Vocalisations and Reproductive Pattern of Boana Pombali (Caramaschi Et Al., 2004): a Treefrog Endemic to the Atlantic Forest

Herpetology Notes, volume 12: 1121-1131 (2019) (published online on 03 November 2019)

Vocalisations and reproductive pattern of Boana pombali (Caramaschi et al., 2004): a treefrog endemic to the Atlantic Forest

Marina dos S. Faraulo1,*, Caroline Garcia1 and Juliana Zina1

Abstract. Boana pombali is an endemic species of the Atlantic Forest whose biology and ecology are still little known. In the present study we aimed to describe the reproductive patterns adopted by the species and characterise the behaviours associated with reproduction, including the description of its advertisement and territorial calls. From April 2016 to March 2017 we conducted 96 nocturnal field trips in which we collected data on habitat use, abundance and behaviours in two water bodies located in the interior of the Parque Estadual Serra do Conduru, municipality of Uruçuca, State of Bahia, northeast Brazil. Males of B. pombali were observed in calling activity during the whole studied period, using the vegetation of the water bodies and surroundings as vocalisation sites. We recorded a higher number of males in the chorus during the months of higher rainfall and, consequently, formation of temporary water bodies. We registered only one female on April, when, although the water bodies were dry, there were males calling from large epiphytic bromeliads. The temporal distribution pattern as well as the behaviours presented by the species corroborate with the known for prolonged breeding species. The data presented here enhances the knowledge about the autoecology of B. pombali and on the group of B. semilineata.

Keywords. Advertisement Call, Amphibia, Autoecology, Behaviour, Natural History, Reproduction

