Anais da Academia Brasileira de Ciências (2016)

(Annals of the Brazilian Academy of Sciences)

Printed version ISSN 0001-3765 / Online version ISSN 1678-2690
http://dx.doi.org/10.1590/0001-3765201620140380
www.scielo.br/aabc

Ecology of the bromeligenous frog Phyllodytes luteolus (Anura,

Hylidae) from three restinga remnants across Brazil’s coast

Tatiana Motta-Tavares1, Thiago Maia-Carneiro1, Leonardo F. Dantas2, Monique

Van Sluys1, Fábio H. Hatano3, Davor Vrcibradic4 and Carlos F.D. Rocha1

1
Departamento de Ecologia, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier,
524, Pavilhão Haroldo Lisboa da Cunha, Maracanã, 20550-019 Rio de Janeiro, RJ, Brasil
2
Programa de Pós-Graduação em Saúde Pública e Meio Ambiente, Fundação Oswaldo Cruz, Escola Nacional de
Saúde Pública Sérgio Arouca, Rua Leopoldo Bulhões, 1480, Manguinhos, 21041-210 Rio de Janeiro, RJ, Brasil
3
Instituto Socioambiental e dos Recursos Hídricos, Universidade Federal Rural da Amazônia,
Av. Presidente Tancredo Neves, 2501, 66077-830 Terra Firme, Belém, PA, Brasil
4
Departamento de Zoologia, Instituto de Biologia, Centro de Ciências Biológicas e Saúde, Universidade
Federal do Estado do Rio de Janeiro, Av. Pasteur, 458, Urca, 22240-290 Rio de Janeiro, RJ, Brasil

Manuscript received on July 22, 2014; accepted for publication on January 16, 2015

ABSTRACT
In this study, we analyzed diet, sexual dimorphism and bromeliad use in three populations of the hylid frog
Phyllodytes luteolus from restinga habitats along the Brazilian coast. We found 13 arthropods categories in
161 stomachs. Ants and termites were the dominant prey items. The similar trophic niche across populations
suggests this species has a conservative diet. We found sexual dimorphism regarding body size and jaw
width. We recorded P. luteolus in five bromeliad species, but predominantly in Aechmea blanchetiana
(35.6% of individuals recorded). We recorded solitary individuals in 44% of occupied bromeliads, and
never found two males sharing the same bromeliad. The data is suggestive that populations of P. luteolus
has a conservative diet independent of area, with ants and termites the being most relevant prey items. The
sexual dimorphism in jaw and the solitary males may suggest that this species have territorial behavior.
Key words: Atlantic forest, bromeliad, diet, sexual dimorphism, territorial behavior.

INTRODUCTION be different among areas, differences in periods of

collection, altitudes, and/or phylogeny (Sabagh et
Anurans commonly consume arthropods as a
al. 2012). Anurans can also use different types of
primary food resource (Duellman and Trueb microhabitat, such as leaf-litter on the forest floor,
1986, Lima and Moreira 1993, Ferreira et al. rocks, streams, ponds, lakes, trees, and bromeliads
2012), and kinds and sizes of prey consumed (Eterovick 1999, Almeida-Gomes et al. 2008,
may differ (Sabagh et al. 2012, Maia-Carneiro et Duré et al. 2009, Martins et al. 2010, Ferreira et al.
al. 2013, Coco et al. 2014) between populations. 2012). Bromeligenous frogs reproduce, forage and
This may be due to prey availability, which can complete their entire life cycle inside bromeliads
Correspondence to: Tatiana Motta-Tavares (sensu Peixoto 1995). Such dependence of
E-mail: [email protected] bromeliads is in direct relation with species natural

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2 TATIANA MOTTA-TAVARES et al.

