Artigo Canto a. Bracatta

7/31/2019 Artigo Canto a. Bracatta

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211Braz. J. Biol., 2010, vol. 70, no. 1, p. 211-216

Acoustic communication and vocalization microhabitat

inAmeerega braccata (Steindachner, 1864)

(Anura, Dendrobatidae) from Midwestern Brazil

Forti, LR.a*, Strssmann, C.a,b and Mott, T.a,c

aPrograma de Ps-Graduao em Ecologia e Conservao da Biodiversidade,

Instituto de Biocincias, Universidade Federal de Mato Grosso UFMTAv. Fernando Corra da Costa, s/n, CCBS-II, Boa Esperana, CEP 78060-900, Cuiab, MT, Brazil

bDepartamento de Cincias Bsicas e Produo Animal, Faculdade de Agronomia e Medicina Veterinria UFMTcPrograma de Ps-Graduao em Ecologia e Conservao da Biodiversidade,

Universidade Federal de Mato Grosso UFMTAv. Fernando Corra da Costa, s/n, CCBS-II, Boa Esperana, CEP 78060-900, Cuiab, MT, Brazil

*e-mail: [email protected]

Received November 19, 2008 Accepted February 11, 2009 Distributed February 28, 2010

(With 5 gures)

Abstract

Ameerega braccata is an aposematic, small dendrobatid anuran known rom its type-locality, Chapada dos Guimares,in the State o Mato Grosso, and rom a ew additional localities in Mato Grosso do Sul and Gois States, Brazil. Theadvertisement call oA. braccata is composed o a single unpulsed note, with a requency range rom 3.5 to 4.2 KHz(N = 110), and average duration o 65.8 ms (N = 110, SD = 11.6). The territorial call is composed o ve or six repeatednotes, structurally similar to advertisement call notes. The courtship call is emitted in close-range interactions betweenmale-emale during the courtship event and may reach requencies o 2.2 to 5.3 KHz (N = 10), with shorter notes (averageduration 43 ms; N = 10; SD = 4.9). Call duration, note duration and call rate o the advertisement call showed high varia-tion (>15% o coecient o variation), and dominant requency showed low variation (15% de coeciente de variao), ao passo que a requncia do-minante apresenta baixa variao (


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Forti, LR., Strssmann, C. and Mott, T.

212 Braz. J. Biol., 2010, vol. 70, no. 1, p. 211-216

1. Introduction

The production o sound in animals is generally used toadvertise conspecics (Duellman and Trueb, 1994; Lingnauand Bastos, 2003). In anurans, acoustic communication playsan essential role in reproductive biology (sensu Wells, 1977;Kanamadi et al., 1993). One main type o vocalization is theadvertisement call, emitted by males basically to attractemales and to establish territories during breeding seasons(Wells, 1987; Hedges, 1987; Kelley, 2004). Because vocali-zation tends to be species-specic, it also plays an essentialrole in pre-zigotic reproductive isolation by reducing thechances o interspecic mating (Abrunhosa et al., 2001). It isalso a remarkable and important tool or species identication(Guimares and Bastos, 2003; Pombal-Jnior et al., 1995).

Other call types have been also recognised (Wells,1987), including courtship calls (emitted by males incourtship context), territorial calls (emitted by males

in response to invader males), encounter calls (emit-ted by males in close-range agonistic interactions withother males), reciprocation calls (emitted by emales incourtship context), release calls (emitted by unreceptivemales or emales in response to amplexus), and distresscalls (emitted by either sex, in response to disturbance)(Duellman and Trueb, 1994; Wells, 2007).

Microhabitats and perching sites selected or vocaliza-tion usually dier among species, and may be related tobody-size and morphology (Bertoluci and Rodrigues, 2002).In complex communities, however, specic patterns o habi-tat occupation can be infuenced also by the diversity o spe-cies sharing limited habitat resources in reproductive aggre-gations (Bertoluci and Rodrigues, 2002).

Herein we describe the physical structure o three kindso calls (advertisement, territorial, and courtship calls) andvocalization microhabitat o individuals rom a topotypi-cal population oAmeerega braccata (Steindachner, 1864).This species belongs to the Dendrobatidae amily, placedin the Ameerega picta (Bibron in Tschudi, 1838) groupand is recorded or Cerrado habitats in Mato Grosso State,midwestern Brazil, and probably occurs in Bolivia andParaguay (Frost, 2007). Besides the type-locality, Chapada

dos Guimares, in Mato Grosso, the species is presentlyknown in a ew additional localities in this State, and inthe States o Mato Grosso do Sul and Gois as well (Frost,2007). Data o natural history oA. braccata are scarce andacoustic parameters have not been described yet (Haddadand Martins, 1994; IUCN, 2006).

