Behavioral Ecology Vol. 9 No. 6: 582-591
Variance in female responses to the fine
structure of male song in the field cricket,
Gryllus integer
Ann Hedrick* and Theo Weber*
"Neurobiology, Physiology and Behavior, University of California, Davis, CA 95616, USA, and bMaxPlanck-Institut fur Verhaltensphysiologie, Abteilung Huber, Seewiesen, Germany
Although female mating preferences are a focus of current controversy, little detailed information exists on female preferences
within natural populations. In the field cricket Gryllus integer, male calls attract sexually receptive females, and females preferentially move toward male calls with longer calling bouts (periods of calling containing no pause greater than 0.10 s in real
time). This study investigated female preferences for other variables of the male song, including syllable period, chirp pause,
and number of syllables per chirp. Male song was measured in the field to determine mean values for each variable in nature.
Female preferences were determined using a locomotor-compensator device, on which females ran in response to sequential
playbacks of synthesized male song. Mean female preferences corresponded roughly to mean male song variables. Nonetheless,
females varied greatly in their responses to synthesized calls differing in syllable period, syllable number, and chirp pause.
Moreover, individual females who were more selective for any one variable also tended to be more selective for others. These
results show that females may differ from one another in their mating preferences and degrees of selectivity, even within a
single population. Key words: crickets, female mating preferences, Gryllus integer, mate recognition, phonotaxis, song. [Behav
Ecol 9:582-591 (1998)]
O pcciation involves the evolution of reproductive isolation
O between groups of organisms. Therefore, the factors that
promote and maintain reproductive isolation are important
to evolutionary biology (Futuyma, 1986; One and Endler,
1989). Many studies have demonstrated that reproductive isolation in animals can be maintained by differences in mate
recognition systems, in which males display and females respond to these displays before mating (Ryan, 1990). Females
often rely on the mating displays of males to distinguish conspecific from heterospecific males (Endler, 1989; Ryan, 1990).
This reliance suggests that elements of the male display might
be relatively invariant within a species and that females might
exert stabilizing selection on these traits to avoid interspecific
matings (Butlin et al., 1985).
However, work on sexual selection has shown ample variation, both phenotypic and genetic, among males in characters
related to mate recognition, such as mating displays (e.g.,
Charalambous et al., 1994; Hedrick, 1988; Moore, 1990), and
among females in their responses to those characters (e.g.,
Houde, 1988; Wagner et al., 1995). Females often use variation in male characters to choose mates (Andersson, 1994).
Moreover, variation in male mating characters, along with directional female preferences, is thought to be one avenue by
which new species can be formed (Endler, 1989; Lande,
1981). Thus, it becomes important not only to document variation in males, but also to characterize variation in female
preferences within populations and species (Gerhard t, 1991,
1994).
In addition, female mating preferences within populations
may strongly affect the evolution of male courtship signals
(Andersson, 1994; Bakker and Pomiankowski, 1995; KirkpaAddress correspondence to A. Hedrick, Neurobiology, Physiology
and Behavior, University of California, Davis, Davis, CA 95616, USA.
E-mail: avhedrick©ucdavis.edu.
Received 9 September 1997;firstrevision 23 February 1998; second
revision 6 April 1998; accepted 8 April 1998.
O 1998 International Society for Behavioral Ecology
trick and Ryan, 1991; Ryan and Keddy-Hector, 1992). The selection pressures acting on mating preferences are matters of
current debate (Andersson, 1994), yet little detailed information has been gathered on the precise preferences of females within most animal mating systems (but see Ritchie,
1996).
Auditory mate recognition systems, in which males call and
females move toward the source of the call, are particularly
amenable to experimentation because parameters of the
male's display can be mimicked and modified electronically.
In the laboratory, females will often move toward a speaker
playing their own species' song, but not toward the source of
heterospecific song, and will move toward some conspecific
songs more readily than others. The use of playbacks in the
laboratory, as opposed to the use of real males, to investigate
auditory mating preferences means that songs with particular
properties can be synthesized for experiments and that the
response of the female does not depend on her interactions
with a particular male (Hedrick, 1986).
Work on auditory mate recognition in a species of field
cricket from Texas, USA, with a trilling one-syllable song
(sometimes called "Gryllus integer" but probably a different
species of Gryllus; Smith and Cade, 1987; Wagner et al., 1995;
Weissman et al., 1980) revealed that the syllable repetition
rate is approximately 70 syllables/s (Hz) (Souroukis et al.,
1992). Although the role of syllable repetition rate in species
recognition has not been investigated for this cricket, females
walk toward trills with 20 to 80 syllables per trill, even when
some syllables (up to 28%) are miwing, and respond to calls
with inter-trill pauses of 100-450 ms (Wagner et al., 1995).
