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South American Journal of Herpetology, 6(2), 2011, 87-97 © 2011 Brazilian Society of Herpetology

Temporal and spatial patterns of reproductive activity in Rhinella hoogmoedi (Anura: Bufonidae) from a tropical rainforest in northeastern Brazil, with the description of it’s advertisement call Igor Joventino Roberto1,4*, Lucas Brito2,3, and Paulo Cascon2,3 Sertões Consultoria Ambiental e Assessoria. Rua Bill Cartaxo, 135, Bairro Sapiranga. CEP 60688‑185, Fortaleza, CE, Brasil. E‑mail: [email protected] 2 Programa de Pós-Graduação em Ecologia e Recursos Naturais, Departamento de Biologia, Universidade Federal do Ceará – UFC. Avenida Humberto Monte, 2.977, CEP 60455‑760, Fortaleza, CE, Brasil. 3 Laboratório de Zoologia Experimental, Departamento de Biologia, Universidade Federal do Ceará, Campus do Pici. CEP 60455‑760, Fortaleza, CE, Brasil. 4 Corresponding author. 1

Abstract. The study of ecological and behavioral aspects of anuran reproduction is fundamental for the understanding of the evolution of life history traits. In this study we present the temporal and spatial patterns of reproductive activity in Rhinella hoogmoedi, as well as the description of its advertisement call, in a population from a remnant of tropical rainforest in Northeastern Brazil. Calling activity began before the start of the rainy season and lasted from November to April; vocalization activity was not correlated with the amount of rainfall. Reproductive males called on a variety of substrates close to or in permanent or temporary water bodies, during both day and night. Male behavior at high and low densities, calling sites occupancy and reproductive period indicate an unusual explosive breeding pattern for the species. Rhinella hoogmoedi presented a multi-pulsed call, composed of pulse group calls, similar to Rhinella paraguayensis, Rhinella castaneotica, Rhinella martyi, populations of Rhinella gr. margaritifera from Bolivia, Rhinella margaritifera from French Guyana, and Rhinella gr. margaritifera from Cusco, Peru. Acoustic parameters such as call duration, number of pulse groups per call, number of calls per minute, note duration, number of notes per minute, pulse rate, dominant frequency, and amplitude modulation types of call, were good parameters to discriminate among the species of the Rhinella margaritifera group, as in the members of the Bufonidae family. New descriptions of complete advertisement calls and molecular studies will help elucidate taxonomic, biogeographic, and phylogenic patterns for this complex of species. Keywords. Amphibia, Natural History, Rhinella margaritifera, Vocalization.

Introduction The knowledge of ecological and behavioral aspects of amphibian reproduction, such as reproductive mode, temporal and spatial patterns, and communication are helpful in the understanding of amphibian evolution and can be also useful to elucidate phylogenetic relationships (Wells, 1977; Duellman and Trueb, 1994). Knowledge of temporal and spatial patterns of reproduction, as well as on recruitment dynamics are also relevant if proper conservation plans are to be made. Vocalization is an important aspect of anuran communication, playing a major role in species recognition and mate attraction, and being used also in territorial behavior and as a defensive mechanism (Duellman and Trueb, 1994). Advertisement calls are known to be species-specific and may be seen as a prezygotic reproductive barriers, being, therefore,extremely important for taxonomic studies (Vences and Wake, 2007). The Rhinella margaritifera species group is currently composed of 15 species, although several

other cryptic species remain to be described (Fouquet et al., 2007a,b; Avila et al., 2010). One unique and unreversed synapomorphy supports the monophyly of this group: the expansion of the posterior ramus of the pterygoid (Pramuk, 2006). In the last 50 years this group has been recognized as having a complex and difficult taxonomy, and the inclusion or exclusion of species in this group has been a common practice (Hoogmoed, 1986; Hoogmoed, 1990; Fouquet et al., 2007a,b). The integrative taxonomy proposed by Dayrat (2005) has been applied in amphibian taxonomic studies in the last decade with multiple approaches, using a variety of data such as morphological, molecular, behavioral, and bioacustical. Such approaches have helped elucidate complex taxonomic problems, and resulted in the description of several cryptic species (e.g., Grant et al., 2006; Fouquet et al., 2007; Padial and De La Riva, 2009). The leaf toad Rhinella hoogmoedi Caramaschi and Pombal Jr, 2006 is the only species in the Rhi‑ nella margaritifera group that occurs in the tropical rainforests of Brazil’s Atlantic coast (Caramaschi and

