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Life in bromeliads: reproductive behaviour and the monophyly of the Scinaxperpusillus species group (Anura: Hylidae)Ricardo Alves-Silva a; Hélio Ricardo da Silva a
a Universidade Federal Rural do Rio de Janeiro, Laboratório de Herpetologia, Instituto de Biologia -Departamento de Biologia Animal, Rio de Janeiro, Brazil
Online Publication Date: 01 January 2009
To cite this Article Alves-Silva, Ricardo and da Silva, Hélio Ricardo(2009)'Life in bromeliads: reproductive behaviour and themonophyly of the Scinax perpusillus species group (Anura: Hylidae)',Journal of Natural History,43:3,205 — 217
To link to this Article: DOI: 10.1080/00222930802568808
URL: http://dx.doi.org/10.1080/00222930802568808
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8/3/2019 ALves-Silva & Silva - 2009 - Life in Bromeliads Reproductive Behaviour and the Monophyly of the Scinax us Species Group
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Life in bromeliads: reproductive behaviour and the monophyly of the
Scinax perpusillus species group (Anura: Hylidae)Ricardo Alves-Silva and Helio Ricardo da Silva*
Universidade Federal Rural do Rio de Janeiro, Laboratorio de Herpetologia, Instituto deBiologia – Departamento de Biologia Animal, Rio de Janeiro, Brazil
(Received 1 February 2008; final version received 23 September 2008)
Several aspects of the reproductive behaviour of species of the Scinax perpusillusgroup (S. perpusillus, S. v-signatus, S. littoreus, and three other not yet describedspecies) obtained from direct field observations and nocturnal video filming are
presented and evaluated. Males of the observed species have behaviouralcharacters, including aspects of their call, that are indicative of territory defence.Vocalizations are elaborate and represent intra- and inter-sexual communicationmechanisms. Females present behaviour relating to the inspection of egg-layingsites (bromeliad leaf-tanks), reduced and partitioned clutch. This set of behaviours is not only indicative of a sophisticated control mechanism over egglaying and spermatozoid release, but also of the existence of a behaviouralrepertoire that probably originated in the ancestor of these species and could beconsidered a synapomorphy for this group of species. Furthermore, thebehaviours described herein comprise a new reproductive strategy for frogs thatreproduce in bromeliads.
Keywords: Bromeliaceae; calls; clutch size; phytotelmata; reproduction; courtship;lekking
Introduction
Bromeliads are an example of a terrestrial or arboreal plant that encloses an aquatic
environment or phytotelmata (Varga 1928; Laessle 1961; Frank 1983), and as such,
bromeliads are an important resource in the form of shelter, water source and
reproduction site for several species of anurans (Lannoo et al. 1986). In the Atlantic
rain forest of Brazil many species of anurans use bromeliads only for shelter (Peixoto
1995), but some hylid treefrogs spend their whole life cycle, from eggs to adult,
associated with these plants (Peixoto 1995). Among these, the most dependent onthese plants are species of the genus Phyllodytes (Giaretta 1996; Peixoto et al. 2003)
and species in the Scinax perpusillus group (Peixoto 1987). All of the species in these
groups reproduce in, and are associated with bromeliads throughout their lives.
Although considered characteristic of the nine species (Brasileiro et al. 2007) in the S.
perpusillus group (Faivovich 2002), this strong association with bromeliads (Lutz
1973; Peixoto 1995) has not been investigated for most of the species. The presence
of tadpoles in the water accumulated in the central tank and the other leaf-tanks of
the bromeliads, and the colour pattern in the inguinal area of adult frogs caught
calling from bromeliads, are direct evidence of group membership.
*Corresponding author. Email: helio@ufrrj.br
Journal of Natural History
Vol. 43, Nos. 3–4, January 2009, 205–217
ISSN 0022-2933 print/ISSN 1464-5262 online
# 2009 Taylor & Francis
DOI: 10.1080/00222930802568808
http://www.informaworld.com
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There are several advantages to frogs of using bromeliads. The plants provide a
source of water (sometimes only as moisture) even during drier seasons, which is not
available to non-bromeliad inhabitants. The microhabitat in the rosette is generally
free of the predators that occur in ponds, rivers or swamps (Magnusson and Hero
1991). Also, competition with other frogs is minimized, especially during larval
stages (Woodward 1982; Loschenkohl 1986; Kupferberg 1997). However, there are
disadvantages to this microhabitat as well. These include the unpredictability of
water availability (water may become scarce) and spatial limitations for large
clutches, which impose limits on the number of offspring that can develop in this
microhabitat, even when reproduction takes places in larger species of bromeliads
such as Alcantarea glaziouana, which may hold more than a litre of water in each
leaf-tank.