2. Materials and Methods

Field observations were made rom October 2007 toMarch 2008, in one locality in Chapada dos Guimares mu-nicipality (1524 S and 5550 W; 650 m.a.s.l.), and an-

other in Cuiab municipality (15 20 S and 55 53 W; 250m.a.s.l.), both in Mato Grosso State, Brazil. Mean annualprecipitation in Chapada dos Guimares ranges rom 1800to 2000 mm and mean temperature is 22.8 C in July, and27.2 C in October (Pinto and Hay, 2005). In Cuiab, the cli-mate is semi-humid with mean annual temperature between

24 to 26 C, mean annual precipitation ranges rom 1250 to1500 mm (Carvalho and Nogueira, 1998).

Vocalizations o 15 males were recorded (9 romChapada dos Guimares, and 6 rom Cuiab) under naturalconditions with a Sony TCM 5000EV tape recorder and adirectional YOGA EM 9600 microphone. From 15 males

11 advertisement call sequences were obtained, 4 territorialcall sequences (during territorial disputes) and 1 courtshipcall sequence (during the courtship event). Recordings weremade rom a distance o approximately 50 cm rom eachmale. The sound digitalisation, analysis and the ocillogramsand Sonograms were made in Cool Edit 96 (Syntrillium),with a16 bits resolution and Fast Fourier Transormation(1024). For each male, 10 calls were analysed. Among these,we selected or our Figures 1 to 3 calls associated to temper-ature data, low levels o acoustic intererence and acousticparameters near the mean values recorded or the species.Seven recorded males were captured, three o them were

collected (IBAMA license register number: 2075225) anddeposited in the Coleo Zoolgica da Universidade Federalde Mato Grosso (UFMT 7713, 7695, 7752).

Air temperature and relative humidity were taken witha digital termo-higrometer (Instrutherm). Snout-vent-length(SVL) o the individuals were obtained with a digital cali-per (BTS) with precision o 0.01 mm. The variation in theproperties o the advertisement call was assessed using theCoecient o Variation (CV) as suggested by Gerhardt andHuber (2002). The Coecient o Variation was evaluatedamong individuals and inside individuals oA. bracatta.

Microhabitats used by calling males were described re-garding the nature o the substratum and height above theground, in the exact point where each animal was ound.

3. Results

3.1. Vocalizations

Ocillograms and spectrograms o advertisement, ter-ritorial, and courtship calls o individuals oA. braccata(rom Chapada dos Guimares UFMT 7713 and CuiabUFMT 7695) are presented in Figures 1, 2 and 3, respec-tively. Acoustic parameters o each distinct call type aresummarised in Table 1. Territorial calls are dierent romother call types mainly by having ve to six notes. Thecourtship calls were recorded during male-emale interac-tions and it has wider requency range and shorter call du-ration than other call types.

In Table 2, a comparison o the advertisement callcharacteristics o our species in the genus Ameerega ispresented.

Considering the advertisement calls among individu-als, the call duration, note duration and call rate wereabove 15% o variation, and were variable than dominantrequency, minimum requency and maximum requency

(Figure 4). Even at individual level, call or note durationwere relatively variable properties, with mean o 7.15%(5.68) o variation (Figure 5). Dominant requency, mini-mum requency and maximum requency showed respec-tively mean o 0.54 (0.23), 2.35 (0.8) and 1.7 (0.69) ovariation at individual level.


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Acoustic Communication in Ameerega braccata, midwestern Brazil


a

b

Figure 1. a) Ocillogram o the advertisement call oAmeerega braccata rom Cuiab, Mato Grosso, Brazil. b) Spectrogramo the advertisement call o the same individual oA. braccata (air temperature: 24.5 C; relative humidity: 92%).

b

a

Figure 2. a) Ocillogram o the territorial call oAmeerega braccata rom Chapada dos Guimares, Mato Grosso, Brazil. b)Spectrogram o the territorial call o the same individual oA. braccata (air temperature: 25.0 C; relative humidity: 87%;SVL = 22.4 mm; mass = 0.75 g).

