Mate choice in the neotropical frog, Eleutherodactylus coqui

Anita. Behav., 1991,41,757-772

Mate choice in the neotropical frog, Eleutherodactyluscoqui P A M E L A T. L O P E Z * & P E T E R M. N A R I N S Department of Biology, University of California, Los Angeles, CA 90024, U.S.A. (Received 18 June 1990; initial acceptance 25 June 1990; final acceptance 27 September 1990; MS. number: A5764)

Abstract. The degree of intra-populational variation in male body size and condition, as well as spectral

and temporal features of the advertisement call ('co qui'), was extensive in a population of Eleutherodactylus coqui at E1 Verde, Puerto Rico. Dominant frequency of the 'qui' note was significantly, although weakly, associated with male body size and condition; call rate was not associated with either male attribute. In both laboratory two-choice trials and natural observations of courtship initiation, females showed no preference for call dominant frequency, but a strong preference for calls of relatively high rate. All mated males called at a rate that was greater than both the populational average and the average rate for unmated males, and all males reached their peak calling effort (maximum number of calls produced per minute) prior to 2300 hours. No size-assortative mating or large-male advantage regarding mating success was observed. Therefore, differential male mating success is not manifested through size-related variation in the spectral qualities of the advertisement call in this population of E. coqui. However, males may enhance their mating opportunities by calling rapidly, early in the night. Female mate choice in frogs is commonly based on some quality, or combination of qualities, of the advertisement call (see review by Gerhardt 1988). The assessment of males via acoustic cues is facilitated if the specific call attribute (1) is temperatureindependent, or if it is temperature-dependent there is a compensatory shift in the female auditory system (see Gerhardt 1978 for an example of the absence of temperature coupling), (2) varies little between nights for individual males and (3) accurately reflects some aspect of male quality that either directly (e.g. male territory quality) or indirectly (sensu Fisherian runaway sexual selection; Fisher 1930; or good genes arguments, Zahavi 1975; Hamilton & Zuk 1982) affects female reproductive success. In many species, call dominant frequency is negatively associated with male body size (e.g. Narins & Smith 1986; Morris & Yoon 1989), and because male size may affect fertilization success (e.g. Robertson 1990) or offspring fitness (e.g. Woodward et al. 1988), it has generally been proposed that females should prefer to mate with larger males. However, the occurrence of a largemale mating advantage via female choice is rare and is best documented for Physalaemus pustulosus (Ryan 1980). Additionally, because there is little *Present address: Department of Biology, Austin College, Sherman,. Texas 75090, U.S.A. 0003-3472/91/050757+16 $03.00/0

evidence for true, intensity-independent frequency discrimination by females (see Gerhardt 1988), this issue is rather controversial. Female preference for calls of high rate has been documented through laboratory trials (e.g. Klump & Gerhardt 1987; Arak 1988) and through direct observation of female choice in the field (Morris & Yoon 1989). Preference for this parameter is of interest because, in all species that have been examined, there is a positive association between call rate (and overall calling effort) and the metabolic costs of calling (e.g. Taigen & Wells 1985; Prestwich et al. 1989). Moreover, gradual decreases in energy reserves during the breeding season may reflect the costs associated with vocalizing and territory maintenance (e.g. Woolbright & Stewart 1987; Given 1988); physical differences between males may therefore be indicated by relative calling effort. Additionally, the relative rates at which males call may affect their mating success via the relative ease with which they are located by females (sensu Parker 1983). Our aims were to examine the degree of intrapopulational variation in spectral and temporal features of the advertisement call of a neotropical frog, Eleutherodactylus coqui (Leptodactylidae), and to determine whether females can reliably assess male size or physical condition via these call attributes. Additionally, we investigated the

9 1991 The Association for the Study of Animal Behaviour 757

758

Animal Behaviour , 41, 5

influence of female preference for call frequency and rate on male mating success through laboratory preference trials and field observations. Eleutherodaetylus eoqui is a continuously breeding polygynous anuran with extensive male parental care (Drewry 1970; Townsend et al. 1984). Males utter a two-note call ('co qui', Fig. la-c) whose components function, respectively, in intrasexual and intersexual communication (Narins & Capranica 1976, 1978). This phenomenon is reflected in the sexually dimorphic frequency sensitivity of the species' auditory system (Narins & Capranica 1976, 1980). A gravid female approaches and initiates courtship with a calling male, which then leads the female to the oviposition site, where internal fertilization occurs (Townsend et al. 1981). The male broods the eggs for 17-26 days (Townsend et al. 1984), during which calling activity is generally absent and foraging effort is minimal; males probably incur high energetic costs during this period (Simon 1983; but see Townsend 1986 who suggests that energetic costs of brooding are low in E. coqui). Hatching success is enhanced by providing parental care throughout the developmental period (Townsend 1986). Therefore, the influence of female choice for male quality should have a significant effect on male mating success in E. eoqui. METHODS Study Area and General Methods The study area was situated at the E1 Verde field station in the Luquillo Mountains of northeastern Puerto Rico (latitude 18~19'N, longitude 65~ elevation 350 m). Mean annual rainfall is 3456 mm and mean monthly temperature and relative humidity during this study (July-August 1985, September 1986, August-September 1987, and July-September 1988) varied from 24-25~ and 85-95%, respectively. We selected an irregularly shaped polygonal area (approximate area: 4400 m 2) containing typical E. coqui habitat in June 1985. This area was censused nightly for males to determine activity periods and characterize various attributes of calling-site preference. The area was searched systematically and each calling male was captured by hand. Males were individually bagged and a uniquely numbered flag was tied to each individual's perch site. The snout-vent length (SVL) of each frog was measured

