowship from Conselho Nacional de
Desenvolvimento Científico e Tecnológico
CNPq to GCC.
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Mesquita et al.
... Nyctimantis Boulenger, 1882 comprises seven species of Casque-headed treefrogs distributed in the Amazonian and Atlantic rainforests (Blotto et al. 2020). Nyctimantis brunoi (Miranda-Ribeiro, 1920) is the most well-known species of the genus, with several studies related to ecological issues (e.g., Trueb 1970, Andrade and Abe 1997, Teixeira et al. 2002, Mesquita et al. 2004, Wogel et al. 2006, Jared et al. 2015, Carmo and Woitovicz-Cardoso 2018, Murta-Fonseca et al. 2020). As in other species of the genus, N. brunoi as a eavi ossified s it crania crests rid es and an es r eb 1 . ...
... The species is endemic to Atlantic Forest morphoclimatic domains, occurring from the state of São Paulo to the state of Bahia (Frost 2021), and is relatively common in sandy coastal environments, being one of the anuran species most frequently recorded in this ecosystem in southeastern Brazil (Rocha et al. 2008). Although the taxon is found mainly associated with bromeliads (see Teixeira et al. 2002, Mesquita et al. 2004, it uses temporary swamps and periodica ooded areas for breedin and spawning during the rainy season (Freire et al. 2019). ...
... We categorized adults, juveniles, males, and females based on Mesquita et al. (2004). These categorizations were made through direct observation of gonads, vocal slits, nuptial pads and snout-vent length (SVL). ...
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In the present study we monitored a population of Nyctimantis brunoi, a species commonly found in restingas of southeastern Brazil. Field activities were carried out in the Parque Nacional da Restinga de Jurubatiba (PNRJ), a protected area located in the northern portion of the state of Rio de Janeiro. Specimens were sampled through a complete species inventory. We analyzed 218 individuals, 32 (14.7%) of which have anomalies. Additionally, a subsample of 15 specimens were radiographed to verify the occurrence of skeletal anomalies not externally detectable and to verify if the classification of anomalies attributed by means of external examination are detectable in the osteological structure of the specimen. There are 12 types of anomalies recognized in this population, three of them only detectable through internal investigation (radiography). We verified that most of anomalies externally detectable were correctly classified when compared to the osteological morphology of the radiographed specimens. Thus, in this investigation, the study of external malformations was capable to detect 60% of the types of anomalies. We conclude that further ecotoxicological and epidemiological studies of the population of N. brunoi in the PNRJ are necessary to establish the origins of anomalies in this species.
... Aparasphenodon brunoi Miranda-Ribeiro, 1920 is the most well-known taxon of the genus, with several studies focusing on its ecological and osteological aspects (e.g. Trueb, 1970;Andrade and Abe, 1997;Teixeira et al., 2002;Mesquita et al., 2004;Wogel et al., 2006;Jared et al., 2015;Carmo and Woitovicz-Cardoso, 2018). Sexual dimorphism in overall size and in some external characters (Teixeira et al., 2002;Mesquita et al., 2004), as well as ontogenetic variation on dermal bones (Trueb, 1970), have previously been reported in the literature for the species with the use of traditional morphometric analyses. ...
... Trueb, 1970;Andrade and Abe, 1997;Teixeira et al., 2002;Mesquita et al., 2004;Wogel et al., 2006;Jared et al., 2015;Carmo and Woitovicz-Cardoso, 2018). Sexual dimorphism in overall size and in some external characters (Teixeira et al., 2002;Mesquita et al., 2004), as well as ontogenetic variation on dermal bones (Trueb, 1970), have previously been reported in the literature for the species with the use of traditional morphometric analyses. ...
