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Trade-Offs and Upper Limits to Signal Performance during Close-Range Vocal Competition in
Gray Tree Frogs Hyla versicolor.
Author(s): Michael S. Reichert and H. Carl Gerhardt
Reviewed work(s):
Source:
The American Naturalist,
Vol. 180, No. 4 (October 2012), pp. 425-437
Published by: The University of Chicago Press for The American Society of Naturalists
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vol. 180, no. 4 the american naturalist october 2012
Trade-Offs and Upper Limits to Signal Performance during
Close-Range Vocal Competition in Gray
Tree Frogs Hyla versicolor
Michael S. Reichert* and H. Carl Gerhardt
Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211
Submitted January 9, 2012; Accepted June 6, 2012; Electronically published August 16, 2012
Dryad data: http://dx.doi.org/10.5061/dryad.kq6kh.
abstract: Performance limitations on signal production constrain
signal evolution. Variation in signaling performance may be related
to signaler quality and therefore is likely to be a salient aspect of
communication systems. When multiple signal components are in-
volved in communication, there may be trade-offs between com-
ponents, and performance can be measured as the degree to which
signalers approach the upper limits of the trade-off function. We
examined vocal performance in the gray tree frog Hyla versicolor,in
which females prefer values of call duration and rate exceeding the
usual range of variation within and among males. We recorded in-
teractions between pairs of males calling on mobile platforms that
allowed us to manipulate intermale distance and place males in highly
competitive environments. We found that, although there was a clear
upper boundary on the ability of males to maximize call duration
and call rate simultaneously, call effort did not remain constant in
this highly competitive situation. Our estimates of an upper limit to
vocal performance were corroborated by analyses of calling behavior
in the context of close-range mate attraction. We discuss potential
constraints on signaling performance and the relevance of this mea-
sure of performance for both intrasexual and intersexual
communication.
Keywords: trade-offs, vocal performance, advertisement call, ener-
getics, competition.
Performance is an important concept in evolutionary bi-
ology, because it links morphological characteristics to
measurements of fitness (Arnold 1983; Irschick et al.
2008). Ultimately, an organism’s performance for any
given trait will be limited by trade-offs with other traits
(Stearns 1992; Roff 2002). Trade-offs themselves have im-
portant consequences for evolution because of the con-
straints that they place on the evolutionary trajectories of
* Corresponding author. Present address: Department of Biological Sciences,
University of Wisconsin, Milwaukee, Wisconsin 53201; e-mail:
reicherm@uwm.edu.
Am. Nat. 2012. Vol. 180, pp. 425–437. 䉷2012 by The University of Chicago.
0003-0147/2012/18004-53568$15.00. All rights reserved.
DOI: 10.1086/667575
phenotypic characteristics (Arnold 1992; Roff and Fair-
bairn 2007). Trade-offs have received the most attention
in studies of key life-history traits, such as growth and
survival (Reznick 1985; Stearns 1989; Sinervo and De-
Nardo 1996; Zera and Harshman 2001). However, trade-
offs can also be important for the performance of indi-
vidual behaviors that nonetheless have a large impact on
fitness, such as those related to foraging, parental care, and
mating (Andersson et al. 2002; Roff et al. 2003; Simmons
and Emlen 2006; Mitchell et al. 2007). Questions on the
general nature of trade-offs as well as the identification of
specific factors that determine the configuration of trade-
offs between traits are therefore significant for many as-
pects of organismal biology (Roff and Fairbairn 2007).
The competition for mates that is characteristic of sexual
selection plays an important role in the fitness of many
organisms (Andersson 1994). Because of this, performance
characteristics of morphologies and behaviors related to
mating are subject to potentially strong selection (reviewed
in Byers et al. 2010). At the same time, however, many of
the characteristics subject to sexual selection are integrated
within organisms in such a way that trade-offs in invest-
ment in different sexually selected characteristics are likely
(Simmons and Emlen 2006; Evans 2010; Engqvist 2011).
Models of life-history trade-offs show that, although trade-
offs are expected at the individual level, high between-
individual variation in the resources available to invest in
performance can break negative correlations between per-
formance traits at the population level (van Noordwijk
and de Jong 1986; de Jong and van Noordwijk 1992). Thus,
although there are trade-offs caused by upper limits to
performance, individuals may vary in their performance
abilities, and those individuals that can allocate more over-
all resources will be able to perform at a higher level (Ho¨g-
lund and Sheldon 1998; Lailvaux and Irschick 2006).
A major component of mate attraction in many species
is signaling behavior (reviewed by Andersson 1994; Ger-
426 The American Naturalist
hardt and Huber 2002; Greenfield 2002). Signals are en-
ergetically costly and mechanically constrained and are
thus expected to be subject to trade-offs (Ryan 1986, 1988;
Podos 1996). Specifically, multiple signal characteristics
may be important for mate attraction, but signalers may
be unable to simultaneously maximize the performance of
both characteristics if each is challenging to produce
(Podos et al. 2004, 2009). Such trade-offs between signal
characteristics have been described both within and be-
tween species in a variety of taxa (Shutler and Weatherhead
1990; Andersson et al. 2002; Badyaev et al. 2002; Gillooly
and Ophir 2010; Wagner et al., forthcoming). However, it
is also well known that signaling strategies vary with factors
in the social environment and, in particular, with the level
of competition (Wells 1988; Greenfield 2005; Price et al.