Because of the limitations imposed by bromeliads as breeding sites, and the
intricate behavioural repertoire related to anuran reproduction in general (e.g.
courtship, egg deposition, tadpole development), it seems unlikely that frogs that
reproduce in this microhabitat do so opportunistically. Physalaemus spiniger may layeggs in bromeliads opportunistically, but tadpoles have never been found developing
in this microhabitat (Haddad and Pombal 1998). Furthermore, frogs that breed in
bromeliads have various strategies that seem to favour success in their reproductive
efforts in this microhabitat. Such strategies include oophagy (feeding of tadpoles
with eggs laid by a mother) as in the hylids Osteopilus brunneus (Lannoo et al. 1986;
Thompson 1996), Osteocephalus oophagus (Jungfer and Weygoldt 1999) and
Anotheca spinosa (Jungfer 1996), and the dendrobatid Oophaga pumilio (Weygoldt
1980, 1987). Another reproductive strategy is the laying of a few large eggs with large
amounts of yolk that give rise to non-feeding tadpoles, as in the microhylid Syncope
antenori (Krugel and Richter 1995) and the bufonid Dendrophryniscys brevipolicatus(Peixoto 1995). Finally, in species of the hylid genus Phyllodytes, few eggs are laid
and the larvae are cannibalistic (Weygoldt 1981). Another reproductive strategy in
this environment is the deposition of a smaller clutch size. This would increase the
chances of survival because lower densities mean decreased competition among the
larvae for food and dissolved oxygen, and decreased pollution of the small water
body by larval waste. Although investigated for other bromeliad-inhabiting species
(Peixoto 1995), such reproductive strategies are not fully understood within the S.
perpusillus group. Only male activity and the role of plant selection during
reproduction have been investigated (Oliveira and Navas 2004). In this paper we
describe the reproductive behaviour of both males and females of three species of theS. perpusillus group and provide additional indirect observations of egg-laying
behaviour for three other populations of unnamed species, thereby revealing details
of the lives of these highly bromeliad-dependent frogs and their use of bromeliads for
reproduction.
The Scinax perpusillus group: taxonomy and distribution
Nine species are currently recognized that belong to the S. perpusillus group: Scinax
alcatraz (Lutz, 1973), S. atratus (Peixoto, 1989), S. arduous Peixoto, 2002, S. littoreus
(Peixoto, 1988), S. melloi (Peixoto, 1989), S. perpusillus (Lutz and Lutz, 1939), S. v-
signatus (Lutz, 1968) and S. peixotoi Brasileiro et al., 2007 and S. faivovichi
Brasileiro et al., 2007. However, it is evident from the use of cf. (e.g. Scinax cf.
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perpusillus) by some authors (Heyer et al. 1995; Pombal and Gordo 2004; Oliveira
and Navas 2004; Zaher et al. 2005) that more species may still be hidden under the
name S. perpusillus, and that these populations are only tentatively identified as
such. The group is endemic to the Atlantic forest of southeastern Brazil, from the
State of Espırito Santo to Sao Paulo (Figure 1), but the range may be extended
further south to the State of Santa Catarina based on information on an unnamed
species from there (see http://calphotos.berkeley.edu and http://www.ra-bugio.
org.br/ver_especie.php?id5146).
In the phylogeny of the genus Scinax presented by Faivovich (2002) a test of the
monophyly of the group was not performed, because only one species was available
to represent the group. Therefore, association with bromeliads (with tadpoles raised
within these plants leaves) is the only evidence supporting group membership. All the
known species are found exclusively in terrestrial and epiphytic bromeliads (e. g.
Peixoto 1995; Oliveira and Navas, 2004).