history, influencing different aspects of its ecology restinga remnants, and to evaluate the relationship
(Giaretta 1996, Ferreira et al. 2012, Lantyer-Silva of frogs with the bromeliads. We specifically aimed
et al. 2014). to assess i) the differences in array of prey types
Phyllodytes luteolus is a bromeligenous anuran consumed and trophic niche among populations,
species predominantly found in restinga habitats, and among adult males, adult females and juveniles,
where they inhabit tank bromeliads (Peixoto 1995, ii) sexual dimorphism in body and head size in the
Ferreira et al. 2012). Restingas are sandy, usually species, and iii) the bromeliad species used by the
open coastal habitats interspersed within the Atlantic individuals.
forest biome of Brazil. Phyllodytes luteolus occurs
along the Brazilian coast from the state of Paraíba MATERIALS AND METHODS
southwards to the north portion of the state of Rio Study Areas
de Janeiro (Vrcibradic et al. 2006, Frost 2013),
with the most inland record being from the state Field work was carried out between November
of Minas Gerais, where it occurs in some forest 1999 and March 2000, in three restinga sites along
remnants (Feio and Caramaschi 2002). In addition, the east coast of Brazil: Setiba district (20° 35’ S
an introduced population has been recorded for the and 39° 13’ W) in the municipality of Guarapari,
municipality of Rio de Janeiro (Salles and Silva- Guriri district, in the municipality of São Mateus
Soares 2010). This species is common inside (18° 41’ S and 39° 45’ W), both in the state of
bromeliads from open areas, and avoids bromeliad Espírito Santo, and one site in the municipality
axils containing less than 100 ml of water (Teixeira of Prado (17° 18’ S and 39° 13’ W), in the state
et al. 1997). Phyllodytes luteolus lay up to three of Bahia (Fig. 1). The mean annual temperature
eggs in bromeliad axils, where the larvae develop on these regions is around 23 °C and the annual
and feed on debris (Peixoto 1995, Giaretta 1996). rainfall ranges between 1000 and 1350 mm (Nimer
Papp and Papp (2000) showed a drastic population 1979). Setiba and Guriri are separated by 210 km,
reduction of P. luteolus after a fire in the Linhares whereas Guriri and Prado are 160 km apart, and
municipality, in the state of Espírito Santo. This fire Setiba and Prado 380 km apart. The bromeliad
destroyed more than 99.9% of the bromeliad Vrisea species composition varied among localities.
neoglutinosa (Rocha et al. 1996), supporting the
species strong dependence on bromeliads. Data Collection and Statistical Analyses

Inter-population studies regarding trophic and

We conducted diurnal and nocturnal surveys inside
spatial ecology are important to explain species
bromeliads through visual encounter surveys
niche breadth, position in local trophic webs,
(Crump and Scott 1994) (total of 80 sampling
foraging behavior, and metabolic necessities
hours). Moreover, 200 tank bromeliads of different
(Duellman and Trueb 1986, Toft 1980, 1981, Wells
2007). Furthermore, it enables the elucidation species were randomly sampled in each area (total
of whether these parameters are conservative or of 600). All individuals of P. luteolus found, were
variable among localities. In addition, an inter- collected (IBAMA collection permit No. 096/99).
population study about ecology and behavior of During the collections in the field amphibians
P. luteolus may help to elucidate how individuals were killed with anesthetic overdose (sodium
correlate with each other in a limited space (the pentobarbital) as recommended by the protocols
bromeliads) inside a limited habitat (the restinga of the American Society of Ichthyologists and
remnants). The goal of this study was to investigate Herpetologists (ASIH), the Herpetologists’ League
the diet of three populations of P. luteolus from (HL) (1987), the American Veterinary Medical

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 ECOLOGY OF A BROMELIGENOUS FROG 3

Figure 1 - Map showing restinga habitats where Phyllodytes luteolus

were collected: Guriri (18°41’S and 39°45’W) and Setiba (20°35’S
and 39°13’W), in the state of Espírito Santo, and Prado (17°18’S and
39°13’W), in the state of Bahia.