2006; Freeberg and Harvey 2008). Because of the costs of
increased performance, individual performance may be
maximized only under extreme conditions of high com-
petition (Irschick 2003; DuBois et al. 2009). Importantly,
this process of increased performance under high com-
petition implies within-individual variation in the invest-
ment in signaling performance. Thus, negative trade-offs
between signal traits may be broken not only by variation
between individuals that is related to differences in re-
source acquisition (van Noordwijk and de Jong 1986;
Shutler 2011), but also because there may be differences
in signal performance within individuals based on differ-
ences in the intensity of competition. The latter possibility
has received little attention (DuBois et al. 2009) but has
important implications for the understanding of signaling
performance, which in turn is an important component
of sexual selection in many organisms. In this article, we
address these issues by examining the role of competition
in signaling performance and trade-offs between acoustic
call characteristics in the gray tree frog Hyla versicolor.
In anuran amphibians, males gather in choruses and
broadcast loud advertisement calls to attract females (re-
viewed in Gerhardt and Huber 2002; Wells and Schwartz
2006). In many species in which males do not defend
territories, mate selection is based largely on female eval-
uation of call properties, and males alter various call char-
acteristics in response to vocal competition from other
nearby males (Wells 1988). Vocal competition has been
well-studied in H. versicolor (Fellers 1979; Wells and Taigen
1986; Runkle et al. 1994; Schwartz et al. 2002). Playback
studies and observations of artificial choruses revealed that
males trade off temporal properties of their advertisement
calls in response to changes in chorus density or in re-
sponse to similar changes in the calls of nearby neighbors
(Wells and Taigen 1986; Schwartz et al. 2002). Specifically,
with increasing competition, males increased the duration
of their calls while decreasing the rate at which they called
(Wells and Taigen 1986; Schwartz et al. 2002). Both call
duration and call rate are positively correlated with en-
ergetic expenditure (Taigen and Wells 1985), but because
call duration increased while call rate decreased, the total
amount of calling energy, or duty cycle, remained ap-
proximately constant (Wells and Taigen 1986). Other com-
ponents of advertisement calls that may be related to en-
ergetic output, such as call amplitude and call frequency,
do not vary with the level of competition (Gerhardt 1975,
1991; Love and Bee 2010). Females are more attracted to
long calls than to short calls, even when the duty cycles
of the two alternatives are equivalent (Klump and Gerhardt
1987; Gerhardt et al. 1996; Schwartz et al. 2001). Thus,
the changes in male calling behavior with increased com-
petition mirror female advertisement call preferences in
this species. Call duration has also been observed to in-
crease dramatically before amplexus when a male detects
a female via visual or tactile cues. Indeed, females usually
solicit amplexus by touching the male, which is not always
immediately successful in locating and clasping her. Dur-
ing this process, males often produce one or two excep-
tionally long calls, which were characterized by Fellers
(1979) as courtship calls.
The findings of earlier studies that there are trade-offs
between call duration and call rate that results in relatively
constant duty cycles were obtained under moderate levels
of vocal competition simulated by either the playback of
synthetic advertisement calls at an average distance away
from the subject (Wells and Taigen 1986) or by monitoring
the calling behavior of males in natural or artificial
choruses of moderate densities (Wells and Taigen 1986;
Schwartz et al. 2002). In average conditions, there may be
reduced demands on performance, such that most indi-
viduals may be capable of producing an adequate response
(Irschick 2003). Meaningful differences in male quality,
which are pertinent for studies of sexual selection in an-
urans (Welch et al. 1998), may be revealed only when
signaling performance is assessed in response to more chal-
lenging, highly competitive situations (Candolin 1999;
Penteriani 2003). Close-range vocal competition is a reg-
ular occurrence in this species’ choruses and may represent
an extreme challenge to vocal production abilities (Fellers
1979; Reichert and Gerhardt 2011). Thus, we determined
how vocal responses changed as the distance from their
nearest competitor was reduced to the point that the males
were calling at extremely close range. We specifically ex-
amined whether the negative trade-off between call du-
ration and call rate was maintained under high levels of
acoustic competition. In addition, we introduce a new
metric of vocal performance to the anuran literature by
describing the upper boundaries on the abilities of males
to simultaneously maximize call duration and call rate.
Similar upper boundaries on vocal production abilities
have been described for birdsong in several species and
Vocal Performance in Gray Tree Frogs 427
have been interpreted to reveal important morphological
constraints on signaling (Podos 1997, 2001; Podos et al.
2004, 2009; Cramer and Price 2007). Furthermore, the
deviation from the upper boundary of vocal performance
may itself be a signal that is attended to by receivers (Bal-
lentine et al. 2004; de Kort et al. 2009; DuBois et al. 2009,
2011). We determined whether such an upper boundary
exists for advertisement calling during close-range male-
male competition in H. versicolor and describe its potential
implications for communication in this species. We also
determined whether the estimated boundary applied to
another context in which elevated calling activity had been
observed by examining vocal performance during a short
period after simulated tactile contact with a female elicited
one or more courtship calls from a male.