Material and methods
All observations described were obtained either by direct observation or by
videotaping frogs in the field at night, using a Sony Handy Cam CCD TRV – 480 or
a Sony Digital DCR – HC36, both with a night vision system (Night Shot Plus). This
permitted the observer to get close (sometimes within centimetres) of the frogs
apparently without disturbance. We searched for calling males to locate suitable
bromeliads; observations and filming used these plants and males as foci. Sound
Figure 1. Map of southeastern Brazil with the type locality of the species in the Scinax
perpusillus group indicated. The location of three unnamed populations investigated in thecurrent study (S. sp1, S. sp2 and S. sp3) are also indicated. Note that for three species in the
State of Sao Paulo, the points represent small coastal islands not represented in this scale.
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analyses used the program SOUND RULER ACOUSTIC ANALYSIS (Version 0.9.4.1) with
sound digitized from the video camera. Once a bromeliad and calling male were
located, we searched for the presence of nearby females, which were identified by
their larger size. The behaviour of both the male and female was then recorded on
video from the time a female was detected until all behaviour relating to amplexus
and egg laying had ceased, or the couple escaped from our view. Descriptions of
behaviour were taken from direct observation in the field and from videos analysed
in the laboratory.
We collected data for S. littoreus (Itacoatiara, Municipality of Niteroi, State of
Rio de Janeiro – 22u589370 S, 43u019410 W; 300 m), S. perpusillus (Pao de Acucar,
Municipality of Rio de Janeiro, State of Rio de Janeiro – 22u579030 S, 43u099060 W;
sea level), Scinax sp1 (Fazenda Bom Jardim, Municipality of Mangaratiba –
22u559020 S, 44u069140 W; 180 m, and Ilha da Gipoia, Municipality of Angra dos
Reis, State of Rio de Janeiro – 23u029380 S, 44u219230 W; sea level), S. v-signatus
(Municipality of Petropolis, State of Rio de Janeiro – 22u329130 S, 43u129260 W;
860 m), Scinax sp2 (Municipality of Cariacica, State of Espırito Santo – 20u189030 S,40u269040 W; 200 m), and Scinax sp 3 (Praia do Avetureiro, Ilha Grande,
Municipality of Angra dos Reis, State of Rio de Janeiro – 23u109590 S, 44u189540
W; sea level). Although we observed Scinax sp1 calling from arboreal bromeliads,
because of the difficulty with accessibility at night and safety concerns, we only
filmed frogs on bromeliads naturally growing on the ground (Figure 2A). The three
unidentified species (S. sp1, S. sp2 and S. sp3) represent unnamed populations that
are in the process of formal description. We made observations and filmed during all
12 months of 2006. All the observed species are reproductively active after rains all
year round (although more individuals may be observed during the summer). All the
sites where observations were made had bromeliads growing naturally on graniterock faces.
Figure 2. (A) Alcantarea glauziouiana (Bromeliaceae) growing on a costal granite outcrop on
the basis of Sugar Loaf in Rio de Janeiro, were specimens of Scinax perpusillus are foundcalling at night. (B) Male Scinax v-signatus calling in head-down position on the leaf of a
terrestrial bromeliad in the Municipality of Petropolis in the State of Rio de Janeiro, Brazil.
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Results
We recorded 176 hours of observations – 30 hours of filming and 146 hours of direct
observations in the field (S. littoreus, 74 hours; S. perpusillus, 42 hours; S. v-signatus,
8 hours; S. sp1, 28 hours; S. sp2, 12 hours; and S. sp3, 8 hours). These observations
allowed us to distinguish a set of apparently stereotypical behaviours that wedescribe below, organized separately for males and females for each observed
species. A summary of the number of observations and time spent performing each
of these behaviours in our filming sample is presented in Table 1.
Calling males
We observed and recorded aspects of the behaviour of calling males of S. littoreus, S.
perpusillus, S. v-signatus and S. sp1. Males of these species usually call from the tip of
the bromeliad leaf [S. littoreus, 51 of 68 (75%) observations; S. perpusillus, 26 of 35
(74%); S. v-signatus, 18 of 23 (78%); and S. sp1, 18 of 42 (71%;)] with their heads
pointing to the interior of the bromeliad (Figure 2B). Although as many as five maleswere observed calling on a single bromeliad (observed for all six species), only one
male calls from a leaf. More frequently, only one male called from each plant.
