ArticlePDF Available

Comparison of female and male vocalisation and larynx morphology in the size dimorphic foot-flagging frog species Staurois guttatus Herpetological Journal

Authors:

Abstract and Figures

In anurans, males have larger laryngeal structures than females and produce conspicuous species-specific calls in various social contexts. Knowledge of female vocalisations is not well established and we start by summarising available spectral and behavioural information on calls in females. We then present novel data on female and male calls in Staurois guttatus and ask how larynx morphology influences call characteristics. While there was no difference in the dominant frequency between the sexes, sound pressure of female calls was lower than in males suggesting that they could be masked by ambient stream noise in the natural habitat. In an experimental setup, unreceptive females started calling when approached by a male less than 30 cm away, indicating an agonistic function of calling behaviour. In accordance with the overall size dimorphism in S. guttatus, laryngeal muscles as analysed by microCT were larger in females than in males whereas a reverse dimorphism was reported for most anuran species with silent and vocal females. We argue that in noisy environments such as streams, small male larynx size associated with high frequency calls is advantageous due to reduced masking and discuss the functional differences and communalities in signalling behaviour between the sexes and in the genus Staurois.
Content may be subject to copyright.
187
Comparison of female and male vocalisaon and larynx
morphology in the size dimorphic foot-agging frog species
Staurois guatus
Doris Preininger1,2, Stephan Handschuh3, Markus Boeckle4, Marc Sztatecsny2 & Walter Hödl2
1Vienna Zoo, Maxingstraße 13b, 1130 Vienna, Austria
2Department of Integrave Zoology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria
3VetCore Facility for Research, Imaging Unit, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria
4Department for Psychotherapy and Biopsychosocial Health, Donau-Universität Krems, Doktor-Karl-Dorrek-Straße 30, 3500 Krems, Austria
Herpetological Journal FULL PAPER
Correspondence: Doris Preininger (d.preininger@zoovienna.at)
Volume 26 (July 2016), 187–197
Published by the Brish
Herpetological Society
In anurans, males have larger laryngeal structures than females and produce conspicuous species-specic calls in various
social contexts. Knowledge of female vocalisaons is not well established and we start by summarising available spectral and
behavioural informaon on calls in females. We then present novel data on female and male calls in Staurois guatus and ask
how larynx morphology inuences call characteriscs. While there was no dierence in the dominant frequency between the
sexes, sound pressure of female calls was lower than in males suggesng that they could be masked by ambient stream noise
in the natural habitat. In an experimental setup, unrecepve females started calling when approached by a male less than 30
cm away, indicang an agonisc funcon of calling behaviour. In accordance with the overall size dimorphism in S. guatus,
laryngeal muscles as analysed by microCT were larger in females than in males whereas a reverse dimorphism was reported
for most anuran species with silent and vocal females. We argue that in noisy environments such as streams, small male larynx
size associated with high frequency calls is advantageous due to reduced masking and discuss the funconal dierences and
communalies in signalling behaviour between the sexes and in the genus Staurois.
Key words: anuran, female calls, laryngeal structures, noisy environment, visual signal
INTRODUCTION
The communication of anuran amphibians is
characterised by disnct sexual dierences in acousc
signalling behaviour. Males are well known for their
remarkable adversement calls to out-signal competors
and aract females (Wells, 1977). Most males are even
able to display a repertoire of calls depending on the social
context (Duellman & Trueb, 1986): for example courtship
calls are emied when detecng a female or during mang
and disnct territorial signals are used to display a more or
less aggressive defence of resources against rivals (Toledo
et al., 2014). Females on the other hand are generally
considered silent although female vocal behaviour has
been known for over 250 years (Rösel von Rosenhof,
1758). Female calls are produced by over 50 species in
various social contexts (Boistel & Sueur, 2002). The female
repertoire includes release calls when unwillingly clasped
by a male (e.g., Weintraub et al., 1985), reproducve calls
to aract and smulate mates (Schlaepfer & Figeroa-Sandí,
1998) and in some cases even aggressive or territorial
vocalisaons (Capranica, 1968; Wells, 1980; Stewart &
Rand, 1991). Several studies invesgated female defensive
vocalisaons (distress or alarm screams emied when
seized by a predator (Hödl & Gollmann, 1986; Toledo et
al., 2009; Toledo et al., 2011)). Aside from release and
defensive calls, reproducve and aggressive female calling
behaviour is currently described in detail for 21 species
(Table 1) and briey reported for further 12 species (Table
2). The female aggressive call of the common rocket frog
(Colostethus inguinalis) is a so, close range, low-intensity
chirp, given during encounters with either conspecific
sex, predominantly ending with contact and somemes
wrestling with the opponent (Wells, 1980). Vocalisaons
of bullfrog (Lithobates catesbeianus) and common coqui
(Eleutherodactylus coqui) females are similarly given in
defence of territories and if the intruder does not retreat,
a physical attack follows (Capranica, 1968; Stewart &
Rand, 1991). In all reported cases of female aggressive
calls, females exhibit a larger body size, a lower dominant
frequency and shorter call duraon than conspecic males
(Table 1).
Anuran call characteriscs are anatomically constrained
by body size, the morphology of the laryngeal structures
and neuronal mechanisms. Male body size, which
corresponds to laryngeal size (McClelland et al., 1996)
188
D. Preininger et al.
and vocal cord mass (Wilczynski et al., 1993), is inversely
correlated to calling frequency (Ryan & Brenowitz, 1985;
Roelants et al., 2004), generally enabling larger frogs to
produce lower pitched calls (Gerhardt & Huber, 2002).
Temporal characteristics are variable between and
within calls and are considered as dynamic call properes
(Gerhardt & Bee, 2006) mediated by the nervous
system (Walkowiak, 2006). Calls are mainly powered
by contracons of the trunk muscles (Wells, 2001) and
intensity is increased or concentrated to certain frequencies
by the vocal sac (Gridi-Papp, 2008). All females lack vocal
sacs and even in cases of larger body size have smaller
laryngeal structures (McClelland et al., 1997) and trunk
muscles (Gerhardt & Bee, 2006) compared to conspecic
males. Small larynx and trunk muscle size imply shorter
call duraon, higher or similar calling frequency and less
intense calls. Observaons of female call characteriscs,
however, do not always follow predicons derived from
body size and vary across species (Schlaepfer & Figeroa-
Sandí, 1998).
The most impressive distinction between body
size and call characteriscs comes from the concaved-
eared torrent frogs (Odorrana tormota) living near noisy
streams in China (Feng et al., 2006). Female body and
larynx size almost doubles that of males (Suthers et al.,
2006) but female reproducve vocalisaons have a higher
fundamental frequency extending into ultrasound (Feng
et al., 2002; Shen et al., 2008). The acousc signals of
males and females of O. tormota might avoid masking and
facilitate communicaon in low-frequency background
noise produced by streams (Narins et al., 2004). Frogs of
the genus Staurois also occur along fast-owing mountain
streams of Borneo and the Philippines. Alternavely and
addionally to high-frequency vocalisaons, males display
foot-agging signals in agonisc male-male encounters
(Grafe & Wanger, 2007; Preininger et al., 2009; Grafe
et al., 2012) to avoid masking in noisy stream habitats
(Boeckle et al., 2009; Grafe et al., 2012). In S. guatus
females also display territorial foot-agging signals in the
presence of signalling conspecic (Grafe & Wanger, 2007)
and heterospecic (e.g., S. latopalmatus; DP pers. obs.)
males. Staurois guatus is the only species of the genus
with reported female vocalisations (Grafe & Wanger,
2007). A few individuals of this diurnal ranid frog species,
endemic to Borneo, constuted the founding generaon
for a conservaon breeding and research program in the
Vienna Zoo (Preininger et al., 2012) and provided the
possibility to invesgate the infrequent calling behaviour
of females rarely observed in the eld.
The aim of this study was to (i) characterise female
calls and compare them to male calls in light of masking
interference of the environmental noise, (ii) compare
conspecific laryngeal structures and (iii) investigate
incidents triggering female calls to beer understand their
funcon and social context.
METHODS
Study site and acousc recordings
We studied a populaon of Staurois guatus from March
to April 2010 in the Ulu Temburong Naonal Park, Brunei
Darussalam, Borneo (see Grafe et al., 2012 for details on
the study site), where we recorded male and female calls
in the frogs’ natural habitat. From our study populaon
we imported ve males and six females to the Vienna Zoo,
Austria, where all proceeding experiments and recordings
were conducted from April to June 2011 in a bio-secure
container facility (Preininger et al., 2012).
In the eld, we recorded adversement calls of ve male
S. guatus from distances of 1 m using direconal (sound
left) and omni-directional (sound right) microphones
(Sennheiser ME 66, ME 62) and a digital recorder (Zoom
HN4, see Grafe et al. 2012 for details on the recording
methods) at mean temperatures of 25.5°C (±SE 0.08).
