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NORTH-WESTERN JOURNAL OF ZOOLOGY 8 (1): 107-111 NwjZ, Oradea, Romania, 2012

Article No.: 121104 www.herp-or.uv.ro/nwjz



Description of the advertisement call and morphometry
of Haddadus binotatus (Spix, 1824)
from a population from southern Bahia, Brazil.

Iuri Ribeiro DIAS
1,
*, Ricardo LOURENO-DE-MORAES
2
and Mirco SOL
1,2

1. Programa de Ps-Graduao em Zoologia, Universidade Estadual de Santa Cruz (UESC),
Rodovia Ilhus-Itabuna, km 16, Ilhus, Bahia, CEP 45662-000, Brazil.
2. Programa de Ps-Graduao em Ecologia e Conservao da Biodiversidade, Universidade Estadual de Santa Cruz (UESC),
Rodovia Ilhus-Itabuna, km 16, Ilhus, Bahia, CEP 45662-000, Brazil.
* Corresponding author, I.R. Dias, E-mail: iurirdias@hotmail.com


Received: 14. July 2011 / Accepted: 08. December 2011 / Available online: 08. January 2012 / Printed: June 2012

Abstract. Currently there are only two recognized species in the genus Haddadus; however advertisement
calls are known for neither of them. Herein, we describe the advertisement call of Haddadus binotatus from
males recorded at the Serra Bonita reserve in the municipality of Camacan in southern Bahia, Brazil and
provide morphometric data to allow further comparison with individuals from other localities. The
advertisement call of the studied population can be characterized as short and low-pitched, with a low
volume sound, consisting of a single note made up of 3-6 pulses and a length of 0.012-0.033 s. The dominant
frequency ranges from 1033.6-1464.3 Hz. The SVL of males ranged between 32-38.6 mm and females between
50-55.8 mm. Females were significantly larger than males. Our data can help solving identity problems within
this species, which is thought to be a species complex.

Key words: Craugastoridae, Bioacoustics, Atlantic Forest, Bahia, Brazil.

Introduction

Haddadus binotatus is a frog that lives on the leaf
litter of Atlantic Rainforest remnants and has a
wide geographical distribution ranging from the
states of Bahia to Rio Grande do Sul (Sluys & Ro-
cha 2008). It is characterized by direct develop-
ment of their terrestrial eggs, which are deposited
on fallen logs (Izecksohn & Carvalho-e-Silva 2001).
Using morphological and molecular data
Hedges et al (2008) divided the family Eleuthero-
dactylidae into several families and genera. Due to
some very distinct characters observed in the clade
Eleutherodactylus binotatus, the authors proposed
a new genus for this species, Haddadus and placed
there the two species of the clade (Eleutherodacty-
lus binotatus and Eleutherodactylus plicifer), in-
cluding them in a new family Craugastoridae.
This family comprehends the genus Haddadus to-
gether with the genus Craugastor (Cope 1862).
Both genera share similar morphological and mo-
lecular characteristics, counting almost 113 species
within the family.
Haddadus binotatus shows large morphological
variability throughout its distribution, probably
containing more than one valid species under this
name (Ribeiro et al. 2005, Forlani et al. 2010).
Haddad & Sazima (1992) drew attention to the
large size of H. binotatus from southeastern Brazil
and questioned the application of this name to
these populations. As in the original description
Spix (1824) did not determine the type locality of
H. binotatus, these authors believe that Spix gave
that name to specimens from the states of Esprito
Santo and Bahia, however Bokermann (1966) at-
tributed the city of Rio de Janeiro as the probable
type locality of this species.
Bioacoustic studies have become a pivotal tool
in taxonomic studies of frogs, since the advertise-
ment call is a mechanism of pre-zygotic isolation
between sympatric species (Duellman & Pyles
1983) and each species has a distinct call (Fou-
quette 1960, Lingnau et al. 2008, Caldart et al.
2011). The structure of the advertisement call has
been used to solve taxonomic problems (e.g. Kwet
et al. 2001, Heyer & Junc 2003, Haddad & Sazima
2004).
Herein we describe the advertisement call of a
population of Haddadus binotatus from southern
Bahia and provide data on the morphology of this
population, thus supporting further taxonomic
studies aimed at defining the specific limits of this
species.