to the nearest 0.5 mm, and each frog was weighed with a Pesola spring scale to the nearest 0-1 g, uniquely identified by toe clipping, and then released at the site of capture. We used the residuals of the regression of body mass on SVL as an index of each male's physical condition. Acoustic Measurements We recorded the following information of each male prior to capture: perch locality within the study area, perch type (identification of plant species or structure), perch height (distance between male and the ground, in centimetres), orientation (vertical, horizontal or approximating a 45 ~angle relative to the horizon) and degree of cover (following the scheme of Narins & Hurley 1982). Additionally, a minimum of 25 complete ('co qui') calls were recorded for each male using a cassette recorder (Sony TC-D5M) and a directional shotgun microphone with windscreen ( A K G CE-8, with an SE5E- 10 power module). The microphone was held at perch height, 1 m from and directly in front of the male, such that interference as a result of vegetation was minimized. We measured call intensity (sound pressure level; dB SPL) with a precision sound level meter (GenRad 1982, set to flat weighting and peak response) held at the same orientation and distance as the microphone. Five samples of each of the two call notes were taken with the centre frequency of the octave filter set at 1 kHz for the 'co' note and at 2 kHz for the 'qui' note. Because note frequencies were not exactly 1 and 2 kHz, values of note intensity were corrected by using the octave band filter characteristic of the sound level meter. Average call intensity (re 2 x 10- 5 Pa) was calculated separately for 'co' and 'qui' notes for each male. Because ambient temperature was found to be stable throughout a single night (the maximum observed variation for multiple measurements taken within a night was 0.4~ and because the time spent working with each male was less t h a n 15min, we measured temperature and humidity (Bacharach sling psychrometer) only at the beginning of each census. We determined the degree of intra-populational variance in the male advertisement call as follows: 20 randomly selected calls from each of 113 males, recorded during 1985-1988, were spectrally and temporally analysed using a real-time sonagraph (Kay DSP 5500; sampling rate = 20 480 Hz; degree of frequency resolution=40 Hz). The frequency

Lopez & Narins: Female choice infrogs component of maximum amplitude (hereafter referred to as dominant frequency, measured in Hz) of both call notes was determined. The duration (ms) of each call note, inter-note interval and of the entire call (inter-note interval and both notes) were also measured. Values of dominant frequency reported for each male represent the calculated average of the 20 calls analysed. Additionally, we used calls recorded during 1985 (N=31 males) to investigate the degree of frequency modulation in the 'qui' note. Using a high resolution spectrum analyser (Bruel & Kjaer 2033), the dominant frequency of the first 80 ms and of the last 80 ms of the 'qui' note were determined to the nearest 12.5 Hz.

Field Observations of Male Calling Activity and Mating Success We investigated patterns of male calling activity during July-August 1988. The calling pattern of a focal male ( N = 38) was quantified during a single night, between 2000 and 0030 hours. We acoustically located an isolated calling male (nearest neighbour distance > 1 m) and noted its dorsal colour pattern to facilitate identification and capture at the end of the observation period. We recorded, while sitting 1 m away, the number of complete calls ('co qui') and the number of singlenote calls ('co') produced each minute during a 5min period every 12 min for 4 h or until the male ceased calling. Headlamps producing dim red light were used during all observations; we observed no obvious effect on male calling activity nor did we observe any behavioural changes in response to this light. Temperature and relative humidity as well as male height, orientation and cover were recorded at hourly intervals for each focal male. In addition, we recorded a minimum of 25 complete calls for each male using a cassette recorder (Sony TC-D5M) and a directional shotgun microphone with windscreen (AKG CE-8, with SE5E-10 power module). At the end of the observation period each male was captured, measured for SVL and weighed with a Pesola spring scale. We operationally defined call rate as the number of complete calls a male produced per minute. Average call rate was calculated by taking the ratio of the total number of'co qui' calls counted to the number of l-min observation periods. In cases

