Behavioral Ecology Vol. 13 No. 2: 149-153
© 2002 International Society for Behavioral Ecology
Female preference function related to precedence effect in an amphibian anuran (Alytes cisternasii): tests with non-overlapping calls
a Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain b Centro de Biologia Ambiental, Faculdade de Ciências, Universidade de Lisboa, Bloco C2, Campo Grande, P-1700 Lisboa, Portugal
Address correspondence to J. Bosch. E-mail: bosch{at}mncn.csic.es .
Received 29 November 2000; revised 23 March 2001; accepted 23 March 2001.
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ABSTRACT |
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We quantified precedence effect (measured as female preference for the leading calls in an acoustic interaction between two males) with non-overlapping, simulated male calls presented with various phase relationships to female Iberian midwife toads (Alytes cisternasii) in two-speaker phonotaxis playback tests. The resulting information determines the shape of the female preference function for intercall delays. Females preferentially approached leading callers for most tested phase angles. We found a gradation in the degree to which females selected the leader. They tended to exert a strong preference for the leader in 30° test, and at higher phase angles, the overall preference was weaker and graded (the higher the phase angle, the lower the preference). Other parameters of female preference (latency and repeatability) also had a graded relationship with phase angle value. The sharp difference in probability of approach between 30° and 60° is consistent with a mechanism of male calling inhibition immediately after hearing a competitor's call previously described in other taxa. In natural interactions, male A. cisternasii adjust the timing of their calls to a phase angle that provides a slight but significant advantage to the leading caller.
Key words: Alytes cisternasii, anurans, calling, female preference, midwife toads, precedence effect.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The precedence effect has been defined as the phenomenon that "when two binaural sounds are presented with a brief delay between them, and are perceived as a single auditory event, the localization of that event is determined largely by the directional cues carried by the earlier sound" (Zurek, 1987
: 85). The
precedence effect has also been used to describe female preference for leading
calls in multimale interactions in species with acoustic or visual signals for
sexual advertisement (Backwell et al.,
1998; Vencl and Carlson,
1998; Wallach et al.,
1949; Wyttenbach and Hoy,
1993; Zurek,
1980). It has even been proposed that this perceptual bias or the
resulting difference in attractiveness to females may result in the
synchronization of calls between neighboring males
(Greenfield et al., 1997).
In insects and amphibians, a preference for the leading call has been
observed when the calls of competing males overlap in time (i.e., when masking
between the two signals occurs; see review in
Klump and Gerhardt, 1992, also
Greenfield and Rand, 2000).
This effect may result from the relative importance of the initial transient
(raise time) in localization, and the fact that the initial transient of the
second signal is masked by the leading signal
(Zurek, 1987). However,
precedence effect in the absence of masking between the signals has also been
described for very short sounds in humans (see review in
Zurek, 1987) and in insects
(Minckley and Greenfield,
1995; Snedden and Greenfield,
1998). To date, only Minckley and Greenfield
(1995) have explored the
changes in strength of female preference with several call delays between
males in a study of the acridic orthopteran Ligurotettix planum. The
authors showed that only males emitting calls immediately following another
male's calls would be discriminated against by females, the effect being
nonsignificant for males responding with longer delays. This result pointed
toward the determination of the length of the delay that would trigger this
female preference for leaders and the associated strategies that males had to
follow to avoid this critical delay affecting the mechanisms regulating call
timing.
Among amphibians it is more difficult to find examples of studies of
mechanisms regulating call timing that include the study of the effect of call
exchanges without call overlap (but see Dyson and Passmore,
1988a,b;
Grafe, 1996,
1999;
Narins, 1982;
Zelick and Narins, 1983), and
there are even fewer examples of studies of non-overlapping acoustic
interactions between males with different phase angle relationships
(Bosch and Márquez,
2001a). We studied female preference in relation to the precedence
effect in the Iberian midwife toad Alytes cisternasii,
(Discoglossidae), a species in which males have short, simple tonal
advertisement calls and relatively long intercall intervals
(Márquez and Bosch,
1995). Female reciprocal calling has been reported in A.
cisternasii (Márquez and
Verrell, 1991), and female calls have been described in Bosch and
Márquez (2001b). This
behavior has been related to advertising receptivity in Alytes
muletensis (Bush et al.,
1996).
