Naturwissenschaften (2001) 88:434–437 DOI 10.1007/s001140100261
S H O R T C O M M U N I C AT I O N
Jaime Bosch
Female reciprocal calling in the Iberian midwife toad (Alytes cisternasii) varies with male call rate and dominant frequency: implications for sexual selection Received: 4 February 2001 / Accepted in revised form: 1 August 2001 / Published online: 30 August 2001 © Springer-Verlag 2001
Abstract Male midwife toads (Alytes cisternasii) responded differently depending on the call frequency and call rate of other males. I tested female Iberian midwife toads with the same set of stimuli used earlier with males. Females responded faster to high call rates, and female vocal activity was greater in response to low-frequency male calls. Thus, in both sexes, the vocal response differs in the same direction according to signal frequency variation, but the magnitude of the response is greater in males than in females. In the light of these results, I discuss the implications for sexual selection of this reciprocal calling.
Introduction Since Darwin, the processes of sexual selection have been classified into two categories: intrasexual selection and intersexual selection. To date most studies of intrasexual selection have focused on male–male competition, and those on intersexual selection have emphasized female choice. Theoretically, parental effort or investment is thought to be a key variable controlling the operation of sexual selection via effects on rate of reproduction (Trivers 1972). Competition for mates usually characterizes the sex which makes the lesser investment and choice characterizes the sex with the greater investment (Trivers 1972). In situations where females provide parental care, breeding systems are usually characterized by male– male competition and female choice. However, there are several species of birds, amphibians, and fish where only males provide parental care (Andersson 1994). It is in these species where male choice and competition among females might be expected. In fact, competition among females has been described in some fish and in many polyandrous birds (see for example Gwynne 1991), and J. Bosch (✉) Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain e-mail:
[email protected]
male choice has been demonstrated in a variety of species, predominantly ectotherms (see references in Bush et al. 1996). The Iberian midwife toad, Alytes cisternasii, like all species within the genus, has a remarkable reproductive strategy in which males carry the eggs twined around their hind legs on land from fertilization to hatching. Although the precise energetic investment in reproduction by both sexes is not known, paternal investment must be substantial (Márquez and Bosch 2001). Also, since there is an upper limit to the number of female clutches that a male can carry at one time, male parental care may be a limited resource under conditions of a female-biased sex ratio. In anurans, vocalization plays a major role in sexual selection, and only males call in the great majority of species (but see Emerson and Boyd 1999). It is not surprising, therefore, that experimental work has confirmed that male Alytes produce calls that function in both male–male competition and attraction of females (Bosch and Márquez 1996). What is interesting and unusual is that female Alytes also call during courtship (Márquez and Verrell 1991; Bush and Bell 1997). Both close-range exchanges of vocalizations among breeding females and between breeding females and breeding males have been reported (Márquez and Verrell 1991; Bush and Bell 1997). In addition, competition among females for mates, through physical fighting, has been found in captive A. obstetricans (Verrell and Brown 1993). An open question is whether female vocalizations are limited to improving female location and/or informing the males about female receptivity, or conversely, whether female calls are also involved in (or are part of) female–female competition and/or male choice. To begin to address this question, the first step is to analyze whether there is some degree of variation in female vocal response, and if this variation is related to certain male traits. Therefore, since some measurable degree of variation has been found in A. cisternasii female calls (Bosch and Márquez 2001), in this paper I examine whether female vocal response varies according to vari-
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ous male bioacoustic characteristics. In addition, I study whether the female vocal response is the same as the male response to variation in male calls.