Calling took place from sunset to dawn. In all six species investigated in this study,
males on the same or on a nearby plant formed pairs and alternated calls
(antiphony), such that little or no overlap between call notes would occur
(Figure 3A). After a pause in calling by males, calling would resume with one of
an alternating pair emitting notes at a faster rate and with fewer pulses (Figure 3B);
we have no data to determine whether resuming the call is always initiated by the
same individual. Before the interruption of a call, another sequence of notes would
be emitted, apparently signalling the end of a call session. When in pairs, both maleswould emit these ‘‘end notes’’ before stopping their vocalization (Figure 3C).
Intrusion by a male into an already occupied leaf resulted in a series of
stereotypical behaviours by both the resident male and the intruder (28 observations:
16 for S. littoreus, nine for S. perpusillus and three for S. v-signatus). On detecting the
Table 1. List of behavioural unities observed for males („„) and females (RR) for three species
in the Scinax perpusillus group
Behavioural unit Scinax littoreus Scinax perpusillus Scinax v-signatus
„„Calling forming duets 24.75¡6.6s (n563) 21.75¡3.20 s (n552) 30.4¡10.01s (n512)„ Stretching toe III – 5 to 9 s (n53) –
Intruding „ 2 to 9 s (n516) 1 to 8 s (n59) 0.5 to 3 s (n53)
„6„ amplexus – 6¡3 s (n518) –
RR inspecting leaf-tank 20.3¡4 s (n538) 20.4¡4 s (n529) 19.2¡2.4s (n531)
RR inspecting leaf-tank
and moving away
n51 n52 –
R touches „ before
amplexus
n59 n57 n52
Egg laying n538 n535 n59
Values between parentheses are mean¡standard deviation. Time was measured directly fromthe film, with the chronometer on the screen of the video program. Behavioural units are
explained in the text.
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intruder, the resident emitted a series of rapidly repeated notes (Figure 4). If the
intruder failed to react by moving away, the resident approached the intruder and
passed over him while calling rapidly. This behaviour (the crawling/passing over the
intruder) was repeated several times, during which time both males emitted the same
‘‘rapid’’ call. In S. perpusillus, calling was accompanied by both males alternately
folding and stretching their third toes (which could also be trembled faster) until the
intruder moved off to another leaf. In S. perpusillus we also observed that in a few
Figure 3. Oscillogram illustrating call interactions between two males of Scinax v-signatus(antiphony). (A) A male closer to the microphone calls („1) – higher amplitude variation – and
the other, farther from the microphone („2) enters the call. Note that the calls do not overlap.
(B) Initial notes of the call of both males. (C) Final notes of the call of both males.
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instances the intruding male would engage in amplexus with the resident male. When
this happened the resident would emit the same ‘‘rapid’’ call described above which
suggests that it may function as a release call as well as a territorial call.
Female before amplexus
We observed and collected data on females before amplexus for S. littoreus, S.
perpusillus and S. v-signatus. Females occurred at lower densities than males at all
locations for all six species (S. littoreus: 22 females, 120 males; S. perpusillus: 20
females, 100 males; S. v-signatus: three females, 20 females; S. sp1: five females and
21 males; S. sp2: two females, 10 males, S. sp3: two females, 15 males). They moved
between bromeliads and within a bromeliad, using the bottom of the leaves near the
water, sometimes squeezing within narrow spaces between the leaves to move from
one leaf to the next (observed in females of S. perpusillus, S. littoreus and S. v-
signatus). The sequence of behaviour that follows, with females entering the
bromeliad from near the base of the leaves, seems to indicate that, although the onset
of female activities seems to be influenced by the presence of a calling male, which
probably attracted her to the plant, the sequence of the behavioural repertoire may
not be influenced by him.
Once at the margin of the water, females turn their bodies and slowly dip their
hind limbs and lower trunk into the water. They remain with their body half
submerged for a while before submerging their whole body and swimming from side
to side of the pool. This behaviour may be repeated several times, with the female
moving from leaf base to leaf base, apparently unnoticed by the resident male. This
‘‘inspection’’ does not always terminate with an interaction between the female and
the resident male. In some instances the female moves away to another leaf or
bromeliad.
Figure 4. Oscillograms of four independently registered sections of the confrontation call of
Scinax v-signatus. Time scale is just for duration of each call section and does not represent the
duration of a single event of confrontation.
