Behavioral
Ecology
The official journal of the
ISBE
International Society for Behavioral Ecology
doi:10.1093/beheco/art024
Advance Access publication 1 April 2013
Original Article
Condition-dependent signaling and adoption
of mating tactics in an amphibian with
energetic displays
Sarah C. Humfeld
Division of Biological Sciences, University of Missouri, 213 Tucker Hall, Columbia, MO 65211-7400,
USA
Most alternative reproductive phenotypes are interpreted as alternative tactics within a conditional strategy: all individuals are predicted to
choose among behavioral tactics based on some measure of their physiological condition or competitive status. The factors determining a
male’s tactic at any particular time are generally unknown. Thus, most researchers have measured potential correlates of competitive ability
(such as male body size) rather than directly measuring fighting ability, for example, in males adopting alternative mating tactics. In species
in which sexual competition primarily involves production of acoustic signals, an individual’s choice of mating tactic may largely depend
on physical characteristics, such as age, strength, or condition, which determine its ability to compete acoustically by producing attractive
calls. Male green tree frogs (Hyla cinerea) often switch tactics (caller or satellite), but body size changes very little during the breeding season. I tested the hypothesis that mating-tactic switches are mediated via the effects of changing body condition on advertisement call characteristics. My field study shows that the switch between tactics is predicted by condition but not by size. Moreover, short-term changes in
body weight result in condition-dependent changes in several properties of the advertisement call. The demonstration of condition-dependent advertisement calling and tactic adoption links a physical characteristic correlated with mating-tactic adoption with actual competitive
status (calling performance). Vocal fatigue may constrain males to produce relatively unattractive advertisement calls, thus increasing the
potential fitness payoffs associated with adoption of the satellite tactic.
Key words: acoustic communication, condition, Hyla, mating tactics, vocal fatigue. [Behav Ecol]
Introduction
In many species, male reproductive behavior is manifest in 2 or
more distinct phenotypes (Andersson 1994; Shuster and Wade
2003; Oliveira et al. 2008). If intense sexual selection limits the proportion of males that can successfully employ the dominant mating
tactic (Kodric-Brown 1986), adoption of less common alternative
male mating behaviors may represent different solutions to the
problem of obtaining mates (Shuster and Wade 2003). Most alternative reproductive phenotypes are interpreted as alternative tactics within a conditional strategy, in which individuals are predicted
to choose among mating tactics based on their competitive status
(Dominey 1984; Gross 1996). Although individuals probably possess heritable variation in their responsiveness to environmental or
physical cues that can influence this “decision” (Hazel and Smock
2000; Shuster and Wade 2003), the theory generally predicts
that an individual’s age, size, or condition at any particular time
Address correspondence to S.C. Humfeld. E-mail: humfelds@missouri.
edu. Received 1 February 2012; revised 21 February 2013; accepted 26
February 2013.
© The Author 2013. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved. For
permissions, please e-mail: [email protected]
will determine its competitive status and hence the probability of
adopting an alternative tactic (Dawkins 1980; Oliveira et al. 2008).
In many instances, the facultative adoption of an alternative
mating tactic appears to depend on a male’s ability to compete
directly with other males for access to mates (reviewed by Oliveira
et al. 2008). For example, in mating systems in which males
compete directly for females or for resources needed by females,
large males may be better fighters than small males and thus
better able to secure and defend territories required by females
(e.g., Alcock 1979; Howard 1984). Indeed, most studies of size and
condition-dependent tactic use have been conducted in species that
engage in aggressive male interactions (frogs: Halliday and Tejedo
1995; Wells 2007; insects: Brockman 2008; fish: Taborsky 2008;
nonprimate mammals: Wolff 2008).
In many other animals, female choice may also strongly affect
male mating success (Andersson 1994). In species with lek mating systems, where both intra- and intersexual competition influence mating success and females do not receive any direct benefits
from males, the quality of sexual advertisement signals is often a
major determinant of a male’s competitive status. In circumstances
when a male can only produce relatively unattractive signals, the
Behavioral Ecology
860
likelihood that it will adopt a nonsignaling tactic is predicted to
increase (Arak 1988). Surprisingly few studies have considered
the role of intersexual interactions in the expression of alternative
reproductive tactics (Henson and Warner 1997; Alonzo 2008).
In this study, I addressed the question of whether size and
condition influence the choice of a male’s mating tactic via their
effects on the quality of the male acoustic advertisement display. This question is particularly tractable in systems where the
choice of an alternative mating tactic is behaviorally mediated
over a short timeframe rather than developmentally determined.