759

where courtship was initiated by a female during the observation period, we included data up to the point when the female was first seen in close proximity to the focal male in our calculation of average call rate and in our analysis of call rate patterns. Because the male's acoustic response to contact with females is instantaneous and discrete (call rate increases and call intensity decreases dramatically; personal observation), we feel confident that our data represent the calling effort of each male prior to courtship initiation. We used cumulative sum analysis for each male (N= 38; Woodward & Goldsmith 1964) to determine whether call rate was stable during the observation period, and if not, to determine when changes in rate occurred. Raw data were transformed into cumulative sum values, which were plotted against observation number (time). Visual inspection of this plot allowed us to identify potential 'turning points' in the male's vocal display, defined as points where the slope of the curve changed. Using the original, non-transformed call rate data, we then tested for significant differences between the mean call rate on each side of each turning point (Student's t-test or Mann-Whitney U-test). A 'span' was defined as a period of calling at a rate that was significantly different from the adjacent span(s), and the slope of the cumulative sum plot indicated whether call rate was above (positive slope), below (negative slope), or equal to (slope of zero) the male's long-term average. To assess the possible influence of male size (SVL and mass) on mating success, we carried out diurnal surveys for males incubating one or more clutches ('brooders'). These surveys were concurrent with our nocturnal surveys of males that were vocalizing when located and were presumed to be nonbrooders ('callers'). All accessible potential nesting sites within the study area were carefully examined, including fallen Sierra palm, Prestoea montana, fronds and flower sheaths, curled leaves (primarily of Cecropia peltata), and moss-covered rocks. We limited our searching to sites that were located between ground level and a height of approximately 1 m because the density of nesting material above this height was extremely low. Body mass and SVL were measured for each brooder, and data on nest and clutch characteristics were also recorded. Additionally, we measured SVL and mass for all mated pairs found during the study to investigate the occurrence of size-assortative mating in the study population.

AnimalBehaviour, 41, 5

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Table I. Spectral and temporal specificationsof stimuli used in two-choice preference trials with females of E.

coqui Dominant frequency (Hz) Stimulus type

Co

Qui 1

Qui2

Call rate

Low Standard High

1330 1425 1520

2285 2430 2575

2460 2600 2740

12 21 31

All calls had the following temporal characteristics: 'co' duration=98 ms, 'qui' duration= 124 ms and pause duration = 142 ms. 'qui 1' and 'qui2' refer to the dominant frequency of the first and last 80 ms, respectively,of the 'qui' note.

Female Preference Trials

Two-choice trials of female preference for call dominant frequency and rate were performed at E1 Verde in an arena measuring 2"5 x 2 m. The arena was situated in a sound-absorbing room that we constructed by attaching cardboard egg cartons to all four walls from ground level to a height of 1.5 m. Miniature loudspeakers (10-cm cone diameter, covered with black cloth) were placed on the ground facing each other, each situated 1 m from the centre of the arena. A grid was painted on the floor to facilitate the recording of female movements and positions. We conducted all trials under dim red light at ambient temperature and humidity. Gravid females, which were presumably receptive, were collected in the forest surrounding the study area at E1 Verde and individually housed in small plastic bags for a maximum of 24 h prior to experimentation, We derived the stimuli used in female preference trials from our analysis of vocalizations (10-20 calls from each of 31 males) recorded during 1985. Mean values for each parameter (Table I) were used to construct a 'standard' call produced by an 'average' male in the population (Fig. ld-f). Stimuli of'high' (above average) or 'low' (below average) calls were based on the observed maxima and minima of call dominant frequency and rate for the study population. Therefore, these stimuli are made up of calls with spectral qualities that are representative of the natural variation found in the study population during 1985. Note duration was held constant for all stimulus types and equalled that of a 'standard' call.

Stimulus tapes were generated with a portable animal sound synthesizer (Narins & Capranica 1978) that was calibrated with a high resolution spectrum analyser (Bruel & Kjaer 2033). All stimuli were recorded on to low noise tapes (Scotch 208), using a Uher 4200 Report Stereo IC tape recorder (tape speed = 19 cm/s). Stimuli were delivered with two Uher 4200 tape recorders. We equalized the signal output from each speaker by measuring stimulus intensity with a precision sound level metre (GenRad 1982) placed on the floor, directly in front of each speaker at a distance of 1 m. Field measures of average call intensity ( N = 60 males) were used to determine 'standard' speaker output levels ( ' c o ' = 6 7 d B SPL, s2= 12.5; ' q u i ' = 8 5 dB SPL, s 2 = 8.9). In all trials one speaker broadcast a series of 'standard' calls and the other broadcast calls that were of either 'high' or 'low' dominant frequency or rate, with calls from each speaker alternating. In frequency preference trials, the stimulus pairs delivered were either standard versus low dominant frequency or standard versus high dominant frequency (with call rate held constant at the standard rate of 21 calls/min). Similarly, in rate preference trials, the stimulus pairs were either standard versus low rate or standard versus high rate (with dominant frequency held constant at the standard values observed for each note). We randomized speaker output with respect to stimulus type to control for any bias towards either side of the choice arena. All trials were performed between 1900 and 0430 hours, the active period ofE. coqui. Prior to experimentation we thoroughly dampened the floor of the arena with water and measured the ambient temperature and relative humidity of the room. Each female, still in a plastic bag, was placed in the arena for a 15-min acclimation period prior to a trial. During this time the female was exposed to ambient light conditions and the acoustic stimuli. The female was then removed from the plastic bag and placed on the floor at the centre of the arena, equidistant from the two speakers and oriented towards the back wall so that she was facing neither speaker. We then observed the female for 15 min while she was exposed to the stimuli. Each movement of the female was recorded, including time, position within the arena and orientation. We defined a preference as entry into a circle of radius 26.5cm (5% of the total area of the arena) surrounding either speaker. Each female was tested only once, and following experimentation females

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Figure 2. Frequency distribution of SVL for a population ofE. coqui (N= 113 males, El; 161 females, Ill) at E1 Verde, Puerto Rico (altitude: 350 m). were measured for SVL and egg diameter, weighed, toe-clipped and either released at the site of capture or housed in aquaria for use in another study.