In contrast, male Gryllus integer from the Davis, California,
USA, population do not trilL Rather, they produce fast trains
of chirps containing either 2 or 3 syllables per chirp delivered
at a rate of approximately 1 syllable per 14 ms at a 4.5 kHz
carrier frequency. Between chirps, there is a chirp pause of
approximately 30 ms (Figure 1). Additionally, individual males
of this population vary in the duration of uninterrupted calling (defined as a period of calling containing no breaks of
583
Hedrick and Weber • Female responses to male song in field crickets
syllable period
chirp pause
chirp
syllable
TIME —>
Figure 1
GryUus inUgn song. Diagram represents 2 chirps, each with S
syllables, and shows the syllable period, consisting of the syllable
plus the time interval until the next syllable in a chirp; the chirp,
consisting of three syllables; and the chirp pause (i.e., the time
interval between consecutive chirps). Singing bouts are made up of
long trains of chirps.
0.10 s or more). This duration of uninterrupted calling (caUing bout length) is highly heritable (heritabihty = 0.75; Hedrick, 1988). Previous experiments demonstrated that females
prefer to move toward the source of calls with longer calling
bouts (Hedrick, 1986) when calls vary only in their railing
bout lengths.
Here, we present data on the fine structure of song in 20
male G. integer from the Davis, California, population and
give the results of experiments performed on a locomotor
compensator (described below) to examine female preferences in this population. We conducted 4 experiments on a
set of 22 females (total number of trials «= 1032) to gauge
their responses to synthesized male songs. These experiments
were designed to eluddate spedes recognition and phenotypic variation in song preferences by females of this population.
Spedes recognition and intraspecific mate choice often act
simultaneously, and female evaluation of males as potential
mates encompasses both processes (Ryan and Rand, 1993; Ritchie, 1996). Therefore, rather than separating these phenomena, we treat them together by comparing a set of systematically varied male signals with the behavioral responses of females to those signals (Ritchie, 1996). We operationally define
mate recognition as any female behavior that indicates that
she considers a male an appropriate mate, even if she is incorrect (Ryan and Rand, 1993), and mating preference as any
female behavior that indicates that she will mate with one
male (or kind of male) more readily than others.
MATERIALS AND METHODS
Males
Male song was recorded in the field from the Davis, California, population of GryUus integer when males were singing
from cracks in the ground (their usual habitat) in which the
temperature was 25° ± 1°C Song variables for 20 different
males were measured using a GW Instruments 16-bit analogto-digital converter and Superscope, a software program emulating an oscilloscope, sampling at 1000 points/s. We calculated averages for each male from a sample of 10 or 11 measurements per variable.
In the song of GryUus integer (Figure 1) we measured the
number of syllables per chirp, the syllable periods, and the
chirp pauses. Population means for these temporal properties
of calling song were estimated by averaging the mean values
for each of the 20 males. Because this method may obscure
variation among maW, we also conducted one-way analyses of
variance on the raw data.
Females
Female GryUus integer used in these experiments were virgins
and were chosen randomly from the first laboratory generation derived from mothers caught in the field in Davis, California, from the same population as males recorded for call
characteristics. Females were maintained in individual jars
with food and a water source (lettuce) inside a walk-in incubator with a 12:12 h light/dark cycle and a temperature of
26°C Males of this species were not present No female was
tested more than once per day, and most were not tested on
consecutive days. We conducted tests at 25°C using a spherical
locomotor compensator (Kramer, 1976), which has been used
to identify the most important components of male cricket
calls to conspedfic females in European spedes of GryUus
(Weber et al., 1981). Previous work on the Davis population
of GryUus integer had shown that female movement toward
the source of a male call represents an actual mating decision
(Hedrick, 1988).
Female preference trials '
Before the start of a trial on the compensator, a small dot of
light-reflecting foil was placed on the female's thorax. Then
the female was placed carefully on top of the compensator
sphere (50 cm diam) inside an echo-free (>2 kHz) room, and
the room was completely darkened. The departure of the female from the top of the sphere was detected by an infrared
sensor system. This sensor relayed information to an electronic device that caused compensatory rotation of the sphere so
that the cricket always remained on the top of the balL Movements of the sphere were recorded as x- and y-coordinates
versus time on a computer, which stored and displayed data
so that an animal's movements could be monitored from outside the test room on a computer screen. Experiments began
after approximately 2 min when the female had settled down
(either she stopped running chaotically or she moved for the
first time). Then, computer-synthesized rails were presented
in an alternating sequence from two speakers placed at an
angle of 115° from one another, with 2 min allocated to each
presentation, 1 min per speaker. Each test offered the female
a series of different calls in turn, from 5 to 18 different sounds
per test These rails, which had been low-pass filtered to avoid
aliasing, were all delivered at a carrier frequency of 4 3 kHz
and an amplitude of 70 dB above background in the silent
room, measured at the female's position. A computer program controlled the sequence of calls offered, and a female
was tested only once per sequence. Calls were offered in the
same order to all females because pilot tests and prior experiments showed no evidence that the order of presentation
affected female responses.