Introduction 2011; Nali and Prado, 2012). Moreover, these data can be used for the development of strategies, actions Studies about the basic biological aspects of anurans and interventions necessary for the protection of the raise fundamental information for the behavioural and species. ecological characterisation of taxonomic units (species, Even in the face of all the above-mentioned genus or groups of species) (see Ryan and Rand, 1993; importance, descriptive researches have been neglected Narvaes et al., 2009, Köhler et al., 2017). Data of this by the academy and by the scientific data publishing nature can be taken isolated or immersed in a set of spaces, which privilege studies that evidence more data to trace phylogenies (see Ryan and Rand, 1993; de global biological and ecological patterns (see Guerra Queiroz and Wimberger, 1993; Duellman et al., 2011; et al., 2018). However, these same studies highlight the de Sá R.O. et al., 2014). In addition to contributing to importance of natural history data to obtain a reliable and the descriptive content, studies conducted under this legitimate data matrix to make projections and evidence perspective elucidate questions related to the structure patterns closer to the real (see Haddad et al., 2008; of the populations (occurrence, abundance and use of Campos et al., 2017; Guerra et al., 2018; Lourenço- the environment) and communities (richness, diversity, de-Moraes et al., 2019). In Anura, many of these data composition, spatial and temporal structure), as well come from studies on their reproductive biology, since as mechanisms behind the intra and interspecific reproduction seems to be an important factor that relationships (e.g. Wells, 1977a, b; Montanarin et al., organises the populations and communities of the group (e.g. Becker et al., 2007; Loyola et al., 2008). Despite the knowledge about the reproductive aspects of anurans has increased in the last decades (e.g. Nali and Prado, 2012; de Sá F.P et al., 2016; Guerra et al., 1 Departamento de Ciências Biológicas (DCB), Universidade 2018), it is still insipient considering the volume of Estadual do Sudoeste da Bahia (UESB), Campus Jequié, Av. José Moreira Sobrinho, s/n, Jequiezinho, CEP 45208-091, data about the natural history of the species and the Jequié, Bahia, Brasil. amount of species not yet studied. Some points can * Corresponding author. E-mail: [email protected] be raised to explain this lack of knowledge about the 1122 Marina dos S. Faraulo et al. natural history of anurans, such as: recent description Data collection.—We performed 10 field trips of taxonomic unities not yet studied (e.g. Taucce et (duration between six to 16 consecutive days) between al., 2015), idiosyncrasies related to behavioural and April 2016 and March 2017, totalling 96 nocturnal ecological patterns (e.g. explosive reproductive pattern sampling days. Two water bodies were surveyed: a (Nomura, 2003)), use of microhabitats not accessible pond (14º29’42.94”S 39º08’07.76”O) surrounded by to researchers (e.g. use of high epiphytic bromeliads trees and an herbaceous vegetation located in an open (Juncá et al., 2012a; Campos et al., 2014)), and/or a very area (13 m of maximum diameter and 1.2 m maximum restrict geographical distribution and occurrence (e.g. depth), and a swamp (14º29’37.66”S 39º08’07.36”O) Napoli et al., 2011; Taucce et al., 2015). To date, even surrounded by trees with aerial roots and an herbaceous widely studied species have inedited biological aspects vegetation located in a shaded lowland area (6.5 m of recently described (e.g. Boana albopunctata (Spix, maximum diameter and 0.8 m maximum depth). Both 1824) (Furtado et al., 2016) and B. crepitans (Wied- environments were about 50 m apart from each other. Neuwied, 1824) (Nascimento et al., 2015)). The data collection started around 17:30 h and finished Boana pombali is a medium-sized hylid (snout-vent when the activity of the males decreased (between 00:00 length (SVL) 49.0-55.6 mm in males, 53.9-60.7 mm h and 01:00 h during the period of highest rainfall and in females, Caramaschi et al., 2004) that belong to B. around 21:30 h during the dry months). We extended semilineata group (Faivovich et al., 2005; Peloso et al., our observations until dawn in 10 field days to confirm 2018). The species presents a restricted distribution to the daily vocal activity pattern. In total, we performed areas of the Brazilian Atlantic Forest, in a geographic approximately 530 h of observations. We used the range that goes from the states of Minas Gerais to methodology of visual and acoustic search (Heyer et al., Sergipe, Brazil (Frost, 2019). Although it has been 1994). described 15 years ago, few information on the natural For each water body we obtained the following history is available for this species (see Caramaschi et al., information: microhabitat characteristics of the calling 2004; Juncá et al., 2012b; Brunetti et al., 2015a). Thus, sites (perch type and height relative to the ground), the aim of this study was to describe the autoecology, number of individuals in vocal activity, distance between vocalisation and some reproductive aspects of B. the males in vocal activity and displacement of these pombali. individuals throughout the night. In order to measure the displacement of the individuals we first monitored the Material and Methods reproductive sites marking and recording all the males in calling activity, then we walked thought the same sites Study area.—The Parque Estadual Serra do Conduru verifying the perches. In case of recapture, we verify the (PESC) (14º29’42.5”S; 39º08’1.6”W) is located in the distance between the initial and final perches. district of Serra Grande, municipality of Uruçuca, south For behavioural observations we used the focal state of Bahia, Brazil. The PESC covers an area of 9,275 animal method (Lehner, 1996). When we finished hectares of Atlantic Rainforest in good conservation each observation, we weighed the observed individuals state (Bahia/Semarh, 2005). with dynamometer (Pesola ®) with a 0.1 g precision, The climate of the region is type Af (Köppen, 1936), measured the SVL with a calliper of 0.1 mm precision characterised as hot and humid, with no defined dry and marked them using toe clipping method modified season and a high annual precipitation well distributed from Martof (1953). Then, we returned the individuals throughout the year (annual average of 2471 mm; Inema, to where they were captured. Whenever possible, 1996). The average month temperature is between 20 we marked all the individuals in the first day of each and 26ºC, with annual average around 24ºC (Inema, field trip to avoid a possible negative influence on the 1996; Bahia/Semarh, 2005). In the period of the data animals´ behaviour. collection occurred an atypical drought, due to El Niño We collected one gravid female and seven males during the years 2015 and 2016. Therefore, some usually during the period of study. These individuals were permanent- water bodies dried up, presenting temporary euthanised with lidocaine at 5%, fixed in formalin characteristic. Thus, exceptionally, during the period of 10%, kept in alcohol 70% and housed in the zoological this study, rainfall was concentrated during the months collection of the Universidade Estadual do Sudoeste of July 2016 to March 2017, with higher indexes in July, da Bahia (UESB) - Campus Jequié (MHNJCH – 1083; October and March, totalling 1,299.1 mm of rainfall MHNJCH – 1084; MHNJCH – 1085; MHNJCH – 1087; (CPTEC/INPE, 2017). MHNJCH – 1088; MHNJCH – 1089; MHNJCH – 1094; Vocalisations and reproductive pattern of Boana pombali in the Atlantic Forest 1123