... Geometric Morphometrics offers precise morphological description and provides effective means for visualization, interpretation and communication of the results (Zelditch et al., 2004). Herein we aim to test two main hypotheses through the use of such technique: (1) There are both ontogenetic and static allometry in the head of Aparasphenodon brunoithis hypothesis is based on the fact that many studied vertebrates present conspicuous allometry in such region (Meyer, 1990;Zeffer et al., 2003;Monteiro et al., 2005;Ponssa and Vera Candioti, 2012;Prevosti et al., 2012;Murta-Fonseca and Fernandes, 2016;Murta-Fonseca et al., 2019); and (2) A. brunoi presents sexual dimorphism in head shape -we based this hypothesis considering that females and males tend to differ in size as well as other external characters (Teixeira et al., 2002;Mesquita et al., 2004). We believe that such morphological variation studies are extremely relevant to provide in-depth knowledge about the causes of taxa morphological complexity (Vukov et al., 2018a). ...
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Sexual dimorphism and allometry feature is the main categories of intraspecific variation found in the animal kingdom, and techniques such as Geometric Morphometrics are effective to investigate variations in shape. Considering that many vertebrates exhibit substantial allo-metry and sexual dimorphism, we test the hypotheses that (1) Aparasphenodon brunoi displays ontogenetic and static allometry; and that (2) there is sexual dimorphism in head shape in this species. We analyzed 75 specimens of A. brunoi from Parque Nacional da Restinga de Jurubatiba and found significant ontogenetic and static allometries in head shape, as well as sexual dimorphism after size correction. Regarding sexual dimorphism, females tend to have larger heads, besides slightly anteriorly positioned nostrils, smaller eyes, larger canthal ridges, narrower and longer frontoparietal ridges, and larger and laterally shifted squamosal ridges. We discuss the relevance of head morphology variation in the species, as well as the presumed consequences on the species fitness.
... 2002; Mesquita et al., 2004). Studies on the diet of A. brunoi suggest that this species is a generalist that preys mainly on arthropods including Araneae, Orthoptera, Hemiptera, Diptera and Coleoptera (e.g., Teixeira et al., 2002;Mesquita et al., 2004). ...
... 2002; Mesquita et al., 2004). Studies on the diet of A. brunoi suggest that this species is a generalist that preys mainly on arthropods including Araneae, Orthoptera, Hemiptera, Diptera and Coleoptera (e.g., Teixeira et al., 2002;Mesquita et al., 2004). ...
... The diet items confirm bromeliads as a foraging spot for Xenohyla truncata (Silva & Britto-Pereira 2006) among other frogs (e.g. Aparasphenodon brunoi, Mesquita et al. 2004). In fact, for both study sites, we found other species of frogs in bromeliads (Scinax cuspidatus and Thoropa miliaris) and exotic reptiles (Hemidactylus mabouia) that were found in bromeliads and probably use these plants as foraging inside. ...
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Analyses of the diets of frog species in a range of different habitats have shown that these amphibians feed primarily on arthropods. In general, frogs are not selective predators, but may vary in their capture mode along a continuum between active and passive foraging. In the present study, we assessed the diet of two bromeliad-breeding frogs of the genus Ololygon (= Scinax) through taxonomic and functional identification (trophic guilds). We innovate in use of trophic guilds of frogs’ preys and use the phytophagous consumption as proxy for favoring bromeliads by frogs. We also assessed the potential relationship between the size of the frogs and that of the prey they ingest, whether consumption rates varied seasonally, and the foraging mode. The results indicated a diet composed predominantly of phytophagous arthropods for both Ololygon species (O. littorea and O. perpusilla). Most of the arthropods consumed belonged to the orders Hemiptera, Diptera and Hymenoptera. We found no significant differences among the number of arthropods ingested in the rainy and in the dry seasons in either Ololygon species, nor significant relationship found between the frog size and corresponding prey ingested by individual frogs. The foraging mode of frogs was restricted only to vegetative parts of bromeliads and they did not feed on any potential pollinators. Taken together, these results suggested that frogs may favor the host bromeliad and suggest a potential trophic cascade among frogs, bromeliads, and phytophagous arthropods.
... Sexual dimorphism is defined as phenotypic differences between conspecific males and females (Shine 1989). In anurans, it might be observed for many traits, such as coloration, skin texture and skin glands, vocalization, dermal ornamentations, vocal sacs (males), and breeding behavior, body size, and shape (Mesquita et al. 2004). Some differences persist throughout adult life, but others develop in response to gonadotropic hormones and therefore are present only during the active reproductive cycle. ...