Chirps with diffeieut syllable periods
Males of G. integer from Davis, California, call with either 2
or 3 syllables per chirp. We constructed synthetic calls with
either 2 syllables (experiment 1) or 3 syllables (experiment 2)
per chirp and manipulated the pauses between the syllables
to determine the importance of syllable period (Le., syllable
repetition rate). Syllables were 8 ms long, except in the two
shortest syllable periods, the 8-tns period (in which we used a
4-ms syllable and 4-ms pause) and the 10-ms period (in which
we used a 6-ms syllable and 4-ms pause). Chirps were separated by pauses of 36 ms to mimic natural song. Durations of
syllable periods ranged from 10 to 60 ms in experiment 1 (10,
12,14, 20, 24, 32, 60 ms), and from 8 to 32 ms in experiment
2 (8, 12, 20, 24, 32 ms).
Behavioral Ecology Vol. 9 No..6
584
Calls with different chirp p u n a
G. integer males from Davis pause between 2- and 3-syllable
chirps, whereas males from Texas call in continuous trills. To
investigate whether the pause is critical to species recognition
in Davis crickets and to see what variation in the pause is
acceptable to females, we constructed model calls with 3 syllables per chirp and a syllable period of 20 ms and varied only
the pause between chirps. Syllables were 8 ms long. Durations
of the pause ranged from 4 to 100 ms (4, 6, 8, 12,16, 24, 56,
52, 70, 100 ms). We tested 19 females.
Calls with different numbers of syllables
Females of the trilling Gryllus species from Texas respond to
calls with 20-80 syllables per trill (Wagner et aL, 1995). In
contrast, G. integer from Davis, California, typically call with
only 2 or 3 syllables per chirp. Thus, we tested 16 females for
their responses to calls with different numbers of syllables per
chirp. We constructed model f~»\U with one repeated syllable
(trills) and others with 2-16 syllables per chirp (2, 3, 4, 6, 8.
12, 16). In these model calls, the syllable period was 20 ms,
the syllable duration was 8 ms, and the chirp pause was 36
ms.
The computer program provided two linear measurements of
female responses: L» the distance each female ran while she
heard each call from two different speakers, and Db her displacement, the distance from the point where she was when
the call began to the point she had reached when die call
finished. If she ran in a perfectly straight line, L, and Dt were
die same; if she changed course during die run, L, was greater
than DL It also gave two angular measurements: Aj, die female's angle (compass direction) when die call ended, relative to a defined 0° point in the room (the two loudspeakers
were placed at 90° and 205°); and a* die angular deviation of
her headings around die angle A, (Zar, 1984).
Because of die large volume of data obtained, we simplify
our presentation here by reporting only linear measurements.
Linear and angular measurements were significantly correlated (see below). Major departures in a female's orientation
from die angle of die active (broadcasting) speaker were rare
and were usually seen in conjunction widi very small linear
measurements.
To compare a female's responses to different calls during
an experiment, we first calculated die total distance diat she
ran during all die tests, L, = 2 (Lj), (» = 1 to n tests). We
then standardized each of her measured displacements to this
total and expressed it as a percentage:
Relative Distance,, Run = (D/L,) 100
Thus, if a female ran in a perfectly straight line in response
to only one call, but was motionless during all die others, her
Relative Distance(0 Run (RDR) for call t would be 100%; she
would be perfectly selective for diat call.
RDR corresponded closely to angular measurements. When
female angles (AJ were compared to speaker angles (90° and
205° from a defined zero point in die room), and the resulting departures from die "correct" (active) speaker heading
were analyzed widi RDRs from the same trials, we found that
RDR and the aeetsaey with which females tracked die active
speaker were significantly correlated. Mean RDRs (averaged
across females) for die different male rails were negatively
correlated with mean departures from die correa heading (n
= 30, Kendall correlation coefficient T = -0327, p - .001)
and negatively correlated widi mean angular deviation, a mea-
sure of the variance around females' angles (n = SO, Kendall
T = -0.448, p = .0005). Larger RDRs were associated with
more accurate headings and less meandering. Larger RDRs
were also correlated with more accurate headings for individual females (Kendall rank correlations, p < .05 for all 12 of
12 females participating in 3 or more experiments, n = 2030 test calls per female). Moreover, for each experiment, chisquare tests showed that female angles of orientation were
significantly clustered in a sector ±60" from the active loudspeaker's angle, as compared to the two sectors of the circle
which were farther away (2-syllable period: speaker 1, x* =
53.90, speaker 2, x1 = 37.90; df = 2, p < .001 both tests; 3syllable period: speaker 1, x l = 41.15, speaker 2, x* = 34.97,
df = 2, p < .001 both tests; chirp pause: speaker 1, x* =
110.25, speaker 2, x* = 77.06; df = 2, p < .001, both tests;
syllable number speaker 1, x* = 136.55, speaker 2, x* =
124.21; df = 2, p < .001, both tests). Finally, when females
were responding to the same calls offered from the two different speakers (positioned at 90° and 205° from the designated 0° point), female angles (AJ of orientation were significantly different (Wilcoxon signed-ranks test, t = —4.60, n •»
30 angle pairs, p < .01). Therefore, we are confident that RDR
provides an accurate measure of female responses, without
the presentation of angular data.