Here, short-term changes in physical traits, display quality, competitive environment, and mating behavior can be directly correlated within a particular individual. Acoustic signaling is a
distinctive aspect of the mating systems of most anuran amphibian (frog) species. Many of these have prolonged breeding seasons in which males do not defend territories and female choice
and endurance rivalry are the dominant forms of sexual selection (Andersson 1994; Wells 2007). Male reproductive success
probably depends on a male’s ability to maximize chorus participation (Halliday and Tejedo 1995) and attract females via call
production (Gerhardt and Huber 2002). Acoustic contest competition between nearby callers serves to maintain spatial separation, which, in turn, decreases acoustic interference and masking
(Gerhardt and Huber 2002). In a variety of anuran amphibians,
some males, termed “satellites,” remain silent in close association
with a calling male and attempt to intercept females attracted
to that calling male (Perrill et al. 1978; Gerhardt et al. 1987).
I hypothesized that short-term mating-tactic decisions are mediated, in part, via the effects of size and condition on a male’s ability to compete acoustically for access to mates.
Absolute body size is frequently observed as a correlate of mating-tactic choice in frogs (Andersson 1994; Oliveira et al. 2008).
Size-dependent patterns of tactic adoption might arise if 1) females
assess acoustic displays to identify large males (e.g., Morris and
Yoon 1989) or 2) large males successfully defend calling sites (e.g.,
Howard 1984). If size impacts the ability to compete using acoustic
signals, it might explain the observation that the satellite males of
some frog species are smaller than other calling males (Forester and
Lykens 1986; Gerhardt et al. 1987; Moravec 1987), even though
these species tend to lack high levels of physical aggression (Wells
2007). In fact, dominant frequency is inversely correlated with body
size (Martin 1971) and is a property that influences female choice in
many species (Gerhardt and Huber 2002).
Size does not, however, appear to constrain tactic choice in many
species of hylid frogs (Fellers 1979; Perrill 1984; Roble 1985), in
which males switch tactics between and within nights (reviewed in
Zamudio and Chan 2008). Because males of these species grow
very little during the breeding season (Given 1988), body size per se
is unlikely to be the sole determinant of mating-tactic choice over
such short timescales. Because many sexual displays are presumed
to be energetically expensive in order to maintain signal honesty
(Zahavi 1977), energetic reserves required for signal production
might also impact the adoption of low-cost alternative mating tactics (Wells 2001). The high energetic cost of calling (Taigen and
Wells 1985; Prestwich et al. 1989) and resulting short-term changes
in body mass (Table 1; reviewed in Halliday and Tejedo 1995) are
well documented. Aside from some limited evidence indicating that
satellite males of some species are prevented from calling purely
through energetic constraints (Robertson 1986; Leary et al. 2004),
there is no evidence to assess the hypothesis that males in poor condition switch tactics because they produce relatively unattractive
advertisement signals (Gerhardt and Huber 2002; Wells 2007;
Lucas and Howard 2008).
I addressed condition dependence of mating-tactic expression in
the North American green tree frog, Hyla cinerea, a species in which
individual males dynamically switch between calling and satellite
mating tactics. I tested for size and condition dependence of tactic
adoption by experimentally manipulating the competitive environment of satellite males in the field. To assay the effects of size and
condition on advertisement calls, I analyzed field recordings and
conducted a repeated-measures feeding experiment in the laboratory. I predicted that 1) condition, but not size, affects short-term
behavioral switches in tactic and 2) short-term reductions in body
condition affect the quality of advertisement calls. Rather than simply assuming that tactic-specific physical differences correlate with
differences in male competitive status, my study, taken together with
published accounts of female acoustic preferences in this species, is
one of the first to examine condition-dependent tactic choice based
on the quality of a male’s sexual advertisement signal.
Materials and Methods
Study system
In the green tree frog (H. cinerea), males aggregate in a breeding
chorus and call vigorously. Mate selection mainly rests with the
females, which exhibit strong preferences for frequent, loud, and
low-pitched calls (Höbel and Gerhardt 2003; Humfeld 2008).
The incidence of satellite behavior is fairly high in this species; on
average, 16% of calling males are associated with at least 1 satellite
(Perrill et al. 1978; Gerhardt et al. 1987). Males switch between
calling and satellite tactics both within and between nights (Perrill
et al. 1982; Gerhardt et al. 1987; personal observations). Satellite
males are smaller, in poorer condition, and produce advertisement
calls higher in frequency and shorter in duration than calling males
(Humfeld 2008).