MHNJCH – 1102). From the gravid female we obtained emission of note within the note groups we performed a the mass of the oocytes and from the males the testicular linear regression (considering the number of notes within mass. We weighed all the materials in analytical balance the note groups the dependent variable and the number of 0.0001 g precision. The percentage of the ovarian and of males in chorus the independent variable).To verify mature testicular mass in relation to the corporal mass if the interval between the notes groups diminished with was used as a measure of reproductive investment (RI). the increase in the number of notes within the notes groups, we used a Spearman correlation test (using the Call recording and analyses—The advertisement interval between the note groups and the number of and territorial calls of B. pombali were obtained notes within the groups as variable). with a Marantz® PMD660 digital record coupled to In the cases of metrics with distinct magnitudes, we a Sennheiser® ME66 directional microphone. We logarithmised the values with log 10. analysed the calls using the software Raven Pro 1.4 To compare the height of the perches used during the (Bioacoustics Research Program, 2011) (window type dry and rainy season we applied the Student´s t-test. We = WAVE, window size = 512 samples, sampling rate of obtained data on total rainfall for each month sampled 44.1 kHz, 16-bits precision, and overlap = 75 %). The from the Proclima online platform (CPTEC/INPE, call types were attributed according to the context of 2017). emission following the review proposed by Toledo et al. For all the statistical analyses we tested the normality (2015). We analysed 17 calls per male (SD = 4.6; range= of the data and homogeneity of the variance. All the 10-29; N = 27 males) with approximately 35 notes per statistical analysis were performed using SigmaStat 3.5 male (SD = 0.6, range = 35-37 notes per male). After (2006). We considered significant values of P < 0.05 each recording we obtained the temperature and relative (Zar, 2010). air humidity using a thermohygrometer with 0.1 °C precision. Results We analysed the following acoustic parameters: dominant frequency (DF), 1st quartile frequency (1QF), All the information about the SVL, body mass, and 3rd quartile frequency (3QF), frequency 5% (F5) and RI of males and females of B. pombali are summarised frequency 95% (F95), inter-quartile range bandwidth in the Table 1. There was no significant correlation (IQB50), bandwidth 90% (B90), inter-note interval between testicular mass and body mass (r = 0.51; P = (IN), inter-call interval (IC) (inter-note group interval), 0.23) or SVL (r = 0.2; P = 0.78) of the males. repetition note rate and note duration (delta time) Use of habitat and reproductive period.—A total of 88 (Charif et al., 2010). The units of the analyses of the males of B. pombali were found calling throughout the vocalisations were notes (see Köhler et al., 2017). The study period, being October the month of higher activity beginning and end of each note was determined from (Figure 1). The swamp was the environment with the oscillograms (wave forms), using as reference 10% of higher number of calling males (49 totals, against 30 in the maximum note amplitude (Littlejohn, 2001). the pond). None marked male was found at a different This study was conducted with appropriate permissions reproductive site (swamp or pond) from where it was and guidelines from the responsible authority—licence initially registered. Mostly males of B. pombali used the (49225-4) issued by “Instituto Chico Mendes de Conservação da Biodiversidade” (ICMBio) that also evaluates protocols for our collection and research. This research was approved by the ethics committee on the Table 1. Snout vent length (SVL), body mass of males and use of animals (CEUA-UESB 127/2016). female of Boana pombali, recorded in the Parque Estadual 1 Statistical analyses.—To verify the possible Serra do Conduru, district of Serra Grande of the municipality of Uruçuca, State of Bahia, Brazil, between the years of relationship between the air temperature and monthly- 2016 and 2017. The values represent the means ± standard accumulated rainfall to the abundance of calling males, Table 1. Snout vent length (SVL), body mass of males and female of Boana pombali, recorded in the Parque deviation.Estadual Serra do Conduru, district of Serra Grande of the municipality of Uruçuca, State of Bahia, Brazil, we performed multiple regression. To verify if the between the years of 2016 and 2017. The values represent the means ± standard deviation. testicular mass of males is related to their body mass, we Males Female used a Pearson correlation test. Similarly, to verify if the testicular mass of males is related to their SVL, we used SVL (mm) 55.03 ± 3.76 61.80 Body Mass (g) 6.66 ± 1.25 10.10 the Spearman correlation test. To verify if the increase in the number of males in chorus would increase the RI 0.06% ± 0.01 16.23%

Table 2. Perches height mean used by males of Boana pombali in calling activity, recorded in the Parque Estadual Serra do Conduru, between the years of 2016 and 2017, district of Serra Grande of the municipality of Uruçuca, State of Bahia, Brazil. The values represent the means ± standard deviation.