Data (RDRs) from each experiment were analyzed using
two-way ANOVAs with replication, allowing us to examine die
effects of test condition, individual females, and interactions
between test conditions and individual females. Percent data
were arc-sine transformed to meet the assumptions of ANOVA. Post-hoc tests (Tukey) were applied in some cases; for
these, we used experimentwise error rates (a <: 0.05) adjusted for the total number of pairwise comparisons of means
(Zar, 1984). To provide a measure of variation in preferences
within females, we also calculated coefficients of variation (CV
= SD/mean) in a female's responses to the different calls she
experienced within one experiment CVs allowed us to measure the degree of variation in the female's responses to different test conditions that she encountered on one day. These
were then compared to her variation in responses to another
set of conditions on a different day. Repeatabilities, which are
used to measure the consistency of behavior in individuals
over time and thus can set an upper limit on heritability, were
not calculated because we did not test individual females with
the same calls on different days.
RESULTS
Song profiles of males
Analysis of the fine structure of calls in 20 G. integer males
gave the following overall means, calculated from the mean
values for each male: syllable period, 14.0 ± 0.2 ms; chirp
pause, 30.4 ± 5.0 ms; and syllable number, 2.84 ± 0.24. Individual variation in call components was present among
males (Figure 2). For each of the three variables we measured,
we found statistically significant interindividual variation using
one-way ANOVA (syllable period, df = 19, 198, F - 7.66, p <
.0001; chirp pause, df = 19,198, F = 16.81, p < .0001; syllable
number, df = 19, 199, F = 6.25. p < .0001). Coefficients of
variation ranged from 0.067 for syllable period to 0.166 for
chirp pause. Significant correlations were not found among
any of these components.
A significant negative correlation was found between duration of calling bouts and die chirp pause (r = - 3 8 2 , n •»
13, p « .035). Here, duration of calling bouts was measured
indirecdy by counting die number of bouts per 5 min of calling, with a bout defined as a period of calling containing no
pause greater than 0.10 s. Males with many bouts in 5 min
Hcdrick and Weber • Female responses to male song in field crickets
585
(hence with shorter bout lengths) tended to have longer
chirp pauses.
A
I . I .
K of Mates
and 2s female phonotaxis to flilijm with
different syllable periods
In experiments 1 and 2, females were offered model calls with
either 2 or 3 syllables per chirp, respectively. For experiment
1, 14 females were tested for their responses to two-syllable
chirps with different syllable periods ranging from 10 ms to
60 ms. The mean response for all females was highest when
the syllable period was 20 ms. However, the responses of different females varied (Figure 3A), with the majority responding most strongly to periods of either 14 or 20 ms. Four females showed no preference for a particular syllable period.
A two-way ANOVA with replication demonstrated that syllable
period exerted a statistically significant effect on female response (df >• 6, 98; F = 54.69, p < .00001). Female identity
was also statistically significant (df = 13, 98; F = 3.19, p <
.0005), and a significant interaction was found between syllable period and female identity (df = 78, 98; F = 4.19, p <
.00001). Thus, females differed from one another in their patterns of responses to calls that differed in syllable periods.
To investigate this variation in female preference further,
we examined the ranking of conditions by each female. The
strongest and second strongest response (as measured by DJ
ZJ was tabulated for each female. In 11 of 14 females, the
first-ranked syllable period was 20 ms. In the three remaining
females, the first-ranked period was 14 ms. Second-ranked syllable periods for the 14 females were mixed and ranged from
10 ms to 32 ms. Additional variance was seen in differential
responses of females to the other syllable periods offered. A
post-hoc Tukey test of the ANOVA results confirmed that the
20-ms syllable period elicited a significantly stronger response
(mean RDR = 8.30) than the lower ranked periods, 24 ms
(mean RDR = 4.08, Tukey q = 16.88, p < .001) and 14 ms
(mean RDR = 3.55, Tukey q = 18.97, p < .001).
As a measure of selectivity or variance in each female's behavior, we calculated the CV for each female's set of responses. In general, a female's CV was higher when the range
in her responses to different calls was greater. CVs for females
in this experiment ranged from 0.45 to 1.39, and the mean
CV was 0.72.
hi experiment 2, 20 females were tested for dieir responses
to calls with 3 syllables per chirp and 5 different syllable periods
ranging from 8 ms to 32 ms. Once again, a two^vay ANOVA
with replication demonstrated a significant effect of syllable period (df =» 4, 100; F = 83.51, p < .00001) and a significant
interaction between syllable period and female identity (df =
76, 100; F = 3.07, p < .00001). However, female identity alone
was not a statistically significant effect (df = 19, 100; F = 1.66,
p = .0558); females responded similarly to one another to calls
with different periods. Calls with 20-ms and 12-ms periods elicited the most response (Figure SB). Nine females responded
most strongly to calls with a syllable period of 12 ms; 8 responded most strongly to calls with a 20-ms period. One female responded most strongly to <~aH< with an 8-ms period, and 2 most
strongly to calls with a period of 24 ms.