Material and Methods
Experiment 1: Vocal Performance in
Male-Male Interactions
Experiments involving interactions between males were
conducted over three breeding seasons (May–July 2008,
May–June 2009, and April–June 2010). We captured male
Hyla versicolor from local ponds in Boone County, Mis-
souri, and transported them to an indoor greenhouse ar-
tificial pond facility for testing (for details, see Schwartz
et al. 2001; Reichert and Gerhardt 2011). Experiments were
performed nightly in ambient light conditions under the
glass roof of the greenhouse during the time of peak cho-
rusing activity (2100–0200 h). We stimulated males to be-
gin calling by placing them in the pond in the afternoon
and then simulating a rainstorm by means of a sprinkler
located above the pond. Chorus noise was broadcast from
a speaker located above the pond beginning at 2000 h.
These conditions ensured that large numbers of males
called on most nights.
Experimental Design. Calling males were placed individ-
ually atop one of several Styrofoam platforms scattered
throughout the pond. The platforms were surrounded by
a wire-mesh enclosure to prevent frogs from escaping be-
fore testing. Males that continued to call after being caged
were selected haphazardly for testing, and no attempts
were made to pair competitors on the basis of size. For
each test, we transported a pair of males from the pond
to a testing arena located approximately 3 m outside of
the pond. The arena consisted of a long runway (1.8 m
long, 0.3 m wide) in which single frogs were placed on
wheeled platforms situated on either end. We removed the
cage from each male before testing to allow them to in-
teract freely with one another.
We varied the intermale distance by pulling ropes at-
tached to each platform. We recorded calling at three sep-
arate positions. Males in the distant position were 1.8 m
apart, and we allowed each male to call at least 10 times
in this position. We then pulled the males toward one
another until they reached the intermediate position, in
which they were 0.9 m apart. We recorded 10 calls from
each male at the intermediate position and then pulled
the males toward one another until their platforms abutted
one another. At this abutting position, we recorded males’
calling as they engaged in competitive interactions over
the calling space. In some cases, these interactions escalated
to aggressive calling and physical fighting. In the abutting
position, we continued audio recording until one of the
males was determined to be the loser of the competitive
interaction because it either stopped calling for at least 5
min or moved at least one platform length away from its
competitor, which continued to call. Previous studies have
shown that body size plays a minimal role in these inter-
actions, but that certain aggressive-call characteristics may
be important in determining the outcome of contests
(Reichert and Gerhardt 2011; M. S. Reichert and H. C.
Gerhardt, unpublished data). These frogs have no weap-
onry, and we never detected any injuries resulting from
physical contact. The negative consequences for contest
losers are likely to be limited to a brief loss of calling time
while searching for a new calling space. Changes in ad-
vertisement calling performance before the resolution of
an interaction are, however, likely to affect a male’s chances
of attracting a female. Here, we examined the changes in
advertisement call properties that occurred with increased
competition as males were moved closer to one another.
We recorded each male’s calling throughout the exper-
iment onto separate channels of a digital audio recorder
(Marantz PMD-660 and PMD-661; 16-bit stereo PCM
files; 44.1 KHz sampling rate). Each male’s calls were re-
corded with a separate directional microphone (Sennheiser
ME-66, ME-67, and ME-80) mounted on a boom above
the platform. After all tests, we measured each individual’s
cloacal temperature. Males that participated in experi-
mental trials were given unique toeclips for individual
identification and were not used again in subsequent tests.
Males that were not used on any given night were main-
tained in captivity to serve as test subjects on subsequent
nights and generally were returned to their home popu-
lation within 7 days after capture. We recorded a total of
185 interactions, but our sample sizes did not always reach
this total, because not all males produced a sufficient num-
ber of calls at all positions (see below), particularly in the
abutting position, where they often gave few advertisement
calls before switching to aggressive calls.
Analyses of Temporal Call Characteristics. We measured ad-
vertisement call characteristics separately for each male at
428 The American Naturalist
each of the three positions using custom-designed software
(Signan, created by G. Klump and modified by D. Poleet)
that allowed for the automated analysis of the temporal
properties of advertisement calls. For some recordings,
high levels of temporal overlap of the subject males’ calls
precluded automated analysis. For these recordings, we
analyzed call characteristics manually with Raven Pro 1.3
software (Cornell Laboratory of Ornithology) on a per-
sonal computer. We also used the Raven Pro 1.3 software
to verify the accuracy of the values measured from Signan.
We measured the duration of each call. We calculated the
call period as the time between the onsets of consecutive
calls and used these values to determine call rate, which
was the reciprocal of call period, as the number of calls
per second. We calculated duty cycle, which was a measure
of calling effort, as the product of call duration and call
rate. Each characteristic was averaged separately for each
male at each position. Average call characteristics were
corrected to a common temperature (23.4⬚C) before sta-
tistical analyses using the parameters of linear regressions
between temperature and each call characteristic. For a
given male and position, we only included the mean call
characteristics in the data set if we obtained at least five
measures of that characteristic at that position. Thus, sam-
ple sizes varied depending on the specific position and the
call characteristic analyzed. Analyses of aggressive calls,
which males often produced in the abutting position in
addition to advertisement calls, will be presented elsewhere
(M. S. Reichert and H. C. Gerhardt, unpublished data).