Height of vocalization perches (m) Dry season 1.04 ± 0.71 Rainy season 3.83 ± 2.49

Table 3. Temporal characteristics of calls of Boana pombali, recorded in the Parque Estadual Serra do Conduru, between the years of 2016 and 2017, district of Serra Grande of the municipality of Uruçuca, State of Bahia, Brazil. The values represent the means ± standard deviation. DT = delta time; IN = Inter-note interval; IC = Inter-call interval.

Temporal characteristics of calls Types of call Note DT (s) IN (s) IC (s) ------0.239 ± 0.036 2.006 ± 0.741 1º 0.054 ± 0.004 ------2º 0.047 ± 0.003 ------Advertisement call 3º 0.046 ± 0.003 ------4º 0.045 ± 0.003 ------5º 0.044 ± 0.006 ------0.197 ± 0.004 14.189 ± 9.654 Territorial call 1º 0.030 ± 0.005 ------2º 0.100 ± 0.020 ------

1124 Marina dos S. Faraulo et al.

eight metres above the ground), far (more than 100 metres) from the monitored areas. In April, we recorded a gravid female perched in a tree next to the pond. Males presented conservation of the calling site at night and during the breeding season. Among the 31 males marked, we recaptured 11. In one of the cases, the male was registered in the same site for three sequential months. The highest rates of capture and recapture occurred in the months of higher rainfall (Fig. 2) and Figure 1. Number of individuals of Boana pombali observed in also with a greater number of individuals registered each month, monthly accumulated rainfall (mm) and average (Fig. 1). The minimum distance between calling males monthly temperature (ºC) registered in the Parque Estadual was 1.5 m, during the rainy season. Serra do Conduru, between the April 2016 and March 2017, The number of calling males was positively related district of Serra Grande of the municipality of Uruçuca, State with the monthly rainfall and air temperature (r2 = of Bahia, Brazil. 0.603; P = 0.04). Boana pombali presented a nocturnal calling activity. The peak of call activity of B. pombali was between 19:30 h and 21:00 h (Fig. 3), both during the dry and rainy session. The height of the perches used vegetation at the edge of the water bodies as calling sites by the males was significantly distinct between the dry (47.54%), followed by aquatic vegetation or on trunks and1 rainy seasons (t= -8.906; P< 0.001) (Table 2). within the water body (34.42%) and vegetation located more than 50 cm away from the edge of the water body Vocalisations: Advertisement call.—The advertisement Table 1. Snout vent length (SVL), body mass of males and female of Boana pombali, recorded in the Parque (18.02%). The perches used varied from iridaceous callEstadual was the Serra most do common Conduru, vocalisation district of Serra emitted Grande by ofB. the municipality of Uruçuca, State of Bahia, Brazil, (Iridaceae) (30.52%), tree branches (Melastomataceae) pombalibetween males. the years This of vocalisation 2016 and 2017. consists The values in the representemission the means ± standard deviation.

(22.10%), bromeliads (Bromeliaceae) (18.94%), Males Female aquatic macrophytes (Juncaceae) (9.47%), shrubs SVL (mm) 55.03 ± 3.76 61.80 (Melastomataceae) (8.42%), peace-lily (Araceae) Body Mass (g) 6.66 ± 1.25 10.10 (3.15%) and, to a lesser extent, stumps, fallen trunk, Table 2. Perches height mean used by males of Boana pombali RI 0.06% ± 0.01 16.23% ground and creepers (7.36%). In the swamp the in calling activity, recorded in the Parque Estadual Serra do Conduru, between the years of 2016 and 2017, district of Serra individuals were visualised using more iridaceous and Grande of the municipality of Uruçuca, State of Bahia, Brazil. bromeliads, while in the pond they were more perched Table 2. Perches height mean used by males of Boana pombali in calling activity, recorded in the Parque TheEstadual values Serra represent do Conduru, the means between ± standard the deviation.years of 2016 and 2017, district of Serra Grande of the municipality of on trees. Uruçuca, State of Bahia, Brazil. The values represent the means ± standard deviation. Between April and June 2016, when the reproductive sites were dry, we heard males of B. pombali vocalising Height of vocalization perches (m) only from large epiphytic bromeliads (approximately Dry season 1.04 ± 0.71 Rainy season 3.83 ± 2.49

