Dias Et Al Advertisement Call Haddadus Binotatus Nwjz 2012

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NORTH-WESTERN JOURNAL OF ZOOLOGY 8 (1): 107-111 NwjZ, Oradea, Romania, 2012Article No.: 121104 www.herp-or.uv.ro/nwjz

Description of the advertisement call and morphometry

ofHaddadus binotatus (Spix, 1824)

from a population from southern Bahia, Brazil.

Iuri Ribeiro DIAS1,*, Ricardo LOURENO-DE-MORAES2 and Mirco SOL1,2

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: [email protected]

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 advertisementcalls are known for neither of them. Herein, we describe the advertisement call of Haddadus binotatusfrommales recorded at the Serra Bonita reserve in the municipality of Camacan in southern Bahia, Brazil andprovide morphometric data to allow further comparison with individuals from other localities. Theadvertisement call of the studied population can be characterized as short and low-pitched, with a lowvolume sound, consisting of a single note made up of 3-6 pulses and a length of 0.012-0.033 s. The dominantfrequency ranges from 1033.6-1464.3 Hz. The SVL of males ranged between 32-38.6 mm and females between50-55.8 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 leaflitter of Atlantic Rainforest remnants and has awide geographical distribution ranging from thestates of Bahia to Rio Grande do Sul (Sluys & Ro-cha 2008). It is characterized by direct develop-ment of their terrestrial eggs, which are depositedon 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 tosome very distinct characters observed in the cladeEleutherodactylus binotatus, the authors proposeda new genus for this species, Haddadus and placedthere 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 specieswithin the family.

Haddadus binotatusshows large morphological

variability throughout its distribution, probablycontaining more than one valid species under thisname (Ribeiro et al. 2005, Forlani et al. 2010).Haddad & Sazima (1992) drew attention to thelarge size of H. binotatus from southeastern Braziland questioned the application of this name to

these populations. As in the original descriptionSpix (1824) did not determine the type locality ofH. binotatus, these authors believe that Spix gavethat name to specimens from the states of EspritoSanto and Bahia, however Bokermann (1966) at-tributed the city of Rio de Janeiro as the probabletype locality of this species.

Bioacoustic studies have become a pivotal toolin taxonomic studies of frogs, since the advertise-ment call is a mechanism of pre-zygotic isolation

between sympatric species (Duellman & Pyles1983) and each species has a distinct call (Fou-quette 1960, Lingnau et al. 2008, Caldart et al.2011). The structure of the advertisement call hasbeen used to solve taxonomic problems (e.g. Kwetet al. 2001, Heyer & Junc 2003, Haddad & Sazima2004).

Herein we describe the advertisement call of apopulation of Haddadus binotatus from southernBahia and provide data on the morphology of thispopulation, thus supporting further taxonomicstudies aimed at defining the specific limits of thisspecies.

Material and Methods

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


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Sennheiser ME45 microphone with a K6 power moduleconnected 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 50cm from the frogs.

From each individual 20 advertisement calls wereanalyzed. Temporal (call duration, pulse duration and in-terval between calls and pulses and repetition rate) andspectral 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. Sonogramswere 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 deSanta Cruz, Ilhus, Bahia.

Seventeen morphometric characters from five adultmales 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 (tibialength), FL (foot length), 3FD (third finger disk diameter),and 4TD (fourth toe disk diameter). Other two measuresused were the length of the first (F1) and the second fin-ger (F2). All measures were taken with a Mitutoyo caliperwith an accuracy of 0.05 mm. The gender of frogs was de-termined through the presence of eggs in females andcalling 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. Onespecimen (MZUESC 8421; SVL = 32 mm) was call-ing on the stem of a shrub 20 cm of the soil withan air temperature of 21.4C, on May 1, 2010 at22:25 pm. Another male (MZUESC 8611; SVL 38.6mm) was encountered on July 26, 2010 calling on adry stick 30 cm above the ground leaning against atree trunk, with an air temperature of 17.7C at22:40 pm. The third male (MZUESC 8906;SVL=33.7 mm) was calling on a fallen log 40 cmfrom the ground with an air temperature of 20.5Con 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 analyzed60 advertisement calls. Each call is composed of asimple note made up of three (21.7%), four(28.3%), five (41.7%) or six pulses (8.3%). Notelength is 0.021 0.006s (0.012-0.033s), issued at in-

tervals of 31.98 17.15s (16.16-100.36s). Noteemission rate was 0.51 notes/min. The duration ofthe 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 lowerintensity 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 rangewas 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 ofthe analyzed specimens always showed the samedominant frequency at 1033.6 Hz. In some calls itis possible to observe a second frequency band be-tween 2300 and 4100 Hz (Fig. 2). A summary ofthe acoustic measures of each recorded individualis given in Table 1.

Twelve other individuals were observed vo-calizing in herbaceous vegetation, shrubs or onfallen 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 monthlyvisits from January to December 2010. Usually thecalling activity initiated or increased soon afterrainfall in the study area. Frogs were generally ob-served calling in groups of 3-10 individuals insidethe forest, but a few males were observed callingisolated from other males.