Material and Methods

The advertisement calls of three males were recorded in
the Serra Bonita reserve, in the municipality Camacan,
state of Bahia, Brazil (15 25'19.4'' S; 39 32'26.6'' W). Two
individuals (MZUESC 8421, 8611) were recorded using a
Dias, I.R. et. al

108
Sennheiser ME45 microphone with a K6 power module
connected to a Tascam DR1 digital recorder. The third in-
dividual (MZUESC 8906) was recorded using an Olym-
pus VN-3100PC digital recorder with an internal micro-
phone. Recordings were made from a distance of about 50
cm from the frogs.
From each individual 20 advertisement calls were
analyzed. Temporal (call duration, pulse duration and in-
terval between calls and pulses and repetition rate) and
spectral features (dominant frequency and frequency am-
plitude) of the call were analyzed using the software Ra-
ven Pro 1.3 at 44.1 kHz and 16 bit resolution. Sonograms
were made with FFT of 150 points, 90% overlap and win-
dows hamming. Terminology follows Duellman & Trueb
(1986). Air temperature was measured with a digital hy-
grometer with an accuracy of 0.5 C. Vouchers were de-
posited at the zoological collection of Universidade de
Santa Cruz, Ilhus, Bahia.
Seventeen morphometric characters from five adult
males and five adult females were measured in millime-
ters. Fifteen measurements followed Napoli (2005): SVL
(snout-vent length), HL (head length), HW (head width),
ED (eye diameter), UEW (upper eyelid width), IOD (in-
terorbital distance), IND (internarial distance), END (eye-
nostril distance), NSD (nostril to tip of snout distance),
TD (tympanum diameter), THL (thigh length), TL (tibia
length), FL (foot length), 3FD (third finger disk diameter),
and 4TD (fourth toe disk diameter). Other two measures
used were the length of the first (F1) and the second fin-
ger (F2). All measures were taken with a Mitutoyo caliper
with an accuracy of 0.05 mm. The gender of frogs was de-
termined through the presence of eggs in females and
calling activity of males in the field. The t test (Zar 1984)
was used to verify the significance of the differences be-
tween measures of males and females.


Results

Individuals were recorded inside the forest. One
specimen (MZUESC 8421; SVL = 32 mm) was call-
ing on the stem of a shrub 20 cm of the soil with
an air temperature of 21.4C, on May 1, 2010 at
22:25 pm. Another male (MZUESC 8611; SVL 38.6
mm) was encountered on July 26, 2010 calling on a
dry stick 30 cm above the ground leaning against a
tree trunk, with an air temperature of 17.7C at
22:40 pm. The third male (MZUESC 8906;
SVL=33.7 mm) was calling on a fallen log 40 cm
from the ground with an air temperature of 20.5C
on September 18, 2010 at 18:50 pm.
The advertisement call (Fig. 1) of the surveyed
population can be characterized as short and low-
pitched, with a low volume sound. We analyzed
60 advertisement calls. Each call is composed of a
simple note made up of three (21.7%), four
(28.3%), five (41.7%) or six pulses (8.3%). Note
length is 0.021 0.006s (0.012-0.033s), issued at in-
tervals of 31.98 17.15s (16.16-100.36s). Note
emission rate was 0.51 notes/min. The duration of
the pulses was 0.0026 0.0009s (0.001-0.006s), is-
sued at intervals of 0.00285 0.0014s (0.001-
0.006s). The first pulse of the note shows a lower
intensity and is sometimes hard to identify (Fig. 2).
The dominant frequency was 1172.9 122.9 Hz
(1033.6-1464.3 Hz) and the used frequency range
was between 456 and 1999 Hz. The analyzed indi-
viduals used only five dominant frequency values
(1033.6; 1205.9; 1292.0; 1378.0; 1464.3 Hz). One of
the analyzed specimens always showed the same
dominant frequency at 1033.6 Hz. In some calls it
is possible to observe a second frequency band be-
tween 2300 and 4100 Hz (Fig. 2). A summary of
the acoustic measures of each recorded individual
is given in Table 1.
Twelve other individuals were observed vo-
calizing in herbaceous vegetation, shrubs or on
fallen tree trunks 20-80 cm up from the ground.
Only three were calling on the leaf litter. We ob-
served males in calling activity during all monthly
visits from January to December 2010. Usually the
calling activity initiated or increased soon after
rainfall in the study area. Frogs were generally ob-
served calling in groups of 3-10 individuals inside
the forest, but a few males were observed calling
isolated from other males.
Morphometric data has been summarized in
Table 2. The SVL of females was significantly lar-
ger than that of males (t= 12.14; p<0.0001). For the
studied population HL was a bit larger than HW,
SVL was smaller than the sum of THL+TL, ED
was approximately 1/3 of HL, TD was approxi-
mately 2/5 of ED and F2 approximately 3/5 the
length of F1. No vocal slits or expanded vocal sacs
were found in males.