Post-hoc Tukey tests separated die top two syllable periods
(20, 12 ms) from the third-ranked period, 24 ms (20 versus
12 ms, Tukey q = 4.05, ns; 20 versus 24 ms, Tukey q =13.11,
p < .001; 12 versus 24 ms, Tukey q =• 9.06, p < .001). CVs for
individual females ranged from 0.26 to 1.20, with a mean of
\ 0.75.
\ Although 11 of 14 females responded most strongly to the
2fr-ms period in 2-syllable chirps, and 8 of 20 females preferred die 20-ms period in S-«yilable chirps, mean syllable period for males was only 14.0 ms.
6 -
t 2
1 ".
10 13
12
14
16
18
Syllable Period, ms
4 ~\
1 -
n
20 22 24 26 28 30 32 34 36 38 40 42
Chap Pause, ms
12 1086 4 2 -
P- P.
2.2
2.4
2.6
2.8
Syllable Number
Figure 2
Frequency histogram! for the (A) mean syllable period (ms), (B)
mean chirp pause (ms), and (Q mean number of syllables per
chirp, of 20 males. Overall means, ranges and coefficients of
variation (CV) are: syllable period, mean «• 14.0 ms, range 12.616.0, CV = 0.067; chirp pause, mean => 30.4 ms, range 21.2-41.6,
CV - 0.166; and syllable number, mean - 2.84, range 2.18-3.00,
CV - 0.085.
Experiment 3: female phoaotaxb to calls with difleiem
To determine the importance of the pause between chirps to
female G. integerfromDavis, California, 19 females were test-
Behavioral Ecology Vol. 9 No. 6
586
2-Syllable Chirp
10
12
14
20
24
32
60
Syllable period, ms.
3-Syllable Chirp
figure 3
Relative distance run (RDR;
%) for females experiencing
call* with different syllable periods. (A) RDR for 14 females
responding to calls with 2 syllables per chirp and different
syllable periods (x-axis). Each
line represents an individual
female's responses to a series
of different calls. (B) RDR for
20 females responding to calls
with 3 syllables per chirp and
different syllable periods. Each
line shows an individual female's responses to different
calls.
ed for their responses to calls with different chirp pauses ranging from 4 to 100 ms in duration.
Mean response of the 19 females (Figure 4A) was highest
for a range of 24-70 ms, with a peak response at 36 ms. Females could be divided into three groups depending on their
responses in this experiment The majority of females (12)
were selective for chirp pauses of either 24 or 36 ms, with a
lower but continued response to 52 and 70 ms (Figure 4B).
Four females were unselective and responded well to most
calls, with a slow decline in response evident at pauses greater
than 36 ms (Figure 4 Q . Finally, three females showed multiple peaks of response (Figure 4X>), with mavimal responses at
pauses of 16, 36, and 52 ms. A two-way ANOVA with replication showed that chirp pause had a highly significant effect
on female response (df - 9, 190; F = 35.05, p < .00001), as
did female identity (df =• 18, 190; F - 7.82, p < .00001).
There was also a significant interaction between chirp pause
and female identity (df = 162, 190; F = 3.58, p < .00001).
Post-hoc Tukey tests demonstrated that for all females, the
response to the 36-ms pause (mean RDR =. 5.184) was statis-
12
20
24
32
Syllable period, TO.
tically distinguishable from that to the 52-ms pause (RDR 4.094, Tukey q «= 6.19, p < .005 ), and also significantly different from responses to 24-ms and 70-ms pauses (both, RDR
= 3.451; 36 versus 24, 70 ms, Tukey q = 9.85, p < .001). CVs
for individual females ranged from 0.21 to 1.34, with a mean
of 038.
4: female phonoburis to chirps with different
syllable numbers
We tested 16 G. m&gcrfemales for their responses to calls with
different numbers of syllables per chirp, ranging from 1 (trill)
to 16 syllables (Figure 5).
One-syllable calls (trills) evoked at most a weak response
from G. integer females. The overall ranking of calls by all
females, from strongest female response to weakest, was 2syllable calls, then 3-, 4-, 6-, 8-, 16-, 12-. and 1-syllable call*.
Most females responded best to calls with 2 or 3 syllables (Figure 5A-D). Of the 16 females tested, 11 oriented most strongly to 2-syOable calls. For 7 of these females, the 3-syOable call
587
Hedrick and Weber • Female responses to male song in field crickets
All Females, Mean Response
4
6
8
12
16 24 36 52
CNrpPsUM, ITS.