... Miranda-Ribeiro (1920) described the anuran genus and species, Aparasphenodon brunoi, of Aparasphenodon are recognized (Frost 2017). Like other casque-headed hylids, species of Aparasphenodon fusion of the overlying skin to the bone below is thought to reduce desiccation (Trueb 1970), as well as protect the frogs hiding inside bromeliads and bamboos from intruders and predators (Teixeira et al. 2002, Mesquita et al. 2004, Lantyer-Silva et al. 2014. The skulls of both A. brunoi and the casque-headed hylid Corythomantis greeningi Boulenger, 1896 are covered with bony spines; poisonous secretions that are more lethal than the venom from pitvipers of the genus Bothrops are delivered through these spines (Jared et al. 2015). ...
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The eyes of frogs and toads (Anura) are among their most fascinating features. Although several pupil shapes have been described, the diversity, evolution, and functional role of the pupil in anurans have received little attention. Studying photographs of more than 3200 species, we surveyed pupil diversity, described their morphological variation, tested correlation with adult habits and diel activity, and discussed major evolutionary patterns considering iris anatomy and visual ecology. Our results indicated that the pupil in anurans is a highly plastic structure, with seven main pupil shapes that evolved at least 116 times during the history of the group. We found no significant correlation between pupil shape, adult habits, and diel activity, with the exception of the circular pupil and aquatic habits. The vertical pupil arose at least in the most recent common ancestor of batrachians, and this morphology is present in most early-diverging anuran clades. Subsequently, a horizontal pupil, a very uncommon shape in vertebrates, evolved in most neobatrachian frogs. This shape evolved into most other known pupil shapes, but it persisted in a large number of species with diverse life histories, habits and diel activity patterns, demonstrating a remarkable functional and ecological versatility.
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Aim The diversity of brood size across animal species exceeds the diversity of most other life‐history traits. In some environments, reproductive success increases with brood size, whereas in others it increases with smaller broods. The dominant hypothesis explaining such diversity predicts that selection on brood size varies along climatic gradients, creating latitudinal fecundity patterns. Another hypothesis predicts that diversity in fecundity arises among species adapted to different microhabitats within assemblages. A more recent hypothesis concerned with the consequences of these evolutionary processes in the era of anthropogenic environmental change predicts that low‐fecundity species might fail to recover from demographic collapses caused by rapid environmental alterations, making them more susceptible to extinctions. These hypotheses have been addressed predominantly in endotherms and only rarely in other taxa. Here, we address all three hypotheses in amphibians globally. Location Global. Time period Present. Major taxa studied Class Amphibia. Methods Using a dataset spanning 2,045 species from all three amphibian orders, we adopt multiple phylogenetic approaches to investigate the association between brood size and climatic, ecological and phenotypic predictors, and according to species conservation status. Results Brood size increases with latitude. This tendency is much stronger in frogs, where temperature seasonality is the dominant driver, whereas salamander fecundity increases towards regions with more constant rainfall. These relationships vary across continents but confirm seasonality as the key driver of fecundity. Ecologically, nesting sites predict brood size in frogs, but not in salamanders. Finally, we show that extinction risk increases consistently with decreasing fecundity across amphibians, whereas body size is a “by‐product” correlate of extinction, given its relationship with fecundity. Main conclusions Climatic seasonality and microhabitats are primary drivers of fecundity evolution. Our finding that low fecundity increases extinction risk reinforces the need to refocus extinction hypotheses based on a suggested role for body size.