Temporal characteristics of calls Types of call Note DT (s) IN (s) IC (s) ------0.239 ± 0.036 2.006 ± 0.741 1º 0.054 ± 0.004 ------2º 0.047 ± 0.003 ------Advertisement call 3º 0.046 ± 0.003 ------4º 0.045 ± 0.003 ------Figure 2. Number of captures and recaptures of Boana pombali Figure 3. Peak of the call 5º activity of 0.044 the males± 0.006 of Boana ------per month (captures in dark grey and recaptures in grey) in the pombali during the dry and rainy--- session in the- --Parque Estadual 0.197 ± 0.004 14.189 ± 9.654 Parque Estadual Serra do Conduru, district of Serra Grande of SerraTerritorial do Conduru, call district of 1ºSerra Grande 0.030 of ±the 0.005 municipality ------the municipality of Uruçuca, State of Bahia, Brazil. of Uruçuca, State of Bahia, Brazil. 2º 0.100 ± 0.020 ------

Vocalisations and reproductive pattern of Boana pombali in the Atlantic Forest 1125

Figure 4. Oscillogram and spectrogram of the advertisement call (MZ001146) (snout-vent length = 58.0 mm, recorded at a temperature of 20.8°C.) (A) and territorial call (MZ001142) (snout-vent length = 63.6 mm, recorded at a temperature of 21.6°C.) (B) of Boana pombali recorded in the Parque Estadual Serra do Conduru, district of Serra Grande, municipality of Uruçuca, State of Bahia, Brazil. Oscillogram – axis y: Amplitude (u); axis x: Time (s). Spectrogram - axis y: Frequency (Hz); axis x: Time (ms).

of simple notes or note group with up to five of these higher duration, while the other notes of the note units (mean = 2.21; SD = 0.74; mode = 2; range = 1-5; groups presented gradual decrease in duration (Table 3). N = 913 calls; Fig. 4A). Advertisement calls composed When in chorus, the neighbouring males of B. pombali by simple notes normally occurred in the beginning of vocalised in antiphony, avoiding overlapping. the calling activity or when the calling male was away Although we did not measure, we observed that the from other males. The notes are multipulsed, with an note rate per call was lower at the beginning of the average of 9.85 pulses per note (SD = 2.18; range = vocalisation activity, when the male was isolated and/ 3-16; mode = 10; N = 1507) (Fig. 4A). We observed or when there was some perturbation (e.g. torrential that the addition of notes to the note group is positively rains, gales, presence of the researcher and presence related to the number of calling males in the reproductive of predator- personal observation). The spectral and chorus (r2 = 0.828; P < 0.001). Moreover, we observed temporal parameters of the advertisement call are that the addition of notes to the note group is negatively summarised in Tables 3 and 4. correlated with the interval between the note groups (r2 Territorial call.—This type of vocalisation is emitted = -0.662; P < 0.001). between consecutive advertisement calls or isolated, The notes were emitted at an average note rate of 63 when there is a presence of a conspecific male nearby. notes/minute (SD = 27.2; range = 14-128 notes/minute; It is composed by a set of two multipulsed notes, with N = 45 minute). The first note of the note group has an average of 6 pulses per note (DP = 2.8; range = 6-12; 1

Table 1. Snout vent length (SVL), body mass of males and female of Boana pombali, recorded in the Parque Estadual Serra do Conduru, district of Serra Grande of the municipality of Uruçuca, State of Bahia, Brazil, between the years of 2016 and 2017. The values represent the means ± standard deviation.

Males Female

SVL (mm) 55.03 ± 3.76 61.80 Body Mass (g) 6.66 ± 1.25 10.10

RI 0.06% ± 0.01 16.23%

Height of vocalization perches (m) Dry season 1.04 ± 0.71 Marina dos S. Faraulo et al. 1126 Rainy season 3.83 ± 2.49

Table 3. Temporal characteristics of calls of Boana pombali, recorded in the Parque Estadual Serra do Conduru, between the years Table 3. Temporal characteristics of calls of Boana pombali, recorded in the Parque Estadual Serra do Conduru, of 2016 and 2017,between district ofthe Serra years Grande of 2016 of andthe municipality2017, district of of Uruçuca, Serra Grande State ofof Bahia,the municipality Brazil. The of values Uruçuca, represent State the of Bahia,means ± standard deviation.Brazil. DT The= delta values time; represent IN = Inter-note the means interval; ± standard IC = Inter-call deviation. interval. DT = delta time; IN = Inter-note interval; IC = Inter-call interval.