RESULTS

Size Relationships A significant sexual dimorphism in size occurred for both SVL ( t = - 3 0 - 6 8 , df=250, P<0.001; Fig. 2) and mass ( t = -26.55, df= 208, P<0.001). Females were longer and weighed more than males; SVL ranged from 37.0 to 55-0 mm (.~+ s~ = 44.7+0.3, N = 161) and mass ranged from 3-3 to 8-9 g O(___sE= 5.3_+0.1, N - - 161). Male SVL ranged from 32'0 to 39.5mm (.~_+SE=35'5+0'2, N = 113) and ranged in mass from 2-1 to 4.0g (.~+SE=2"8_0"03, N = l I 3 ) . Snout-vent length was found to explain a significant proportion of the variance in mass ( Y = -3"84+0.19X, r2=0.67, F=227.21, d f = l , l l l , P<0.001). The degree of variation in male condition (.~_+SE= -- 0.0001_+ 0-0945, N = 113) was less than that for SVL and greater than that for mass.

Call Dominant Frequency and Duration Intra-populational variation Significant differences were found between years for temperature (ANOVA, F=4.91, dr=3,112,

P<0-005) and relative humidity (ANOVA, F = 30.76, df=3,112, P<0.001). However, call note dominant frequency and duration were not significantly associated with temperature or humidity within years (Spearman rank correlations, all P > 0.05). Therefore, we analysed recordings made over the 4-year study as a single data set. We found a considerable amount of intrapopulational variation in the spectral and temporal composition of both call notes (Table II), although note duration tended to be less variable than note dominant frequency, Note dominant frequency and duration as well as call ('co' +interval + ' q u i ' ) duration were normally distributed (Fig. 3). Coefficients of variation among males for note duration were approximately twice those for note dominant frequency ('co' duration=7.07%, 'co' dominant frequency=4.02%; 'qui' duration--8.46%, 'qui' dominant frequency---3.87%). Based on the distributions of spectral and temporal call parameters, it c~,n be predicted that a female would most often encounter males producing average calls.

Male size, condition and call dominant frequency Male SVL and mass were significantly associated with both spectral characteristics ('co' and 'qui' dominant frequency) measured in this study (Pearson product-moment correlations, all P<0.05). Simple linear regression analyses were performed to investigate the observed variance in

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Table II. Summary of spectral and temporal features of E. coqui vocalizations recorded during 1985-1988 Parameter

-~

SE

Range

'Co' dominant frequency (Hz) 'Qui' dominant frequency (Hz) Pause duration (ms) 'Co' duration (ms) 'Qui' duration (ms) 'Co' qui duration (ms)

1468.6 2254.5 137.1 94.7 129.9 361.8

5.6 8.2 1-5 0.6 1.0 1.9

1326-0-1610.0 2027-0-2464-0 96.3 193.0 78. I-114.7 91.8 166.2 312.4~412-1

Twenty complete 'co qui' calls were analysed for each of 113 males (N = 2260 calls). call frequency as a function of male size. Male SVL and mass explained a significant proportion of the variance in spectral parameters (Table III). In both cases, the coefficients of determination (r z) were quite low, indicating that male size explains a significant, albeit small amount of the variance in spectral features of the advertisement call of E. coqui. The regression equations indicated that the dominant frequency of the 'co' and 'qui' notes changed by 17 and 29 Hz, respectively, for each l m m change in SVL and by 77 and 132Hz, respectively, for each 1 g change in body mass. Male condition was significantly associated with 'qui' dominant frequency (Pearson productmoment correlation = - 0.22, N = 113, P < 0-05), but not with 'co' dominant frequency (Pearson product-moment correlation= - 0 . 1 6 , N = 113, NS). A significant, although very small, amount of the variance in 'qui' dominant frequency was explained by male condition (Table III).

Female preference for callfrequency Females responded in 37% of the frequency preference trials, while in the remaining trials the females moved throughout the arena in a seemingly random fashion or never moved from the centre of the arena. When a distinct preference was shown, females typically oriented quickly to and made direct hops towards the speaker of preference, often ending their movement on top of the speaker. Females did not show a preference for either the 'low' or the 'high' frequency calls over the 'standard' call ( N = 32 trials, ;~z= 1.13, df= 1, NS; N = 19 trials, z a = 0"47, df=l, Ns, respectively). In addition, we observed no significant association between female SVL or mass and preference for 'high', 'low' or 'standard' calls (Pearson product-moment or Spearman rank correlations, all P > 0-05).