Reproduction of Rhinella hoogmoedi

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Pombal Jr, 2006). Data on its biology are scarce and restricted to tadpole description (Mercês et al., 2009) and a couple of reports on vocalization sites (Pombal Jr. and Gordo, 2004; Silva-Soares et al., 2010). Most reproductive biology data available for species in the Rhinella margaritifera group comprise scattered information (such as calling period and site) obtained in occasional field observations (Duellman, 1978; Hoogmoed, 1990; Lescure and Marty, 2000; Fouquet et al., 2007), with the exception of a few detailed field studies (e.g., Wells, 1979). According to these authors, such species usually have an explosive breeding pattern, with a diverse array of calling sites and a multi-pulsed call, typical of Bufonidae. In the present study we provide information regarding use of calling sites and reproductive period of Rhinella hoogmoedi in a small remnant of humid forest in Northeastern Brazil, and describe its advertisement call. We hope the information provided will help in the elucidation and better understanding of the extremely complicated taxonomy of the R. mar‑ garitifera group. Material and Methods Study area We conducted fieldwork at in Parque das Trilhas, municipality of Guaramiranga, Ceará State, northeastern Brazil (04°16’S, 38°56’W)). The area is located in Serra de Guaramiranga, a natural tropical rain forest remnant 880 meters above sea level inserted in the Caatinga Biome (Figueiredo and Barbosa, 1990).

The average annual temperature is 21°C and historical (1974‑2008) average annual rainfall is 1711 mm (range 818‑2399 mm), concentrated from January to May (Funceme, 2010). Average monthly rainfall (1974‑2008) in Guaramiranga ranges from 29.5 mm (September) to 303.2 mm (April), with a seven-month period (January-July) in which rainfall is above 100 mm (Figure 1). However, rainfall was highly atypical during our fieldwork, with above average rainfall from April 2009 to July 2009 and below average from August 2009 to June 2010 (April 2010 was an exception) (Figure 1). Maximum and minimum air temperatures ranged from 23.0‑30.6°C and 18.7‑22.8°C, respectively. Air humidity’s maximum and minimum values ranged from 81‑99% and 57‑92%, respectively. Natural history data We visited the area once every month from April 2009 to June 2010, in trips that lasted from 2 to 7 days, except for January and March when it was visited twice, with a total of 6 field days each. Observations took place at five different artificial water bodies, as follows: WB1, a lake fed by little rivulets that pass through forested areas; WB2, a lake resulting from mining operations in the early nineties with 50% of the margin occupied by a vertical rock wall ranging from 2‑15 meters; WB3, an artificial lake with about 40% of its margins surrounded by tall (> 15 m) trees and 60% by grass; WB4, an artificial lake located near a few houses, from where it receives waste water; WB5, a small (1 meter wide; 50 meters long;

Figure 1. Average rainfall (1974‑2008; white bars) and rainfall during the present study (April 2009-June 2010; black bars) in Guaramiranga, Ceará.

Roberto, I. J. et al.

5 cm deep) temporary artificial stream connecting WB2 to WB3. All five water bodies are surrounded by secondary humid cloud forest. Individuals observed had their snout-vent length and weight measured with a digital caliper (0.01 mm precision) and a Pesola scale (0.5 g precision), respectively, and were then released at the same place where they were captured. We used an index of calling activity to analyze the relationship between calling activity and rainfall. The index ranges from 0 to 3, where: 0 = no calling activity; 1 = sporadic calls (number of calling individuals (ic) ≤ 5); 2 = frequent calling activity spaced by long pauses (5  15). As rainfall variables we used the amount of rainfall on the day in which the observations took place, one day, three days and one week prior to observations, as well as monthly rainfall. We used these four variables to test for a delay in the anurans’ response to rainfall. Call Recordings We recorded calls of two males with a Sony TCM 5.000 EV tape recorder, and an unidirectional Senheiser ME 66 microphone, on April 14, 2006 in the locality of Sítio Sinimbu; and on March 3, 2010 in the locality of Parque das Trilhas (21.6°C; 93%), both in the municipality of Guaramiranga, recorded between