Individuals at the Vienna Zoo were separated and
housed in terraria sized 0.6 x 1 m with constantly owing
water and several tree branches with large leaves (the
preferred nightly resting sites) and mean temperature
of 24.5°C (±SE 0.03). Aer an adapon period of three
weeks, all six females were sll unrecepve (no visible
eggs) and consistently perched on the same branches in
their terraria. We recorded female vocalisaons using a
direconal microphone (Sennheiser Me 66), placed 1m
from the focal individual, connected to a digital recorder
(Zoom HN4; sengs: 44.1 kHz, 16-bit resoluon). We also
measured peak sound pressure level (SPL) with a sound
level meter (Voltkraft SL-100, Germany: settings: fast/
max) during each sound recording at a distance of 1 m
to the focal individual. The A-lter frequency weighng
was used because it is approximately at from 1 to 8 kHz,
which comprises the call range of S. guatus. To reduce
reverberaon, the terrarium walls were lined with acousc
foam (egg-box prole, 40 mm deep) and a 5 x 5 cm grid
was drawn on the foam to esmate distances between the
observed individuals.
Call analysis
To describe spectral and temporal call parameters, we
used recordings from the directional microphone and
analysed call duraon, note duraon, mean-, minimum-
and maximum frequency. The acousc features of stereo
recordings were extracted and measured using custom
built programs in PRAAT v. 5.2.22 DSP package (Boersma &
Weenik, 2011) that automacally logged these variables in
an output le (Grafe et al., 2012; Preininger et al., 2013a).
To assess the relatedness of female calls recorded in the
eld (n=2) and the zoo (n=6), we randomly selected 20
notes of the mul-note calls in each case. We calculated
the Euclidean distance for each pair of calls entering the
me and frequency parameters note duraon, minimum-,
maximum- and mean frequency together and generated
an acoustic dissimilarity matrix using a transformed
value range between 0 and 1. We generated an expected
dissimilarity matrix, similar to the acoustic matrix, by
dening call pairs from the same locaon as most similar
(similarity=0) and from dierent locaons as most dierent
(similarity=1). We used a Mantel test to determine if the
dissimilarity matrices of observaon-pair distances and
expected-pair distances are correlated (Bonnet & Van de
Peer, 2002). The probability of rejecng the null hypothesis
was based on 10000 randomisaon simulaons.
189
Female call of Staurois guttatus
We compared spectral and temporal characteriscs of
male and female calls using linear mixed models (LMMs).
The LMMs allow for repeated measurements of the same
individual to be ed in the model as random variable
and controlling for diering number of calls per individual
and note per call. The values of the parameter frequency
and note duraon were entered as dependent variables
in respecve LMMs, with male and female as predictor
variables. The idenes of individual (call) and call (note)
were again entered as nested random variables. The same
comparison was applied for call duraon and note number
with identities of individual (call) entered as nested
random variables.
Sound pressure (SP) values for comparisons of call
and noise were obtained by analysing omni-direconal
microphone recordings. A period of 1 s aer each male
advertisement call of field recordings was selected to
generate ambient noise files. To obtain SP values of
ambient noise within the frequency range of male and
female calls (ltered ambient noise) we applied a hand
band filter to the spectrum of ambient noise files for
frequencies from 3600–5100 Hz. The extracted relave SP
values for call and noise were transformed into absolute
SP (Pa) by dening the most intensive SP of the complete
sound le (SP absolute=SP relave*SP measured/SP most
intensive). ‘‘SP measured’’ corresponds to the maximum
sound pressure recorded in the eld or Zoo. To test the
hypothesis that S. guatus uses frequencies less masked
by background noise, we compared maximum SP values
of male advertisement calls recorded in the field and
female calls recorded in the Zoo to ambient noise and
ltered ambient noise The SP values of ambient noise,
ltered ambient noise, female and male calls with every
call consisng of 12 or 2 values for every note respecvely,
were entered in the LMM as a dependent variable,
with ambient noise, ltered ambient noise and calls as
predictor variables. The identities of individual (call)
and call (note) were entered in nested terms as random
variable. For post-hoc tests, we used Student’s t stasc
with sequenal Bonferroni correcon for alpha because
of repeated pairwise comparisons. All analyses were
performed using IBM SPSS v. 19.
Laryngeal structures
Three male and female S. guatus specimens originang
from our study populaon were obtained from the Vienna
Natural History Museum. The animals were completely
dehydrated in a graded series of ethanol and subsequently
stained in a soluon of 1% elemental iodine (I2) in absolute
ethanol (Metscher 2009) for seven days. Aer staining,
specimens were rinsed in absolute ethanol for several
hours and mounted in plasc tubes lled with absolute
ethanol for microCT-scanning. Specimens were scanned
using a SCANCO µCT 35 (SCANCO Medical AG, Brüsellen,
Switzerland) equipped with a Hamamatsu microfocus
x-ray source and a 2048*256 pixel digital x-ray detector.
Samples were scanned with 70keV source voltage and
114µA intensity, and projecon images were recorded
with an angular increment of 0.18° over a 180°rotaon.
Depending on specimen size, isotropic voxel size in the
reconstructed volumes varied between 6µm and 10µm.
Reconstructed image stacks were then imported into the
3D soware package Amira (v.5.3.3, Visage Imaging, Berlin,
Germany). In Amira, larynx musculature (for an anatomical
descripon see Trewavas, 1932) was manually segmented
in the Segmentation Editor, and muscle volumes were
extracted based on voxel segmentaon using the Material
Statistics tool. It is, however, important to note that
dehydraon and iodine staining cause some shrinkage of
so ssues, thus the measured muscle volumes do not
exactly resemble muscle volumes in the living animal.
RESULTS
We recorded 34 adversement calls of ve males in the
eld. During data collecon of male calls, we recorded two
coincidental vocalisaons of females on two occasions:
In the first case, a female sitting close to the stream
waterline was approached by the focal male. The female
A
B
C
Fig. 1. Multi-note calls of female (A-B) and male (C)
Staurois guatus. Waveform (±0.5 amplitude relave
20 μPa) and spectrogram of a female territorial call
(A) and a close-up of the two indicated notes (B). A
male advertisement call (C) recorded at the stream.
Spectrogram sengs: FFT method; window length: 0.005
s; number of me steps: 1000 and frequency steps: 1000;
Gaussian window; dynamic range: 40 dB (A-B), 20 dB (C).
190
D. Preininger et al.
Species Call
type
Mean dominant frequency Mean call duraon Mean SVL Reference
[kHz] (± SD) [ms] (± SD) [mm] (± SD)
Mang calls
Alydae
Alytes cisternasii
female 2 1.41 (0.05, n=19) 144 (173, n=13) 34-43aBosch & Márquez, 2001
male 1 1.44 (0.04, n=14) 149.4 (12.4, n=14) 33-39aMarquez & Verrell, 1991
Alytes muletensis
female 2 1.70 (0.16, n=11) 62 (15, n=11) 38b Bush, 1997
male 1 1.80 (0.14, n=28) 102 (17, n=28) 30.6 (2.4, n=28 )
Alytes obstetricans
female 2 1.38 (n=1) 119 (n=1) 47 (n=1) Heinzmann, 1970
male 1 1.34 (n=1) 162 (n=1) 45 (n=1)
Craugastoridae
Craugastor podiciferus
female 2 3.10 (n=3) 57,7 (n=3) 24.1 (n=1) Schlaepfer & Figeroa-Sandí, 1998
male 1 2.7 (n=2) 43,7 (n=2) 15.9 (n=1)
Ceratobatrachidae
Platymans viensis
female 2 0.92 (0.03, n=1) 22100 (5600, n=1) 56.5 (n=1) Boistel & Sueur, 1997
male 1 2.10 (0.10, n=1) 17400 (3400, n=1) 35.7 (n=1)
Dicroglossidae
Euphlycs cyanophlycs
female 2 0.74 (0.04, n=12)c20 (4, n=12 )cNA Roy et al., 1995
male 1 1.65 (0.04, n=34)c615 (155, n=34)c69 Daniels, 2005
Fejervarya limnocharis
female 2 1.53 (0.20, n=14)c61 (27, n=14)b60dRoy et al., 1995
male 1 2.14 (1.25, n=40)c 503 (101, n=40)b39-43d
Eleutherodactylidae
Eleutherodactylus guanahacabibes
female 2 2.03 (0.14, n=1) NA NA Diaz & Estrada, 2000
male 1 2.40 (0.53, n=5) NA NA
Eleutherodactylus cysgnathoides
female 2 3.12-4.60 (n=14)a48-462 (n=14)a 16.0–25.8a,b Serrano et al.,
male 1 3.17-4.96 (n=82)a 124-763 (n=82)a 16.0–23.5a,b pers. communicaon
Leptodactylidae
Leptodactylus syphax
female 2 1.01 (0.02, n=32) 19.1 (2.4, n=32) 71.7 (5.8, n=15) da Silva et al., 2008
male 1 1.80 (0.16, n=25) 72 (7.3, n=25) 74.7 (3.2, n=10) da Silva & Giarea, 2009
Pelobadae
Pelobates cultripes
female 2 0.58 (n=5) 68.8 (n=5) 74.6 (5.7, n=66) Lizana et al., 1994
male 2 0.54 (n=5) 69.0 (n=5) 71.9 (6.0, n=76)
Pelobates fuscus
female 2e5.93 (n=8)f NA 58.1 (2.7, n=8) Andreone & Piazza, 1990
male 1 4.47 (n=6)fNA 47.3 (3.5, n=6)
Table 1. Female reproducve and aggressive vocalisaons among anuran species, excluding release and distress
calls. Call types include (1) adversement-, (2) courtship- and (3) territorial calls. Mean dominant frequency, call
duraon, snout-vent length (SVL) and respecve standard deviaon (SD) are presented if not indicated otherwise.