Male mating success Six observations of courtship initiation were made in the field in 1988. These 'mated' males ( N = 6 ) were not significantly different from 'unmated' males ( N = 43) studied during the same year with respect to SVL, mass, perch quality and orientation, or spectral qualities of the advertisement call (Student's t-tests, all P > 0.05). Additionally, male status ('mated' or 'unmated') was not significantly associated with any spectral quality of the advertisement call or with any call site characteristic (Spearman rank correlations, all P>0"05). Snout-vent length and mass of the male and female in mated pairs (N=29) were not significantly correlated (Pearson product-moment correlations, all P > 0-05); therefore, there was no evidence for size-assortative mating in this population of E. coqui. The female was longer and weighed more than the male in all pairs. Because we found significant differences in mean male SVL and mass for brooders and callers between years (one-way ANOVA, all P < 0-05), we analysed the incidence of size-dependent mating success separately for each year. There was no significant difference in SVL or mass between brooders and callers during each year of this study (Mann-Whitney U-test, all P > 0-05, N = 109 brooders during 1985-1988, N = 113 callers during 1985-1988; Fig. 4). Therefore, male mating success appears to be size-independent in this population of

E. coqui. Call Rate

Intra-populational var&tion There were significant differences in temperature (ANOVA, F=7.83, df=25,169, P<0-001) and

Animal Behaviour, 41, 5

764

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'1

0-2000

505

2[50 2500 Quidominonffrequency(Hz)

525

5'#5

565

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Figure 3. Distribution of (a) 'co' and (b) 'qui' dominant frequencyand (c) 'co qui' duration for a population of E. coqui (N= 113 males) at El Verde, Puerto Rico.

relative humidity (ANOVA, F = 6.26, df= 25,169, P<0-001), both measured at the location of each focal male, between the 26 days of this study.

However, there was no significant association between call rate and temperature (Pearson product-moment correlations, all P>0-05) or

Lopez & Narins: Female choice in frogs

765

Table III. Regression equations and r 2 values of the relationship between call note dominant frequencyversus SVL, mass and condition for males ofE. coqui 'Qui' dominant frequency

'Co' dominant frequency Equation

SVL Mass Condition

P

r2

Y=2091- 17.5X 0 . 2 4 Y= 1686-76.9X 0 . 2 4 Y= 1469-9.2X 0.03

Equation

<0.001 <0.001 >0.05

relative humidity (Spearman rank correlations, all P > 0-05). Therefore, call rate data were compared between nights. Average 'co qui' rate for the population in 1988 was 14.8 calls/min (N=38 males, range: 5-6--22-6 calls/min; Fig. 5). Male SVL, mass and condition were not significantly associated with call rate (Pearson product-moment correlations, all P > 0'05). The coefficient of variation for call rate (30.26%) was much higher than that observed for call note dominant frequency or duration.

Patterns of calling All males called at their maximum rate before 2300 hours (Fig. 6). The distribution of time of peak calling effort, defined as the maximum number of calls produced per minute, was significantlyskewed toward the early night when compared to a normal distribution (Z2 = 1018.5, df= 8, P < 0.001). None of the 38 males maintained a constant call rate during the night. In general, significant changes in call rate occurred from one to five times within a night (Fig. 7). Twenty-two (58%) males consistently called at a rate above or equal to their average rate before or at 2300 hours (as in Fig. 7a,c). We observed a gradual increase or decrease in call rate with one significant change in rate in 40% (N= 15) of the focal males (Fig. 7a,b). Ten males (26%) reached a stable period of calling at their average rate, with two significant changes in rate during the night (Fig. 7c,d). Two to five changes in call rate, with spans alternating between below and above average rate, were observed in the remaining 13 males (34%; Fig. 7e,f). Female preference for call rate Females met our criterion for making a distinct choice for call rate in 33% of the trials. Among these trials, females showed a strong preference for

rz

Y= 3278-28.8X 0 . 2 9 Y=2627-132X 0.32 Y=2254-- 18.7X 0 . 0 5

P <0-001 <0.001 <0.05

calls of relatively higher repetition rate (standard rate versus low rate: N = 11 trials, Zz = 7.36, df= 1, P<0-01; standard rate versus high rate: N = 1 8 trials, Z2 =,5-56, df= 1, P<0"025).

Male mating success The average call rate of mated males (N= 6, X__ SE= 19.4_+ 1-6) was significantly different from that of unmated males (N= 32, .~+ sE --- 13.9 + 0.7; Mann-Whitney U=562.0, P<0.025). Additionally, five of the six mated males called at an average rate that was greater than the overall populational average (Fig. 5). Based on our cumulative sum analysis, only three of the mated males had spans of calling at a rate less than average for the population or for unmated males, and the proportion of spans during which call rate was less than the male's overall average was not significantly different between mated and unmated males (Mann-Whitney U = 101, P>0'05). Additionally, mated and unmated males were not significantly different with respect to the proportion of time spent calling at a rate less than, greater than, or equal to their overall average (Mann-Whitney U-test, all P > 0'05). Mated males differed from unmated males in the rate of'co qui' calls plus 'co' notes produced (mated . ~ + s ~ = 2 1 . 5 + 1.9; unmated X+SE= 15-4--+0-7; Mann-Whitney U=561.0, P<0.025). However, mated and unmated males did not differ in the proportion of single 'co' notes produced ( M a n n Whitney U = 121, P > 0.05). Average SVL and mass of mated and unmated males were not significantly different (Mann-Whitney U-test, all P > 0.05). Comparison of call rates of both mated and unmated males within each of the six nights on which matings were observed (Table IV) allowed us to examine the effects of call rate on mating success within a single night for two males that were located within l0 m of each other. In five of the pairs, the