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7‑8 pm. We digitalized recordings at 44.1 kHz, 16 bit resolution, and the spectral parameters were a FFT 512 (1024 for power spectrum), 3 dB filter bandwith, 124 Hz; hop size 256 with Raven 1.2 software (Charif et al., 2004). Terminology for acoustic parameters follows Martin (1972) and Heyer et al. (1990): Call: acoustic unit of a frog vocalization, may be broken either into identical or different notes; Note or pulse group: Calls are often broken into smaller subunits by 100% amplitude modulation with only short intervals between them relative to the length of the note. A call with 100% amplitude modulation is said to be made up of notes; one which is modulated at less than 100% is said to be pulsed (Pulsed group); Pulse: the smallest named subunit of a call, produced by amplitude modulation which may be 100% but often less. We compiled available data on the advertisement calls of the Rhinella margaritifera group, for comparisons with R. hoogmoedi calls and to facilitate new bioacoustics and taxonomic studies regarding this complex of species (Table 1). Statistical Analyses Data were tested for normality using the D’Agostino test (Zar, 1996). Since data did not meet normality assumptions, Spearman’s Rank Correlation was used to test if rainfall was statistically related to calling activity. Significance level considered was

Figure 2. Index of calling activity for Rhinella hoogmoedi and monthly rainfall at Guaramiranga, from May 2009 to June 2010. Bars indicate index of calling activity. Values are as follow: 0 = no calling activity; 1 = sporadic calls (individuals calling (ic) ≤ 5); 2 = frequent calling activity spaced by long pauses (5  15).

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90

Table 1. Acoustic parameters in the Rhinella margaritifera group. Values are mean ± standard deviation, range in parentheses. Legends – PGC: Pulse group/call; CD: call duration(sec); ID: Intercall duration (sec); CM: call per minute; ND: note duration (sec); InI: Intercall interval (sec); NM: Notes per minute; PR: Pulse rate(pulses per second); PD: Pulse duration; FR: Frequency range (Hz); DF: Dominant Frequency (Hz); Ppg: Pulses/pulse group; LP: Last pulse note; L/S: locality/State; C: country; R: reference.

TC*

R. paraguayensis II

R. proboscidea I

PGC

6.5 ± 0.6 (5-8)



CD

0.3 ± 0.04 (0.2-0.42) 0.5 ± 0.015 (0.22-0.98) 39.3 ± 6.4

0.12 ± 0.01 (0.08-0.14) —

0.03 ± 0.01 (0.01-0.07) 0.02 ± 0.01 (0.01-0.04) 504.8 ± 113 (262.4-792.4)

ID CM ND InI NM

R. gr. margaritifera I

R. gr. margaritifera II

R. martyi II

R. lescurei I

R. gr. margaritifera —

6.75 ± 0.957

6



6

0.26 (0.23-0.29)

0.29 ± 0.045

0.29 ± 0.013



0.27 ± 0.010

0.35 (0.17-0.67)







69 ± 4.24













PD PR



FR

618.9-1771.8

DF

0.97 ± 0.017 81 ± 21.21

1-10

90

0.09 ± 0.1179

0.03 ± 0.164

0.08 ± 0.1184

0.026 ± 0.007

0.025 ± 0.004-



0.097- ± 0.018





480-



0.008 ± 0.0007

0.009 ± 0.0012

0.003 ± 0.0016

0.008 ± 0.0012

89.68 ± 5.30 (79.88-97.02) 1630-3200

33 (31-41)





















1651(1574-2016)

1265 ± 35

1169 ± 40

1161 ± 15

1407 ± 37

PPg

1438.7 ± 70.5 (1113.7-1568.5) —





2

2

4.83 ± 0.787

2

LP







3.25 ± 0.5

4.75 ± 0.96



4.5 ± 0.577

L/S

Poconé/Mato Grosso Brazil

Manaus/ Amazonia Brazil

Kaw Mountains









French Guyana

French Guiana

Suriname

French Guiana

French Guiana

Hass, 2004

Fouquet et al. 2007

Fouquet et al. 2007

Fouquet et al. 2007

Fouquet et al. 2007

C R

Avila et al. 2010 Zimmerman and Bogart, 1988

α = 0.05. All analyses were conducted using Biostat 5.0. Data throughout the paper are presented as mean ± S.D. Results Temporal and spatial patterns of reproduction We heard calling males from November 2009 to April 2010 in WB2‑WB5, from 8:00 am‑10:00 pm, with a peak between 5:30‑7:30 pm. We observed R. hoogmoedi (Figure 3) calling from several different sites, from inside the water grabbed onto dead debris to nude ground away from water, both in temporary and permanent water bodies. Mean air

temperature and moisture during calling activity was 22.7 ± 0.3°C and 86.2 ± 4.16%, respectively. Males found calling (n = 13) ranged in size from 52.06 to 63.94 mm (57.58 ± 2.52) and weighed 14.8 ± 1.7 g (11‑19 g). Males would actively change their location on nights of intense calling activity, interrupting their calling to go nearer the water or climb up the margin towards the leaf-litter, after which they would re-start vocal activity. Males of R. hoogmoedi actively searched for females around calling sites in these dense aggregations. We observed some males apparently attempting to amplex with male conspecifics; a specimen grasped tightly onto the author’s finger during data collection, as if trying to amplex; and another individual displayed the same behavior towards the author’s boots. Calling males spaced

Roberto, I. J. et al.