NA=informaon not available, SE=standard error. b esmates retrieved from “amphibiaweb.org”; c n=number of calls,
not number of individuals recorded; d esmates retrieved from “frogsoorneo.org”; e also duet call data available; f
maximum frequency; g esmates for the species; h approximaon from spectrogram; i approximaon of the author.
191
Female call of Staurois guttatus
Pipidae
Xenopus laevis
female 2 1.20 (n=8) 500 (300, n=8) 110bTobias et al., 1998
male 1 1.80 (SE 0.03, n=33) NA 83bWetzel & Kelley, 1983
Ranidae
Babina daunchina
female 2 1.30 (n=2) 3195 (777, n=2) 45-50gCui et al., 2010
male 1 0.87 (0.47, n=18) 1740 (500, n=18) 45-50gChen et al., 2011
Clinotarsus curpes
female 2 0.93 (0.25, n=13) 60 (10, n=13) 59.2 (4.2, n=38) Krishna & Krishna, 2005
male 1 1.22 (0.49, n=22) 1090 (475, n=21) 46.2 (2.3, n=40)
Hylarana erythraea
female 2 1.05 (0.11, n=14)c32 (9, n=14)c78bRoy et al., 1995
male 1 2.46 (0.04, n=15)c224 (4, n=15)c48b
Lithobates virgapes
female 2 0.72 (n=2) NA 55 (n=2) Given, 1987
male 1 0.46-0.72 (n=2)aNA 52 (n=2)
Odorrana tormota
female 2 7.2 – 9.8a< 150 56 Shen et al., 2008
male 1 5-9 (n=21)
50-100; 100-400
(n=21) 32.5 Feng & Narins, 2008
Aggressive calls
Eleutherodactylidae
Eleutherodactylus coqui
female 3 1.10-1.50 (n=6)a1050 (SE 120, n=6) 44 (n=25) Stewart & Rand, 1991
male 3 1.40-1.60 (n=4)a1140 (SE 120, n=6) 34 (n=35)
Ranidae
Lithobates catesbeianus
female 3 0.3-0.5h 1400-1800a125b Capranica, 1968
male 3 0.5-0.8 400-600a95-110a,b
Staurois guatus
female 3 4.24 (0.08, n=6) 3060 (465, n=6) 50.1 (0.7, n=6) current study
male 1 4.67 (0.11, n=7) 301 (29, n=7) 36.1 (1.4, n=5) Grafe & Wanger, 2007
Dendrobade
Colostethus inguinalis
female 3 2.5iNA 27 (n=141) Wells, 1980
male 1 3.20-4.55 (n=6)aNA 25 (n=90)
Species Call
type
Mean dominant frequency Mean call duraon Mean SVL Reference
[kHz] (± SD) [ms] (± SD) [mm] (± SD)
started vocalising, crossed the stream and connued to
move away without the male following it. In the second
case, we accidentally disturbed a female at its resng site
and caused it to jump away. The female approached two
nearby males and started calling at a distance of approx.
0.5–1 m from them. Calling connued for 10 min before
it moved away without the males following it.
In the Vienna Zoo we recorded 76 calls of six females.
The females’ predictable behaviour made it possible to
place a male in their terraria and observe the behavioural
response for a period of 30 minutes. The males usually le
their plasc transport boxes within 5 minutes and started
advertising once they discovered the female. Female
calls could be smulated when a male approached the
female to distances less than 30 cm with and without
accompanied vocalisation. Male calls from distances
greater than 30 cm did not evoke calling in females.
Notably, when males actively moved from branch to
branch and gradually approached, females displayed a
series of calls somemes accompanied by foot-agging
behaviour. Staurois guatus females possess no vocal
sac and calls were emied with an open mouth (Video
1, see <hp://www.thebhs.org/pubs_journal_online_
appendices.html>). In response to female vocalisaons,
males either retreated from their posion or remained
moonless at their posion for the rest of the test period.
We never observed any physical contact between tested
individuals.
Males give a short two note call with narrow
frequency bands, whereas a female call consists of a
Table 1. Connued.
192
D. Preininger et al.
series of high pitched, frequency-modulated notes with
up to four harmonics (Fig. 1). Males keep their mouths
closed whereas females call with the mouth opened.
Zoo recordings of female calls had an average of 12
notes (range 3–35), and vocalisaons recorded in the
eld consisted of 21 and 25 notes. Euclidean distances
calculated from four acousc note parameters did not
correlate with the expected distances (Mantel test
Pearson correlation: r=-0.008, one-tailed p=0.446)
suggesng high similarity between female vocalisaons
recorded in the eld and in the Zoo.
Female vocalisaons diered in temporal parameters
from male calls, but apart from harmonics no dierences
in spectral call characteriscs could be observed (Table
2). Comparison of SP of male and female calls and noise
produced by the stream revealed signicant dierences
between the sexes (LMM: F3,808=184.670; p<0.001, Fig.
2). Male calls had higher estimated SP values (0.049
Pa±SE 0.003; 68 dB) than female vocalisaons (0.019
Pa±SE 0.002; 60 dB) (LMM: pairwise comparison: ß=0.03;
SE=0.002; t=16.869, p<0.001). Both, female and male
calls, however, had less SP than the noise produced by
the stream (0.064 Pa±SE 0.003; 70 dB, LMM: pairwise
comparison: female: ß=-0.044; SE=0.003; t=-16.657,
p<0.001; male: ß=-0.015; SE=0.003; t=-4.987, p<0.001).
The SP of male adversement calls exceeded the SP of the
stream ltered in the frequency range of the call (0.015
Pa±SE 0.003; 58 dB, LMM: pairwise comparison: ß=0.034;
SE=0.003; t=11.711, p<0.001), but the vocalisaon of
females did not (LMM: pairwise comparison: ß=-0.005;
SE=0.003; t=-1.692, p=0.091).
Female S. guatus were larger (snout-urostyle-length,
SUL±SE: 50.1±0.3 mm, n=6) and heavier (body mass±SE:
9.74±0.2 g, n=6) than males (SUL: 33.6±0.4 mm, n=14,
body mass: 2.69±0.07 g, n=14). The micro-CT scans
Family Species Call type Reference
Bombinatoridae
Bombina variegata courtship Savage, 1932
Ceratobatrachidae
Ceratobatrachus guentheri courtship Yoshimi et al., 1996
Conrauidae
Conraua a. alleni adversement Rödel, 2003
Dicroglossidae
Limnonectes leporinus courtship Emerson, 1992
Limnonectes poilani* courtship Orlov, 1997
Eleutherodactylidae
Eleutherodactylus angusdigitorum adversement Dixon, 1957
Hyperoliidae
Afrixalus fornasini aggressive Stewart, 1967
Hyperolius marmoratus marginatus aggressive Stewart, 1967
Leptodactylidae
Leptodactylus fallax courtship G. Garcia, M. Goetz & R. Boistel (pers. com.)
Ceratophryidae
Telmatobius culeus courtship G. Garcia & M. Goetz (pers. com)
Ranidae
Pelophylax esculentus aggressive Wahl, 1969
Pelophylax ridibundus adversement Frazer, 1983
Rhacophoridae
Polypedates leucomystax adversement Roy, 1997
Table 2. Female reproducve and aggressive vocalisaons menoned without available data on call characteriscs,
excluding release and distress calls. Call types as described by the authors. *presumably misidened Vietnam samples
(Frost, 2015)
Fig. 2. Comparison of sound pressure of female and male
calls of Staurois guttatus and the background noise.
Shown here are estimated means (points), standard
errors (boxes) and 95% condence intervals (whiskers)
of female territorial calls, male advertisement calls,
background noise and noise ltered in the frequency
range of female and male calls. Values without the same
superscript leer (a, b, c) dier signicantly at p<0.001.
193
Female call of Staurois guttatus
revealed laryngeal muscles of females to have a higher
volume than those of males (Table 3). On average the
dilator and constrictor muscle of females respecvely
had 70% and 66% more volume than in males. We were
unable to measure vocal cord size from the museum
samples due to preservaon eects, however, laryngeal
structures of all three female samples exceeded those of
males (Fig. 3).