Previous studies of A. cisternasii determined that larger males
emitted advertisement calls with lower frequencies, that females were
preferentially attracted to lower frequency calls (Márquez,
1995a,b),
and that larger males obtained more matings per season
(Márquez, 1993).
Concerning the acoustic interaction among males, additional published studies
have shown that pairs of males interacting naturally have extremely limited
overlap between their calls, that they tend to time their calls with a phase
angle of 78° (±13.6), and that acoustically interacting males
alternate the role of leading and following in natural interactions
(Bosch and Márquez,
2000).
We aimed to determine whether a precedence effect exists in simulated
two-male interactions without call overlap in A. cisternasii.
Furthermore, we sought to determine the shape of the female preference
function based on the relative timing of male calls (phase angle,
sensu Klump and Gerhardt,
1992). Thus, we attempted to quantify the relative importance of a
precedence effect with simulated male calls presented with various phase
relationships. We tested whether this shape adjusts to a shelf model (the
advantage for the leading call is flat and drops to nonsignificance after a
given delay) or if it is a graded, gradual loss of advantage. This information
not only will illuminate aspects of the mechanism of the precedence effect,
but it will also contribute to our understanding of the evolutionary
significance of timing in intermale acoustic interactions (see
Bosch and Márquez,
2001a; Greenfield and Rand,
2000).
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METHODS |
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We studied A. cisternasii in October 1998 and 1999 in a liveoak forest or "dehesa" near the city of Mérida (235 m above sea level, Extremadura, west-central Spain, 38°59' N, 31°24' W). Gravid females (with mature eggs visible through the lower part of the abdomen) were collected at the beginning of the reproductive period and kept in captivity for 1-2 weeks under controlled conditions and fed ad libitum with fly larvae.
We synthesized synthetic calls at a sampling rate of 44.1 kHz and 16-bit
resolution with Sound Maker 1.0.4 software. A digital tone generator produced
a pure tone sinusoid, and the intensity envelope was visually adjusted to fit
the envelope of a representative call of the population. We adjusted the
duration (175 ms) and the dominant frequency (1491 Hz) of the synthetic calls
to the population average (Márquez
and Bosch, 1995).
We tested six different phase angles: Two speakers were placed behind
opposite sides of a square 1.8 x 1.8 m arena under low-intensity light.
The walls of the arena were formed by thin, black cloth hanging down from a
semi-rigid frame. The speakers emitted the synthetic calls alternately.
Synthetic calls were produced directly by an Apple PowerBook G3 and broadcast
through a custom-made amplifier and speaker system. The speakers and channels
were switched between trials. Sound level of the synthetic calls was adjusted
to 70 dB in the middle of the arena with a digital Realistic Sound Pressure
Meter (fast response, A weighting). We placed each female under a cylinder of
plastic mesh in the center of the arena for 30 s while the stimuli were
emitted. Subsequently, the cylinder was lifted and the female's movements were
monitored. We scored a choice only if the female reached an area within 10 cm
of the base of a speaker. A trial provided no data when the female reached the
edge of the arena away from the speakers or when no edge was reached 2 min
after we freed the female. Each speaker emitted calls of one male at regular
intervals (calling rate of 29 calls/min, equivalent to an intercall interval
of 1884 ms), a calling rate which is within the range found in the natural
population (intercall interval range: 819-6939 ms;
Márquez and Bosch,
1995).
The speakers broadcast the calls in pairs so that one of the speakers (leader) emitted its call before the other (follower). We tested six different phase angles: 30°, 60°, 90°, 120°, 150°, and 180° (therefore 0, 168, 339, 508, 678, and 747 ms of delay between the end of the leader call in one channel and the onset of the follower call in the opposite channel). We used a phase angle of 180° as a control, and before the trial, we selected randomly one channel and assigned it as the leader speaker.