All variables were checked for normality by examination
of Q-Q plots and Shapiro-Wilk tests before statistical test-
ing. Those variables that did not meet the assumption of
normality were transformed using an inverse square root
transformation. We used repeated-measures ANOVAs to
determine whether each advertisement call characteristic
changed across the three positions and therefore was af-
fected by the distance between males. Because responses
of the two individuals in each interaction cannot be con-
sidered to be independent from one another, we included
status as the winner or loser as an additional repeated-
measures factor, as suggested by Briffa and Elwood (2010).
We calculated full-factorial models that included the in-
teraction between position and contestant status.
Repeated-measures analyses generally failed to meet the
assumption of sphericity, and we thus present all Pvalues
for these analyses as the value after correction using the
Greenhouse-Geisser method. The purpose of this article
was to examine changes in advertisement call character-
istics with increased competition, and the division of data
points into the categories of winner and loser was done
primarily to obtain statistically independent groups for
analyses. The majority of the interactions we describe also
involved aggressive calling and, in some cases, physical
combat (Reichert and Gerhardt 2011); therefore, the ad-
vertisement call characteristics that we examined were un-
likely to be the sole determinants of individual success in
contests. Nonetheless, our data provide some insights into
contest behavior in this species by quantifying the extent
to which changes in advertisement call characteristics are
associated with contests.
Previous studies have demonstrated a trade-off between
call rate and call duration in H. versicolor (Wells and Taigen
1986; Schwartz et al. 2002). Females, however, prefer calls
that are both longer and delivered at higher rates (Gerhardt
et al. 1996; Gerhardt and Brooks 2009). Thus, we were
particularly interested in simultaneous changes in call du-
ration and call rate with position (see “Measures of Vocal
Performance”). We therefore graphed the change in call
duration against the change in call rate for each change
in position (distant to intermediate, intermediate to abut-
ting). Each quadrant of the graph corresponded to an
increase or decrease in one or both call characteristics with
proximity. We then quantified the number of males in
each quadrant to determine the distribution of proximity-
related changes in calling.
Measures of Vocal Performance. We measured vocal per-
formance by adopting the methods of Podos (1997, 2001).
Earlier studies (Wells and Taigen 1986; Schwartz et al.
2002) demonstrated a trade-off between call duration and
call rate in H. versicolor. Thus, we defined vocal perfor-
mance as the degree to which males simultaneously max-
imized both the duration and rate of their calls. To quantify
this, we divided call duration into bins of 100 ms and, for
each bin, determined the call duration with the maximum
call rate. We combined the call durations and call rates
across both contestants at all three positions to measure
the maximum limits of calling performance. We then en-
tered these maximal values as data points in a linear least
squares regression to calculate the upper bound of the
relationship between call duration and call rate. In one
case, a single male gave the maximum call rate for two
different call duration bins. In this case, we randomly se-
lected one of these values to drop from the analyses and
replaced this data point with the second-highest call rate
in that bin to ensure statistical independence. If there is
an upper boundary on the degree to which males can
simultaneously maximize call duration and call rate, then
the upper bound regression line should have a negative
slope, with the remaining data points assuming a trian-
gular distribution below the upper bound line.
We quantified each male’s vocal performance relative to
the upper boundary by measuring “performance devia-
tions,” defined as the orthogonal distance between each
male’s coordinate on the graph of call duration on call
rate and the upper bound regression line (Podos 2001).
Vocal Performance in Gray Tree Frogs 429
Table 1: ANOVAs of Hyla versicolor call characteristics
Call characteristic, effect df FP
Call duration:
Proximity 2, 214 45.12 !.001
Contestant 1, 107 1.49 .23
Proximity #contestant 2, 214 6.55 .004
Call period:
Proximity 2, 194 1.94 .16
Contestant 1, 97 2.37 .13
Proximity #contestant 2, 194 3.49 .047
Duty cycle:
Proximity 2, 194 40.17 !.001
Contestant 1, 97 .08 .78
Proximity #contestant 2, 194 8.05 .003
Performance deviation:
Proximity 2, 182 13.2 !.001
Contestant 1, 91 .94 .33
Proximity #contestant 2, 182 3.11 .06
Note: Repeated-measures analyses show the effects of prox-
imity, status of the contestant as winner or loser of the interaction,
and the interaction between proximity and contestant status on
each call characteristic. Call periods were not normally distributed
and were inverse square root transformed for the calculations
presented here. Pvalues are reported with the Greenhouse-
Geisser adjustment.
Larger performance deviations indicate males with rela-
tively lower performance compared with the upper limit
on vocal performance suggested by the upper bound re-
gression line. Males ( ) whose vocal performanceNp12
was above the regression line were assigned the negative
orthogonal distance between the point and the upper
bound line, which denoted mathematically that their vocal
performance deviated from the upper bound line in a
different direction than that of males whose vocal perfor-
mance was below the regression line. We used repeated-
measures ANOVAs to determine whether deviation from
the upper bound line could be explained by variation in
proximity, status as winner or loser of the interaction, and
the interactions between these variables.