Association (AVMA) (2000) and the Canadian (Howard et al. 1999). Prey items were identified to
Council on Animal Care (CCAC) (1993), followed the taxonomic level of order (or family, in the case
by 10% formalin solution for fixation. of Formicidae). Unidentified arthropod remains
We measured snout-vent length (SVL) and jaw and plant residues were not considered in total
width (JW) of the frogs with calipers to the nearest volumetric analysis.
0.01 mm. We analyzed gonads to determine sex; We estimated the volume of each prey using
those individuals whose gonads were not developed the formula for an ovoid spheroid: V = 4/3π
were considered juveniles. We analyzed stomach (length/2) (width/2)² (Dunham 1983). We used
contents using a stereomicroscope, and characterized Pianka’s overlap index (Pianka 1973) to determine
the diet in terms of number of individual prey items the trophic niche similarity between populations:
consumed (N), total volume of prey (V, in mm³), n
and frequency of occurrence (F) of each prey ∑ pij × pik
category. Additionally, for each category of prey Ojk =
i =1
n n
we calculated an index of importance value (Ix): Ix
= [(nx/N) + (vx/V) + (fx/F)]/3, where nx, vx, and fx
∑ pij 2 ∑ pik 2
i =1 i =1

are number, volume, and frequency of prey item x,

respectively, and N, V, and F are summations of the where j and k refer to the populations under compa­
number, volume, and frequency of all prey items rison and pi is the proportion of prey component

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4 TATIANA MOTTA-TAVARES et al.

i. We calculated food niche overlap using the Systat 11 software, and used PAST software for
proportional values of number and volume of prey ANOSIM and NMDS analysis.
consumed. To determine if the frogs from each
populations statistically differed in terms of prey RESULTS
consumption, we performed a one-way analysis of
We analyzed 161 stomach content of P. luteolus from
similarity (ANOSIM) with Bray–Curtis distance
three restinga remnants in Brazil, of which 58 were
measure (Clarke 1993). We also did a nonmetric
from Setiba (27 males, 23 females, six juveniles
multidimensional scaling (NMDS) based on a
and two unknown), 43 from Guriri (20 males, 10
Bray-Curtis dissimilarity matrix to compare prey
females, 10 juveniles and three unknown) and 60
consumption by each frog from each population.
from Prado (29 males, 26 females, two juveniles
Mean prey volume was estimated as the mean
and three unknown). A total of 21 stomachs were
volume of the three largest prey items consumed
empty of which: five were from Setiba (8.6%;
per frog (or all items when stomach contained
two males, three females), 14 from Guriri (32.6%;
less than three). We tested for differences between
10 males, two females, two juveniles), and two
populations in the number of prey and in the
were from Prado (3.3%; one male, one juvenile).
mean prey volume consumed per frog using one-
Thirteen different arthropod categories were found
way analysis of variance (ANOVA), followed by
Scheffe’s post hoc test (Zar 1999) when the results in the stomachs (Table I). Formicidae and Isoptera
were significant. We used Simple Regression were the most numerous and frequent prey (Table
Analysis between prey number and frog SVL I). These two taxa accounted for more than 90% of
and between mean prey volume and frog JW, to prey consumed in each population, and were the
evaluate if the number of prey items or the prey most important (Ix) prey items. Isoptera represented
volume were associated to body size and JW. the highest proportional volume in the stomachs
We identified the bromeliad species occupied (55.2% in Setiba, 53.0% in Guriri; 43.0% in Prado),
by P. luteolus when the frog was first seen. Additio­ followed by Formicidae (19.3% in Setiba; 16.4% in
nally, in Setiba and Guriri restingas, we counted Guriri; 38.7% in Prado).
the number of frogs per bromeliad, identified the There was no difference in the mean number
ontogenetic stage (juvenile or adult) and sex, and of prey items consumed by males, females and
searched for eggs and/or tadpoles in the bromeliad juveniles of P. luteolus (ANOVA, F2,118 = 1.350, P =
phytotelmata (i.e. axils and central rosette). 0.263; Table II). The mean volume of prey ingested
To assess whether there was sexual dimorphism differed among males, females and juveniles
in body size and head width of P. luteolus, we used (ANOVA, R2 = 0.091, F2,117 = 5.890, P = 0.004).
one-way ANOVA for differences in SVL and in JW Juveniles ingested smaller prey compared to
between males and females of each population. We males (Scheffe, P = 0.019), and females (Scheffe,
used analysis of covariance (ANCOVA, with SVL P = 0.004). There was no difference in the mean
as a covariate; Zar 1999) to test for differences in volume of prey consumed between adult males and
relative jaw width between sexes. females (Scheffe, P = 0.639).
Descriptive statistics are presented throughout The number of prey items consumed per frog
the text as mean ± one standard deviation. All data was not related to frog SVL in any population
were tested for normality and for homogeneity of (Regression Analysis, Setiba: F1,45 = 3.133, P =
variances before performing statistical analyses, 0.083, Guriri: F1,45 = 3.133, P = 0.956, and Prado:
and were log-transformed when necessary. We F1,53 = 0.499, P = 0.483). For Setiba population, the
performed ANOVA and ANCOVA analysis with volume of prey was influenced by JW (Regression