70 100
Selective
12 16 24 36 52 70 100
Chirp piuM, n .
Multiple Peaks
Unselecttve
4
6
8
12
16 24 36 52 70 100
Chirp psuM, ra*
UMtt
12
16 24 36 52 70 100
ChkppauM, ira.
Figure 4
Relative diitance run (RDR; %) for females hearing calls with different chirp pauses. (A) Mean RDR for all females with each call. (B)
Responses by each of 12 females classified as giving a selective response. Each line represents a female. (Q RDRi of four females showing an
unselective response. (D) RDRs of three females whose responses were classified as having multiple peaks.
was almost as effective. Four females responded most strongly
to 3-syflable "»n«, with 2-syllable calls a close second. Only 1
female preferred 4-and 6-syilable calls.
A two-way ANOVA with replication demonstrated that there
was a significant effect of syllable number on female response
(df = 7,128; F- 43.19, p < .00001). Again, a significant effect
of female identity was also found (df = 15, 128; F = 7.35, p
< .00001), along with a Tignifirant interaction between syllable number and female identity (df - 105, 128; F = 2.76, p
< .00001). Females showed different patterns of responses
from one another to calls with different numbers of syllables.
A Tukey test showed that responses to 2-syllable calls (RDR
= 7.36) were significantly stronger than those to 3-syilable
calls (RDR = 5.37; Tukey q = 6 3 5 , p < .001). However, 3 and
4 syllables (both, RDR = 4.80) did not differ significantly in
attractiveness, nor did 4 (RDR = 4.80) and 6 syllables (RDR
» 3.75). In contrast, 4 and 8 (RDR = 2.80) syllables did differ
significantly in attractiveness (Tukey q = 637, p < .001).
Much of the variance in female response was associated with
4 or more syllables. Many crickets showed only a slight decline
in their activity when the 4-syllable call was presented (Figure
5). However, others responded poorly to 4 syllables, or sharply
dropped activity with this stimulus (Figure 5B J)). In contrast,
one animal that had not responded well to the S-syllable call
showed increased activity when the 4-syllable call was presented (Figure 5F). Variation was also present in female responses
to greater syllable numbers.
To summarize the different responses, we divided females
into the following categories based on their response curves
to the offered stimuli: selective (n = 4; Figure 5B), broad
response, type 1 (n «• 4; Figure 5C), broad response, type 2
(n « 5; Figure 5D), unselective (n = 2; Figure 5E), and unusual (n = 1; Figure 5F). Selective females responded well to
only one call (the 2-syllable chirp), and poorly to the others.
In contrast, unselective females rejected only the l-syilable call
(the trill) and responded well to all remaining calls. Females
with a broad response of type 1 responded best to either 2 or
3 syllables, but also responded to greater syllable numbers,
588
Behavioral Ecology VoL 9 pJo. 6
B
All Females, Mean Response
A
Selective
10
i
4
6
8
Sytabtanumbtr
12
16
Broad Type 1
Broad Type 2
10 T
4
6
8
Syfabla Number
E
12
16
Unsdcctlve
10
12
16
Figure 5
Rotative distance run (RDR; %) by 16 females responding to calls with different numbers of syllables per chirp. (A) Mean RDR for all
females in response to different calls. (B) Individual RDRs of four females classified as selective. (C) RDRs of four females with a broad type
1 response. (D) RDRs of five females with a broad type 2 response. (£) RDRs of two females with unselective responses to different calls. (F)
RDRs of one female with unusual responses to different gills. She did not prefer natural numbers of syllables.
Hedrick and Weber • Female responses to male song in field crickets
Tmble 1
Correlations between coefficient* of variation in responses of nine
females to different song components
Syllable
number
Chirp pause
Syllable number
IWfyllable period
0.916***
Twosyllable
period
Threesyllable
period
-0.110
-0.040
0.786**
0.696*
0.071
-0.040
' p < .05; •• p < .01; •** p < .001.
with a slowly declining response as syllable number increased.
In females with a broad response of type 2, activity dropped
steeply after S or 4 syllables, although there was an occasional
resurgence of activity to calls with more syllables. Finally, one
female had unusual responses, responding best to either 4 or
6 syllable chirps, which occur only rarely (4 syllable) or not
at all (6 syllable) in nature.
CVs in RDR [(£>, / I J 1 0 0 ] were calculated for each female
in the experiment. The CVs for selective and broad type 2
females (n = 9, mean = 0.821) differed significantly from the
CVs for unselective and broad type 1 females (n = 6, mean
= 0.425; F,, u = 5.730, p = .031). CVs for all females ranged
from 0.31 to 1.63, with a mean of 0.66. Although the majority
of females responded more strongly to calls with 2 syllables
versus 3 syllables, males were more likely to call with 3 syllables
(Figure 2C).