DISCUSSION
Female Staurois guatus emit high pitched calls with an
open mouth that do not dier from male adversement
calls in their dominant frequency but show rich harmonics
and have a signicantly lower SP. The observed dierences
between the sexes most likely originate from the opened
mouth and the lack of a vocal sac in females. The vocal sac
enhances calling ecacy by recycling air and amplifying
the signal (Rand & Dudley, 1993; reviewed in Starnberger
et al., 2014). During calls with open mouth the whole
pulmonary volume is exhaled. These vocalisaons are
generally produced during defensive calls to startle
a predator or interrupt an attack (Hödl & Gollmann,
1986; Toledo et al., 2009). The open mouth likely has
an addional relevance as defensive or agonisc visual
signal. In some species, including S. guttatus, males
perform open mouth displays without vocalisation
during agonisc male-male encounters (Hartmann et al.,
2005; Grafe & Wanger, 2007; Toledo et al., 2011). While
calling an opened mouth causes call energy to spread
over a range of harmonics as demonstrated by arcially
generated calls on euthanised male frogs (Gridi-Papp,
2008). Accordingly, a closed mouth causes the dominant
frequency to be more intense and concentrated in
a narrower frequency range (Gridi-Papp, 2008) as
observed in the male S. guatus call. Gridi-Papp (2008)
and Purgue (1995) suggest that radiang structures and
the frog’s ssue act as lter to narrow the bandwidth of
the call. In addion, laryngeal anatomy contributes to the
heterotypical call characteriscs in anurans. Laryngeal
structures and muscles in male frogs are generally twice
the size of females (McClelland & Wilczynski, 1989;
McClelland et al., 1997). The sexual dimorphism is also
consistent in species with vocalising males and females
(Sassoon & Kelley, 1986; Yager, 1996) corresponding to
less intense and shorter female calls (Emerson & Boyd,
1999). Surprisingly, this common sexual size dimorphism
was reversed in S. guatus with laryngeal muscles being
larger in females. Despite larger muscle size, SPL of female
calls was lower than in males and calls were masked
by noise of the stream measured at a distance of 1 m.
However, females started calling when the distance of an
approaching male was below 30 cm in the experimental
setup. At this inter-individual distance, the reported SPL
of calls would almost triple and improve female acousc
conspicuousness for perceiving males. Male calls need to
be detectable at larger distances to aract females and
detecon and discriminaon of male calls in the genus
Staurois are enhanced by high frequencies (Grafe &
Wanger, 2007; Boeckle et al., 2009; Grafe et al., 2012). As
male body size correlates with vocal cord mass and call
frequency (Gerhardt & Huber, 2002; Roelants et al., 2004;
Narins et al., 2007), sexual selecon might have favoured
smaller males in stream dwelling frogs that produce high
Call parameter Female (n=6) Male (n=5) LMM results
mean frequency [Hz] 4234 (SE 34) 4195 (SE 50) F1/761=0.813; p=0.367
minimum frequency [Hz] 3661 (SE 29) 3699 (SE 45) F1/761=0.884; p=0.347
maximum frequency [Hz] 4807 (SE 41) 4747 (SE 62) F1/761=1.279; p=0.258
call duraon [s] 3.06 (SE 0.19) 0.22 (SE 0.28) F1/106=68.443; p<0.001
note number/call 12.1 (SE 0.7) 1.8 (SE 0.9) F1/106=73.943; p<0.001
note duraon [s] 0.033 (SE 0.001) 0.041 (SE 0.001) F1/765=75.769; p<0.001
Table 3. Comparison of spectral and temporal call characteriscs of male and female Staurois guatus. Values represent
esmated means, standard errors (SE) and p-values of Linear Mixed Models (LMM).
Characteriscs Females Males
1 2 3 mean (±SD) 1 2 3 mean (±SD)
Snout-urostyle-length (mm) 49.1 47 48.2 48.1 (1.1) 32.6 33.4 33.3 33.1 (0.4)
Head width (mm) 15.2 14.2 13.2 14.2 (1.0) 9.5 9.2 9.6 9.4 (0.2)
Body mass (g) 9.91 8.17 7.07 8.38 (1.43) 2.17 2.29 2.56 2.34 (0.20)
Dilator muscle volume (mm3) 2.664 2.601 2.960 2.741 (0.192) 1.794 1.182 1.851 1.609 (0.371)
Constrictor muscle volume (mm3) (mm3) - 1.263 1.549 1.406 (0.202) 0.836 0.848 - 0.842 (0.008)
Table 4. Absolute and mean values of morphological characteriscs of 3 female and 3 male specimens of Staurois
guatus scanned in the micro-CT.
194
D. Preininger et al.
pitched calls less masked by low-frequency stream noise
(also see Fig. 5 in Boeckle et al., 2009). The only other
report about a larger larynx in females compared to male
frogs comes from the ultrasonic signalling species O.
tormota also living along streams and waterfalls (Suthers
et al., 2006).
The note number of two female calls recorded in the
eld was higher than the average note number recorded
under Zoo sengs. In male and female aggressive calls
of E. coqui shorter vocalisaons are used as low level
warnings and longer calls when an aack is imminent
(Stewart & Rand, 1991). We never observed an aack
or aggressive behaviour in S. guatus; however, males
foot agged in succession to female calls. Foot agging
functions as agonistic signal to defend perching sites
(Preininger et al., 2009; Preininger et al., 2013b) and
most likely evolved from kicking aacks (Preininger et al.,
2013c). We suggest female calls followed by foot-agging
displays are similar to male signals in their behavioural
context and could constitute a stereotyped agonistic
display ritualised from a former costly aggressive
behaviour of direct contact.
Acousc and visual signals of anuran communicaon
as well as the morphological and physiological features
involved in their production are shaped by sexual
selection. Signallers influence receivers via sensory
stimulus, which in turn provides information to the
receiver. Several anuran call characteriscs are related
to physiological and morphological attributes (Ryan,
1988; Gerhardt & Huber, 2002). Males adverse not only
their species identy, locaon and size, but also sexual
recepveness with aracve or aggressive calls (Wells &
Schwartz, 2006). Likewise female signals emied to show
recepveness or unrecepveness (e.g., Ellio & Kelley,
2007) can be used by male receivers to determine the
relevant response. In the present study, males responded
to female calls by stopping adversing and approaching
the female. According to the behavioural context, we
propose that vocalisaons in S. guatus idenfy females
as potenal territorial competors and/or non-recepve
individuals rather than potenal mates.
Staurois guttatus is the only species of the genus
Staurois with reported female calls. Males of sympatric
S. latopalmatus and S. parvus also display agonistic
foot-flagging signals in succession to high frequency
calls and experience similar environmental background
noise (Boeckle et al., 2009; Preininger et al., 2009;
Grafe et al., 2012), but female signalling behaviour
was never observed. The reproductive behaviour in
the three Staurois species seems very similar, but only
male and female S. guatus foot ag during amplexus
when approached by conspecic or heterospecic (S.
latopalmatus) males (DP pers. obs.). Hence, divergent
female signalling behaviour in S. guatus can currently
not be explained by evoluonary responses to diering
environmental factors or reproductive character
displacement, its functional significance in regard to
related species remains unanswered. Grafe and Wanger
(2007) reported an addional so and short call in female
S. guatus, which could not be observed in the present
study. While mate locaon is the most common context
for female reproducve calls (Emerson & Boyd, 1999),
the call repertoire is probably much larger than currently
known. Further investigations of the genus Staurois
would help to expand our understanding of the anuran
communicaon system and evoluonary development
that shapes morphological and physiological features for
signalling in closely related species.
Fig. 3. Cross secons of female and male Staurois guatus retrieved from microCT-scans showing laryngeal structures.
(A) female, (C) male, br brain, c constrictor muscle, d dilator muscle, hy postero-medial process of hyoid plate, ie inner
ear, la larynx, pg pectoral girdle, ph pharynx, sk skull. (For absolute values of dilator and constrictor muscle volume
see Table 4).
AB
195
Female call of Staurois guttatus
ACKNOWLEDGEMENTS
We thank the Universi Brunei Darussalam and the sta
of the Kuala Belalong Field Studies Centre (KBFSC). Special
thanks to T.U. Grafe for his assistance in the eld. We are
grateful for the support of D. Schraer, A. Weissenbacher,
T. Wampula and the sta of the rainforest house from the
Vienna Zoo. We also thank two anonymous reviewers
and F. Toledo for their valuable input. The study was
supported by the Austrian Science Fund (FWF): P22069
and P25612, the Society of Friends of the Vienna Zoo,
and the University Vienna.
REFERENCES
Andreone, F. & Piazza, R. (1990). A bioacoustic study on
Pelobates fuscus (Amphibia: Pelobatidae). Bollettino di
Zoologia 57, 341–349.
Boeckle, M., Preininger, D. & Hödl, W. (2009). Communicaon
in noisy environments I: Acoustic signals of Staurois
latopalmatus Boulenger 1887. Herpetologica 65, 154–165.
Boersma, P. & Weenik, D. (2011). PRAAT: Doing phonecs by
computer (version 5.2.22) [computer program]. Available
from: <http://www.praat.org/>. Accessed: 10 September
2011.
Boistel, R. & Sueur, J. (1997). Comportement sonore de la femelle
de Platymans viensis (Amphibia, Anura) en l’absence du
mâle. Comptes Rendus de l’Académie des Sciences - Series III
- Sciences de la Vie 320, 933–941.
Boistel, R. & Sueur, J. (2002). XVIIth Symposium of the
internaonal bioacousc council - Abstracts. Bioacouscs 13,
77–102.
Bonnet, E. & Van de Peer, Y. (2002). zt: a soware tool for simple
and paral Mantel tests. Journal of Stascal soware 7,
1–12.
Bosch, J. & Márquez, R. (2001). Female courtship call of
the Iberian midwife toad (Alytes cisternasii). Journal of
Herpetology 35, 647–652.