Methods Gravid females of A. cisternasii (with mature eggs visible through the lower part of the abdomen) were collected at the beginning of the reproductive period in a live oak forest, or ‘‘dehesa’’, near the city of Mérida (Extremadura, west central Spain, 38°59′N, 31°24′W). Of 30 females collected, I selected 12 that responded positively to pilot playback experiments. I used the same four different series of stimuli that had been used in previous work to test male responses to neighbor size (via call frequency) and calling rate (Bosch and Márquez 1996). However, the synthetic calls were resynthesized at a sampling rate of 44.1 kHz and 16-bit resolution with SoundMaker 1.0.4 software. The synthetic call duration (170 ms) was the average for the population studied (Márquez and Bosch 1995). The dominant frequencies and call repetition rates used were within ±1.5 SD of the population mean (i.e., always within the population range). The four different series were: HS (High frequency, Slow rate: 1,618 Hz, 11.4 calls/min), HF (High frequency, Fast rate: 1,618 Hz, 42.3 calls/min), LS (Low frequency, Slow rate: 1,364 Hz, 11.4 calls/min) and LF (Low frequency, Fast rate: 1,364 Hz, 42.3 calls/min). One speaker was placed 90 cm away from the release point, behind a wall of an indoor square arena (1.8×1.8 m) under very low intensity light. The walls of the arena were formed by thin black cloth hanging down from a semi-rigid frame. The speaker emitted the series of synthetic stimuli directly from an Apple PowerBook G3 in random order. Sound level of the synthetic calls was adjusted to 70 dB at the release point (a value found in nature for males calling at 70 cm) with a digital Realistic Sound Pressure Meter (fast response, A weighting). A Sennheiser ME 66 directional microphone was placed close to the speaker approached by the female. Temperature in the arena ranged from 17.2 to 19.7°C. Each female was tested once in each of the four experiments presented in random order. A female was placed under a cylinder of plastic mesh at the release point for 30 s while the stimuli were emitted. The cylinder was then lifted and the movements of the female were monitored. Female calls were recorded with a Sony WM D6 tape recorder until the female approached within 10 cm Fig. 1 Mean values (± SE) for approach time (a), call duration (b), dominant frequency (c) and call repetition rate (d) of female responses during the four playback experiments. HS High frequency–Slow rate experiment, HF High frequency–Fast rate experiment, LS Low frequency–Slow rate experiment, LF Low frequency–Fast rate experiment
of the base of the speaker, no matter how long it took, or for 3 min if the female touched the speaker sooner. For every trial, the approach time (this is, the time from when the cylinder was lifted to when the female touched the speaker) was noted. The last 3 min of every recording was digitized at a sampling rate of 44.1 kHz and 16-bit resolution with Canary 1.2 software and an Apple PowerBook G3 computer. Signalyze 3.12 software was used to obtain several call characteristics: call duration, initial dominant frequency (through fast Fourier transforms, width 1,024 points) and call repetition rate. After testing for normality, the results of the playback tests were analyzed using two-way ANOVAs for repeated measurements with Statistica 5 software. In order to compare the magnitude of the response (calling activity) between the sexes, I used the results from previous experiments using the same stimuli conducted with males from the same population (Bosch and Márquez 1996). I compared intercall interval between the sexes because it was the only call characteristic that showed significant variation among males in the previous tests. For females, I defined intercall interval as the internote interval. This was done because female vocal responses were sometimes arranged as a series of notes but with more than one note in a call. However, in 75% of the cases female responses to stimuli were composed of a single note (Bosch and Márquez 2001). In this case, a three-way ANOVA with sex, frequency, and repetition rate as main factors was used.
Results Mean values (± SE) for approach time, call duration, dominant frequency and call repetition rate of female responses to the four different male stimuli are shown in Fig. 1. Male call rate had a statistically significant effect on female approach time (F1,11=22.7, P=0.0006) but frequency did not (F1,11=0.1, P=0.7136). That is, females took less time to approach when male calling rate was higher. However, females did not approach faster when male calls were of low frequency. Female call repetition rate was greater in response to lower frequency calls of males (F1,11=17.7, P=0.0015) but not in response to faster male repetition rates
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Fig. 2 Internote interval for males (white circles) and females (black circles) during the four playback experiments (mean ± SE). HS High frequency–Slow rate experiment, HF High frequency–Fast rate experiment, LS Low frequency–Slow rate experiment, LF Low frequency–Fast rate experiment
(F1,11=0.1, P=0.7304). That is, the repetition rate of female vocalizations was faster in response to low-frequency male calls as compared to higher frequency. Neither the duration nor dominant frequency of female reciprocal calls differed among the four different playback tests (P>0.1223 in all cases). Significant differences between sexes in vocal responses were obtained (F1,25=26.2, P