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TABLE I
Diet of Phyllodytes luteolus in three restinga remnants along Brazil’s coast (Setiba, Guriri and Prado). N = Number of prey items; F = Frequency of occurrence;
V = Volume (in mm³), and Ix = Index of Importance Value. U.A.R = Unidentified arthropod remains.
  Setiba Guriri Prado
Prey category N (%) F (%) V (%) Ix N (%) F (%) V (%) Ix N (%) F (%) V (%) Ix
 
Arachnida
Acari - - - - 3 (1.9) 3 (7.0) 0.2 (< 0.1) 3.0 11 (1.6) 5 (8.3) 3.7 (0.1) 3.4
Araneae 3 (0.5) 3 (5.2) 53.6 (2.6) 2.8 - - - - 2 (0.3) 2 (3.3) 35.7 (1.2) 1.2 (1.6)
Chilopoda 1 (0.2) 1 (1.7) < 0.1 (< 0.1) 0.6 - - - - - - - -
Hexapoda
Blattaria - - - - - - - - 1 (0.1) 1 (1.7) 19.6 (0.6) 0.8
Coleoptera
Adult 24 (4.4) 16 (27.6) 191.7 (9.3) 13.8 6 (3.8) 4 (9.3) 23.3 (2.9) 5.3 22 (3.3) 17 (28.3) 334.2 (11.0) 14.2
Larvae - - - - - - - - 1 (0.1) 1 (1.7) 6.7 (0.2) 0.7
Diptera
Adult 9 (1.6) 5 (8.6) 20.7 (1.0) 3.8 - - - - - - - -
Pupa 2 (0.4) 1 (1.7) 0.1 (< 0.1) 0.7 - - - - - - - -
Hemiptera - - - - - - - - 1 (0.1) 1 (1.7) 0.9 (< 0.1) 0.6
Hymenoptera
Formicidae 207 (37.8) 36 (62.1) 395.4 (19.3) 39.7 75 (47.5) 15 (34.9) 133.0 (16.4) 32.9 327 (48.4) 52 (86.7) 1175.4 (38.7) 57.9
ECOLOGY OF A BROMELIGENOUS FROG

Others 3 (0.5) 2 (3.4) 54.0 (2.6) 2.2 - - - - - - -

Isoptera 294 (53.7) 24 (41.4) 1132.9 (55.2) 50.1 74 (46.8) 14 (32.6) 429.3 (53.0) 44.1 309 (45.7) 28 (46.7) 1305.9 (43.0) 45.1
Lepidoptera larvae - - - - - - - - 1 (0.1) 1 (1.7) 18.7 (0.6) 0.8
Insecta egg 4 (0.7) 1 (1.7) 0.1 (< 0.1) 0.8 - - - - 1 (0.1) 1 (1.7) 0.8 (< 0.1) 0.6
Plant material 10 (17.2) 203.3 (9.9) 6 (14.0) 136.1 (16.8) 7 (11.7) 63.8 (2.1)
Mineral 10 (17.2) 432.2 (21.1) 8 (18.6) 224.3 (27.7) 10 (16.7) 134.6 (4.4)
U.A.R. 4061.6 217.8 1956.3
Empty 5 (8.6) 14 (32.6) 2 (3.3)
Total 547 (100) 58 (100) 2052.0 (100) 158 (100) 43 (100) 810.1 (100) 676 (100) 60 (100) 3036.1 (100)
5

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6 TATIANA MOTTA-TAVARES et al.