We tested each female in a total of four trials for each treatment on different nights. The probability of approach to the leader speaker was calculated for each female. Thus, if a female approached the leader speaker twice and the follower speaker once and exhibited no response in the fourth trial, she would be assigned a probability of 2/3. Only females responding twice or more in the four trials of any of two-choice experiments were considered for the statistical analyses.
We used several measures to assess the strength of female preference for
each experiment. We measured the latency of the choice for each female
(averaged among trials), as well as the probability of calling for each
female. We also calculated the repeatability of the choice for each female.
For each female, a single measure of repeatability and probability of call was
obtained for the four trials in a similar fashion as for the probability of
approach. These probabilities were compared with the expected probability of
0.5 with one-sample sign tests. We compared trends between the tests with
different phase angles using the Jonckheere test for ordered alternatives
(Siegel and Castellan,
1988).
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RESULTS |
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Females preferentially approached speakers initiating the acoustical exchanges (leaders) for most tested phase angles (30°: n = 18, p <.0001; 60°: n = 18, p =.0352; 90°: n = 14, p =.0386; 120°: n = 23, p =.0768; 150°: n = 24, p =.0213; Figure 1A). For the 180° phase angle, the females chose randomly between the speakers, as we expected (n = 23, probability of approach = 0.558, p =.4545). We found a gradation in the degree to which females selected the leader (Jonckheere test for ordered alternatives, J* = 7.98, p <.0001, and the preference found in the 30° test was higher than in the rest (Friedman test,
2 = 19.67, p
=.0014). If the 30° test is omitted for the analyses, the graded trend
still remains significant, but the differences between individual tests are no
longer significant (Friedman test, 2 = 8.76, p
=.0675). Thus, we can conclude that female A. cisternasii tend to
exert a strong preference for the leader in 30° test, and that at higher
phase angles, the overall preference is weaker and graded (the higher the
angle the lower the preference).
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The latency of the choice also had a graded (positive) relationship with phase angle value (Figure 1B; latency: Jonckheere test for ordered alternatives, J* = 2.399, p <.0084). The latency of the choice was short for low values of phase angle and long for high values of phase angle. Similarly, the probability of female calling also had a graded relationship with phase angle value (Figure 1C; Jonckheere test for ordered alternatives, J* = 3.556, p <.0023), although the trend was in the opposite direction—the higher the phase angle, the lower the probability of female call.
Finally, the repeatability was higher in experiments with low values of phase angle than in experiments with high values of phase angle (Figure 1D; Jonckheere test for ordered alternatives, J* = 8.428, p <.0001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The female preference function in our study is a population-level preference function, and not enough repeated tests were performed on individual females to adequately describe individual preference functions (see Murphy and Gerhardt, 2000
).
The female preference function obtained is similar to some extent to that
presented by Minckley and Greenfield
(1995) for the acridic
orthopteran Ligurotettix planum, in which males emitting calls
immediately following another male's calls were strongly discriminated against
by females. Our female preference function, though, allows for an additional
level of resolution, as five higher phase angles (60-180°) were tested.
The graded degree of attractiveness of these additional five values is a
feature of the female preference function of A. cisternasii, which
has not been described for either anurans or orthopterans to the best of our
knowledge.
The sharp difference in probability of approach between the values of
30° and 60° is consistent with a mechanism of male calling inhibition
that occurs immediately after hearing a competitor's call, which has
previously been described for some orthopterans
(Greenfield, 1994;
Greenfield and Minckley, 1993;
Minckley et al., 1995). The
results also blend in nicely with the model suggested by Moore et al.