Variation in both components of vocal performance, call
duration and call rate, is positively correlated with ener-
getic expenditure (Wells and Taigen 1986). Thus, we es-
timated the energetic costs of calling along the upper
bound line. We measured these costs indirectly by cal-
culating predicted duty cycles from the upper bound re-
gression equation across the range of call rates that we
observed in this study. We then converted these duty cycles
into predicted metabolic rates ( with units of mL
˙
V
O
2
) using the equation given by Wells and
⫺1⫺1
O#g#h
2
Taigen (1986) modified to account for our measurement
of call rates in the units of calls per second: ˙
V
O
p
2
. We plotted estimated duty0.092 ⫹9.216 #(duty cycle)
cycle and metabolic rate along the range of call rates to
illustrate the changes in the energetic cost of calling along
the upper bound line. Finally, we calculated estimated met-
abolic rates for each of the males in this study to obtain
an estimate of mean and maximum energetic expenditures
for comparison with previous studies of metabolic rates
in anurans.
Experiment 2: Vocal Performance and Courtship Calling
Calling performance in the context of courtship calling
was assessed by analyzing recordings (Nagra IV reel-to-
reel or Sony ProWalkman cassette recorders and Senn-
heiser 415 or ME80 microphones) made in the field in
1985 in a study of courtship calling (H. C. Gerhardt and
G. M. Klump, unpublished data). Briefly, a calling male
was touched once or twice with a hand-restrained male
or female gray tree frog after a series of approximately 10
advertisement calls had been recorded to provide a baseline
estimate of average call duration. The tactile stimulus elic-
ited exceptionally long calls from the male, which have
been described as courtship calls (Fellers 1979). In this
study, we analyzed 10 or more advertisement calls of eight
males following the production of at least one courtship
call. Although the sole focus of the unpublished study was
on courtship call duration and call duration after stimu-
lation, we noted at the time that the rate of advertisement
call output after stimulation was also highly elevated. Thus,
its analysis has provided an independent estimate of limits
to total vocal performance. We examined the change in
vocal performance after the production of courtship calls
by comparing the temporal properties of advertisement
calls given by males in the baseline and post-stimulus pe-
riods using paired t-tests.
Statistical Analyses. All statistical tests were performed in
SPSS software, version 16.0.1. We report two-tailed Pval-
ues, and we evaluated statistical significance using a cri-
terion of .ap0.05
Results
Experiment 1: Vocal Performance in
Male-Male Interactions
Changes in Temporal Call Characteristics. Repeated-
measures analyses of advertisement call characteristics
showed that there was a significant interaction effect of
proximity and contestant status on each call characteristic
(table 1). Call duration increased with decreasing intermale
distance for both winners and losers, but the rate of in-
crease was greater for losers (fig. 1A). Call period was
relatively constant across the three levels of proximity for
winners. For losers, however, although their call periods
430 The American Naturalist
0.1
0.13
0.16
Distant Intermediate Abutting
Performance deviation
0.1
0.15
0.2
0.25
Distant Intermediate Abutting
Duty cycle
5
6
7
Distant Intermediate Abutting
Call period (s)
0.7
0.8
0.9
1
Distant Intermediate Abutting
Call duration (s)
AB
CD
Figure 1: Changes in call characteristics with proximity. Data are shown separately for winners (filled circles, solid lines) and losers (open
circles, dashed lines). Circles represent mean values at each position, and error bars represent Ⳳ1 SE. A, Call duration ( ). B, CallNp108
period ( ). Statistical tests were performed on inverse-square-root–transformed call periods, but we present untransformed valuesNp98
in this figure. C, Duty cycle ( ). D, Performance deviation ( ).Np98 Np92
were similar to those of winners at the distant and abutting
positions, there was an increase in call period (i.e., a de-
crease in the rate of calling) at the intermediate position
(fig. 1B). Duty cycles showed a pattern similar to that of
call duration; they increased with decreasing intermale dis-
tance for both winners and losers, but the rate of increase
was greater for losers (fig. 1C).
With each change in position, the most common re-
sponse was for males to increase their call duration while
decreasing call rate (fig. 2). Nonetheless, a substantial mi-
nority of males either showed the opposite response, an
increased call rate with decreased call duration, or in-
creased both call rate and call duration simultaneously (fig.
2).
Upper Boundaries on Vocal Performance. Plots of call du-
ration against call rate revealed a triangular distribution
of data points with a clear upper bound for vocal perfor-
mance defined by the upper bound regression line (fig.
3A). The upper bound regression showed a strong and
significant negative relationship between call duration
and call rate (linear regression: , ,
Fp52.1 df p1, 12
, , ). A repeated-measures
2
bp⫺3.46 Rp0.81 P!.001
analysis of variation in performance deviation revealed that
the only factor that significantly affected performance de-
viation was proximity, although there was a nonsignificant
trend for an effect of the interaction between proximity
and contestant status on performance deviation (table 1).
Post hoc tests showed that males’ performance deviations
decreased as the distance between competitors decreased
(fig. 1D; paired t-test with Bonferroni adjustment: distant
vs. intermediate, , , ; distant vs.
tp3.53 df p249 P≤.001
abutting, , , ; intermediate vs.
tp5.31 df p249 P!.001
abutting, , , ). In other words,
tp3.42 df p249 Pp.003
on average, males increased their vocal performances as
they moved closer to one another.
The duty cycle, and thus the energetic cost of calling,
was not constant across the upper bound line (fig. 3B).