Responses of individual females across experiments
To investigate whether a female's selectivity in one experiment
was correlated with her selectivity in another one (on a different call component), we characterized each female's selectivity in any one experiment by calculating the CV for her set
of responses (response measured as RDR). If the female was
selective, her responses to different test conditions (calls) differed markedly, and she had a high CV. In contrast, unselective females responded similarly across all test conditions and
had low CVs.
• When we compared the CVs across experiments for the
nine females that participated in all experiments, we found
that a female's selective behavior extended across different
components of male song. Selectivity for syllable period (as
measured by CV of responses to 3-syilable calls), chirp pause,
and syllable number were all significantly correlated (Table
1). The only component of male song that was not correlated
with the others in female selectivity was the syllable period for
2-syllable chirps.
DISCUSSION
The mate recognition system of GryOus integer
On the whole, mean responses of females in our experiments
roughly corresponded with the mean song components of
males. For example, male G. integer from Davis, California,
call with 2 or 3 syllables per chirp, but most commonly with
3 (mean = 2.84). Females in our experiments tended to respond more to 2 syllables than to 3, but both syllable numbers
drew strong responses. Similarly, the average chirp pause for
Davis males was 30.4 ms, and individual values ranged from
21.2 to 41.6 ms. Females responded most strongly to 36 ms,
with tolerance of pauses from 24 ms to 70 ms.
Not all song components matched up between males and
females. For example, male mean syllable periods were 14.0
589
ms. In the 3-syllable tests, although 9 of 20 females chose a
12-ms syllable period, 8 females responded most strongly to a
20-ms period. Moreover, in the 2-syllable tests, 11 of 14 females responded most strongly to a 20-ms syllable period. Because the syllable period of males ranged from 12.6 to 16.0
ms, the syllable repetition rate by males in this population may
be slightly faster than that preferred by the majority of females. If shorter syllable periods (faster syllable repetition
rates) imply greater energetic investment per unit time (as
suggested by Wagner et al., 1995), then our finding would
counter the assertion that females should prefer male displays
that are energetically more costly (Ryan, 1988). However, it is
not known whether males with shorter syllable periods actually expend more energy in calling because other call variables may change as syllable period changes. In this study,
calling bout duration, a trait that strongly affects female preferences (Hedrick, 1986), was not significantly correlated with
either 2- or 3-syllable periods, nor was chirp pause duration
or syllable number. Nonetheless, our sample of males was relatively small (n = 20), and investigation of a larger sample of
males from this population might reveal more co-variation
among call components.
Comparisons with aOopatric and sympatric species
In the European species Grylhis campestris, <-all« are organized
into 4-syllable chirps, with chirps repeated 2 to 4 times per
second and a syllable repetition rate within each chirp near
30 Hz (Thorson et al., 1982). Mate recognition in Grylhis campestris and in G. bimaculatus, another species with 4-syllable
chirps, seems to rely most strongly on syllable repetition rate
(Weber and Thorson, 1989). Pauses between chirps do not
appear to be critical, as some females will walk toward continuous trills (Thorson et al., 1982). Species in the genus TeleogryUus have more complex songs containing both chirps and
trills (1-syllable chirps), and T. commodus females attend to
the different syllable repetition rates of each (Doolan and Pollack, 1985; Hennig and Weber, 1997; Pollack and Hoy, 1981).
In contrast to G. bimaculatus and G. campestris that rely
heavily on syllable repetition rate within chirps to identify appropriate mates, G. integer apparently uses additional components to identify and select mates. Preferences for these
components vary among females. Although some females respond indiscriminately as long as the syllable repetition rate
is acceptable, many are also selective with regard to syllable
number and chirp pause. In general, trills are not attractive.
At least 2 syllables but no more than 6 are preferred, and a
distinct interval of 6 ms or more between chirps seems to be
important
Most male G. integer from California call with 3 or close to
3 syllables per chirp. However, most California females prefer
2 syllables, and an Arizona population of G. integer calls exclusively with 2 syllables per chirp (Hedrick, personal observation) . Possible reasons for the difference in syllable number
between male calls and female preferences in the California
population are not clear. Notably, the Californian G. integer is
relatively intolerant of increased syllable numbers. Although
some G. integer females show little decline in responsiveness
as syllable number is increased, most females respond less as
syllable number gets larger than 3 or 4. Thus, G. integer fails
to demonstrate a "supernormal stimulus" effect (Ryan and
Keddy-Hector, 1992) with respect to syllable number. This pattern might reflect selection against interspecific matings or
costly encounters with a congener, G. Hneaticeps, that is often
found in the same habitat as G. integer and has a call with 7syllable chirps. G. Bneatiteps has a slower syllable repetition
rate than G. integer (Weissman et al., 1980), and it is not
known whether these species ever interbreed. However, they
590
often are found in close proximity to one another (occasionally even in the same cracks; Hedrick, personal observation),
and may compete for food or other resources.