(1989) and discussed by Klump
and Gerhardt (1992), whereby
an absolute refractory period [defined by Klump and Gerhardt
(1992: 158) as "during
this period an external stimulus cannot elicit a call with a short response
latency"] would occur immediately after hearing the call of another
male, and this would be followed by a relative refractory period
["period during which fewer calls are given than expected from a random
placement of calls with reference to the acoustic stimulus"
(Klump and Gerhardt, 1992:
158; see also Zelick and Narins,
1983)]. Curiously enough, if we apply the trend of female
preference observed in our tests and if the relative refractory period
coincided with the higher values of phase angles (60-180°), female
preference would favor males that delay their response as much as possible,
thus approaching 180°. This would favor males that delayed their calls,
potentially reaching values above 180° and thus becoming leaders in the
following interaction. This would be consistent with the observation of
Márquez and Bosch
(2001), who found that A.
cisternasii males alternate the role of leader and follower in the same
calling session (same night). Márquez and Bosch failed to find a
significant correlation between percentage of interactions as leader and other
male parameters (size and temperature).
In this species, when two males engage in interactions in nature, the
average phase angle is 78° (±13.6)
(Márquez and Bosch,
2001). This suggests that males are adjusting the timing of their
calls to a phase angle that provides a slight but significant advantage to the
leading caller. The graded trend found for the 60-180° tests is less
sharp. In probability of approach, preference for the leading call is not
significant (but near significance) and is significant again for 150°.
Although the phase angle value found in natural acoustic exchanges between
males is similar in another congeneric species (A. obstetricans),
female preference for followers has been described in this species. However,
the differences in results may be related to the effect of the experimental
temperature because the test with A. obstetricans was performed at
relatively low temperatures (average 10.4°C;
Bosch and Márquez,
2001a). Furthermore, for A. cisternasii, a decrease in
the strength of female preference for leading callers in acoustical
interactions between males has been observed with decreasing temperature, to
the point that a reversal of preferences (i.e., preference for follower) has
been found at low temperatures (Bosch and Márquez, unpublished data).
Further testing is necessary to determine if these observations may be as
relevant as other effects of temperature on call characteristics and female
preferences (e.g., Gerhardt,
1978).
The graded effect found for all four aspects of female preference contrasts
with the trend described for the katydid othopteran Neoconocephalus
spiza by Greenfield and Roizen
(1993), in which a sharp,
nearly shelflike change in female preference function was found for changes in
phase angle between 0° and 45°. However, the lack of gradation
observed may possibly be due to the fact that the authors did not test enough
phase angles in the critical zone. Our results are more in line with the data
presented by Minckley and Greenfield
(1995), who found that females
were attracted to the leading call, and that the preference was strong for a
short intermale interval and progressively weaker as the interval between
calls increased.
An explanation for the observed precedence effect (without call overlap)
may be related to mechanisms to avoid the confounding information about the
location of sound source from reflected sounds (echoes). The best information
about the source of the sound will be provided by the beginning of the sound,
which is likely to reach the subject through the most direct (fastest) route.
This is a particularly serious problem for the species studied, for which
finding the precise location of the calling male may be a challenge for
females (Bosch and Márquez,
2000). Under some circumstances, in our recordings echoes appear
with substantial power in the call of males and up to 50 ms after the end of
the call of the male (unpublished data). A female preference function biased
toward the beginning of the call may thus prove adaptive for an expedient
location of the caller. The general application of such a hypothesis remains
to be tested.
It is interesting to note that, from a mechanistic perspective, there is a marked difference between precedence effect with overlapping calls and non-overlapping calls. When the leading call overlaps the beginning of the following call, the leading one may physically mask the transients at the beginning of the following call. When there is no overlap, some sort of central mechanism is likely. For example, a leading call heard on one side may lead to desensitization of the contralateral ear for some period into the future, a form of forward masking (Greenfield MD, personal communication). Further experiments are necessary to determine the nature of the underlying mechanism.
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ACKNOWLEDGEMENTS |
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J. Falagán helped in the laboratory. M.D. Greenfield and U. Grafe revised the manuscript. The Agencia de Medio Ambiente of Junta de Extremadura extended permits for field work. Partial funding was provided by project PB 97-1147 Ministerio de Educación y Cultura of Spain (P.I: I. De la Riva).
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