TABLE II
Number of prey and prey volume (mm3) per stomach for males, females and
juveniles of Phyllodytes luteolus in three restinga remnants along Brazil’s coast.
SD = Standard deviation.
Number of prey Prey volume
Mean ± SD Range Mean ± SD Range
Males (N=57) 9.8 ± 8.8 1 - 41 5.4 ± 7.1 0.1 - 30.7
Females (N=49) 14.0 ± 15.8 1 - 71 5.9 ± 6.6 0.03 - 30.5
Juveniles (N=15) 6.8 ± 5.1 1 - 16 1.8 ± 2.3 0.04 - 6.8
Total (N=121) 11.1 ± 12.0 1 - 71 5.2 ± 6.6 0.03 - 30.7

Analysis, F1,45 = 19.876, R2 = 0.31, P < 0.0001). The food niche overlap among populations was
In Prado population, the volume of prey had a high, both in terms of numerical and volumetric
nearly significant influence by JW (F1,45 = 3.778, proportions of prey items, with values of 0.90
P = 0.057), but Guriri’s population showed no or higher in all cases (Table III). The ANOSIM
relationship (F1,20 = 1.781, P = 0.197). indicated divergence in prey consumption between
There was no difference in the mean number populations, but with an R close to zero (R = 0.0470,
of prey items per stomach among P. luteolus P = 0.0195). Prado population had the most divergent
populations (ANOVA, F2,121 = 0.694, P = 0.502). prey consumption in comparison with the others
The mean volume of the three largest prey ingested (ANOSIM, Prado vs. Setiba: R = 0.0567, P = 0.0118;
per frog differed among populations (ANOVA, F2,121 Prado vs. Guriri: R = 0.0895, P = 0.0466). Setiba and
= 3.757, P = 0.026). Frogs from Prado consumed Guriri populations had similar prey consumption
larger prey than frogs from Setiba (Scheffe, P = (ANOSIM, R = - 0.0415, P = 0.8687). The prey
0.025) but not from Guriri (Scheffe, P = 0.193; Fig. consumption between indivi­duals (Fig. 3) can be
2). Prey ingested by frogs from Setiba and Guriri interpreted as similar, with just a few individuals
did not differ in mean volume (Scheffe, P = 0.947). from Prado standing out (stress = 0.1148).

TABLE III
Diet niche overlap for Phyllodytes luteolus in three
remnants of restinga along the Brazilian coast based on
proportional values of prey items and prey volume.
Prey items Prey volume
Setiba x Guriri 0.98 0.99
Guriri x Prado 0.99 0.90
Prado x Setiba 0.98 0.99

Female were larger (SVL) than males in Prado

(ANOVA, R2 = 0.31, F1,55 = 24.801, P < 0.0001),
but not in Setiba (ANOVA, F1,46 = 0.033, P = 0.856)
Figure 2 - Mean volume (log-transformed) of the three largest
nor in Guriri (ANOVA, F1,28 = 2.785, P = 0.106)
prey items ingested per stomach of Phyllodytes luteolus in three (Table IV). Across the populations, males had
remnants restinga along the eastern coast of Brazil (Setiba, comparatively wider jaws than females, irrespective
Guriri and Prado). The asterisk means that the volume of prey
consumed was significantly different between these populations. of body size: Setiba – ANCOVA, R2 = 0.589, F1,1,45 =
Sample sizes: Setiba = 47, Guriri = 22 and Prado = 55. 47.220, P < 0.0001, Guriri – ANCOVA, R2 = 0.710,

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 ECOLOGY OF A BROMELIGENOUS FROG 7