Individuals calling near either extreme of the upper bound
line had lower duty cycles and estimated metabolic rates
Vocal Performance in Gray Tree Frogs 431
-0.8
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
0.8
-0.5 -0.3 -0.1 0.1 0.3 0.5
CD +, CR -
N = 169/321
52.6%
CD -, CR -
N = 24/321
7.5%
CD +, CR +
N = 76/321
23.7%
CD -, CR +
N = 52/321
16.2%
-0.8
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
0.8
-0.5 -0.3 -0.1 0.1 0.3 0.5
CD +, CR +
N = 67/255
26.3%
CD +, CR -
N = 84/255
32.9%
CD -, CR -
N = 29/255
11.4%
CD -, CR +
N = 75/255
29.4%
A
B
Figure 2: Individual changes in call characteristics with position.
Each data point represents an individual male’s change in call rate
in calls per second (X-axis) and call duration in seconds (Y-axis)
from (A) the distant position to the intermediate position and (B)
from the intermediate position to the abutting position. The legend
in each quadrant shows the direction of change in terms of whether
the call rate and call duration increased or decreased and the number
and percentage of individuals that exhibited this pattern of call
change out of the total sample of males that called at both of these
positions.
than individuals calling near the center of the line. The
average (ⳲSD) metabolic rate (pooled across all males at
all positions, ) was .Np892 1.51 Ⳳ0.43 mL O /(g #h)
2
For the 14 data points used to calculate the upper bound
line, however, the average (ⳲSD) estimated metabolic rate
was . The largest estimated2.35 Ⳳ0.65 mL O /(g #h)
2
metabolic rate for any male at any position was 3.39
.mL O /(g #h)
2
Experiment 2: Vocal Performance and Courtship Calling
Courtship (long-duration) calls given in response to brief
tactile stimulation had an average duration of 2.43 s
( , range: 1.37–3.71 s). The duration of calls pro-Np11
duced in the post-stimulus period was significantly longer
than that of calls produced during the baseline period
(paired t-test, , , ). Because theretp4.92 df p7Pp.002
was no significant difference in call rate ( ,tp1.73 df p
, ), duty cycles were significantly greater in the7Pp.13
post-stimulus period than in the baseline period (tp
, , ). On average, males’ performance3.10 df p7Pp.017
deviations were lower in the post-stimulus period than in
the baseline period, but this difference was not significant
( , , ). Males’ post-stimulus calltp1.83 df p7Pp.11
characteristics largely fell along or near the upper bound
line that was estimated in experiment 1 (fig. 4).
Discussion
Competition, Trade-Offs, and Signal Performance
The allocation of resources into multiple traits is aproblem
faced by all organisms and has received a great deal of
attention in both theoretical and empirical studies (Stearns
1992; Roff 2002). The specific question of how animals
are expected to allocate resources into costly signaling dis-
plays in different contexts has received limited attention
(Kokko 1997; Polak and Starmer 1998; Lindstro¨m et al.
2009; Shutler 2011) yet is central to our understanding of
animal communication behavior and has important im-
plications for studies of sexual selection. Models of com-
munication strategies differ in the degree to which signals,
and by extension the allocation of resources toward sig-
naling behavior, are expected to vary in different contexts
(Enquist and Leimar 1983; Payne and Pagel 1996a, 1996b;
Payne 1998; Johnstone et al. 2009). Empirical studies in-
volving a variety of species show that animals often allocate
more resources to signaling under highly competitive con-
ditions (Griffith and Sheldon 2001; Reading and Backwell
2007; Gautier et al. 2008; Wong and Svensson 2009; Ga-
vassa et al. 2012), although the precise relationship be-
tween resource allocation and signal escalation is rarely
described. Given current debates in the literature regarding
signaling strategies in both agonistic and mate-choice con-
texts (Arnott and Elwood 2009; Briffa and Elwood 2009;
Johnstone et al. 2009; Botero et al. 2010), explorations of
signal variability in competitive contexts are an important
432 The American Naturalist
0
0.3
0.6
0.9
1.2
1.5
1.8
0 0.1 0.2 0.3 0.4 0.5
Call duration (s)
Call rate (calls/s)
A
B
0
1
2
3
0
0.1
0.2
0.3
0 0.1 0.2 0.3 0.4 0.5
Estimated VO2 (ml/(g·hr)
Estimated duty cycle
Call rate (calls/s)
Figure 3: A, Plot of call rate on call duration illustrating the upper
boundary of vocal performance for males calling in staged interac-
tions (experiment 1) in Hyla versicolor. Each data point (open circles)
represents an individual male’s mean temperature-corrected call rate
and call duration. The data points that contributed to the upper
bound regression are marked as filled squares. Trend line is the linear
least squares regression line calculated from the upper bound data
points ( ). ; data combined acrossyp⫺3.461x⫹1.9826 Np892
both competitors at all positions. Data points that contributed to
the upper bound line are independent of one another. B, Relationship
between duty cycle, metabolic rate, and call rate at the upper bound
line. Duty cycles were calculated across the range of call rates by
multiplying call rate by the call duration estimated from the upper
bound regression equation. Metabolic rates ( ) were calculated
˙
V
O
2
using the formula given in Wells and Taigen (1986) converted for
duty cycles calculated from a call rate with the units of s
⫺1
:
. Duty cycles and estimated en-
˙
V
O
p0.092 ⫹9.216 #(duty cycle)
2
ergetic costs are not constant along the upper bound line but instead
are lowest at the extremes of the line. The peak duty cycle is at an
intermediate value.
starting point for understanding the relationship between
variation in resource allocation and signaling strategies.