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Table 1 (continued). Acoustic parameters in the Rhinella margaritifera group. Values are mean ± standard deviation, range in parentheses. Legends – PGC: Pulse group/call; CD: call duration(sec); ID: Intercall duration (sec); CM: call per minute; ND: note duration (sec); InI: Intercall interval (sec); NM: Notes per minute; PR: Pulse rate(pulses per second); PD: Pulse duration; FR: Frequency range (Hz); DF: Dominant Frequency (Hz); Ppg: Pulses/pulse group; LP: Last pulse note; L/S: locality/State; C: country; R: reference.

TC*

R. gr. margaritifera —

R. gr. margaritifera —

R. gr. margaritifera II

R. gr. margaritifera II

R. castaneotica II

R. magnussoni III

R. margaritifera II

PGC





7.9 ± 0.6 (7-8)

6.3 ± 0.6 (5-7)

9.1 ± 1.1 (7-12)



(5-8)

CD

0.24 ± 0.013

0.239 ± 0.024

0.487

0.490 ± 204

0.238 ± 0.022 (0.197-0.291) —

0.204 ± 0.025 (0.180-0.273) —

9.9 ± 4.5 (3.3-23.1) —



ID

0.316 (0.291-0.339) —

CM

60 ± 2.8

59.8 ± 4.2

57.0 ± 18.6 (31.3-95.2) —





160

0.0105 ± 0.038 (0.005-0.020) —

0.06 ± 0.01 (0.02-0.09) 0.12 ± 0.02 (0.07-0.26) —

0.04







900-2600

1600-2820





InI





82.52 ± 1.66 (80.9-84.9) 0.0225 ± 5.35 (14-41) —

NM









97.9 ± 15.62 (84.8-125.7) 750-1450

0.005 (0.001-0.009) 102.1 ± 17.4 (52.2-149.2) — 1332.3 ± 107.0 (1211.5-1544.7) 2.0 ± 0.5 (1-4)

1650

1890-2550

1200







ND



PD



2647.9 ± 86.7 (2500-2775)

— —

PR

23.3 ± 2.89

25.4 +-3.6

FR





DF

1315 ± 134

1335 ± 128

PPg





1140 ± 10 (1130-1150) 2.0 ± 0.73 (1-4)

LP















Provincia Yacuma/Beni Bolivia

La Bola/Santa Cruz Bolivia

Cobija/Pando

Belterra/Pará

Bolivia

Brazil

Cusco/Madre de Dios Peru

L/S C R

Dubulay Ranch Ceiba Biological Center Guyana Guyana

Bourne and York, Bourne and York, Köhler et al. 1997 De La Riva et al. 2001 2001 1996

themselves and remained stationary at low densities, calling from concealed locations, as opposed to the behavior at high densities where males call exposed, frequently changing positions and exploring different calling sites. Upon being manipulated, some specimens emitted release calls that strangely seemed to trigger males to start calling. There was no significant relationship between calling activity and amount of rainfall on the day of observation (rs = 0.1589; p = 0.57), one day (rs = ‑0.17; p = 0.54), three days (rs = ‑0.04; p = 0.88), and one week (rs = 0.01; p = 0.97) prior to observations or with monthly rainfall (rs = ‑0.17; p = 0.54; Figure 2). However, the first month in which we observed calling activity (November) and the month in which we observed the most intensive calling activity (December)

Köhler and Lötters, 1999

Lima et al. 2007 Duellman, 1978

were both before the onset of the wet season, but after the first rains (≈ 10 mm in November and ≈ 15 mm in December) following an above average drought. Froglets (SVL  70) on the margins of WB1 on April 2009; and in both WB1 and WB5 on February 2010 and April 2010 respectively. We did not observe clutches or tadpoles during the study period. Advertisement Call Rhinella hoogmoedi has a multi-pulsed call (Figure 4) composed of 5.55 ± 0.58 pulse groups (3‑7, n = 110), with a duration of 0.248s ± 0.026 (0.175‑0.316, n  =  163), followed by intercall