Morphometric data has been summarized inTable 2. The SVL of females was significantly lar-ger than that of males (t= 12.14; p


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Advertisement call of Haddadus binotatus 109

Figure 1. Oscillogram and corresponding spectrogram of the advertisement call (single note with five pulses) ofHaddadus binotatusfrom 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 binotatusshows a seasonal reproduction at the beginning ofthe rainy season. In our study we observed thespecies calling throughout all the study period(January to December), which leads us to believethat this population may reproduce throughout

the year in the study area, and that its reproduc-tion is directly linked to rainfall. As the climate insouthern Bahia is of type Af, characterized as hotand humid without a defined dry season (Kppen1936), 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 callingactivity were sighted between 20 and 80 cmheight. We presume that individuals use higherplaces to call in order to allow a better spread of

the sound in the environment since their call isvery short and low. Such a behavior has been ob-served by Bernarde & Anjos (1999), who reportedon males calling in bushes up to 1,50 m from theground inside a forest in Londrina, Paran.


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Table 1. Parameters of the advertisement call of each individual recorded of Haddadus binotatusfrom the RPPNSerra 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 0.39Pulse 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 3-4Interval 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 RPPNSerra 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 SDSnout-vent length 53.1 50 55.8 2.3 34.5 32 38.6 2.5Head length 21.8 21.2 22.9 0.7 13.5 12.7 14.5 0.6Head width 21.3 20.5 22.5 0.7 12.5 11.8 13.3 0.5Eye diameter 6.2 5.8 6.8 0.4 4.5 4.2 4.9 0.3Tbia length 31.1 30.2 31.7 0.5 19.1 18.4 21 1.1Thigh length 29.3 28.3 30.4 0.7 18.1 17.2 19.3 0.8Foot length 42.3 40.3 44.5 1.5 26.3 25.3 28.8 1.4Length of finger I 11.1 10.6 12.0 0.6 6.9 6.5 7.4 0.4Length of finger II 6.4 6.0 7.1 0.5 3.9 3.6 4.15 0.2Interorbital distance 5.3 4.8 5.5 0.3 3.4 3.1 4.2 0.4Internarial distance 4.4 4.0 4.7 0.3 3.1 2.7 3.3 0.2Eye-nostril distance 6.5 6.2 7.0 0.3 4.4 4.2 4.8 0.2Nostril to tip of snout distance 2.8 2.5 3.2 0.3 1.9 1.6 2.2 0.2Upper 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 0.1Third finger disk diameter 1.1 0.9 1.3 0.1 0.7 0.5 0.9 0.2Fourth 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-ciferis known only from the holotype, being mor-phologically very similar to H. binotatus, butsmaller (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) definedthe call of de Haddadus binotatus from Rio de Ja-neiro state as whistled notes, issued quickly.This observation drew our attention because it isdifferent from the herein described, a short andlow call with notes that are not repeated rapidlyand do not resemble a whistle. Given this, thepopulation 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, SoPaulo State, is 38.8 mm (32.3-44.7 mm; n = 10) andthat 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 SVLthan those of Boracia (males = 34.5 mm (32-38.6mm; n = 5) and females = 53.1 mm (50-55.8 mm; n= 5). The morphometric data for this populationfrom southern Bahia is in agreement with thestatement of Haddad & Sazima (1992) that popula-tions of H. binotatus from Bahia are different fromthose in the southeast of Brazil, but this data mustbe interpreted with caution because of the rela-tively low number of analyzed specimens and the


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Advertisement call of Haddadus binotatus 111

overlap of values. A more specific and compre-hensive study should be conducted to clarify thetaxonomic / morphometric differences betweenpopulations.

Cochran (1955) describes an adult male fromthe municipality of Tijuca, Rio de Janeiro State.The specimen had a SVL of 54 mm; head length of21 mm; width 21 mm; femur of 26 mm; tbia of 30mm; foot of 26 mm and a hand of 14 mm. Thesemeasures differ from males collected in the studyarea in southern Bahia and from the state of SoPaulo, because the measures resemble more that offemales than that of males.

Attempts should be made to acquire bioacous-tic data from other populations along the knowndistribution of H. binotatusin order to allow a bet-ter evaluation of acoustic variability of this spe-cies, as well as a thorough taxonomic revision todefine the species limits and whether there arecryptic species.

Acknowledgments. We thank Andrs Canavero andDiego Santana for helpful comments on the manuscriptand Tadeu Medeiros, Marco Vila Nova, Raoni Rebouasand Danilo Ruas for their help during fieldwork. Wefurther thank Fundao O Boticrio de Proteo Natureza (Project n 0818_20091), Amphibian SpecialistGroup and Instituto Uirau for funding. IRD thanksFAPESB and RLM thanks Capes for scholarships. Frogswere collected under the permit 13708-1 issued by theICMBio to M. Sol.

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Dias Et Al Advertisement Call Haddadus Binotatus Nwjz 2012

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