766

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mean call rate of the mated male was greater than that of the unmated male, although this difference was not statistically significant (two-tailed sign test,

P>0.05). However, a male's mating success was significantly associated with having the higher call rate of the two males (Fisher exact test, P < 0.001).

Loper & Narins: Female choice infrogs

767

4,

II

5

14

Average coil

[7

20

,I, 23

rate (calls/rain)

Figure 5. Average call rate (number of complete 'co qui' calls produced per minute) for six mated ([]) and 32 unmated ( 9 males of E. coqui. The populationat average call rate is indicated by the arrow.

14

IO L

o 2000

_ I l l 2 I00

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2300

1 0000

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Figure 6. Distribution of the first incidenceof peak calling effort (maximum number of calls produced per minute) for males of E. coqui (N= 38) monitored between 2000 and 0030 hours. DISCUSSION

Call Dominant Frequency In this population of E. coqui, variation in male mating success is probably not manifested through female choice for call note dominant frequency. Laboratory preference trials clearly indicate that females do not discriminate between males on the basis of this call parameter, and we observed no large-male mating advantage in our examination of body size and mating success in the field. Although

there does exist a considerable degree of variation in call dominant frequency, the correlation between male SVL (and physical condition) and 'qui' dominant frequency in particular is quite poor. This indicates that a female must be acoustically exposed to males of very different size to detect any size discrepancy. Given the distributions of male size and call frequency (most males produced calls of average 'co' and 'qui' dominant frequency) and the spatial arrangement of calling males in the study area (average nearest-neighbour distance

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770

Table IV. Average call rate (calls/min) for six pairs of males of E. coqui in which a female initiated courtship with one ('mated male') of the two focal males Date

Mated male

Unmated male

17.7.1988 26.7.1988 1.8.1988 5.8.1988 15.8.1988 16.8.1988

21.9 22.7 21.5 21.4 13.6 15.5

18.9 19.1 12.8 15.9 15.2 7.4

between calling males is greater than 1 m, personal observation), the probability of encountering such sparsely distributed males should approach zero. Two-choice trials, most often performed in a laboratory, have been extensively used to demonstrate the intraspeeific frequency preference behaviour of female frogs. Doherty & Gerhardt (1984) and Forester & Harrison (1987) independently showed that females of Pseudacris crueifer prefer calls of the mid-frequency range representative of their study population. A low frequency preference was found for P. pustulosus (Ryan 1980, 1983), Uperolia laevigata (Robertson 1990), and Hyla chrysoscelis (Morris & Yoon 1989). In contrast, females of Hyla cinerea and Hyla gratiosa have been shown to prefer average call frequencies over either low or high frequencies (Gerhardt 1981, 1982), and females of Bufo calamita (Arak 1988), Pseudacris triseriata (Martof & Thompson 1964), and E. coqui (this study), show no frequency discrimination in laboratory trials. Therefore, it appears that across anuran species, frequency discrimination, particularly for low call frequency and large male body size, is not the rule. Although there is no strong theoretical framework for the generally accepted prediction that females should prefer to mate with large males, explanations for the inconsistency of this preference among anuran species are of interest. Prior to physical contact, assessment of males by females is limited to an analysis of the advertisement call, which may or may not provide accurate, reliable information on male size. For example, Sullivan (1982) found a high degree of temperatureindependent, between-night variation in call dominant frequency within individual males of Bufo woodhousei australis. In other species, ambient temperature has been shown to influence female frequency preference (Gerhardt & Mudry

1980; Gerhardt 1982; Arak 1988) and/or male call production (Robertson 1986; Wells & Taigen 1986). Therefore, body temperature may be an important physiological constraint on the ability of females to make reliable mate choice decisions based on call frequency. Very little is known about variation between females in frequency sensitivity, i.e. the sensory basis of female choice for call attributes. Female frequency preference in the laboratory may be influenced by the oversimplified nature of the acoustic environment (Gerhardt 1987; Dyson & Passmore 1988) as in this study, where the calls of males with two very disparate note dominant frequencies were presented as the choices. Moreover, the observations that female frequency preference may not be intensity-independent (e.g. Doherty & Gerhardt 1984) and that frequency selectivity decreases with stimulus complexky (Gerhardt 1982, 1987) suggest that frequency preference may not necessarily play a significant role in mate choice in all anurans. Call Rate

