respuestas vocales en ranas neotropicales

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Journalof Herpetology, Vol. 36 , No. 4, pp. 615420, 2002Copyright 2002 Society for the Study of Amphibians and Reptiles

Vocal Responses to Conspecific Call Virariation in the Neotropical Frog

Physalaemus enesefae

ZAIDA TARANO'

Postgrado en Cietncias Biol6gicas, Universidad Simn6n Bolfvar, Venezuela

ABSTRACT.-Female Physalaemus enesefae prefer long calls, low and average dominant frequency calls,

and calls repeated at short intercall intervals over short calls, high dominant frequency calls, and calls re-

peated at long intercall intervals. I tested the hypothesis that males modify their vocal behavior when faced

with potential competitors in ways that make them more attractive to females and that the more attractive

the competitor, the greater the modification. In playback experiments, I examined the responses of males tothe same stimuli used to test female responses: long and short calls, calls with low or high dominantfrequency, long and short intercall intervals, and average calls for all traits. Among the variables analyzed,

only the intercall interval was modified in the presence of the experimental stimuli. Males significantly

reduced the intercall interval (called at a faster rate) in response to all experimental calls, compared with

that when vocalizing alone, except in response to short calls and to long intercall interval calls. Males did

not respond differently to calls of average and above aver-age attractiveness. There was no difference in the

intercall interval in response to average and above average attractive stimuli. However, the intercall interval

in response to unattractive calls was significantly longer t:han that in response to calls of average attractive-

ness. The results partially support the hypothesis: males modify their spontaneous calling behavior when

faced with a competitor but do not show finely tuned graded responses in relation to the attractiveness ofthe competitor.

The advertisement calls of anurans are in-

volved in female choice and male-male compe-

tition (Greenfield, 1994; Schwartz, 1994). Male

responses to the calls of other males often in-

volve escalation: males increase intensity, rate,

duration, or complexity of their calls, especially

when confronted with males that are attractive

to females (Narins and Capranica, 1978;Schwartz and Wells, 1985; Ryan, 1985; Wagner,

1989; Bosch and Marquez, 1996). Competitive

escalation between males often parallels female

preferences based on acoustic traits. For in-

stance, female tungara frogs (Physalaemus pus-

tulosus) prefer more complex calls, and males

increase call complexitv in response to calls of

other males (reviewed in Ryan, 1985).Acoustic competition between males often in-

volves call duration, intensity, and rate; theseare call properties that tend to vary substantial-ly within individuals (Gerhardt, 1991). Male

Leptodactylus albilabris,Acris crepitans, Hyperolius

marmoratus, and Rana clamitans, however, lower

the dominant frequency of their calls, a propertythat tends not to vary dramatically within in-

dividuals in most anurans studied (summarized

in Howard and Young, 1998), when they hear

the calls of bigger or heavier males (L6pez et al.,

1988; Wagner, 1989; Grafe, 1995; Bee et al., 2000).

Phonotaxis experiments show that call dura-

tion, rate, intensity, and dominant frequency in-

fluience female choice in Physalaemus enesefae(TArano, 1999). Females prefer longer calls, more

intense calls (differences > 3 dB), calls repeated

at higher rates, and calls with lower dominantfrequency (Tarano, 1999). Among these charac-

te istics, only the dominant frequency of the callis negatively correlated with male mass, al-thaugh mass explains only a small fraction of

the variation of this trait (Tarano, 2001). Female

preferences based on the dominant frequency ofthe call may be related to the slight mating ad-

vantage observed among larger males. Obser-

vations of male behavior in the field showed that

males call from relatively stable positions. Fe-males approach them and initiate contact. Malesdo not search for females or attempt to dislodge

peired males (pers. obs.).

If females choose males based on their vocalcharacteristics, one might expect that males alter

their vocal output in relation to the attractive-

ness of their neighbors. Males could increase theattfractiveness of their calls when confronted

w th attractive competitors by reducing intercall

in terval (increasing call rate), increasing call du-ra :ion, or lowering the dominant frequency of

their calls. The more attractive the competitor,the greater the expected change in the male's



ZAIDA TARANO

cal behavior in relation to the attractiveness of

potential competitors to females, specifically,

that males modify their vocal output in ways

that increase their attractiveness to females.