Bush, S.L. (1997). Vocal behavior of males and females in the
Majorcan midwife toad. Journal of Herpetology 31, 251–257.
Capranica, R.R. (1968). The vocal repertoire of the bullfrog
(Rana catesbeiana). Behaviour 31, 302–325.
Chen, Q., Cui, J., Fang, G., Brauth, S.E. & Tang, Y. (2011). Acousc
analysis of the adversement calls of the music frog, Babina
daunchina. Journal of Herpetology 45, 406–416.
Cui, J., Wang, Y., Brauth, S. & Tang, Y. (2010). A novel female call
incites male-female interacon and male-male compeon
in the Emei music frog, Babina daunchina. Animal Behaviour
80, 181–187.
da Silva, W., Giarea, A. & Facure, K. (2008). Vocal repertory
of two species of the Leptodactylus pentadactylus group
(Anura, Leptodactylidae). Contemporary Herpetology 1, 1–6.
da Silva, W.R. & Giarea, A.A. (2009). On the natural history
of Leptodactylus syphax with comments on the evoluon of
reproducve features in the L. pentadactylus species group
(Anura, Leptodactylidae). Journal of Natural History 43, 191–
203.
Daniels, R.J.R. (2005). Amphibians of Peninsular India.
Hyderabad: University Press (India) Private Limited.
Diaz, L.M. & Estrada, A.R. (2000). The male and female
vocalizations of the Cuban frog Eleutherodactylus
guanahacabibes (Anura:Leptodactylidae). Caribbean Journal
of Science 36, 328–331.
Dixon, J.R. (1957). Geographic variaon and distribuon of the
genus Tomodactylus in Mexico. Texas Journal of Science 9,
379–409.
Duellman, W.E. & Trueb, L. (1986). Biology of Amphibians. New
York: McGraw-Hill Publishing Company.
Elliott, T.M. & Kelley, D.B. (2007). Male discrimination of
recepve and unrecepve female calls by temporal features.
Journal of Experimental Biology 210, 2836–2842.
Emerson, S.B. (1992). Courtship and nest-building behavoir of a
Bornean frog, Rana blythi. Copeia 1992, 1123–1127.
Emerson, S.B. & Boyd, S.K. (1999). Mating vocalizations of
female frogs: control and evoluonary mechanisms. Brain,
Behavior and Evoluon 53, 187–197.
Feng, A.S. & Narins, P.M. (2008). Ultrasonic communicaon in
concave-eared torrent frogs (Amolops tormotus). Journal of
Comparave Physiolology A: Neuroethology, Sensory, Neural,
and Behavioral Physiology 194, 159–67.
Feng, A.S., Narins, P.M. & Xu, C.H. (2002). Vocal acrobacs in
a Chinese frog, Amolops tormotus. Naturwissenschaen 89,
352–356.
Feng, A.S., Narins, P.M., Xu, C.H., Lin, W.Y., et al. (2006).
Ultrasonic communicaon in frogs. Nature 440, 333–336.
Frazer, D. (1983). Reples and amphibians in Britain. London:
Collins.
Frost, D.R. (2015). Amphibian Species of the World: an Online
Reference. Version 6.0 (02/2015). Electronic Database
accessible at <http://research.amnh.org/herpetology/
amphibia/index.html>. American Museum of Natural History,
New York, USA.
Gerhardt, H.C. & Bee, M. (2006). Recognion and localizaon
of acousc signals. In Hearing and Sound Communicaon in
Amphibians, 113–146. Narins, P., Feng, A., Fay, R. & Popper,
A. (eds). New York: Springer.
Gerhardt, H.C. & Huber, F. (2002). Acoustic communication
in Insects and Anurans: Common problems and diverse
soluons. Chicago: University of Chicago Press.
Given, M.F. (1987). Vocalizaons and acousc interacons of
the carpenter frog, Rana virgapes. Herpetologica 43, 467–
481.
Grafe, T.U., Preininger, D., Sztatecsny, M., Kasah, R., et al.
(2012). Mulmodal communicaon in a noisy environment:
A case study of the Bornean Rock Frog Staurois parvus. PLoS
One 7, e37965.
Grafe, T.U. & Wanger, T.C. (2007). Mulmodal signaling in male
and female foot-agging frogs Staurois guatus (Ranidae):
An alerng funcon of calling. Ethology 113, 772-781.
Gridi-Papp, M. (2008). The structure of vocal sounds produced
with the mouth closed or with the mouth open in treefrogs.
The Journal of the Acouscal Society of America 123, 2895–
2902.
Hartmann, M.T., Giasson, L.O.M., Hartmann, P.A. & Haddad,
C.F.B. (2005). Visual communicaon in Brazilian species of
anurans from the Atlanc forest. Journal of Natural History
39, 1675–1685.
Heinzmann, U. (1970). Untersuchungen zur Bio-Akusk und
Ökologie der Geburtshelferkröte, Alytes o. obstetricans
(Laur.). Oecologia 5, 19–55.
Hödl, W. & Gollmann, G. (1986). Distress calls in neotropical
frogs. Amphibia-Replia 7, 11–21.
196
D. Preininger et al.
Krishna, S.N. & Krishna, S.B. (2005). Female courtship calls
of the lier frog (Rana curpes) in the tropical forests of
Western Ghats, South India. Amphibia-Replia 26, 431–435.
Lizana, M., Márquez, R. & Martín-Sánchez, R. (1994).
Reproductive biology of Pelobates cultripes (Anura:
Pelobatidae) in central Spain. Journal of Herpetology 28,
19–27.
Marquez, R. & Verrell, P. (1991). The courtship and mang of
the Iberian midwife toad Alytes cisternasii (Amphibia: Anura:
Discoglossidae). Journal Of Zoology 225, 125–139.
McClelland, B.E. & Wilczynski, W. (1989). Sexually dimorphic
laryngeal morphology in Rana pipiens. Journal of Morphology
201, 293–299.
McClelland, B.E., Wilczynski, W. & Rand, A.S. (1997). Sexual
dimorphism and species dierences in the neurophysiology
and morphology of the acousc communicaon system of
two neotropical hylids. Journal of Comparave Physiology A
180, 451–462.
McClelland, B.E., Wilczynski, W. & Ryan, M.J. (1996). Correlaons
between call characteriscs and morphology in male cricket
frogs (Acris crepitans). The Journal of Experimental Biology
199, 1907–1919.
Metscher, B.D. (2009). MicroCT for developmental biology:
A versale tool for high-contrast 3D imaging at histological
resoluons. Developmental Dynamics 238, 632–640.
Narins, P.M., Feng, A.S., Fay, R.R. & Popper, A.N. (2007). Hearing
and sound communicaon in amphibians. New York: Springer.
Narins, P.M., Feng, A.S., Lin, W., Schnitzler, H.-U., Denzinger,
A., Suthers, R.A. & Xu, C. (2004). Old World frog and bird
vocalizaons contain prominent ultrasonic harmonics. The
Journal of the Acouscal Society of America 115, 910–913.
Orlov, N. (1997). Breeding behavior and nest construcon in a
Vietnam frog related to Rana blythi. Copeia, 464–465.
Preininger, D., Boeckle, M., Freudmann, A., Starnberger, I., et
al. (2013a). Mulmodal signaling in the Small Torrent Frog
(Micrixalus saxicola) in a complex acoustic environment.
Behavioral Ecology and Sociobiology 67, 1449–1456.
Preininger, D., Boeckle, M. & Hödl, W. (2009). Communicaon
in noisy environments II: Visual signaling behavior of male
foot-agging frogs Staurois latopalmatus. Herpetologica 65,
166–173.
Preininger, D., Boeckle, M., Sztatecsny, M. & Hödl, W. (2013b).
Divergent receiver responses to components of mulmodal
signals in two foot-agging frog species. PLoS One 8, e55367.
Preininger, D., Stiegler, M.J., Gururaja, K., Vijayakumar, S.,
Torsekar, V.R., Sztatecsny, M., Hödl, W. (2013c). Geng a kick
out of it: mulmodal signalling during male–male encounters
in the foot-flagging frog Micrixalus aff. saxicola from the
Western Ghats of India. Current Science 105, 1735-1740.
Preininger, D., Weissenbacher, A., Wampula, T. & Hödl, W.
(2012). The conservaon breeding of two foot-agging frog
species from Borneo, Staurois parvus and Staurois guatus.
Amphibian and Reple Conservaon 5, 45–56.
Purgue, A.P. (1995) The Sound Broadcasting System of the
Bullfrog. In. The University of Utah, Thesis (Ph.D.) pp 4184
Rand, A.S. & Dudley, R. (1993). Frogs in helium: The anuran
vocal sac is not a cavity resonator. Physiological Zoology 66,
793–806.
Rödel, M.-O. (2003). The amphibians of Mont Sangbé Naonal
Park, Ivory Coast. SALAMANDRA 39, 91–110.
Roelants, K., Jiang, J. & Bossuyt, F. (2004). Endemic ranid
(Amphibia: Anura) genera in southern mountain ranges of
the Indian subcontinent represent ancient frog lineages:
Evidence from molecular data. Molecular Phylogenecs and
Evoluon 31, 730–740.