Both laboratory two-choice trials and observations of courtship initiation in the field provide strong evidence in support of female preference for calls of relatively high rate in this population of E. coqui. This preference is reflected in the increased mating success of those males calling at a relatively faster rate; the average call rate of 'mated' males was significantly greater than that of 'unmated' males in our study area. Similar results have been reported for B. woodhousei, in which males calling at a higher rate enjoy a higher mating success (Sullivan 1983). A corollary to call rate is how calling effort is distributed during a night. Although call rate was unstable within a night for each male examined, all males reached their peak calling effort prior to 2300 hours. Interestingly, the distribution of peak calling effort qualitatively matched the distribution of the availability of females within a night as predicted by Woolbright (1985). He predicted that unmated, receptive females occur at highest density early in the night, before 2300 hours and decrease in availability throughout the night. Moreover, five of the six instances of courtship initiation that we observed occurred prior to 2130 hours. Therefore, calling at a high rate relative to other males, early in the night, may enhance a male's mating opportunities.

Lopez & Narins: Female choice in frogs In contrast to the varied nature of female preference for call frequency, laboratory studies indicate a strong, global preference for calls of high rate (see review by Gerhardt 1988). This is particularly interesting in species such as E. coqui, in which call rate is not significantly associated with male SVL, mass, or physical condition. Therefore, the significance of the association between call rate and male mating success is unclear. Potential benefits that may be accrued by females including mating with a male of better than average quality, regardless of whether the mechanism of choice is passive or active (Parker 1983). Morris (1989) has shown that female preference for male size in H. chrysoscelis may not be the only determinant of male mating success on a seasonal basis. This finding suggests that interpretations of female choice and male reproductive behaviour may be biased by the scale (nightly versus seasonal, or short-term versus long-term) at which they are examined. In E. coqui, if calling effort for individual males is similar between nights and females limit their sampling to small, local subgroups of males, then our short-term analysis of calling behaviour and mating success may provide a reasonable assessment ofintersexual selection pressures. However, long-term observations of both behaviour patterns are preferable.

ACKNOWLEDGMENTS Many thanks to R. Gibson, M. Greenfield, H. C. Gerhardt and an anonymous referee for their invaluable comments and suggestions on the manuscript. F o r excellent field assistance we thank E. Alkaslassy, J. Howland, L. R. Wolfenbarger and N. Simmons. A. Estrada-Pinto provided unselfish help and companionship during the field work, and R. Waide of the Center for Energy and Environmental Research in San Juan, Puerto Rico, allowed us to use the facilities at the El Verde field station. Field work was supported by the Organismic Biology F u n d (Department o f Biology, U C L A ) and a Research Grant from the Graduate Division ( U C L A ) to P.T.L., and N I H grant NS19725 to P.M.N. Financial support during analysis and manuscript preparation was provided by a University Fellowship from the Department of Biology ( U C L A ) and a U C L A Dissertation Year Fellowship to P.T.L.

771

REFERENCES Arak, A. 1988. Female mate selection in the natterjack toad: active choice or passive attraction? Behav. Ecol. Sociobiol., 22, 317 32% Doherty, J. A. & Gerhardt, H. C. i984. Evolutionary and neurobiological implications of selective phonotaxis in the spring peeper (Hyla crucifer). AnOn. Behav., 32, 875-881. Drewry, G. E. 1970. The role of amphibians in the ecology of the Puerto Rican rain forest. In: Puerto Rico Nuclear Center Rain Forest Project Annual Report (Ed. by R. G. Clements, G. E. Drewry & R. J. Lavigne), pp. 16~3. San Juan: Puerto Rico Nuclear Center. Dyson, M. L. & Passmore, N. I. 1988. Two-choice phonotaxis in Hyperolius marmoratus(Anura: Hyperoliidae): the effect of temporal variation in presented stimuli. Anim. Behav., 36, 648~652. Fisher, R. A. 1930. The Genetical Theory of Natural Selection. Cambridge: Oxford University Press. Forester, D. C. & Harrison, W. K. 1987. The significance of antiphonal vocalisation by the spring peeper, Pseudacris crucifer (Amphiba, Anura). Behaviour, 103, 1-15. Gerhardt, H. C. 1978. Temperature coupling in the vocal communication system of the gray treefrog Hyla versicolor. Science, 199, 99~994. Gerhardt, H. C. 1981. Mating call recognition in the barking treefrog (Hyla gratiosa): responses to synthetic calls and comparisons with the green treefrog (Hyla cinerea). J. comp. Physiol., 144, 17--25. Gerhardt, H. C. 1982. Sound pattern recognition in some North American treefrogs (Anura, Hylidae): implications for mate choice. Am. Zool., 22, 581-595. Gerhardt, H. C. 1987. Evolutionary and neurobiological implications of selective phonotaxis in the green treefrog, Hyla cinerea. Anon. Behav., 35, 1479-1489. Gerhardt, H. C. 1988. Acoustic properties used in call recognition by frogs and toads. In: The Evolution of the Amphibian Auditory System (Ed. by B. Fritszch, W. Wilczynski, M. Ryan, T. Hetherington & W. Walkowiak), pp. 455-483. New York: John Wiley. Gerhardt, H. C. & Mudry, K. M. 1980. Temperature effects on frequency preferences and mating call frequencies in the green treefrog Hyla cinerea (Anura: Hylidae). J. comp. Physiol., 137, 1-6. Given, M. F. 1988. Growth rate and the cost of calling activity in male carpenter frogs, Rana virgatipes. Behav. Ecol. Sociobiol., 22, 153-160. Hamilton, W. D. & Zuk, M. 1982. Heritable true fitness and bright birds: a role for parasites? Science, 218, 384-387. Klump, G. M. & Gerhardt, H. C. 1987. Use of nonarbitrary criteria in mate choice by female gray treefrogs. Nature, Lond., 326, 286-288. Martof, B. S. & Thompson, E. F., Jr 1964. A behavioural analysis of the mating call of the chorus frog, Pseudacris triseriata. Am. Midl. Nat., 71, 199-209. Morris, M. R. 1989. Female choice of large males in the treefrog Hyla chrysoscelis: the importance of identifying the scale of choice. Behav. Ecol. Sociobiol., 25, 275-281.