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Courtship and amplexus
We observed and collected data on courtship and amplexus only for S. littoreus, S.
perpusillus and S. v-signatus. In cases where the female remains in the leaf after
inspecting a bromeliad, she approaches the resident calling male near the tip of that
leaf. Once the male detects the female he increases his calling rate (Figure 5). The
female then moves towards the tip of the leaf and, upon passing the male, lightly
touches him with her snout or hand. She then continues moving past the male’s
calling site. The male follows the female and jumps on her back grasping her in
axillary amplexus, with his feet in her pelvic region. Immediately after engaging in
amplexus the male stops calling and remains silent during oviposition. The female,
with the male on her back, moves towards the water and on reaching it, rotates her
body through 180 degrees, positioning her vent close to the water surface. We
observed one male of S. v-signatus jump from one leaf to another to amplect a
female; in this case, there was no elaborate courtship behaviour before amplexus.
Egg deposition
We observed and collected data on egg laying for S. littoreus, S. perpusillus and S. v-
signatus. The female enters the water, hind limbs first and dives. She swims around the
pool while submerged. She finally emerges and anchors herself to the side of the leaf
with her front limbs, arches her back, and with her vent pointing upwards, lays a single
egg, which sticks to a leaf at the margin of the pool in the water (Figure 6A). Females
Figure 5. Oscillogram of the call when a female approaches a calling mail for Scinax v-
signatus and Scinax perpusillus.
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release at most three eggs (one at a time) in each pool, at intervals of a few secondsbetween oviposition (actual time not measured), performing the same sequence of
oviposition behaviours between postures. Before the female enters the water the male
moves his feet laterally, away from her waist. After egg deposition, the pair moves off to
another leaf and in some cases to another bromeliad and repeats deposition. The
sequence of pools the couple enters does not necessarily reflect what had been inspected
by the female previously. We were unable to follow pairs until the male released the
female but we did observe up to five depositions for couples of S. littoreus (n54) and S.
perpusillus (n53). On a few occasions we observed a pair of S. perpusillus (n52) move
onto a leaf where another male was calling. When this happened, the resident chased
the pair away using the same call as used against male intruders. Females of S. perpusillus do not arch their backs to lay the eggs. The pair floats near the margin of the
small pool and eggs are released while they are floating.
Figure 6. Example of the two observed aspects of egg-deposition site within the bromeliad by
different species of the Scinax perpusillus group. (A) Egg deposited attached to a leaf forming
the side of the tank in the water surface (Scinax v-signatus). (B) Egg deposited stuck to the leaf
outside the water (Scinax sp2 – Espırito Santo). Arrows indicate the eggs.
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Observations on unnamed species
The other three unnamed species also lay a reduced number of eggs; however
these are adhered to the leaves outside water (Figure 6B). In all species the eggs
are similar and are enveloped in a large gelatinous capsule. Although for these
species we observed up to 4 eggs laid together, we suspect they are from differentclutches because the embryos were in different stages of development. For the
undescribed species, we made no films or direct observation of courtship. The
only evidence of breeding was the presence of tadpoles and the eggs. A different
behavioural sequence may exist for those species that deposit the eggs outside the
water.
Discussion
Contrary to previous suggestions (Oliveira and Navas 2004), although males show
behaviours associated with territorial defence (defending sites for reproduction with
acoustic displays, visual displays and physical interactions), male choice of abromeliad, or of a leaf and leaf-pool, does not necessarily imply that the female will
choose the same site for oviposition. Our observations show that female choice of
egg-deposition sites (which necessarily includes more than the pool on the leaf
defended by the male and may not include it) seems to be more important than the
choice of the male, as has been observed for other frogs (Jungfer and Weygoldt
1999). We never observed males ‘‘testing’’ the water, so we infer that if they indeed
choose a bromeliad, their criteria are based on something other than the quality of
the water, as has been suggested by Oliveira and Navas (2004). In this case, males
may be defending a territory so as to enhance their chances of being chosen by
females. Actually, the repertoire we described seems to fit the criteria for thecategorization of the reproductive behaviour of the S. perpusillus group as lekking
species, as described for Scinax ruber (Bourne 1992).