Temporal characteristics of calls Types of call Note DT (s) IN (s) IC (s) ------0.239 ± 0.036 2.006 ± 0.741 1º 0.054 ± 0.004 ------2º 0.047 ± 0.003 ------Advertisement call 3º 0.046 ± 0.003 ------4º 0.045 ± 0.003 ------5º 0.044 ± 0.006 ------0.197 ± 0.004 14.189 ± 9.654 Territorial call 1º 0.030 ± 0.005 ------2º 0.100 ± 0.020 ------

mode = 3; N = 10 notes), both with harmonic (Fig. 4B). Discussion The first note is shorter (mean = 0.030; SD = 0.005; The SVL of B. pombali described by Caramaschi et al. range = 0.019-0.033; N = 5 notes) than the second note (mean = 0.1; SD = 0.02; range = 0.072-0.115; N (2004) was lower, both for the males and females, than = 5 notes). The spectral and temporal parameters of the those found in this study. territorial call are summarised in Tables 3 and 4. The In the present study, we did not observe a significative aggressive interactions between the males occurred by correlation between the body mass and SVL and the vocalisations and no physical combat was registered. testicular mass of B. pombali. This result may be related

2 Table 4. Spectral characteristics of calls of Boana pombali, recorded in the Parque Estadual Serra do Conduru between the years of 2016 and 2017, district of Serra Grande of the municipality of Uruçuca, State of Bahia, Brazil. The values represent the Table 4. Spectral characteristics of calls of Boana pombali, recorded in the Parque Estadual Serra do Conduru means ± standardbetween deviation.the years DFof 2016 = dominant and 2017, frequency; district ofF95 Serra = frequency Grande of that the divides municipality the note of into Uruçuca, two frequency State of Bahia,intervals, which contain 95%Brazil. and The5% ofvalues the total represent energy, the respectively; means ± standard F5 = frequency deviation. thatDF contains= dominant 5% frequency;and 95% of F95 the =total frequency energy, that respectively; divides the note into two frequency intervals, which contain 95% and 5% of the total energy, respectively; F5 = 1QF= inter-quartilefrequency rangethat contains of frequency 5% and that 95% contains of the 25% total and energy, 75% respectively;of the total energy, 1QF= respectively;inter-quartile 3QFrange = of inter-quartile frequency range of frequencythat that containscontains 25%75% and and 25% 75% of of the the total total energy, energy, respectively; respectively; IQB50 3QF = = inter-quartile inter-quartile range range bandwidth of frequency that thatcontains 50% contains 75% and 25% of the total energy, respectively; IQB50 = inter-quartile range bandwidth that contains of the total50% energy of the present total energyin the note;present B90 in =the bandwidth note; B90 range= bandwidth that contains range that90% contains of the total 90% energy of the totalpresent energy in the present note. in the note.

Types of Note Harmonic Spectral characteristics of calls call DF F95 F5 1QF 3QF IQB50 B90 (Hz) (Hz) (Hz) (Hz) (Hz) (Hz) (Hz) Advertiseme 1º --- 2470.84 ± 2028.66 ± 955.19 ± 1320.28 ± 1867.93 ± 543.80 ± 1073.45 ± nt call 221.39 100.90 57.55 144.13 67.41 122.00 72.42 2º --- 2316.41 ± 1970.77 ± 930.76 ± 1126.16 ± 1793.38 ± 667.22 ± 1040.03 ± 191.39 105.53 64.10 105.30 63.46 69.28 76.89 3º --- 2281.40 ± 1942.47 ± 939.76 ± 1104.30 ± 1741.96 ± 636.35 ± 1002.76 ± 196.97 102.01 55.58 84.72 73.17 49.65 71.42 4º --- 2254.64 ± 1924.48 ± 926.90 ± 1085.02 ± 1704.67 ± 624.79 ± 997.61 ± 192.72 96.65 58.26 92.50 77.25 60.64 68.94 5º --- 2182.85 ± 1894.90 ± 904.40 ± 990.55 ± 1636.55 ± 646.00 ± 990.55 ± 104.30 0 60.95 60.88 121.83 60.95 60.88 Territorial 1º 2360.06 ± 1119.7 1313.53 ± 818.28 ± 1012.08 ± 1205.90 ± 193.83 ± 495.25 ± call 207.44 43.05 111.19 43.05 00.00 43.05 108.38 2º 3755.36 ± 1171.42 ± 1507.35 ± 969.03 ± 1098.18 ± 1205.90 ± 107.65 ± 538.33 ± 308.18 47.21 49.70 43.05 43.05 00.00 43.10 82.43