Here, we found that high levels of acoustic competition
led many male Hyla versicolor to increase their overall
calling effort, thus breaking the usual within-individual
trade-off between call duration and call rate. Vocal per-
formance was also highest at the most extreme levels of
competition. These data support the hypothesis that sig-
naling performance is modulated by the social context of
communication.
In general, trade-offs are expected between traits whose
expression depends on allocation from a common pool of
resources (Stearns 1992; Roff 2002). However, many stud-
ies examining traits that were expected to be subject to
trade-offs found either a lack of a negative relationship
between traits or, in some cases, even a positive relation-
ship between traits (Reznick et al. 2000; Bertram 2007;
Ornelas et al. 2009). This paradox has been addressed by
the “Y model” of van Noordwijk and de Jong (1986),
which describes the conditions that favor trade-offs be-
tween traits. In this model, the strength and direction of
the correlation between two traits depends on the relative
amounts of variation in the acquisition of resources and
in the allocation of those resources among traits. When
variation in acquisition is large relative to variation in
allocation, then a positive correlation is expected between
two traits, whereas the opposite is expected when variation
in acquisition is small relative to variation in allocation
(van Noordwijk and de Jong 1986). Most previous studies
examined trade-offs at the population or interspecific level;
that is, the trade-off was measured by determining the
relationships between traits measured either between av-
erage values of individuals or species, respectively (Shutler
and Weatherhead 1990; Karlsson and Johansson 2008;
Blomquist 2009; Ornelas et al. 2009). In this study, we
found evidence for a trade-off at the population level but
not at the level of the individuals sampled. Thus, the Y
model may also apply within individuals. Using this frame-
work, we suggest that within-individual trade-offs were
not observed, because high levels of competition resulted
in large variation within individuals in the resources made
available for allocation into the two different call char-
acteristics. That is, individuals may be willing to invest
different amounts of resources in different situations, and
if variation in resource investment is sufficient, then trade-
offs between traits measured in a static situation may break
down when trait relationships are examined across mul-
tiple contexts. We hypothesize, therefore, that social com-
petition may be an important variable to take into account
in studies of trade-offs and suggest that future studies
address this possibility in a wide variety of species.
Constraints on Signal Performance
Although we argued above that, in close-range competi-
tion in H. versicolor, duty cycle is not fixed and call rate
and call duration can vary somewhat independently of one
another, our examination of the distribution of call rates
and call durations across males suggests a clear upper
bound on the abilities of males to simultaneously maxi-
Vocal Performance in Gray Tree Frogs 433
0
0.3
0.6
0.9
1.2
1.5
1.8
0 0.1 0.2 0.3 0.4 0.5
Call Duration (s)
Call Rate (calls/s)
Figure 4: Plot of call rate on call duration for experiment 2, in which
we examined the response of males to tactile cues simulating a female
solicitation of amplexus. Call characteristics during the baseline pe-
riod are denoted by an X, and those during the post-stimulus period
are denoted by an open circle. The upper bound line determined
from male call characteristics in experiment 1 (see fig. 3A) is included
for comparison.
mize these two call characteristics. The distribution of data
points on the plot of call duration on call rate (fig. 3A)
is remarkably similar in shape to distributions obtained
for vocal performance trade-offs in several bird species
(Podos 1997, 2001; Ballentine et al. 2004; Beebee 2004;
Illes et al. 2006; Cardoso et al. 2007; Cramer and Price
2007). In birds, a significant negative upper bound re-
gression has been interpreted as evidence for mechanical
limits on the ability to simultaneously maximize two call
parameters (Podos 1997, 2001; Podos et al. 2004, 2009).
We argue that our data demonstrate an upper limit on
vocal performance as well, but additional study will be
required to determine what factors are responsible for lim-
iting performance.
The two most likely factors that could limit vocal per-
formance in H. versicolor are mechanical constraints, as
proposed in previous studies of vocal performance in birds
(Podos 1997, 2001), and energetic constraints, which have
been discussed in previous studies of vocal performance
in frogs (Taigen and Wells 1985; Wells and Taigen 1986;
Schwartz 1989; Prestwich 1994; Schwartz et al. 2002; see
also Byers et al. 2010). The mechanics of call production
in anurans remain understudied (Martin 1972; McClelland
et al. 1996), and additional experiments will be necessary
to demonstrate the role of mechanics on setting upper
limits of vocal performance. Based on previous studies of
calling energetics, we estimated that some males incurred
very high energetic costs of calling. The maximum met-
abolic rates that we estimated for calling males were up
to 40 times greater than the average resting metabolic rate
of measured in an earlier study in H.0.08 mL O /(g #h)
2
versicolor (Taigen and Wells 1985) and over twice as large
as metabolic rates estimated from average levels of calling
(Wells and Taigen 1986; this study). However, duty cycles,
and therefore the predicted energetic costs of calling, were
not constant along the upper bound line (fig. 3B). Thus,
under our current understanding of the energetic costs of
calling in H. versicolor, the upper bound line cannot be
considered to represent an absolute limit to short-term
energetic expenditures.