Rösel von Rosenhof, A.J. (1758). Historia Natvralis Ranarvm
Nostravm in qua omes earum proprietates. Die natürliche
Historie der Frösche hiesigen Landes. In. Johann Josef
Fleischmann, Nürnberg
Roy, D. (1997). Communicaon signals and sexual selecon in
amphibians. Current science 72, 923–927.
Roy, D., Borah, B. & Sarma, A. (1995). Analysis and signicance
of female reciprocal call in frogs. Current science 69, 265–270.
Ryan, M.J. (1988). Constrains and paerns in the evoluon
of anuran acousc communicaon. In The evoluon of the
amphibian auditory system, 637–677. Fritzsch, B., Ryan, M.J.,
Wilczynski, W., Hetherington, T.E. & Walkowiak, W. (eds).
New York: John Wiley and Sons.
Ryan, M.J. & Brenowitz, E.A. (1985). The role of body size,
phylogeny, and ambient noise in the evoluon of bird song.
The American Naturalist 126, 87–100.
Sassoon, D. & Kelley, D.B. (1986). The sexually dimorphic larynx
of Xenopus laevis: Development and androgen regulaon.
American Journal of Anatomy 177, 457–472.
Savage, R.M. (1932). The spawning, voice, and sexual behaviour
of Bombina variegata variegata. Proceedings of the Zoological
Society of London 102, 889–898.
Schlaepfer, M.A. & Figeroa-Sandí, R. (1998). Female reciprocal
calling in a Costa Rican leaf-litter frog Eleutherodactylus
podiciferus. Copeia 1998, 1076–1080.
Shen, J.-X., Feng, A.S., Xu, Z.-M., Yu, Z.-L., Arch, V.S., Yu, X.-J.
& Narins, P.M. (2008). Ultrasonic frogs show hyperacute
phonotaxis to female courtship calls. Nature 453, 914–916.
Starnberger, I., Preininger, D. & Hödl, W. (2014). The anuran
vocal sac: a tool for mulmodal signalling. Animal Behaviour
97, 281–288.
Stewart, M.M. (1967). The Amphibians of Malawi. New York:
State University Press.
Stewart, M.M. & Rand, A.S. (1991). Vocalizaons and the defense
of retreat sites by males and female frogs, Eluetherodactylus
coqui. Copeia 1991, 1013–1024.
Suthers, R.A., Narins, P.M., Lin, W.-Y., Schnitzler, H.-U., et al.
(2006). Voices of the dead: Complex nonlinear vocal signals
from the larynx of an ultrasonic frog. The Journal of the
Acouscal Society of America 120, 3325–3325.
Tobias, M.L., Viswanathan, S.S. & Kelley, D.B. (1998). Rapping,
a female recepve call, iniates male–female duets in the
South African clawed frog. Proceedings of the National
Academy of Sciences of the United States of America 95,
1870–1875.
Toledo, L., Marns, I., Bruschi, D., Passos, M., et al (2014). The
anuran calling repertoire in the light of social context. Acta
ethologica, 1–13.
Toledo, L.F., Fernando, C. & Haddad, B. (2009). Defensive
vocalizaons of neotropical anurans. South American Journal
of Herpetology 4, 25–42.
Toledo, L.F., Sazima, I. & Haddad, C.F.B. (2011). Behavioural
defences of anurans: an overview. Ethology Ecology &
Evoluon 23, 1–25.
Trewavas, E. (1932). The hyoid and larynx of the anura.
Philosophical Transacons of the Royal Society of London
Series B, Containing Papers of a Biological Character 222,
197
Female call of Staurois guttatus
401–527.
Wahl, M. (1969). Untersuchungen zur Bio-Akustik des
Wasserfrosches Rana esculenta (L.). Oecologia 3, 14–55.
Walkowiak, W. (2006). Call production and neural basis of
vocalization. In Hearing and Sound Communication in
Amphibians, 87–112. Narins, P., Feng, A., Fay, R. & Popper, A.
(eds). New York: Springer.
Weintraub, A.S., Kelley, D.B. & Bockman, R.S. (1985).
Prostaglandin E2 induces receptive behaviors in female
Xenopus laevis. Hormones and Behavior 19, 386–399.
Wells, K. (2001). The energecs of calling in frogs. Washington,
DC: Smithsonian Instuon Press.
Wells, K. & Schwartz, J. (2006). The behavioral ecology of anuran
communicaon. In Hearing and Sound Communicaon in
Amphibians, 44–86. Narins, P., Feng, A., Fay, R. & Popper, A.
(eds): Springer New York.
Wells, K.D. (1977). The social behaviour of anuran amphibians.
Animal Behaviour 25, Part 3, 666-693.
Wells, K.D. (1980). Behavoral ecology and social organizaon
of a dendrobad frog (Colostethus inguinalis). Behavioral
Ecology and Sociobiology 6, 199–209.
Wetzel, D.M. & Kelley, D.B. (1983). Androgen and gonadotropin
eects on male mate calls in South African clawed frogs,
Xenopus laevis. Hormones and Behavior 17, 388–404.
Wilczynski, W., McClelland, B.E. & Rand, A.S. (1993). Acousc,
auditory, and morphological divergence in three species of
neotropical frog. Journal of Comparave Physiology A 172,
425–438.
Yager, D.D. (1996) 8 Sound production and acoustic
communication in Xenopus borealis. In: The Biology of
Xenopus, 121–141. Tinsley, R.C., Kobel, H.R. (eds.). New York:
Oxford University Press.
Yoshimi, D.H., Payne, D.A. & Slavens, F.L. (1996). Maintenance
and captive breeding of the Solomon Islands leaf frog
(Ceratobatrachus guentheri). In Advances in Herpetoculture,
23–32. Strimple, P.D. (eds): Spec. Publ., Int. Herp. Symp.
Accepted: 30 August 2015
... Vocalization in anuran females has been interpreted as a means to locate partners (Duellman & Trueb, 1994;Roy et al., 1995;Schlaepfer & Figueroa-Sandi, 1998;Emerson & Boyd, 1999). These calls have also been considered as signals that induce competitive behaviour (Cui et al., 2010) and intra-sexual agonistic displays (Stewart & Rand, 1991;Preininger et al., 2016;Goyes Vallejos et al., 2017). Female vocalization in anurans has been related to ecological and reproductive factors, such as prolonged and non-gregarious breeding patterns, relatively simple call structure (Schlaepfer & Figueroa-Sandi, 1998), male parental care and female-biased sex ratio (Bush, 1997). ...
... We hypothesized that calls will differ among populations, as geographical variation of acoustic signals occurs extensively in anurans (Gerhardt & Bee, 2007) and in the genus Eleutherodactylus in particular (Narins & Smith, 1986). We also expected that calls will differ between sexes having dissimilar body shape, because anatomical variations in vocal apparatus are related to differences in body size in various frog species (McClelland, Wilczynski & Ryan, 1996;Preininger et al., 2016). Alternatively, if preliminary observations indicate that these signals are invariant between sexes, their communicative function should be accounted for in terms of their potential involvement in sexual selection and adaptive processes. ...
... Call rate was excluded from these comparisons (see main text). (Emerson & Boyd, 1999;Potter, Bose & Yamaguchi, 2005; but see Preininger et al., 2016), the greater female dimensions in E. cystignathoides do not result in acoustic differences between sexes. Lynch (1970) reported that females of E. cystignathoides lack the characteristic male vocal sac found in other Eleutherodactylus species; however, females tend to inflate their throats like males when vocalizing. ...
Article
Full-text available
The production of advertisement calls in sexual contexts is predominantly an attribute of males in anurans. Female calls occur in a small proportion of species in which these signals typically differ from those of males. The occurrence of such vocalizations has been related to sexual recognition prior to courtship. In the present study, we compared acoustic variables of male and female advertisement calls of two populations of the neotropical frog Eleutherodactylus cystignathoides (Cope, 1877). In order to assess the potential for sexual recognition of these signals, their distinctiveness and variability were measured. Calls have a distinctiveness potential in dominant frequency and call duration, but such variation depends mostly on size differences among sexes, and divergence in call characteristics is larger between populations than between sexes. The restricted sexual differentiation in the advertisement calls of E. cystignathoides suggests that female advertisement calls are deceptive signals promoting male agonistic responses.
... Like the calls of male anurans, female calls can also have several functions related to reproduction (mate attraction and reciprocity to male calls), including nesting defence (Stewart and Rand 1991) and sexual mimicry to evaluate potential mates (Serrano and Penna 2018). In anuran species in which females produce calls, three calling patterns have been identified: (1) female advertisement calls are sexually dimorphic relative to males (Schlaepfer and Figueroa-Sandi 1998;Emerson and Boyd 1999;Goyes Vallejos et al. 2017), (2) females produce aggressive calls towards males during mating events (Cui et al. 2010;Preininger et al. 2016) or non-mating contexts (Capranica 1965;Stewart and Rand 1991); and (3) females produce sexually monomorphic signals that only differ depending on body size dissimilarities with those of males (Serrano and Penna 2018). ...
... In anurans, acoustic signals are known to modulate social interactions mostly in males (Bee 2016). Yet, female anurans can aggregate in lek choruses (Goyes Vallejos et al. 2017), and in some cases exhibit aggressive calls during social interactions (Capranica 1965;Preininger et al. 2016) and nesting defense (Stewart and Rand 1991). The social importance of female calls in our model species, however, could be related to other functions as described in several animal species. ...