Vocalisations and reproductive pattern of Boana pombali in the Atlantic Forest 1127 to the presence of males with small body size and with the reproductive modes of the species (Haddad large testicular mass. This disproportion between SVL et al., 2013), it is also a plastic characteristic strongly and testicular mass of males may be indicative of the influenced by ecological factors (Zina et al., 2014), recruitment of young males to compose the reproductive such as habitat heterogeneity, microhabitat availability, chorus, as observed for other congener long-breeding climatic conditions and pressures of competition and season species (sensu Wells, 1977a) (see Boana predation (e.g. Eterovick et al., 2010). All these factors albopunctata in de Sá F.P. et al., 2014). However, we evidence that the environmental heterogeneity is an do not have enough data to make more inferences. We important element that acts in the maintenance of the suggest that the low rainfall and the late formation of anuran reproductive activities (e.g. Becker et al., 2007; water bodies, normally perennial, after a long drought Eterovick et al., 2010). period, could have influenced in the early entry of new We observed a seasonal difference in the use of calling males in the chorus. sites by males of B. pombali. This has been already The female of B. pombali presented a high reproductive observed for other anurans (see Zina and Haddad, 2006). investment, similar to that observed for other species of This could be related with the increased chances of anurans, such as Leptodactylus chaquensis Cei, 1950 attracting partners, since higher perches would promote (RI = 16%) (Prado and Haddad, 2003), Physalaemus a more effective sound propagation, attracting females albonotatus (Steindachner, 1864) (RI = 16.6%, Prado that would be more dispersed out of the reproductive and Haddad, 2005) and Bokermannohyla ibitiguara season (Richards and Wiley, 1980). In the case of B. (Cardoso, 1983) (RI = 20.26%) (Nali and Prado, 2012). pombali the use of higher perches during the dry season Differently from the female, males presented low rate of could also be related to the use of epiphytic bromeliads, RI in comparison with other species (e.g. Rhacophorus which were the only water bodies available during arboreus (Okada and Kawano, 1924): RI = 5.15% the period with no rains. We highlight that we did not (Kusano et al., 1991), Leptodactylus chaquensis: RI observe the species egg laying in bromeliads. = 4.13% (Prado and Haddad, 2003)). Boana pombali The distinct occupation of the pond and swamp presents complex courtship behaviour (Zina, personal environments by calling males throughout the communication). The low RI of the males of B. pombali year is probably due to differences regarding their may be related to low risk of sperm competition (see configurations and dynamic in rainy and dry periods. Prado and Haddad, 2003) in a complex courtship The higher number of calling males recorded in the scenario in which females interact with only one male swamp during the study may be related to the higher (e.g. B. ibitiguara (RI = 0.29%) (Nali and Prado, vegetation and canopy of this environment. The shadow 2012)). of canopies helps maintain this water body with water Use of habitat and reproductive period.—Boana for a longer time. pombali used from the marginal and interior vegetation The number of males in vocal activity was positively of the water bodies to bromeliads as vocalisation site. correlated with rainfall, result already expected, The distinct calling sites used by this species show since rainfall signals availability of water bodies for plasticity in the use of the habitat (Caramaschi et al., reproduction (Prado et al., 2005; Zina et al., 2007). 2004). The use of different calling sites can be related The highest rates of capture occurred in the periods of to the spatial resource partitioning, in order to avoid higher precipitation and consequent formation of water the overlapping of territories between conspecific body indicating also possible recruitment. We also males (see Wells and Schwartz, 2007). By avoiding observed this tendency for the recaptures, indicating overlapping territory, males can prevent physical that during the rainy season males of B. pombali stayed combats and thus save energy, in addition to avoiding in the same reproductive site, possibly defended it. physical injury and a potentially death (Wells, 1977b). The males generally remain on the same perch Additionally, the use of alternative calling sites, such as throughout the night, this indicates a fidelity to the bromeliads, enable the species to remain in activity for calling site, fact confirmed by the recaptures in the same a longer time throughout the year (prolonged breeding spot or very near to it. The fidelity to the calling site may pattern, sensu Wells, 1977a, see discussion below) even be associated to their quality and demonstrates that the during eventual droughts. species is territorial (Crump, 1972; Rosen and Lemon, Although the use of the microhabitat is associated with 1974). The emission of the territorial calls reaffirms the phylogeny (e.g. Eterovick et al., 2010), as it is related territoriality of the species. 1128 Marina dos S. Faraulo et al.