Discussion

Studies dealing with leaf litter anurans have
shown that Haddadus binotatus is a locally abun-
dant species within forests (Almeida-Gomes et al.
2008, Rocha et al. 2007), but studies on the natural
history of this species are rare (Canedo & Rickli
2006).
Machado & Bernardes (2002) reported that in
the municipality of Londrina, state of Paran, call-
ing activity of this species was linked to the rainy
season (September to February). Canedo & Rickli
(2006), while studying ovarian follicles of a popu-
lation in the municipality of Belmiro Braga, state

Advertisement call of Haddadus binotatus

109


Figure 1. Oscillogram and corresponding spectrogram of the advertisement call (single note with five pulses) of
Haddadus binotatus from RPPN Serra Bonita. Recorded on July 26 2010 at 22:40. Air temperature during recording:
17.7C.



Figure 2. Oscillogram and spectrogram of the advertisement call (single note with four pulses) of Haddadus bino-
tatus from RPPN Serra Bonita. Note the second frequency band and the lowest intensity of the first pulse. Re-
corded on September 18 2010 at 18:50. Air temperature during recording: 20.5C.


of Minas Gerais, concluded that Haddadus binotatus
shows a seasonal reproduction at the beginning of
the rainy season. In our study we observed the
species calling throughout all the study period
(January to December), which leads us to believe
that this population may reproduce throughout
the year in the study area, and that its reproduc-
tion is directly linked to rainfall. As the climate in
southern Bahia is of type Af, characterized as hot
and humid without a defined dry season (Kppen
1936), the species finds suitable conditions for a
prolonged breeding season.
This species is frequently found on the leaf lit-
ter, but most of the individuals observed in calling
activity were sighted between 20 and 80 cm
height. We presume that individuals use higher
places to call in order to allow a better spread of
the sound in the environment since their call is
very short and low. Such a behavior has been ob-
served by Bernarde & Anjos (1999), who reported
on males calling in bushes up to 1,50 m from the
ground inside a forest in Londrina, Paran.




Dias, I.R. et. al

110

Table 1. Parameters of the advertisement call of each individual recorded of Haddadus binotatus from the RPPN
Serra Bonita, Camacan, Bahia, Brazil. Mean standard-deviation and interval in parenthesis.

Call parameters MZUESC 8421
(32,0 mm - 21,4 C)
MZUESC 8611
(38.6 mm - 17,7 C)
MZUESC 8906
(33.7 mm- 20,5 C)
Note duration (s) 0.021 0.0013
(0.019-0.024)
0.027 0.0029
(0.0024-0.033)
0.015 0.0025
(0.012-0.021)
Interval between call (s) 44.71 20.29
(21.39-100.36)
26.49 14.23
(16.16-75.83)
24.72 6.54
(16.92-37.49)
Note/min 0.71 0.42 0.39
Pulse duration (s) 0.0028 0.0011
(0.001-0.006)
0.0026 0.0008
(0.002-0.005)
0.0022 0.0007
(0.001-0.005)
Number of pulses 5-6 5-4 3-4
Interval between pulses (s) 0.0016 0.0005
(0.001-0.003)
0.004 0.0011
(0.001 0.006)
0.0029 0.0005
(0.002-0.004)
Call dominant frequency (Hz) 1033.6 1180 63.1
(1033.6-1205.9)
1304.9 64.2
(1205.9-1464.3)
Frequency amplitude (Hz) 456-1886 726-1999 651-1979


Table 2. Descriptive statistics (in millimeters) of adult males and females of Haddadus binotatus from the RPPN
Serra Bonita, south of Bahia, Brazil. Min = minimum value; Max = maximum value; SD = Standard-deviation.