By chasing competitors away with little or no physical contact, males may be
saving energy and time to dedicate exclusively to calling. Although apparently
contradictory, coordinating their calls and engaging in antiphony may represent an
advantage, even in an apparently highly competitive environment, as evidenced by
the number of physical interactions. By coordinating their calls, males may be
diminishing the noise that would result from coincident call emissions, and also
enhancing the quality of their signal by having it broadcast for a longer time. In this
way, by cooperating, males increase their chances of being found and chosen byfemales (Schwartz 1987). A more extensive investigation of these aspects is
underway. Another aspect of the calling behaviour that deserves comment relates
to the calling position of the males, which call with their heads pointing to the
interior of the bromeliad (head-down position of Faivovich 2002). By calling in this
way, males may enhance their chances of detecting an approaching female – enabling
them to modulate their call accordingly. The existence of a complex interaction
between males and females is supported by the repertoire of calls emitted by males in
different situations. In addition, observing males calling head-down in these species
of the S. perpusillus group indicates that, as proposed by Faivovich (2002), this
behavioural character may not represent a synapomorphy unique to the S. rostratus
species groups, and may be more widespread than previously suggested (Duellman
and Wiens 1992).
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We did not test for differences in the quality of the water or its influence on the
female’s choice of oviposition site, so we are unable to evaluate the behaviour of
‘‘inspecting’’ the water. However, we suspect that this inspection may serve a
function other than assessing water quality. Presumably, females may also be
absorbing water through their skin, so as to provide water for the egg-laying activity.
Further investigation of the species that lay eggs outside water is necessary so as tobetter understand these behaviours and their relationship with female perception of
the site for egg deposition.
The most striking reproductive feature of this group of Scinax relates to the reduced
clutch size and the partitioning of the clutch between bromeliad leaf-tanks, which
represents a previously undocumented strategy for hylid reproduction in phytotelmata.
Known frog strategies include small clutch size with cannibalism, non-feeding larvae,
and parental care (Jungfer 1996; Jungfer and Weygoldt 1999). The species of Scinax
reported here, and perhaps all other species in the S. perpusillus group, show yet
another possible adaptation for coping with the limitations imposed by phytotelmata,
splitting their clutch between several tanks, depositing at most three eggs in each tank(one at a time). Besides having obvious consequences with respect to larval survival,
because smaller numbers of larvae in a small pool increase the chance of surviving, this
strategy represents a major evolutionary change in comparison with other frogs in
general (Duellman and Trueb 1986) or congeners in particular (e.g. S. trapicheiroi , a
possible closer relative, may lay as many as 900 eggs; Rico et al. 2004). The ability to lay
one egg repeatedly requires that females have physiological control over this behaviour.
In addition, to fertilize one egg at a time males may have similar abilities to control the
release of sperm so as to be able to perform multiple-single egg fertilizations. The
suggestion that males may be able to sense the contractions of the female’s oviducts to
know when to release sperm (Duellman and Trueb 1986) would necessitate fine tuningof this behaviour in these species.
This reproductive behaviour is an additional trait unique to the S. perpusillus
group. Peixoto (1986, 1987) suggested that the group could be defined as using
bromeliads for reproduction and by having reduced webbing on the fingers and toes.
Pombal and Bastos (2003) considered the group to be monophyletic because of the
characteristics of their calls. We suggest that the splitting of the egg clutch and the
deposition of few eggs are characters unique to this group of frogs. Therefore, being
able to lay eggs in small clutches, up to three eggs at most, and to split the clutch into
several depositional events is here considered a potential additional synapomorphy
for these species.
Acknowledgements
During most of the field work we were helped by several people. Some went to the field just to
keep us company during the strenuous recording procedures, others helped us locate frogs and
with general field observations. To all these people we are grateful. Rogerio Lourenco helped
in the field and with digital image and sound processing. Discussion on the evolution of
behaviour was stimulated by conversations with our great friend and colleague Alexandre F.
B. de Araujo. He also helped with early versions of the manuscript. Joseph Mendelson III,
Mary S. Linn, Paula C. Eterovick, William E. Duellman and Julian Faivovich made
significant contributions to the manuscript. Part of the funds to observe insular frogs wasprovided by the Brazilian National Council of Scientific and Technological Development –
CNPq (Processo 471081/2004-3). We also benefited from funding by Fundacao Carlos Chagas
Journal of Natural History 215
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Filho de Amparo a Pesquisa do Estado do Rio de Janeiro – FAPERJ (Processo E-26/170.976/
2006). During this study R.A.S. was supported by a fellowship from CAPES.
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