MATERIALS AN]) MET1IODS

I conducted the study at Hato Masaguaral

(8°34'N, 67°35'W), a cattle ranch located 50 km

south of the town of Calabozo at Guarico state,

in the central llanos of Venezuela, from June to

August in 1997 and 1998. 1 collected males from

choruses from 1900 to 2100 h nightly and per-

formed playback experiments from 2200 h to

0100 h, in a dimly lit room. I placed individual

males, each in a plastic bag with water, on a

table 50 cm apart from each other. Males were

able to call from the small volume of water at

the bottom of the plastic bags. I placed a speak-

er (JBL M5 or SONY) 60-80 cm in front of themales in the bags and stimulated them to callby broadcasting a recording of a natural chorus.

When a male called in response to the chorus

for 5 min or more, I carefully removed the other

males from the table; thus, during the experi-

mental session only one male was on the table.I positioned the speaker in front of the calling

male and placed a microphone (Sennheiser

ME62/K6) on the table, at mid distance between

the speaker and the male, oriented to the male.

I connected the microphone to an analog tape

recorded (Marantz PMD 201) and used metaltapes to record male responses during the ex-

periments. I adjusted the stimulus intensity atthe male to 82 dB SP L (re 20 p.Pa) using a sound

pressure level meter (Radio Shack, fast response,

flat weighting). This corresponds to the average

intensity of male calls at 50 cm from the male

(Tarano, 2001). Rvan and Rand (1998) used a

similar approach (broadcast and recorded callsthrough plastic bags) and found that acoustical

distortion was minimal.

I tested males singly and usually only one

male each night. The experimental session con-sisted of an initial control stimulus followed by

several experimental stimuli and a final control.

I presented to the test male the control for 2 min

and recorded his responses during the follow-

ing 2 min. I repeated the same procedure with

all the experimental stimuli. Time interval be-

tween subsequent stimuli was that necessary toretrieve the file containing it, and usually lasted

less than 1 min. Thus, there were short silent

periods between trials. Usually males briefly in-

terrupted calling activity during this silent pe-

riod or immediately after a new stimulus wasbroadcast. This interruption suggests that males

detect changes in their vocal environment and

TABLE 1. Characteristics of the experimental stim-

uli.

Dominant IntercallDuration frequency interval

Experimiienital call (ins) (Hz) (s)

Average call (Control) 720) 900 3.6Long call 860 900 3.6

Short call 440 900 3.6

Low dominant frequency 720 630 3.6

High dominant frequency 720 1000 3.6

Short intercall interval 720 900 2.3

Long intercall interval 720 900 6

I tested each male with several successive

stimuli so that the experimental session of one

male that responded to all the sounds presented

(controls and experimental) lasted around 40min. Trial sequence was randomized fo r eachmale, to control for any order effect. Calls, either

control or experimental, were broadcast while

recording; thus, both the stimulus and the male

response were recorded. I also recorded males

that vocalized spontaneously without stimula-

tion and used these recordings to estimate male

vocal activitv without competitors. Males that

stopped responding during or after a test were

stimulated to resume calling by playing the cho-rus stimulus. I finished the session when the

male did not resume calling after 10 min ofstimulation.

Stiiiili.-Stimuli consisted of typical natural

calls recorded in the field during 1996 and 1997,so that they were within the natural range ofvariation for the population under study (Tara-

no, 2001). 1prepared and broadcast the stimulus

with a PowerBook 1400 cs using SoundEdit 16

software. Control stimuli consisted of a typical

nattural call 720 ms in duration, 900 Hz in dom-

inant frequency and repeated with a period of3.6 sec. Controls represent average attractive

calls for females. Ihe experimental stimuli con-sisted of natural calls, average in all traits but

one. Thus, I chose natural calls from the popu-

lation that were close to the population mean in

two of the three variables analyzed and more

extreme in one of the others. Characteristics ofthe experimental stimuli are summarized in Ta-

ble 1. Experimental stimuli represent above and

below average attractive calls for females.