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Reproduction of Rhinella hoogmoedi

call; and 2.54 ± 1.12 (1‑6, n = 487) pulses per pulse group. The first and last pulses of the pulse group are the most variable; in the first pulse group the mean of pulses is 1.98 ± 0.59 (1‑3, n = 110), and the mean number of pulses in the last pulse group is 4.43 pulses ± 0.81 (2‑6, n = 110). Frequency ranges from 455‑3.926 Hz (n = 60), with dominant frequency of 1341 Hz ± 42.74 (1292‑1378 Hz, n = 89) (Figure 4, Table 1). Discussion Figure 3. Male of Rhinella hoogmoedi vocalizing in locality of the Sitio Sinimbú, municipality of Guaramiranga, State of Ceará (Individual 1, recorded vocalization). (Photo by Ciro Albano).

intervals of 0.353s ± 0.17 (0.178‑1.395, n = 144). Average rate of calls per minute is 111.3 ± 32.1 (36.06‑279), n  =  127), with note duration of 0.029s ± 0.011 (0.013‑0.062, n = 120); inter-notes interval of 0.016s ± 0.006 (0.007‑0.063, n = 96) and 2649 ± 1257.7 (759.5‑6000, n = 96) notes per minute. Average note-rate (pulse groups per second) is 25.06 ± 3.47 pulse groups per second (12.66‑33.33, n = 96), with 13.51 ± 1.24 (9‑17, n = 110) pulses per

Temporal and Spatial Patterns In the present study R. hoogmoedi called from November to April, representing the beginning of the wet season. Among the species of the R. margaritifera complex, R. paraguayensis, R. margaritifera from the Brazilian Amazon and R. gr. margaritifera from Panguana, Peru, breed during the dry season (Aichinger, 1987; Bernarde, 2007; Ávila et al., 2010). The other species belonging to this group seem to follow a different pattern, breeding sometime within the wet season. For instance, in Panama, Wells (1979) observed

Figure 4. Advertisement call of Rhinella hoogmoedi. A waveform of multiple calls; B waveform of two calls (1 = call; 2 = Pulse group; 3 = Single pulse); C Spectrogram of the two calls presented in B; D Power spectrum of the first call presented in B. (Individual 1, recorded on 14 April 2006 in the Sítio Sinimbu, Guaramiranga municipality, Ceará State, Brazil.

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Table 2. Measurements of acoustic parameters for males of Rhinella hoogmoedi, from the municipality of Guaramiranga, State of Ceará, Brazil. Values are means ± standard deviation. Parameters Type of call* Pulse groups/call Call duration Intercall duration Call minute Note duration (pulse duration) Inter-notes interval Notes minute Note rate (pulse group per second) Frequency range Dominant frequency Pulses/Call Pulses/pulse group First Pulse/note Last Pulse/note

Rhinella hoogmoedi – Individual 1 II 5.44 ± 0.54 (5‑7) n = 50 0.22818 s ± 0.01687 (0.20‑0.27) n = 66 0.2679s ± 0.115 (0.178‑0.792) n = 57 128.87.5 ± 32.4.02 (58.3‑279) n59 = 0.0276s ± 0.010 (0.013‑0.054) n = 60 0.015s ± 0.008 (0.007‑0.063) n = 48 1588.1 ± 211.2 (759‑2000) n = 48 26.47 ± 3.52 (12.6‑33.3‑30) n = 48 495.3‑4474.2 (n = 30) 1343.403 Hz ± 42.55 (1292‑1378.1) n = 67 13.12 ± 1.154 (11‑16) n = 50 2.4 ± 1.15 (1‑6) n = 276 1.6 ± 0.49 (1‑2) n = 50 4.62 ± ‑0.96 (2‑6) n = 50

R. gr. margaritifera in breeding activity from August to November, in the mid- to late wet season. Rhinella martyi, R. castaneotica, R. magnussoni, R. probos‑ cidea, R. sclerocephalus, and R. lescuri, all found in forested areas of northern South America, presented breeding activity in the wet season sometime between November to May, and lasting from one to six months (Caldwell, 1991; Mijares-Urrutia and Arends, 2001; Menin et al., 2006; Fouquet et al., 2007; Lima et al., 2007). The lack of a relationship between the number of individuals calling and rainfall observed for R. hoogmoedi was also observed for R. gr. mar‑ garitifera in Panama (Wells, 1979). Nevertheless, field observations suggest a clear effect of rainfall on calling activity. First observations of individuals calling (end of November 2009) occurred after the first rains, that although light (