In this study, satellites were identified in the field as noncalling males
with a deflated throat pouch, positioned within 50 cm of another calling male. Associations between callers and satellites last 30 min on
average, and satellites resume calling or move toward another caller
within 5 min if the calling male is removed (Perrill et al. 1982). Hence,
as in other studies of green tree frogs (Perrill et al. 1978), I defined a
stable satellite association as one that lasted at least 5 min. I observed
the mating behaviors used by male frogs in 2 populations located 35
km apart in southeastern Missouri: Mingo National Wildlife Refuge
(Wayne Co.) in 1999 and Otter Slough Conservation Area (Stoddard
Co.) in 2000 and 2002.
Size-dependent and condition-dependent
mating-tactic adoption
I experimentally manipulated the social setting of a satellite in
order to determine whether size or condition influence the adoption of the calling tactic.
General methods
I located and measured satellite males and calling males in the field
between May and July of 1999 and 2000. Once a satellite association was identified, the frogs were captured by hand and measured.
Each male’s tibia–fibula length (TFL) was measured to the nearest
0.1 mm using dial calipers. After applying pressure to purge water
from the bladder (Buchanan and Taylor 1996), I determined body
weight to the nearest 0.1 g using a Pesola spring balance. A unique
Humfeld • Condition-dependent signaling and mating-tactic adoption
861
Table 1 Published reports of percentages of body weight lost during chorus attendance Species
Nightly weight loss (%)
Chorus tenure weight loss (%)
Reference
Rana catesbeiana
Rana clamitans
Rana temporaria
Hyla gratiosa
Bufo bufo
Bufo calamita
0.57
0.18
0.50
0.99
1.07
0.32
1.71
0.87
0.5
~1.00
—
—
25
—
21
13
7
4.5
20
30
Judge and Brooks (2001)
Wells (1978)
Ryser (1989)
Murphy (1994)
Arak (1983a)
Arak (1983b), Tejedo (1992)
Bufo rangeri
Crinia signifera
Uperoleia rugosa
combination of 2 toes was removed for future identification of
the male.
Methods of calculating condition share the common goal of controlling for absolute body size (i.e., length) when comparing weight
across individuals (Jakob et al. 1996). Authors usually infer that individuals in good condition possess greater quantities of metabolizable tissue (and water) than lighter individuals (Schulte-Hostedde
et al. 2001). I calculated residual condition indices from the regression of log-transformed measures of body weight on TFL to estimate the nutritional state of males. This type of index does not vary
with body size (Jakob et al. 1996; Băncilă et al. 2010) and these condition indices were subsequently used in further statistical analyses
(Schulte-Hostedde et al. 2005). To aid in interpretation, I present figures and summary statistics using untransformed residuals.
Caller-removal experiment
To examine the condition dependence of tactic use within a single
night, I compared the physical characteristics of males solely pursuing
the satellite tactic with those of males that switched from the satellite
to the calling tactic. After capturing the calling male from a satellite
association, I confined it temporarily in a small plastic container. The
subsequent behaviors of the satellite male (commencement of advertisement call production or remaining motionless and noncalling)
were observed. I compared the size and condition of satellite males
that resumed calling with those that remained silent using a multiple
logistic regression.
Cherry (1993)
Lemckert and Shine (1993)
Robertson (1986)
relative to the other harmonics, the low- and high-frequency peaks
typically have about the same relative amplitude (Gerhardt 1981).
The sidebands are asymmetric around the harmonics due to filtering in the vocal tract (Oldham and Gerhardt 1975). The duration
of the call ranges from 120 to 200 ms, and males regularly repeat
these calls at a rate between 85 and 120 calls/min (Gerhardt 1987).
I analyzed 10 consecutive calls from the middle of each male’s
recording session using a Kay DSP Sona-graph Model 5500. In
the oscillograph mode, I determined call duration and call rate
based on visual assignment of signal onset and offset within a 1sec window (512 pt, 10 ms resolution). Call effort was derived by
multiplying call duration by call rate. In the power spectrum
mode, I used a narrowband analysis to resolve spectral information
(1024 pt Hamming, 5 Hz resolution) and measured the frequency
and relative amplitude of the 2 main spectral peaks. Males generally
called from perches on emergent vegetation (Cephalanthus) above the
water surface, and as there is effectively no differential attenuation
Condition-dependent advertisement calling
To determine whether any characteristics of advertisement calls
are size or condition dependent, I recorded and analyzed calls produced by males observed in the field and in a laboratory feeding
experiment.