The Natural Relevance of Signal Performance
The idea of signaling performance is important in studies
of animal communication because of the possibility that
performance is linked to some underlying quality of the
signaler that is relevant to receivers (Searcy and Nowicki
2005). The relationship between performance and signaler
quality has received a great deal of attention for individual
signal traits (Welch et al. 1998; Brandt 2003; Hoefler et al.
2009). More recently, however, theoretical and empirical
studies have emphasized the importance of multiple signal
traits and interactions between signal traits as indicators
of signaler quality (Candolin 2003; Scheuber et al. 2003;
Hebets and Papaj 2005; Bro-Jørgensen 2010; Byers et al.
2010). Trade-offs that exist between signal traits create an
axis of signal variation that can be measured as the degree
to which individuals’ signals approach the upper boundary
line that describes the trade-off. This axis may better rep-
resent signaler quality than that for any individual signal
characteristic. Therefore, receivers may be attentive to sig-
nal performance for multiple signal traits and may in fact
directly attend to deviations from upper boundaries on
the simultaneous performance of multiple signal charac-
teristics. Indeed, the responses of rivals and females of
several bird species during the evaluation of singing males
vary with the song’s distance from the upper boundary of
calling performance (Ballentine et al. 2004; de Kort et al.
2009; DuBois et al. 2009, 2011). Whether this is a more
general phenomenon remains to be studied.
Our data show that signaling performance during in-
tense interactions overrides trade-offs between acoustic
components of advertisement calls in H. versicolor. Males
increased their vocal performance in two specific contexts
that are highly likely to affect their chances of obtaining
a mate. Although earlier studies described a trade-off be-
tween the components of vocal performance (i.e., an in-
crease in call duration and a decrease in call rate) mediated
by the density of competitors (Wells and Taigen 1986;
Schwartz et al. 2002), both contexts in which we observed
434 The American Naturalist
a breakdown of the within-male trade-off in vocal per-
formance, close-range interaction with rivals and mate at-
traction, are extreme situations that can occur indepen-
dently of chorus density. Moreover, the changes in call
characteristics (i.e., increases in both call duration and call
rate) with increased competition were in the direction fa-
vored by female preferences measured in previous studies
(Klump and Gerhardt 1987; Gerhardt et al. 1996; Gerhardt
and Brooks 2009). Because these preferences were mea-
sured in controlled laboratory conditions with no back-
ground chorus noise, the preferred call characteristics do
not appear to give males an advantage in terms of their
detectability within the chorus (Schwartz et al. 2008).
Thus, the evidence is consistent with female preferences
for vocal performance itself in H. versicolor. Why females
have such preferences remains an open question.
Finally, we note that few studies have considered the
long-term implications of within-individual adjustments
in signaling performance. Regardless of the proximate ba-
sis of the performance limit, bouts of high-performance
signaling are likely to affect subsequent signaling behavior.
These effects on subsequent behavior may be seen both
on specific signal characteristics and on the likelihood that
an individual continues to signal over time. Short-term
increases in signal performance may be a necessary aspect
of individual bouts of close-range competition, but indi-
viduals engaging in such behavior may pay costs in the
long term if their signal function in future bouts is im-
paired. Thus, in addition to immediate trade-offs between
individual signal characteristics, the communication sys-
tems of H. versicolor and other animals that signal for long
periods of time are likely to involve longer-term trade-offs
in which increased signal performance at one point in time
leads to reduced signal performance in the future. This
question can be addressed by manipulations of perfor-
mance in simulated close-range challenges, as in this study.
This largely unexplored possibility (Ho¨glund and Sheldon
1998) has parallels in the life-history theory of trade-offs
between current and future activities, such as reproductive
investment (Williams 1966; Bell 1980). In general, more
study is needed regarding the causes and consequences of
trade-offs at multiple levels on signal characteristics. Our
results suggest that an important consideration in such
studies is the intensity of competition, which can have a
strong influence on the relationship between the traits that
determine signaling performance.
Acknowledgments
We thank F. Barbosa and two anonymous reviewers for
helpful comments on previous drafts of this manuscript.
T. Drew, N. Fowler, D. Gruhn, C. Harjoe, W. Li, and B.
Nickelson provided assistance with behavioral trials and
call analyses. Members of the Gerhardt laboratory assisted
with frog collection and testing and provided general ad-
vice on experimental techniques. G. Klump contributed
to the design and execution of the tests of male reactions
to female proximity. Financial support was provided by a
National Science Foundation Doctoral Dissertation Im-
provement Grant to H.C.G. and M.S.R. (IOS-1010791);
grants from the Chicago Herpetological Society, the Gaige
Fund of the American Society for Ichthyologists and Her-
petologists, and a Dean E. Metter Memorial Award from
the Society for the Study of Amphibians and Reptiles to
M.S.R.; and a Graduate Assistance in Areas of National
Need fellowship from the University of Missouri and the
U.S. Department of Education (P200A070476).
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Associate Editor: Thomas N. Sherratt
Editor: Mark A. McPeek
A calling male gray tree frog. Photograph by Carl Gerhardt.