3.2. Habitat

Individuals oA. braccata were ound in two open

physiognomies o Cerrado: the campo sujo and cer-

rado stricto sensu (or a detailed description o these or

other Cerrado physiognomies in the region o Chapada dos

Guimares, see Conceio, 2000). Among 22 reproductive

males observed throughout the study period, the majority

were observed calling on leaves o shrubs and herbaceous

plants (59%); 22% o the individuals were calling on the

ground, 18% on termite mounds, and only 1% on tree

trunks. Calling males were ound at an average height o

31.4 cm above the ground (N = 19, SD = 12.2 cm).

4. Discussion

4.1. Vocalizations

We identied three dierent types o calls in A. braccata

(advertisement, territorial and courtship calls). The adver-

tisement call in this species is composed o single notes,


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Table 1. Mean values or selected acoustic parameters o three distinct types o vocalizations recorded rom individuals oAmeerega braccata in the type-locality, Chapada dos Guimares, and Cuiab, Mato Grosso, Brazil. Call sample size (N),standard deviation (), range, and call rate sample size (n) are also indicated.

Variable Call type

Advertisement call (N = 110) Territorial call (N = 40) Courtship call (N = 10)

Call duration (ms) 65.8 (11.6, 46 - 81.3) 587.1 (95.5, 498.7 - 722.2) 43 (4.9, 38 - 52)

Number o notes 1 5 or 6 1

Notes duration (ms) 65.8 (11.6, 46 - 81.3) 66.2 (11.5, 49.1 - 72.8) 43 (4.9, 38 - 52)

Pulses per note 1 or 2 1 or 2 1

Dominant requency (Hz) 3986.4 (151.4, 3743.3 - 4205.2) 4099.4 (171.1, 3861.2 - 4263.8) 3734.2 (51.7, 3609.8 - 3778.8)

Minimum requency (kHz) 3.5 (0.17, 3.2 - 3.8) 3.5 (0.18, 3.2 - 3.67) 2.25 (0.2, 2 - 2.7)

Maximum requency (kHz) 4.2 (0.12, 4 - 4.4) 4.37 (0.2, 4.1 - 4.6) 5.31 (0.4, 4.4 - 5.8)

Call rate 5.15 (0.86, 3.4 - 6.45) (n = 10) 0.67 (0.14, 0.54 - 0.81) (n = 4) 7 (n = 1)

Table 2. Acoustic parameters o the advertisement calloAmeerega braccata (data rom the present work), A. favopicta,A. picta andA. hahneli. For the last three species, data are romHaddad and Martins (1994).

Variable Species

Ameerega braccata Ameerega favopicta Ameerega picta Ameerega hahneliCall duration (ms) 46-81 480-630 220-280 150-300

Number o notes 1 6 4 6

Notes duration (ms) 65.8 110 50 15

Pulses by note 1 or 2 1 1 1

b

a

Figure 3. a) Ocillogram o the courtship call oAmeerega braccata rom Cuiab, Mato Grosso, Brazil. b) Spectrogram othe courtship call o the same individual oA. braccata (air temperature: 24.0 C; relative humidity: 85%; SVL = 23.1 mm;mass = 1.0 g).


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Acoustic Communication in Ameerega braccata, midwestern Brazil


diering rom A. picta,A. favopicta (Lutz, 1925) andA. hahneli (Boulenger, 1884), whose males emit more thanone note per call (Haddad and Martins, 1994; Table 2). ThecallsoA. hahneli have a wider requency range (2.5 to 7.0KHz) than that oA. braccata (3.5 to 4.2 KHz),A. picta (3.4to 4.3 KHz) andA. favopicta (3.2 to 4.2 KHz). Additionally,the note duration o the A. hahneli call is shorter thanA. braccata (Table 2) (Haddad and Martins, 1994).

The territorial call oA. braccata is similar to the ad-vertisement call oA. favopicta by having ve or six notesper call. Nevertheless, mean durationis 587 ms in our sam-ple, somewhat lower than that inA. favopicta (Haddad and

Martins, 1994).In spite o the intensity not having been measured,

the courtship call oA. braccata seemed to be lower thanthat o the other kinds o calls produced in this species. Ina population oA. favopicta rom central Brazil, similarndings were reported by Toledo et al. (2004), who argued

that the low intensity o courtship call may represent an ad-aptation to avoid detection o a newly ormed reproductivepair by neighbouring males.