General methods
I recorded at least 20 consecutive advertisement calls from each
male under ambient light conditions using a Sony professional
walkman cassette recorder (WM-D6C) and a Sennheiser directional microphone (ME-66) with windscreen positioned 50–100 cm
from the calling frog. The advertisement call produced by male
H. cinerea is a relatively short broadband signal (Figure 1a) consisting of a series of harmonically related components and sidebands (Figure 1b). The low-frequency peak is the fundamental of
the harmonic series and consists of a single component located
between 640 and 1340 Hz (Oldham and Gerhardt 1975). The
high-frequency peak is the third harmonic, ranging between 2200
and 3600 Hz. Although the second harmonic is greatly attenuated
Figure 1 Oscillogram (a) and power spectrum (b) of natural Hyla cinerea advertisement
calls. Advertisement calls averaged 140 ms in duration with a repetition
rate of 110 per min. In the power spectrum, note the single low-frequency
spectral component located at 800 Hz and the high-frequency spectral
component located near 3000 Hz.
862
of frequencies below 9 kHz from elevated sound sources (Gerhardt
1981; Schul and Patterson 2003), small variations in recording
distances should not have affected values of the relative peak
amplitudes.
Field recordings
In addition to recording advertisement calls during 1999, 2000, and
2002, I also measured sound pressure level (SPL in decibels [dB] re
20 µPa) at a distance of 50 cm from the frog with either a Radio
Shack analog (2000) or CEL-383 integrating impulse (2002) sound
level meter (C-weighting, fast RMS). For statistical analyses, measurements in decibels were first converted to a linear measure (µPa)
and subsequently reconverted to dB SPL for the summary statistics.
Ambient environmental temperatures can impact the characteristics of acoustic signals produced by ectothermic animals (reviewed
in Gerhardt and Huber 2002). In order to determine how much
variation is explained by this variable, I measured the dry-bulb air
temperature to the nearest 0.1 °C at each male’s calling location
immediately after his calls were recorded. The average temperature
was 24.9 °C, ranging between 18.6 and 28.6 °C (N = 171). Five of
the call characteristics exhibited temperature dependence to some
extent (P < 0.05); therefore, temperature was used as a variable in
the multiple regression analyses described below.
In order to assess the condition dependence of advertisementcall properties, I computed a multiple regression of body condition, TFL, and temperature on 7 call variables measured from each
male’s first observation (Murphy 1999): low- and high-frequency
spectral components, relative amplitude of spectral components,
call duration, call interval, call effort, and amplitude. Using data
from the subset of males recorded on at least 2 nonconsecutive
nights (average interval = 6 nights, N = 44), I conducted multiple
regression analysis to examine the effects of within-male changes in
weight and TFL on changes in call properties. I used partial regression coefficients to determine the magnitude to which length or
condition predicted call characters. The data were transformed as
necessary to meet parametric assumptions.
Repeated-measures feeding experiment
To more closely examine the effects of body condition on characteristics of advertisement calls, and in an attempt to remove any
confounding effects of different calling environments, I conducted
feeding experiments during the summers of 2001–2003, in which
males were induced to call over the course of several nights in an
artificial pond (description in Schwartz et al. 2002). Call characteristics were compared within the same frog across nights and correlated with changes in body weight.
Males used in this experiment were collected from Otter Slough
Conservation Area early in the breeding season and housed in
the animal care facility at the University of Missouri. I marked
each male uniquely by freeze branding an identification number on its dorsum. I placed groups of 8–10 males in the artificial
pond for up to 5 consecutive nights and induced them to produce
advertisement calls by broadcasting chorus noise from a 30-W
speaker (Radio Shack Omnidirectional Outdoor Speaker, model
OD607) suspended above the center of the pond. On a nightly
basis, I recorded at least 20 consecutive advertisement calls from
each calling male. At the end of each night, males were collected,
weighed to the nearest 0.01 g using an O’Haus portable electronic
balance, and returned to the artificial pond. The temperature was
stable from night to night (27.8 ± 0.6 °C, average ± 1 SD), so air
temperature was not used in analyses.
Behavioral Ecology
Feeding Experiment I—long-term feeding regime. In 2001
and 2002, I haphazardly assigned males to 1 of 2 long-term
feeding regimes. Throughout the summer, males in the high-food
group were fed 3 crickets each, 3 times a week and males in the
low-food group were fed 3 crickets each, once a week. No animals
were observed to fall below the minimum condition observed in
the field (weight/[TFL]3 = 0.0005). Males in both treatments were
not fed during the interval they were calling in the artificial pond.
I assessed the effects of changing body weight on call characteristics
using regression analysis.