DISCUSSION

The three populations of P. luteolus had a diet

composed exclusively of arthropods. The diet
was composed of a relatively wide variety of prey
types, but Formicidae and Isopteras dominated
the prey consumed. Similarly, in the restinga of
Regência in the state of Espírito Santo, Ferreira et
al. (2012) reported on a population of P. luteolus
that fed on 19 different prey types, with Formicidae
and Isoptera being the most important prey. Due
to the high proportion of Formicidae and Isoptera
consumed, these authors suggested that P. luteolus
had a specialized diet, predominantly composed of
colonial arthropods. Because specialization in diet
Figure 3 - Multidimensional scaling analyses of the diet
composition in individuals of Phyllodytes luteolus from Setiba
is a result of evolution, we consider Formicidae
(empty triangles), Guriri (filled dots) and Prado (“X”). Stress and Isoptera as prey preferentially consumed.
= 0.1148. Apparently, P. luteolus has a conservative diet
across sites, independently of local peculiarities and
F1,1,27 = 63.984, P < 0.0001, Prado – ANCOVA, R2 differences among sites. It is possible that access
= 0.922, F1,1,54 = 480.146, P < 0.0001. to Formicidae and Isoptera might be facilitated in
Phyllodytes luteolus was found in five microhabitats that accumulate plant remains, like
bromeliad species (Table V), where in 135 the interior of some tank bromeliads. Formicidae
bromeliads (22.5%) were occupied by at least one is commonly associated with bromeliads (Schimd
P. luteolus. We recorded 102 (25.5%) bromeliads et al. 2010), which may facilitate them being found
containing individuals of P. luteolus in Setiba and and subsequent consumption by frogs. Toft (1980,
Guriri. In 45 of them (44.1%) we found only one 1981) suggests the use of Jacob’s elective index to
individual of P. luteolus inside the bromeliad, of evaluate if a species has a specialized diet, based on
which 28 (27.4%) were males and 17 (16.6%) were prey abundances in the habitat and in the stomachs.
females. Four individuals (one male, one female Thus, to better infer if the diet of P. luteolus is
and two of unknown sex; each one in a different specialized or generalized, it would be necessary to
bromeliad) were found with clutches containing a evaluate whether frogs select prey items or if they
maximum of six eggs. In 57 of the 102 bromeliads consume them according to prey availability inside
containing P. luteolus (55.9%), two to four bromeliads. However, in the absence of specific
individuals were found inside the same bromeliad. studies on the arthropod fauna inside bromeliads, at
In none of the cases, males were found sharing a the study sites, we were not able to confirm to what
bromeliad, but males co-occurred with females, extent P. luteolus specializes in colonial insects. The
juveniles and/or tadpoles. In the 14 cases in which presence of plant remains and sand in the diet of P.
tadpoles were present inside bromeliads, there were luteolus was considered accidental ingestion. The
one to six tadpoles and, in most cases, at least one difference of empty stomachs between populations
frog inside the same bromeliad (11 females, four may be due to prey availability at the moment of
males, one juvenile, and two of unknown sex). the fieldwork in each locality.

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 8

TABLE IV
Number of individuals (N), range, mean and standard deviation (SD) of snout–vent length (SVL, in mm) and jaw width (JW, in mm) of males, females and
juveniles of Phyllodytes luteolus in three restinga remnants along Brazil’s coast.
Setiba Guriri Prado Total
Size metric
N Range Mean ± SD N Range Mean ± SD N Range Mean ± SD N Range Mean ± SD

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SVL
Males 21 18.9 - 25.6 24.2 ± 1.5 20 13.5 - 26.8 23.6 ± 5.4 31 14.0 - 25.8 21.5 ± 3.0 78 13.5 - 26.8 23.1 ± 2.9
Females 27 20.8 - 26.4 24.1 ± 1.5 10 22.8 - 27.2 25.9 ± 1.4 26 20.2 - 27.9 24.9 ± 1.8 57 18.9 - 27.9 24.8 ± 1.7
Juveniles 8 11.4 - 14.8 12.6 ± 1.1 11 9.8 - 25.0 14.5 ± 4.0 5 13.8 - 16.5 15.8 ± 1.1 24 9.8 - 25.0 14.1 ± 3.0
Total 56 11.4 - 26.4 22.5 ± 4.3 42 9.8 - 27.2 22.0 ± 5.5 64 13.8 - 27.9 22.6 ± 3.5 162 9.8 - 27.9 22.4 ± 4.3