Females (N = 5) Males (N = 5)
Mean Min Max SD Mean Min Max SD
Snout-vent length 53.1 50 55.8 2.3 34.5 32 38.6 2.5
Head length 21.8 21.2 22.9 0.7 13.5 12.7 14.5 0.6
Head width 21.3 20.5 22.5 0.7 12.5 11.8 13.3 0.5
Eye diameter 6.2 5.8 6.8 0.4 4.5 4.2 4.9 0.3
Tbia length 31.1 30.2 31.7 0.5 19.1 18.4 21 1.1
Thigh length 29.3 28.3 30.4 0.7 18.1 17.2 19.3 0.8
Foot length 42.3 40.3 44.5 1.5 26.3 25.3 28.8 1.4
Length of finger I 11.1 10.6 12.0 0.6 6.9 6.5 7.4 0.4
Length of finger II 6.4 6.0 7.1 0.5 3.9 3.6 4.15 0.2
Interorbital distance 5.3 4.8 5.5 0.3 3.4 3.1 4.2 0.4
Internarial distance 4.4 4.0 4.7 0.3 3.1 2.7 3.3 0.2
Eye-nostril distance 6.5 6.2 7.0 0.3 4.4 4.2 4.8 0.2
Nostril to tip of snout distance 2.8 2.5 3.2 0.3 1.9 1.6 2.2 0.2
Upper eyelid width 4.7 4.4 5.0 0.2 3.3 2.8 3.8 0.4
Tympanum diameter 2.9 2.7 3.4 0.3 2.0 1.8 2.2 0.1
Third finger disk diameter 1.1 0.9 1.3 0.1 0.7 0.5 0.9 0.2
Fourth toe disk diameter 1.5 1.3 1.6 0.1 0.9 0.7 1.1 0.2


The second species in the genus, Haddadus pli-
cifer is known only from the holotype, being mor-
phologically very similar to H. binotatus, but
smaller (SVL= 17 mm) (Hedges et al. 2008). Unfor-
tunately the advertisement call has not been de-
scribed, thus not allowing a comparison.
Izecksohn & Carvalho-e-Silva (2001) defined
the call of de Haddadus binotatus from Rio de Ja-
neiro state as whistled notes, issued quickly.
This observation drew our attention because it is
different from the herein described, a short and
low call with notes that are not repeated rapidly
and do not resemble a whistle. Given this, the
population reported by these authors may be dif-
ferent from the one described here.
The average SVL of males of Haddadus bino-
tatus from the Biological Station Boracia, So
Paulo State, is 38.8 mm (32.3-44.7 mm; n = 10) and
that of females 57.4 mm (46.4-63.8 mm; n = 10)
(Heyer et al. 1990). On average the analyzed indi-
viduals from southern Bahia have a smaller SVL
than those of Boracia (males = 34.5 mm (32-38.6
mm; n = 5) and females = 53.1 mm (50-55.8 mm; n
= 5). The morphometric data for this population
from southern Bahia is in agreement with the
statement of Haddad & Sazima (1992) that popula-
tions of H. binotatus from Bahia are different from
those in the southeast of Brazil, but this data must
be interpreted with caution because of the rela-
tively low number of analyzed specimens and the
Advertisement call of Haddadus binotatus

111
overlap of values. A more specific and compre-
hensive study should be conducted to clarify the
taxonomic / morphometric differences between
populations.
Cochran (1955) describes an adult male from
the municipality of Tijuca, Rio de Janeiro State.
The specimen had a SVL of 54 mm; head length of
21 mm; width 21 mm; femur of 26 mm; tbia of 30
mm; foot of 26 mm and a hand of 14 mm. These
measures differ from males collected in the study
area in southern Bahia and from the state of So
Paulo, because the measures resemble more that of
females than that of males.
Attempts should be made to acquire bioacous-
tic data from other populations along the known
distribution of H. binotatus in order to allow a bet-
ter evaluation of acoustic variability of this spe-
cies, as well as a thorough taxonomic revision to
define the species limits and whether there are
cryptic species.



Acknowledgments. We thank Andrs Canavero and
Diego Santana for helpful comments on the manuscript
and Tadeu Medeiros, Marco Vila Nova, Raoni Rebouas
and Danilo Ruas for their help during fieldwork. We
further thank Fundao O Boticrio de Proteo
Natureza (Project n 0818_20091), Amphibian Specialist
Group and Instituto Uirau for funding. IRD thanks
FAPESB and RLM thanks Capes for scholarships. Frogs
were collected under the permit 13708-1 issued by the
ICMBio to M. Sol.



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