... amount of chaos, repertoire size, call intensity) depends on age and pregnancy or if these modifications in calls occur based on the social context, requires a systematic monitoring of the ontogeny of vocal behaviour and playback studies. Rhinoderma darwinii illustrates a quite peculiar mode of female calling in anurans, as vocalizations have a monomorphic structure, a condition different from other anurans that also exhibit sexual role reversal, but produce sexual dimorphic vocal signals (Emerson and Boyd 1999;Preininger et al. 2016). Unexpectedly, given that few males carry out parental care and are the ones who presumably monopolize most of the reproductive events in R. darwinii, our data showed that OSR calculated with pregnant males switched in this species from female-to male-biased during the breeding season. ...
Article
Full-text available
Sexual signals in different animals are expected to be dimorphic when both sexes signal, but cases of monomorphism are known to occur, and we lack a clear understanding about the factors that modulate the level of sexual dimorphism in signals. In this study, we evaluated the hypothesis that the lack of dimorphism in sexual signals might evolve in systems experiencing temporal changing conditions of intra-sexual competition. We used the Darwin’s frog (Rhinoderma darwinii), a species with paternal care, as a model. We compared advertisement calls and examined call distinctiveness among females, pregnant and non-pregnant males in a wild population from Chiloé island, Chile. We also recorded the vocal activity of both sexes along the reproductive season. Additionally, we compared the acoustic properties of their advertisement calls in terms of sexual distinctiveness and individual repeatability. We found that the proportion of females and pregnant males vocalizing changed over time following distinct patterns. Females produced calls with lower dominant frequency and longer note and call durations than males, and these acoustic differences were related to body size differences between sexes, but only dominant frequency contributed significantly to the distinctiveness of calls between sexes. Also, individual repeatability was high, indicating that calling can be relevant for social recognition. Overall, our results suggest that mutual selective pressures could be involved in the limited dimorphism of the advertisement calls in Darwin’s frogs, as the sex ratio of individuals vocalizing (i.e. females vs. reproductive males) is reversed along the breeding period. Significance statement Whether sexually monomorphic signals are evidence of adaptive mutual choice or a by-product of genetic constraints on females remains as an open question. In species with exclusive parental care of males, it would be expected that males and females alternate their reproductive availability while performing slightly differentiated sexual signals. Using acoustic recordings and capture-recapture data of the Darwin’s frog, we found that advertisement calls of this frog tend to be monomorphic. Interestingly, the males performing parental care were calling actively and the population had a clear bias in the number of males. Males and females of this endangered frog called actively, but the vocalization rate of each sex peaked at different times along the breeding season. These findings open new questions about the mechanisms of sexual recognition under restricted signal dimorphism.
... Female calls are known for other leptodactylids, such as Leptodactylus syphax Bokermann, 1969and L. troglodytes Lutz, 1926(Silva et al. 2008, Kokubum et al. 2009). Dimorphic acoustic differences, such as the variation in call duration and range frequency in L. fuscus, occur in many other species in at least 11 anuran families (Preininger et al. 2016). Among the factors that may underlie these differences are body size (with females usually being larger than males), vocalization social function, presence of vocal sac that aids in call transmission (only in males), and laryngeal size and complexity (males with larger laryngeal structures than females) (Duellman and Trueb 1986, Monnet and Cherry 2002, Wells and Schwartz 2007, Wilkins et al. 2013, Toledo et al. 2014, Preininger et al. 2016. ...
... Dimorphic acoustic differences, such as the variation in call duration and range frequency in L. fuscus, occur in many other species in at least 11 anuran families (Preininger et al. 2016). Among the factors that may underlie these differences are body size (with females usually being larger than males), vocalization social function, presence of vocal sac that aids in call transmission (only in males), and laryngeal size and complexity (males with larger laryngeal structures than females) (Duellman and Trueb 1986, Monnet and Cherry 2002, Wells and Schwartz 2007, Wilkins et al. 2013, Toledo et al. 2014, Preininger et al. 2016. ...
... Acoustic properties involved in reproductive isolation usually are stereotyped (Gerhardt 1991, Gerhardt andHuber 2002). The large variability in female calls may be functionally signifi cant; thus, female calls are a receptivity signal used only in close-range interactions (Márquez and Verrel 1991, Bosch 2002, Preininger et al. 2016 and may not have a species-recognition function. Indeed, in the case described here, the female call seems not to be a source for reproductive isolation, but instead a signal emitted to advertise immediate availability for a candidate male during courtship. ...
... The lack of these structures, directly related to sound production and radiation in the vast majority of anurans, does not prevent the production of vocal sounds (e.g. Nunes- de-almeida et al. 2016;Preininger et al. 2016; this study). However, the low intensity of acoustic signals, especially in earless species, suggests a limited range over which acoustic communication could occur (Boistel et al. 2011;Womack et al. 2017). ...
Article
Full-text available
Vocal sounds occur in most anurans and are often emitted as simple and stereotyped acoustic signals. Some frog groups, however, have complex signals and others can produce distinctive acoustic structures, such as purely ultrasonic calls. Crossodactylodes is a genus of bromeligenous frogs that is understudied in many aspects. This genus has been historically regarded as voiceless, but recent studies reported briefly on vocal sounds in two species. Here, we provide the first quantitative description of vocalisations of Crossodactylodes frogs and describe the vocal repertoires of three species. Vocalisations are formed of up to three call types, reported herein as creaking, chirp and squeak calls. We discuss the major call patterns and the repertoire of Crossodactylodes. We also discuss the evolutionary and functional implications of the low-intensity calls produced at the water–air interface inside bromeliads. The absence of some morphological structures normally involved in sound reception (elements of the middle ear) in Crossodactylodes frogs indicates that extratympanic pathways might be the main auditory route in these highly specialised leptodactylids.
... Anuran species of the genus Engystomops have complex acoustic components favoured by females (Boul & Ryan, 2004;. It has been demonstrated that their calls, as well as the anatomical structures that produce them, have been evolutionarily changed by sexual selection (Boul et al., 2006;Preininger et al., 2016;Ryan & Drewes, 1990). Regarding the Engystomops' close relative, the genus Physalaemus (Leiuperinae), several studies have observed a great intra-and interspecific acoustic variation in the genus, which might also have some correspondence with vocal structures (see Drewry et al., 1982;Hepp & Pombal, 2020 for a review on bioacoustics in Physalaemus). ...
Article
The anuran larynx is an organ of great evolutionary interest because it impacts male reproductive success in courtships. However, little is known about the diversity of the larynx's anatomy, evolutionary history and systematics importance. Here, we describe and compare the anatomy of the larynx of 10 Physalaemus species of the P. cuvieri clade, focusing on the P. olfersii species group. We also reconstructed the ancestral states and tested the phylogenetic signal for the anatomical features. In all the species, the larynx has a general globular shape with the arytenoid cartilages covering almost its entire dorsal surface, while the anterior process of the cricoid cartilages covers most of the ventral surface. The size of the secondary fibrous mass, the thickness of the vocal membrane, and the attachment position of the vocal membrane's free edge considerably differ among the species. Moreover, only four species of a single clade in the P. olfersii species group have the primary fibrous mass well-developed with a suspended region in the dorsolateral passage. We found a significant phylogenetic signal for all these characters. Ancestral reconstructions pointed to reduction tendencies in the thickness of the vocal membrane and the size of the secondary fibrous mass, and a shift of the ventral attachment of the vocal membrane, increasing the angle of its free edge along the phylogeny. This latter trait can diagnose the entire Physalaemus olfersii group, which has the ventral ends of the arytenoids positioned posteriorly, giving this group the steepest angles for the vocal membrane's free edge in relation to the frontal plane. Based on our results, the larynges can contribute to the Physalaemus olfersii species group's systematics and could be elucidative to understand the evolution of the genus. High levels of anatomical and bioacoustical complexity and diversity observed in the group support the expected correlation between vocal anatomy and bioacoustical signal.
... Physalaemus petersi y sugirieron que la evolución de las llamadas podría tener una morfología subyacente asociada. En los anuros el dimorfismo sexual está relacionado con un tamaño mayor corporal y de las laringes en los machos (Wells, 1977), a su vez con el gasto energético (McClelland et al., 1996), el cual se incrementa si se ve afectado por los sonidos ambientales del hábitat natural (Preininger et al., 2016). ...