The high coecients o variation or call propertiessuch as call duration, call rate and note duration or bothwithin the individual and the population or Ameerega

braccata are in agreement with the common pattern omany anuran species calls (Gerhardt and Huber, 2002).In act, these variables are more susceptible to variationwith climatic eatures and male social context than acous-tic parameters with lower coecients o variation betweenindividuals. Generally these properties that vary a lot areoten the targets o the emales choice and also may beimportant or male territorial deense (Gerhardt, personalcommunication). Because it is a main property used inspecic recognition, however, dominant requency wouldbe probably less subjected to within-population variation(Bernal et al., 2005). Nevertheless, dominant requencymay vary with body size (Bee, 2002; Smith et al., 2003),a relationship that must be investigated in urther studieswithA. braccata.

Previous studies on acoustic communication werebasically descriptive; however, recent investigations haveanalysed acoustic eatures, also rom evolutionary, ontoge-netic, and behavioural perspectives (Kumar, 2003). Thosestudies have beneted rom this integrative approach, be-cause acoustic characteristics may shed light on phyloge-netic relationships among species (Martins and Jim, 2004).Unortunately, call data or each species o the genus

Ameerega were not obtained in a standardised way, thuspreventing statistical comparisons. Furthermore, we lack aphylogenetic hypothesis that includes all species o thepic-ta group; thus, we cannot map the bioacoustic traits onto aphylogenetic hypothesis o the group in order to assess anyevolutionary trend. Twomey and Brown (2008) described anew species o a Peruvian Ameerega species based mainlyon molecular data. The vocalization properties were one othe most important traits to discriminate the new species. Intheir phylogenetic hypothesis,A. braccata was sister groupoA. favopicta, although the position o this group with

the remaining species oAmeerega could not be inerredprecisely. From our bioacoustic comparisons among somespecies opicta group,A. hahneli shows the most distinc-tive vocalization based on range requency and note du-ration. We suggest that researchers should standardise thecollection o bioacoustics data rom several males (at least10 males rom each locality) and analyse at least 10 callsrom each male, but this may change in accordance withthe variation rom each species.

4.2. Habitat

Contrary to the habitat description o Haddad and

Martins (1994), we ound individuals oA. braccata inChapada dos Guimares and Cuiab in open physiognomieso campo sujo and cerrado stricto sensu rather than ingallery orests, in populations rom Chapada dos Guimaresand Barra do Bugres (nowadays Porto Estrela). Accordingto the same authors, males o congenerics usually vocalise

Figure 4. Intra-population coecient o variation (%) oselected properties o 110 advertisement calls oAmeeregabraccata: (CD) call duration, (CR) call rate, (DF) dominantrequency, (MAF) maximum requency, (MIF) minimum

requency and (ND) note duration.

Figure 5. Intra-individual coecient o variation (%) oselected properties o 110 advertisement calls rom 11

Ameerega braccata individuals: (CD) call duration, (DF)dominant requency, (MAF) maximum requency, (MIF)minimum requency and (ND) note duration. The lines inthe gure represent each mean value by property.


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over rocks near streams (A. favopicta), amidst lea litter(A. hahneli), and among dead tree branches on the lea litter(A. picta), thereore diering rom what was observed orA. braccata in its type-locality, with males usually observedcalling on leaves o shrubs and herbaceous plants. Costaet al. (2006), believed thatA. favopicta was the unique spe-

cies among the Dendrobatidae amily known to occupy openareas subjected to high temperatures and low humidity, butin the present study we ound that A. braccata occupy thesame kind o area with a pattern o similar conditions.

Bertoluci and Rodrigues (2002) suggested that anuranspecies that congregate in a reproductive locale tend to segre-gate temporally the microhabitat occupation.A. braccata donot take part in microhabitat segregation with other anuranspecies, because like other dendrobatids (Wells, 1987) thisspecies does not gather in a specic place to reproduce.

Acknowledgements We thank Luiz Antnio Solino or help

during the eldwork, Andr Pansonato or helping with thebioacoustics analysis, Carlos A. Navas Iannini, Itamar AlvesMartins and H. Carl Gerhardt or suggestions on previousversions o the manuscript. LRF and TM thank CAPES ornancial support, Bolsista PRODOC / CAPES.

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Artigo Canto a. Bracatta