I used calls from five males to prepare the

stimuli to reduce the effect of uncontrolled var-

iables. Thus, I had five different controls, and

five different experimental stimuli for each var-iable analyzed. Each stimulus contained one

natural call from one male repeated at a fixed

616



VOCAL RESPONSES IN PHYSALAEMUS ENESEFAE

Intmrcall Interval (s)

45

4

3

25

2

1.5

Control HDF LDF LC SC SIl LIl

Stimulus

FIG. 1. Intercall interval in male responses to allstimulus compared to that during spontaneous vocal

activity (male alone). For each stimulus, the box rep-resents the mean, and the line represents the standard

error. Stimuli: HDF, high dominant frequency; LDF,low dominant frequency; LC, long call; SC, short call;

II, long intercall interval; SII, short intercall interval.**P - 0.05, NS P > 0.10. UResponse to the stimulus;E Alone.

with a PowerBook using SoundEdit 16 (44 kHz,

16 bit). I measured call duration (time from the

beginning to the end of a call) dominant fre-

quency (frequency containing more energy in

the entire call) and intercall interval (time fromthe beginning of a call to the beginning of the

next) in male responses to all stimuli (control

and experimental). Call duration and dominant

frequency were measured in five to 10 calls ran-

domly chosen from the 2-min recording of the

male response for each stimulus. Intercall inter-

val was measured from the oscilogram of the

entire recording of the male response. Spectral

information was obtained by performing a FastFourier Transform (FFT, frequency resolution

176 Hz, 51 6 points) with Canary 1.2.1 (Orni-

thology Laboratory at Cornell).StatisticalAnalysis.-I compared call duration,

dominant frequency, and intercall interval dur-

ing spontaneous vocal activity (male alone)

with those during the responses to the control

and to each experimental stimulus. I also com-

pared male responses to controls (average at-tractive calls) with responses to above average

and below average attractive calls. All compar-

isons were performed by using paired two-

tailed t-tests. Male responses to initial and final

controls were averaged because there was no

significant difference between them in any var-iable measured (t-test, all P > 0.05). Despite the

fact that I used each male in several successive

..5

1.5

2HDF LDF LC SC Sil LIl

Stimulus

FIG. 2. Intercall interval in male responses to ex-pcrimental stimulus compared to control stimulus. For

each stimulus, the box represents the mean, and thelire represents the standard error. Experimental stim-ulas are HDF, high dominant frequency; LDF, lowdominant frequency; LC, long call; SC, short call; LII,long intercall interval; SII, short intercall interval. **F• 0.05, *P = 0.054, NS P > 0.10. UResponse to the

stimulus; P Response to average call (control).

comparisons were performed between sets ofdata obtained from several males, and a male's

response to one stimulus is independent of an-

other male's response to the same stimulus. All

statistical analyses were performed with Stat-giafics 6.0.

RESULTS

I tested a total of 25 males; sample sizes dif-

fe red among tests because several males did not

respond to all stimuli. Intercall intervals were

significantly longer during spontaneous activity

than in response to all stimuli, except for the

long intercall interval and the short call stimuli

(cDntrol: t = 2.27, df = 38, P = 0.03; high dom-

inant frequency: t = 2.07, df = 26 , P = 0.05; low

dominant frequency: t = 2.33, df = 30, P = 0.03;long call: t = 1.80, df = 16, P = 0.05; short call:t = 1.35, df = 18, P = 0.19; short intercall in-

terval: t = 2.52, df = 32, P = 0.02; long intercall

interval: t = 1.24, df = 30, P = 0.22; Fig. 1).There were no significant differences in the in-

tercall intervals between stimuli of above aver-

age and below average attractiveness versus the

control (i.e., stimuli of average attractiveness)

except for the long intercall interval stimuli

(long intercall interval: t = -2.57, df = 36, P =

0.014); the difference approached significance

for the short call stimuli (t = -2.03, df = 22 , P= 0.054, Fig. 2). Thus, males called at similar

rates when exposed to average calls and to at-

Intercall Interval (s)

-I l _______NN S NBS N

FKFF FK617



ZAIDA TARANO

tractive calls, that is , long intercall interval and

short call stimuli, with the exception of high

dominant frequency stimuli.