Thesis
Full-text available
The larval development of the skeleton of Colombian species of frogs of the most diversified families were examined and described: Rhinella marina (Bufonidae), Dendropsophus labialis, D. minutus, Boana xerophylla, Scinax ruber and Trachycephalus typhonius (Hylidae) and Engystomops pustulosus, Leptodactylus insularum and L. colombiensis (Leptodactylidae). These were obtained from biological collections. Differential enzymatic clearing and staining were performed to describe and compare the skeletal structures of craneal and poscraneal regions of the skeleton. Ossification sequences were obtained for analysis of variation of elements and ranks, ossification indexes, and phenotypic divergence. From these sequences and those taken from the literature the heterochronic changes and timing were identified using Parsimov algorithm. It was found that there are differences in the timing of appearance of the first ossified elements among these species, such as the transverse processes of the vertebrae. When considering only the cranium the first ossified elements were the exoccipital, paraesphenoid and frontoparietal, which are common in species of the Hylidae in early stages of development; in Leptodactylidae, was in later stages. The ranks and the number of elements presented ossification variability in all species, being the number smaller in leptodactilids, with respect to the hylids. Taking into account the whole skeleton, it was detected the relevance of the postcraneal elements. In using Parsimov, heterochronic changes in different amphibian groups were identified from the ontogeny of the skeleton, and pedomorphic processes were found in Colombian anurans. https://repository.javeriana.edu.co/handle/10554/50715
... Although the complex acoustic and visual courtship displays of this species have been addressed, unilateral vocal sac inflation has not been reported (Grafe et al., 2006;Grafe & Wanger, 2007;Preininger et al., 2013Preininger et al., , 2016. This suggests that it is infrequent in this species. ...
Article
Cascades and fast-flowing streams impose severe restrictions on acoustic communication, with loud broadband background noise hampering signal detection and recognition. In this context, diverse behavioural features, such as ultrasound production and visual displays, have arisen in the evolutionary history of torrent-dwelling amphibians. The importance of the vocal sac in multimodal communication is being increasingly recognized, and recently a new vocal sac visual display has been discovered: unilateral inflation of paired vocal sacs. In the diurnal stream-breeding Hylodidae from the Atlantic forest, where it was first described, this behaviour is likely to be enabled by a unique anatomical configuration of the vocal sacs. To assess whether other taxa share this exceptional structure, we surveyed torrent-dwelling species with paired vocal sacs across the anuran tree of life and examined the vocal sac anatomy of exemplar species across 18 families. We found striking anatomical convergence among hylodids and species of the distantly related basal ranid genera Staurois, Huia, Meristogenys and Amolops. Ancestral character state reconstruction identified three new synapomorphies for Ranidae. Furthermore, we surveyed the vocal sac configuration of other anuran species that perform visual displays and report observations on what appears to be unilateral inflation of paired vocal sacs, in Staurois guttatus – an extremely rare behaviour in anurans.
... Feathers of birds comprise an initial hydrophobic barrier that adsorbs a large amount of iodine. In comparison, the cornified scales of squamates and alligators, and the hairs of mammals (Gignac et al., 2016) all have variable external layers with higher permeability (Metscher, 2009a(Metscher, , 2009bPreininger et al., 2016). The larger specimens in this study stained less evenly and took longer to stain than the smaller specimen. ...
Preprint
Full-text available
Vocalisations play a vital role in animal communication, as they are involved in many biological functions. Seabirds often breed in large and dense colonies, making successful recognition between mates or between parents-and offspring crucial for reproductive success. Most seabird species, including Cape gannets (Morus capensis), are monomorphic and likely rely on acoustic signals for mate selection and mate recognition. This study aimed to better understand the use of vocalisations for sex and individual recognition in Cape gannets by describing the acoustic structure of their display calls at the nest. Vocalisations of nesting Cape gannets were recorded and acoustic measurements were extracted in both temporal and frequency domains. Values of the fundamental frequency and the average of Inter-Onset-Interval appeared to be the most important acoustic variables for sex determination. Both temporal and frequency parameters showed a potential for individual identity coding, with the average units Inter-Onset-Interval being the most important variable for individual identification for both sexes. This study provides the first evidence of sex-specific and individual vocal signatures in adult breeding Cape gannets. From an applied perspective, identified sex specific differences could potentially be used as a non-invasive method for field-based sex-determination in research and monitoring projects on Cape gannets.
Article
Full-text available
Most anurans are highly vocal but their vocalizations are stereotyped and simple with limited repertoire sizes compared to other vocal vertebrates, due presumably to the limited mechanisms for fine vocal motor control. We recently reported that the call of the concave‐eared torrent frog ( Amolops tormotus) is an exception in its seemingly endless variety, musical warbling quality, extension of call frequency into the ultrasonic range, and the prominence of nonlinear features such as period doubling. We now show that the major spectral features of its calls, responsible for this frog’s vocal diversity, can be generated by forcing pressurized air through the larynx of euthanized males. Laryngeal specializations for ultrasound appear to include very thin portions of the medial vocal ligaments and the reverse sexual size dimorphism of the larynx being smaller in males than in females. The intricate morphology of the vocal cords, which changes along their length, suggests that nonlinear phenomena likely arise from complex nonlinear oscillatory regimes of separate elastically coupled masses. Amolops is thus the first amphibian for which the intrinsic nonlinear dynamics of its larynx, a relatively simple and expedient mechanism, can account for the species call complexity, without invoking sophisticated neuromuscular control.
Article
Full-text available
Male carpenter frogs have a complex vocal repertoire consisting of a 1-10 note advertisement call, a single-note aggressive call, a multi-note aggressive call, a release call, and a growl given during wrestling. Females have a single-note call that is given during courtship. Dominant frequency and intensity of calls are correlated with body size, but strength of the correlation decreases as body size increases. Calling activity occurs between sunset and sunrise, peaks around midnight and is influenced by chorus density. Males increased the number of aggressive calls as stimulus intensity increased and gave more aggressive responses to aggressive calls than to advertisement calls. When males were presented with calls of large and small males, they responded to the calls of the smaller male with more total notes and more single-note aggressive calls. Small males are more likely to retreat in response at a vocal intrusion. -from Author
Article
Full-text available
The most common defensive vocalization in anurans is the distress call. However, few descriptions of this type of call are available in the literature, especially for the Neotropics. We therefore described the defensive calls of 31 anuran species and evaluated correlations between anuran size and call physical structure (sound pressure level, dominant frequency, and call duration). Defensive calls are most likely an ancestral character in anurans, as this character is widespread over several genera and families. A positive relationship may exist between the physical characteristics of distress calls and chances of avoiding predation, i.e., only larger (than a certain size) frogs produce defensive vocalizations and the larger the frog, the higher the sound pressure level of its screams. This study strengthens our knowledge about defensive vocalizations in anurans and will hopefully instigate new challenges for future research.
Article
Among frogs, vocalizations play important roles in their social interactions. Herein we describefi ve new types of vocalizations for two foam-nesting species of the Leptodactylus pentadactylusgroup, L. syphax and L. labyrinthicus. Behavioral observations and recordings were done in fourlocalities within the Cerrado biome, at southeast and central Brazil. Before emitting advertisementcalls, males of L. syphax often started producing a sequence of notes, which gradually turned into theadvertisement call. These different notes may be an introductory call, which would serve to preparethe vocal structures for the emission of the high-frequency/amplitude advertisement calls. A male ofL. syphax was emitting advertisement calls when a female approached and started to emit brief andlow-amplitude calls; these vocalizations probably are reciprocation calls. Males of L. labyrinthicusinvolved in agonistic interactions can emit vocal cracks (encounter call) and deep rough sounds (territorialcalls). Five courting males of L. labyrinthicus released screams with their mouth slightly openedin response to the approach of human observers. We conclude that these screams do not representdistress or territorial calls.
Book
Hearing and Sound Communication in Amphibians is a compendium of the latest research on acoustic communication in these highly vocal vertebrates. The chapters are written by experts currently investigating the physiology and behavior of amphibians both in the laboratory and in the field. This integrated approach guides each chapter and provides a neuroethologically-driven and evolutionary basis for our understanding of acoustic communication and its underlying mechanisms. The intended audience ranges from senior undergraduates to physiologists, zoologists, evolutionary biologists and communication specialists. Contents Peter Narins is Professor in the Departments of Physiological Science, Ecology & Evolutionary Biology, the Brain Research Institute and the Center for Tropical Research at the University of California, Los Angeles. Albert Feng is Professor in the Departments of Molecular and Integrative Physiology & Bioengineering, Neuroscience Program, Center for Biophysics and Computational Biology, and Beckman Institute at the University of Illinois at Urbana-Champaign. Arthur N. Popper is Professor in the Department of Biology and Co-Director of the Center for Comparative and Evolutionary Biology of Hearing at the University of Maryland, College Park. Richard R. Fay is Director of the Parmly Hearing Institute and Professor of Psychology at Loyola University of Chicago. About the series: The Springer Handbook of Auditory Research presents a series of synthetic reviews of fundamental topics dealing with auditory systems. Each volume is independent and authoritative; taken as a set, this series is the definitive resource in the field.
Article
Female mate choice is an important determinant for male reproductive success in anurans. The advertisement call of the males contains information for species recognition. These calls are used by the females to distinguish between heterospecifics and conspecifics and further to discriminate among conspecifics to choose the fittest male for the purpose of mating. In Polypedates leucomystax, the female responds by its feeble reciprocal call to the first calling male of the colony, which also is the largest and heaviest male amongst all other calling males. This male calls persistently throughout the night, or till amplexus is reached, without changing its call pattern. It increases the intensity of its call after the response of the female. The increase in the intensity, increase in the length of the individual call and persistent calling throughout the night make the call of this first calling male conspicuous. The call contains more acoustical energy which is indicative of good physical condition and the responding female chooses this male. Thus mating in P. leucomystax is non-random and influenced by female mate choice.