Thesis
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ABSTRACT Anuran amphibians exhibit a great diversity of reproductive modes. The behaviors of laying eggs in the water or on terrestrial habitats involve different adaptations and terrestriality evolved independently in the group. Morphological differences between males and females and female fecundity are important traits related to the reproductive modes. However, basic information on biology is not available for many species, hampering studies on ecology and evolution of anurans. Thus, the aims of this thesis were to study the biology of one species with arboreal reproductive mode and investigate the interplay among arboreal modes, fecundity and sexual dimorphism in anurans. In the first chapter, we describe the reproductive biology of Dendropsophus haddadi, a species endemic to the Atlantic forest. Two populations were studied in Maceió, Alagoas state, northeastern Brazil. Individuals were observed perched on the vegetation, approximately 3-5 m high, at the margins of temporary water bodies. Males were territorial, emitted calls, visual signs, and engaged in fights. Clutches were found on trunks, leaves and twigs above the water. Number of eggs was positively correlated with clutch size and our observations suggest that, in the absence of rains, females may protect the eggs against desiccation by joining them right after oviposition. This form of parental care is a novelty for the genus. Sexual size dimorphism (SSD) results from natural and sexual selection pressures on both sexes and fecundity is an important selective pressure on female size. Thus, in the second chapter, we investigated the influence of the oviposition site on SSD and female fecundity in Anura and in the Hylidae family. We analyzed 385 anuran species (32 families) exhibiting aquatic (271), arboreal (48), terrestrail hidden (35), and terrestrail exposed (31) clutches. For Hylidae, we analyzed 221 species with aquatic (175), arboreal (30) and hidden (16) clutches. Mean SSD did not vary among species with different oviposition sites; in general, males were ca. 20% smaller than females, what could be related to cloacal juxtaposition and fertilization success. Nonetheless, in species with hidden clutches, males and females tended to have similar body sizes, what could be explained by restrictions to female size increase because of space limitation to amplectant pairs. We also tested the hypothesis that females with arboreal clutches may suffer restrictions to fecundity increase to offset the costs of carrying amplectan males. In general, fecundity was smaller in arboreal breeders compared to that of aquatic breeders. However, in hylids, fecundity tended to be smaller in arboreal breeders compared to all other oviposition sites, what suggests that arboreality may restrict female fecundity increase. Our findings for Anura and Hylidae showed the complex relationship among oviposition site, fecundity and SSD in frogs, suggesting that the reproductive microhabitat may also influence female size and fecundity. Thus, degree and direction of SSD in anurans may result from complex mechanisms operating at different evolutionary scales.
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Bioecological aspects of the hylid frog Phyllodytes luteolus occupying bromeliad mircohabitat were studied in a coastal plain of southeastern Brazil. Samples were taken in August (winter) and in November (spring). In winter, a total of 121 bromeliads were examined, and all hylid frog stages (excluding eggs) were found in 75 plants (62.0%). Only eggs were found in 6 (4.9%); tadpoles in 52 (43.0%); juveniles in 8 (6.6%), and adults in 48 (39.7%). A total of 146 tadpoles, 8 juveniles and 75 adults was found. From the last adults, 32 were male and 43 females. In spring, a total of 125 bromeliads were examined, and all hylid frog stages (excluding eggs) were found in 74 plants (59.2%). Only eggs were found in 19 (15.2%); tadpoles in 54 (43.2%); juveniles in 16 (12.8%), and adults in 34 (27.2%) plants. A total of 187 tadpoles, 22 juveniles and 50 adults was found. From the adults, 26 were male and 24 females. Axil number, plant biomass and water volume showed high importance related to hylid frog abundance in a principal component analysis.
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We examined diet composition of postmetamorphic bullfrogs (Rana catesbeiana) and green frogs (R. clamitans) co-occurring at two study sites in southwest Michigan to gain insight into the nature of potential interactions between the species. Observations during sample collection indicated that bullfrogs tended to be found in the water and green frogs tended to be on land within a few meters of the water's edge. This habitat difference was reflected in diet composition. The percentage of the diet composed of aquatic prey items was significantly higher for bullfrogs on three of four collection dates. Comparisons of adult and juvenile classes of the two species indicated interspecific diet similarity was negatively related to the body size difference between classes. Juvenile frogs were common in the diet of adult bullfrogs, but were almost never consumed by green frogs. The small size of frogs consumed by adult bullfrogs indicated that juvenile green frogs constituted the great majority of frogs eaten. Our results suggest that, because of differences in habitat and body size, the opportunity for substantial competition between these species is probably small, and is restricted to individuals of similar body size. The potential for predatory interactions, however, may be substantial, and is highly asymmetrical, with the interaction largely restricted to adult bullfrogs preying on juvenile green frogs.