I did not find significant differences in call

duration nor in the dominant frequency of the

call in male responses between the spontaneous

vocal activity and the experimental stimuli

(paired t-test, NS for all comparisons), nor be-

tween the control and the experimental stimulus

(paired t-test, NS for all comparisons).

DISCUSSION

The responses of P enesefae males to variation

in conspecific calls supported the hypothesis

that males would alter their vocal activity when

exposed to potential conspecific competitors.

Males reduced their spontaneous intercall inter-

val in the presence of stimuli of average or high

attractiveness to females but did not modify

their spontaneous intercall interval in the pres-

ence of unattractive stimuli. The results, how-

ever, do not support the prediction that males

would adjust their vocal responses to the attrac-

tiveness of the stimuli because their responses

were similar for stimuli of average and above

average attractiveness.

The results of this study show that, among

the variables analyzed, only the intercall inter-

val is dependent on the social context in P ene-

sefae. The selective importance of the modifica-

tion of the intercall interval is straightforward:females show strong and unanimous preferenc-

es for calls repeated at short intervals (TArano,

1999).Despite the fact that males significantly re-

duced the intercall interval in the presence of a

stimulus, compared to their spontaneous vocal

output, a response observed in many anurans

(Wells, 1988), they did not call at relatively

shorter intervals in response to the most attrac-

tive calls to females. This does not seem to re-sult from a trade-off between matching the

stimulus rate and avoiding call overlap, because,albeit there is no correlation between response

rate and stimulus rate, call overlap in response

to stimuli repeated at 3.6-sec or 2.3-sec intervals

do not depart from random in either case (Ta-

rano, 1999). In contrast, the proportion of over-

lapping calls in response to stimuli repeated at

2.3-sec intervals is significantly greater than that

in response to stimuli repeated at 3.6-sec inter-

vals, as expected if males respond randomlv to

the stimulus. Because silence intervals between

successive calls in P enesefae are long, in relation

to call duration (3-4 times longer), randomprobability of placing a call in these intervals,

and thus avoid call overlap, is relatively high:

tween the stimulus calls and male responses re-

mains to be determined, these results indicate

that males do not shift the timing of their calls

in ways that avoid overlap with those of the

stimulus. Call matching has been described inseveraL anurans (Wells, 1988; Schwartz, 2001).

Male Philautus leucorh inus alternate calls with

those of neighbors with few instances of call

overlap, despite considerable variation in call

duration and intercall intervals during each

bout of alternation (Arak, 1983). However, play-

backs do not elicit an increase in call rate insome anurans. Hyla versicolor males always de-

creased calling rate and increase call duration,

regardless of the stimulus presented (Wells and

Taigen, 1986).The lack of correspondence between stimulus

attractiveness and male responses, in P enesefae,

suggests several interpretations. First, males donot perceive the differences between stimuli ofaverage and above average attractiveness. The

percent difference between calls of average and

below average attractiveness was slightly higher

than that between calls of average and above

average attractiveness, 36% and 30%o, respec-

tively. This explanation would be more likely if

there were a profound asymmetry in the re-

sponsiveness of the inner ear, so that differences

between certain pairs of stimuli need to be larg-

er than between others to be detected. Second,

males do perceive the differences between stim-uli of average and above average attractiveness,

but the differences lack biological meaning.

Neurophysiological studies are needed to assess

this hypotheses properly. Third, male responses

to all stimuli, except to unattractive ones, rep-

resent typical responses to a potential compet-

itor. When the social context changes from being

alone to being with another male, the male re-

sponds by increasing its call rate, regardless ofthe characteristics of the potential competitor.