JW
Males 21 7.5 - 9.8 9.1 ± 0.6 20 2.5 - 10.5 9.0 ± 1.7 31 5.5 - 10.3 8.1 ± 1.3 78 5.5 - 25.0 9.1 ± 2.1
Females 27 8.4 - 10.8 9.6 ± 0.6 10 8.0 - 10.0 9.2 ± 0.6 26 8.0 - 10.0 9.2 ± 0.6 57 7.5 - 10.0 9.1 ± 0.6
Juveniles 8 4.0 - 5.4 4.6 ± 0.5 11 2.5 - 9.4 5.0 ± 1.8 5 5.3 - 6.1 5.8 ± 0.3 24 2.5 - 9.4 5.0 ± 1.3
Total 56 4.0 - 10.8 8.7 ± 1.8 42 2.5 - 10.5 7.9 ± 2.4 64 5.3 - 10.3 8.4 ± 1.3 162 2.5 - 25.0 8.5 ± 2.2
TATIANA MOTTA-TAVARES et al.

TABLE V
Number and percentage of individuals of Phyllodytes luteolus found in bromeliads in three restinga remnants along Brazil’s coast.
Locality
Bromeliad species
Setiba (%) Guriri (%) Prado (%) Total (%)

Aechmea blanchetiana (Baker) L.B.Sm. 0 31 (88.6) 17 (38.6) 48 (35.6)

Aechmea lingulata (L.) Baker 20 (35.7) 0 0 20 (14.8)
Neoregelia cruenta (R.Graham) L.B.Sm 0 4 (11.4) 5 (11.4) 9 (6.7)
Vriesea neoglutinosa Mez 21 (37.5) 0 0 21 (15.5)
Vriesea procera (Mart. Ex Schult. F.) Whittm. 15 (26.8) 0 22 (50.0) 37 (27.4)
Total 56 (100) 35 (100) 44 (100) 135 (100)
 ECOLOGY OF A BROMELIGENOUS FROG 9

Such as expected, we observed that juveniles data together with those available in the literature
of P. luteolus tended to consume smaller prey (Ferreira et al. 2012) suggests that P. luteolus has
compared to adults. Anurans ingest prey with some degree of conservatism regarding its trophic
size proportional to their JW, thus consuming niche, feeding on similar prey types (mainly
larger prey as their jaw size increases (e.g. Lima Formicidae and Isoptera) independent of local
and Moreira 1993, Marra et al. 2004, Dietl et al. patterns of prey supply in different sites.
2009, Martins et al. 2010). Smaller preys should Females were larger than males in the Prado
be less energetically profitable for adults, and population, which is consistent with observations for
the consumption of larger prey should result in a congeneric species (e.g. P. wuchereri, Caramaschi
greater amount of energy. et al. 2004; P. maculosus, Cruz et al. 2006). A
There were some inter-population differences possibility for the absence of dimorphism in body
in the mean volume of prey items consumed by size in the other two populations may be due to
P. luteolus. The volume of prey consumed may sample size. Overall, females tend to be larger than
have differed due to variation in prey availability males in most anuran species (Shine 1979). This
among the studied restingas. The distance between difference in body size occurs due to intra-sexual
sites might explain the variation in the volume of selection that favors larger relative body size of
prey consumed. For instance, a study with Rhinella females, which is linked to a capacity to produce
ornata (Spix, 1824) in three different localities larger clutch sizes or larger eggs (Duellman and
(which are at least 27 km distance from each one) Trueb 1986, Martins et al. 2010).
revealed that the populations differed with regard Because no more than one adult male was found
to the number and volume of prey consumed by in the same bromeliad and male P. luteolus have
individuals, but with a more similar diet between larger proportional jaw widths than females, we
the areas closest to each other and with similar propose that males of this species may have territorial
environments (Maia-Carneiro et al. 2013). behavior. Eterovick (1999) did not record territorial
Despite considerable distances between behavior in P. luteolus, contrary to Weygoldt
populations (> 150 km), trophic niches of P. (1981), who observed agonistic interactions among
luteolus were very similar (at least 90% overlap males under laboratory conditions. Teixeira et al.
in all cases). The probality of significance in the (1997) suggested that intra-specific competition
ANOSIM demonstrates a significant difference among males (e.g. for females, preys, shelters and/
between populations, but the R close to 0 indicates or reproductive sites) occurs in P. luteolus, and
similar prey consumption. The similarity between Weygoldt (1981) proposed that the low density of
populations is reinforced by observation of the adults per bromeliad suggests that males of this
NMDS outcomes in Figure 3. These ANOSIM species exhibit intra-specific territorial behavior.
results can be due to the divergence of Prado In the Brazilian restinga of Regência, two studies
from others sites, or the analyzed factor (prey also found a high percentage of solitary P. luteolus
consumption) was a weak factor. Two explanations inside bromeliads (individuals were not categorized
of extensive diet overlap between the populations by sex) − Schineider and Teixeira (2001) observed
are: i) similar arthropod faunas inhabiting that up to 80% of individuals were found alone
bromeliads in the studied restingas, or ii) an within a bromeliad depending on the bromeliad
inherent preference for Formicidae and Isoptera species, and Ferreira et al. (2012) found that 65%
is characteristic of P. luteolus. Evaluation of our of examined bromeliads had only one P. luteolus.