Boana pombali presents typical characteristic of In the present study we provide the first description prolonged breeding species, such as: activity calling of territorial call for a species of the B. semilineata during all the year and territorial behaviour (e.g. Wells, group which is surprising, since some species of this 1977a; Martins and Haddad, 1988). The competition group presents anatomical apparatus (prepolex spine) degree between the males and the opportunity for partner (Faivovich et al., 2005) that can be used in physical selection by the females are strongly influenced by this interactions. Thus, territoriality and physical interactions reproduction pattern (Wells, 2007). The prolonged among males would be expected. We suggest that this is breeder pattern in turn, will influence the strength of the a very interesting field to be explored the relationship selection of important traits for reproduction, such as between the phylogeny of the group and territoriality. territoriality of the males, spawning size and investment The lack of knowledge about the territorial call in gonads (Prado and Haddad, 2005). of species of B. semilineata group is particularly Vocalisations.—The most common vocalisation of B. problematic since a high cryptic diversity in known for pombali was the advertisement call, a pattern generally this species group (see Fouquet et al., 2016). Spectral observed in other species (Lemes et al., 2012; Morais and temporal attributes of territorial call could be used, and Kwet, 2012; Morais et al., 2012). The acoustic in association with other acoustic traits, as taxonomy parameters of the advertisement call of B. pombali are and phylogenetic trait helping in the determination of similar to those described by Caramaschi et al. (2004), discrete species and elucidation of evolutionary history with exception of the number of notes per note group. In of the group. the description of B. pombali, the authors characterised One the other hand, some congener species have had the note groups as composed by only two notes, while its territorial call described (see B. punctata (Schneider, in this study we describe note groups with up to five 1799) (Brunetti et al., 2015b) and B. jaguariaivensis notes. Probably the influence of the social contexts (Caramaschi, Cruz, and Segalla, 2010) (Guerra et al., (i.e. number of co-specifics competitors) produced 2017)). As observed for B. pombali, the territorial call such difference, since the number of notes within the of these species are very similar to their respective note groups is apparently influenced by the number of advertisement calls (Brunetti et al., 2015b; Guerra et al., co-specifics in the chorus, fact also reported for other 2017). anuran species (e.g. Schwartz and Wells, 1985; Lemes The set of new information provided here on the et al., 2012). vocalisation and reproductive pattern of B. pombali The territorial call is emitted by males that defend exemplifies how little we know about the biology specific resources of the territory, such as quality of of relatively common anuran species. The lack of the calling site and proximity and quality of the sites knowledge about species abundance and dynamics in used for egg deposition and larval development (e.g. space and time (e.g. Prestonian shortfall (see Cardoso Martins and Haddad, 1988; Toledo and Haddad, 2005). et al., 2011)) is common in Anura, resulting in the loss This call can be emitted in the presence or even when of fundamental information to elucidate ecological a co-specific is absent (Zina and Haddad, 2006) or not issues (see Hortal et al., 2014) or propose actions of visible. Besides the territorial call itself, the addition conservation. of notes to the note group of advertisement call seems to serve to establish the territorial boundaries between Acknowledgement. We thank Ramon Almeida, Tales Barbosa, the males of B. pombali (see Halliday and Tejedo, Valdinei Teixeira and Thiago Amparo for their assistance 1995; Wells, 2007). The increase in the number of the during the field trip and Victor Dill for the initial review of this emission of notes may indicate the excitement state of manuscript. Gabriel Novaes e Fagundes for the help in the analyses of the vocalisations and Marcia Hoshina for the English version the male, that can be analysed by the females during of the manuscript. To Instituto Chico Mendes de Conservação the process of male choice, and by its opponent as part da Biodiversidade – ICMBio (SISBIO 49225-4) and Inema, for of a stepped process that could culminate in physical the license granted. Parque Estadual Serra do Conduru – PESC, confrontation (see Wells, 2007; Wells and Schwartz, for the structure. To the Universidade Estadual do Sudoeste da 2007). The lack of visualisation of physical aggressive Bahia – UESB, Graduate Program in Genetic, Biodiversity and interactions between males throughout the study suggest Conservation – PPGGBC and FAPESB (No BOL0545/2015) for that the males prioritise the vocal activities to establish the master scholarship granted. territories, thus avoiding disputes that are energetically expensive or cause damages (Wells, 1977b; Wells, 2007). Vocalisations and reproductive pattern of Boana pombali in the Atlantic Forest 1129

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Accepted by Igor Kaefer