Fixed responses to potential competitors might

result from a trade-off between competition fo rfemales and energy conservation. Calling is en-

ergetically expensive in anurans, and energy ex -penditure is related to call rate (Pough et al.,

1992; Prestwich; 1994). Wells and Taigen (1989)found that metabolic rate in Hyla microcephala

increased with increasing calling rate. If females

choose males based on their calling rate, males

would make a better use of their energy re-

serves if they call at their maximum call rate

only when females are in their vicinity, much asPhysalaennis pustulosus only adds chucks, which

increase attraction to both females and frog-eat-ing bats, only in response to vocal competition

with other males (Ryan, 1985). Males would call

618



VOCAL RESPONSES IN PHYSALAEMUS ENESEFAE

their maximum rate only when females ap-

proach them. Field observations support this hy-

pothesis: a chorusing male dramatically increas-

es his call rate, although for short periods, when

a female approaches him (pers. obs.). Similarly,

Wells (1988) found that males of three Neotrop-

ical treefrogs (Hyla ebraccata,H. phlebodes, H. mi-

crocephala) alter their vocal behavior when they

detect a female nearby. Thus the equally strong

response to the controls (average calls) and to

the experimental stimuli (with the exception oflong intercall interval calls and short calls) may

simply be a fixed response to any average or

above average attractive call but not the maxi-

mum response a male is able to produce.

It is also possible that apparent indifference

of males to variation in experimental stimuli ofaverage and above average attractiveness could

be caused by sampling error and not a popu-lation characteristic. Sample size was small for

several tests (short and long calls), and analyses

indicate that power of those tests was below

0.10. Thus, an effect might exist but could not

be detected. In addition, if male vocal respon-

siveness varies with age, population means

would not reflect individual behavior. Green

(1990) found that large male P pustulosus in-

creased the complexity of their calls more than

small males, in response to a novel calling

neighbor.

The response of male P enesefae to calls re-

peated at various intervals is similar to that ob-

served in other species. Male Eleutherodactylus

coqui increase their calling rate in response to

neighbor males, although there is no correlation

between stimulus call rate and male response

call rate (Benedix and Narins, 1999). Males ofthe grasshopper Ligurotettix planum responding

to a stimulus reduce their call rate when ex -posed to unattractive males but not below their

spontaneous call rate (Greenfield, 1994).In this study, I analyzed male P enesefae re-

sponses to calls of fixed levels of attractiveness,high, mid, or low attractiveness, for the study

population. But male responses could be affect-

ed by the relative attractiveness of the compet-

itor in relation to the focal male. Bosch et al.(2000) found that P pustulosus males responddifferently to "fixed frequency" conspecific calls

(calls of high, mid, and low dominant frequency

for the study population) than to "relative fre-

quency" calls (calls of high or low dominant fre-

quency in relation to those of the focal male).

Male responses did not vary among fixed fre-

quency tests. However, males responded withmore whines and chucks to calls of similar orhigher frequency than to calls of lower frequen-

Male P enesefae did not modify either the

dominant frequency or the duration of their

calls in the presence of potential competitors.

T -iis result is not unexpected because only a fewrrale anurans are able to modify the dominant

frequency of their calls, and even in such spe-cies, the change is small, about 2-5% (L6pez et

a]. 1988; Wagner, 1989; Grafe, 1995; Bee et al.,

20)00). The relative stability of the dominant fre-

quency is attributed to morphological restric-

tions (Martin, 1972; Ryan and Drewes, 1990).Morphological correlates of call duration in an-

u 2ans have not been determined but are prob-ably related to limits on air exchange between

tlhe lungs and vocal sac.

Acknowledgments.-This study was part of my

doctoral dissertation submitted at UniversidadSim6n Bolivar. I am grateful to E. A Herrera, M.J. Ryan, C. Bosque, and L. E. Levin for their sug-

gestions throughout the study. M.J. Ryan also

commented on this manuscript. I thank T

B-.ohm for his hospitality while conducting the

fieldwork at his ranch. H. Mirabal and J. I. Del-

gado gifted me their friendship during the long

and hot days at the field. I was supported by a

doctoral fellowship from Consejo Nacional de

Irivestigaciones Cientificas y Tecnol6gicas

(CONICIT) and bv Decanato de Estudios de

Postgrado of Universidad Sim6n Bolivar.

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Accepted: 27 February 2002.

620



COPYRIGHT INFORMATION

TITLE: Vocal Responses to Conspecific Call Variation in the

Neotropical Frog Physalaemus enesefae

SOURCE: J Herpetol 36 no4 D 2002

WN: 0233505199010

The magazine publisher is the copyright holder of this article and it

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respuestas vocales en ranas neotropicales

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