772

Animal Behaviour, 41, 5

Morris, M. R. & Yoon, S. L. 1989. A mechanism for female choice of large males in the tree frog Hyla chrysoscelis. Behav. EcoL Sociobiol., 25, 65-71. Narins, P. M. & Capranica, R. R. 1976. Sexual differences in the auditory system of the treefrog Eleutherodactylus coqui. Science, 192, 378-380. Narins, P. M. & Capranica, R. R. 1978. Communicative significance of the two-note call of the treefrog Eleutherodactylus coqui. J. comp. Physiol., 127, 1-9. Narins, P. M. & Capranica, R. R. 1980. Neural adaptations for processing the two-note call of the Puerto Rican treefrog, Eleutherodactylus coqui. Brain Behav. Evol., 17, 48~56. Narins, P. M. & Hurley, D. D. 1982. The relationship between call intensity and function in the Puerto Rican coqui (Anura: Leptodactylidae). Herpetologica, 38, 287-295. Narins, P. M. & Smith, S. L. 1986. Clinical variation in anuran advertisement calls: basis for acoustic isolation? Behav. Ecol. Sociobiol., 19, 135-141. Parker, G. A. 1983. Mate quality and mating decisions. In: Mate Choice (Ed. by P. Bateson), pp. 141-166. Cambridge: Cambridge University Press. Prestwich, K. N., Brugger, K. E. & Topping, M. 1989. Energy and communication in three species of hylid frogs: power input, power output and efficiency. J. exp. Biol., 144, 53-80. Robertson, J. G. M. 1986. Female choice, male strategies and the role of vocalizations in the Australian frog Uperolia rugosa. Anita. Behav., 34, 773-784. Robertson, J. G. M. 1990. Female choice increases fertilization success in the Australian frog, Uperolia laevigata. Anita. Behav., 39, 639-645. Ryan, M. J. 1980. Female mate choice in a neotropical frog. Science, 209, 523-525. Ryan, M. J. 1983. Sexual selection and communication in a neotropical frog, Physalaemus pustulosus. Evolution, 37, 261-272.

Simon, M. P. 1983. The ecology of parental care in a terrestrial breeding frog from New Guinea. Behav. Ecol. Sociobiol., 14, 61~57. Sullivan, B. K. 1982. Significance of size, temperature and call attributes to sexual selection in Bufo woodhousei australis. J. Herpetol., 16, 103-106. Sullivan, B. K. 1983. Sexual selection in Woodhouse's toad (Bufo woodhousei). II. Female choice. Anita. Behav., 31, 1011-1017. Taigen, T. L. & Wells, K. D. 1985. Energetics of vocalization by an anuran amphibian (Hyla versicolor). J. comp. Physiol., 155, 163-170. Townsend, D. S. 1986. The costs of male parental care and its evolution in a neotropical frog. Behav. Ecol. Sociobiol., 19, 187-195. Townsend, D. S., Stewart, M. M., Pough, F. H. & Brussard, P. F. 1981. Internal fertilization in an oviparous frog. Science, 212, 469~471. Townsend, D. S., Stewart, M. M. & Pough, F. H. 1984. Male parental care and its adaptive significance in a neotropical frog. Anita. Behav., 32, 421~3 I. Wells, K. D. & Taigen, T. L. 1986. The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor). Behav. Ecol. Sociobiol., 19, 9 18. Woodward, B. D., Travis, J. & Mitchell, S. 1988. The effects of the mating system in progeny performance in Hyla crucifer (Anura: Hylidae). Evolution, 42, 784-794. Woodward, R. H. & Goldsmith, P. L. 1964. Cumulative Sum Tests: Theory and Practice. Edinburgh: Oliver & Boyd. Woolbright, L. L. 1985. Patterns of nocturnal movement and calling by the tropical frog Eleutherodactylus coqui. Herpetologica, 41, 1-9. Woolbright, L. L. & Stewart, M. M. 1987. Foraging success of the tropical frog, Eleutherodactylus coqui: the cost of calling. Copeia, 1987, 69-75. Zahavi, A. 1975. Mate selection: a selection for a handicap. J. theor. Biol., 53, 205 214.