G. integer's lack of responsiveness to large syllable numbers
also contrasts with results from the Texan Grylhis (sometimes
referred to as G. mUger), which calls with 20 to 60 syllables
per trill. In their study of the Texan GryBus, Wagner et aL
(1995) showed that females prefer many syllables per trill over
fewer syllables (range = 10-80 syllables) in both two-stimulus
tests and in sequential presentations. In contrast, Grylhis integer females from California found trills unacceptable and
preferred chirps with 2, 3, 4, and 6 syllables to chirps with
more. Additionally, the Texan crickets preferred shorter trill
pauses over longer ones (range "• 100—450 ms) in two-stimulus tests, but Californian G. integer preferred particular chirp
pauses (24—36 ms) in sequential presentations, while accepting somewhat longer ones (up to 70 ms). Given these differences in the call structure and phonotaxis preferences of the
Texan and Californian populations, it is likely that they'are
reproductively isolated by their premating behavior. Hybridization attempts in the laboratory between the two populations produced no viable offspring (Smith and Cade, 1987).
Choosiness of females: patterns among different call
components
Both "choosy" (selective) and "nonchoosy" (unselective) females were found within the test population for particular
song components. In selective females, responses to different
calls within an experiment differed markedly, giving a high
CV. Unselective females responded similarly to all rails and
had low CVs.
Comparison of the CVs from different experiments for each
of the females showed that coefficients of variation from individual females were correlated across experiments. This implied that a female who is selective about one song component also tends to be selective about others, and that a range
of selectivity can be found among females within a population.
These findings contrast with a situation in which females may
make trade-offs between selectivities on different components
(e.g., Doherty, 1985).
Only one song component, the syllable period in 2-syilable
chirps, was not correlated with all of the others on selectivity
(as measured by CVs). This component did not show low variance in CVs.
Behavioral Ecology Vol. 9 No. 6
females vary in their preferences for the number of syllables
per trill and the inter-trill interval and that variation among
females is relatively consistent over 3 days. Here, we have presented evidence for phenotypic variation among female G.
integer from California in the strength and direction of their
mating responses. In all but one of our experiments, a twoway ANOVA demonstrated strong effects of the individual female and an interaction effect between the female and the
call presented. Phenotypic variance was particularly pronounced in responses to syllable number and chirp pause. For
these two components of male song, our experimental group
of females contained two dearly denned subgroups, the selective and the unselective females. To determine whether
such differences in female responses could be heritable in this
species, it will be necessary to test females again and calculate
measures of repeatability.
If the song components studied here are heritable, female
responses could result in stabilizing selection on some aspects
of male call* (e.g., on the syllable number). In other cases, it
seems more likely that the female preferences we have identified could result in directional selection. For example, directional selection imposed by females might favor an increased duration of the syllable period in this population of
GryOus integer.
In conclusion, female mating preferences can play an important role in the evolution of male courtship signals (Andersson, 1994; Kirkpatrick and Ryan, 1991). Although the
form and function of female mating preferences are controversial (Bakker and Pomiankowski, 1995; Ryan and KeddyHector, 1992), little detailed information exists on the preferences of females within populations. Our results on the Davis, California, population of Grylhis integer demonstrate that
individual females vary in their preferences for components
of male rails, that some females are more selective for these
components than others, and that female choice may simultaneously generate stabilizing selection on some call components, and directional selection on others.
We thank Franz Huber and Klaus Schildberger for extensive advice
and discussion, Ursel Heinecke and Heidrun Bamberg for performing choice tests, Monika Schlag for cricket care, Hans-Ulrich Kleindienst for technical assistance, Franz Huber, H. Carl Gerhardt, and
David Able for comments on the manuscript, and Brian Mulloney for
transoceanic consultation!. A.H. was generously supported by a grant
from the Max Planck Society. The experiments reported herein comply with publication no. 86-23 of the National Institutes of Health
(USA) and with the current laws of Germany.
Variance in the mate-recognition system of G. integer
Despite the classical view that mating traits involved in sexual
selection will be relatively invariant (reviewed in Cronin,
1992), increasing evidence has demonstrated both phenotypic
and genotypic variance in sexually selected traits within populations (Hedrick, 1988; Houde, 1988; Ritchie and Kyriacou,
1994; Ryan and Rand, 1993). In G. integer, a relatively large
amount of genetic variance in one aspect of male calling behavior, calling bout length, has already been discovered (Hedrick, 1988). Our present results show phenotypic variance in
additional aspects of the male call. Moreover, variance in calling bout length, a heritable trait, is phenotypically correlated
with variance in chirp pauses. Males who call in shorter bouts
also pause longer between consecutive chirps within a bout
This suggests that chirp-pause duration may also be a heritable trait in this population of G. integer.
Models for the evolution of female choice assume that heritable variance exists among females in their mating preferences (Andenson, 1994), but few studies have carefully examined variation in female preferences. In their study of a
Texan Grylhis species, Wagner et al. (1995) demonstrated that
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