An Acad Bras Cienc (2016)

10 TATIANA MOTTA-TAVARES et al.

Sexual dimorphism in JW (males having relatively de Nível Superior (CAPES) and from FAPERJ.
larger jaws than females) also suggests territorial We thank IBAMA for the collection permit (No.
behavior. Males of P. luteolus use mandibular 096/99).
odontoids during fights (Weygoldt 1981, Duellman
RESUMO
and Trueb 1986), and males with larger jaws are
presumably more successful during territorial Neste estudo, analizamos a dieta, dimorfismo sexual
struggles. e uso de bromélias em três populações do hilídeo
Despite the consumption of a relatively wide Phyllodytes luteolus de habitats de restinga ao longo da
array of prey, particular food items, such as colonial costa brasileira. Encontramos 13 categorias de artrópodes
insects (ants and termites) for Phyllodytes luteolus, em 161 estômagos. Formigas e cupins foram as presas
might predominantly compose the diet of species. dominantes. O nicho trófico semelhante registrado
entre as populações sugere que essa espécie possui uma
Although may occur intra- and inter-population
dieta conservativa. Encontramos dimorfismo sexual
differences in types and sizes of preys consumed
referentes ao tamanho do corpo e largura da mandíbula.
by P. luteolus, in some cases these parameters Observamos P. luteolus em cinco espécies de bromélias,
might be conservative. Sexual dimorphism in mas predominantemente em Aechmea blanchetiana
size jaw width and body size, with males having (35.6% dos indivíduos encontrados). Encontramos
proportionally larger jaws than females and with indivíduos solitários em 44% das bromélias ocupadas,
females larger-sized than males, might confer an e nunca dois machos dividindo a mesma bromelia. Os
advantages during territorial interactions in males dados sugerem que as populações de P. luteolus possuem
and favor greater fecundity in females. uma dieta conservadora independente da localidade,
com formigas e cupins como as presas mais relevantes.
ACKNOWLEDGMENTS O dimorfismo sexual no tamanho das mandíbulas e os
machos solitários podem sugerir que esta espécie possui
We are grateful to G.R. Winck for preparing comportamento territorial.
the map. Special thanks to J.H.F. Mello, K. Palavras-chave: Mata Atlântica, bromélia, dieta, dimor­
Welsh, M. Almeida-Gomes and the anonymous fismo sexual, comportamento territorial.
reviewers for the contributions to the manuscript.
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