Feeding Experiment II—nightly feeding regime. In 2003,
I assigned comparably sized males to 1 of 2 treatment groups in
which they either received no food while they were in the artificial
pond or were fed 1 cricket at the end of each night when they
were in the artificial pond. All males were fed ad libitum while in
animal care. I conducted a repeated-measures analysis of variance
(ANOVA) using call data from the male frogs that produced
advertisement calls on at least 3 nights.
Results
Condition-dependent mating-tactic adoption
I identified 28 satellite associations. Sixteen of these satellite males
resumed calling after the associated caller was removed. Condition
but not TFL was related to this switch. A test of the full multiple
logistic regression model was statistically significant, indicating
that TFL and condition reliably distinguished between behavioral responses (Χ2 = 7.19, df = 2, P = 0.027). The Wald criterion
demonstrated that only condition made a significant contribution
(Χ2 = 5.0, P = 0.028). Satellite males that resumed calling were
in significantly better condition (−0.17 ± 0.76 g, untransformed)
than satellites that remained silent (−0.80 ± 0.38 g, untransformed)
(F1,26 = 7.75, P = 0.010), and visualization of the logistic relationship between condition and resumption of calling indicates that
satellites should resume calling when their (untransformed) residual
condition is above −0.65 g (Figure 2).
In the course of recording advertisement calls (see below), I was
able to document within-male patterns of growth and fluctuation
in body weight. In the 44 calling males observed on multiple nights
(range: 2–8 nights), TFL remained unchanged, even at interobservation intervals of up to 18 days (Figure 3a). Males that participated in the breeding chorus on more than 1 night exhibited large
fluctuations in weight (Figure 3b), ranging between gains of 25%
and losses of 15%, corresponding to daily changes between −4.9%
and +9.7%. There was no relationship between interobservation
interval and amount of weight lost.
Condition-dependent advertisement calling
Field recordings
To determine whether changes in body weight could mediate
mating-tactic switches via condition-dependent calling, I made
body measurements and advertisement-call recordings from 182
H. cinerea males over 3 years (1999: N = 55; 2000: N = 52; 2002:
N = 75). The results of multiple regression analyses exploring how
between-male variation in TFL, weight, and temperature affected
variation in call characteristics are reported in Table 2. The results
of multiple regression analyses based on within-male data from 41
frogs that were recorded on at least 2 nights (1999: N = 27; 2000:
N = 8; 2002: N = 6) are presented in Table 3.
Humfeld • Condition-dependent signaling and mating-tactic adoption
Figure 2 Physical correlates of behavioral switchpoints. The line indicates the
condition threshold at which males are predicted to switch tactics when
levels of local acoustic competition change. Simple logistic regression of
tactic switching (1 = satellite resumes calling, 0 = satellite remains silent)
with TFL (a) and condition (b).
Amplitude. Call intensity varied widely among males (2000:
N = 47, average 88.3 dB SPL, range 82–92 dB SPL; 2002:
N = 71, average 88.9 dB SPL, range 84–93 dB SPL). Multivariate
analyses showed that length, but not condition or temperature,
significantly explained between-male variation in call amplitude
(2000: R2 = 0.33, F3,37 = 6.15, P = 0.002; 2002: R2 = 0.16,
F3,62 = 3.82, P = 0.014). Larger males produced calls of higher
amplitude. Because of the small sample of males measured on
2 nights (N = 11), we conducted Spearman rank correlation
analyses, which indicated that only increases in length were
significantly associated with increases in amplitude (rs = 0.82,
P = 0.002).
Spectral characteristics. Spectral characteristics of the
advertisement call were size and condition dependent. There
were statistically significant relationships among the value of the
low-frequency spectral component, TFL, body condition, and
temperature in all 3 years (1999: R2 = 0.62, F3,47 = 26.02, P < 0.0001;
2000: R2 = 0.59, F3,41 = 19.88, P < 0.0001; 2002: R2 = 0.56,
F3,67 = 28.43, P < 0.0001; Table 2). In all 3 years, there was a
negative linear relationship between the value of the low-frequency
spectral component and size and body condition (Figure 4). In 2 of
3 years, there was a positive linear relationship between the value
of the low-frequency spectral component and temperature. The
condition dependence of the low-frequency spectral component was
further corroborated by the multivariate, within-male analysis of calls
produced on 2 nights (R2 = 0.38, F3,37 = 7.47, P = 0.0005; Table 3),
863
Figure 3 The effect of chorus attendance on changes in TFL (a) and body weight (b).
Each point represents a single male (N = 44, pooled across 3 years) observed
calling on 2 occasions, with the number of nights between recording sessions
indicated on the x axis. Inset histograms show the distribution of length and
weight measurements for the initial and subsequent measurements being
compared. Note the large variance in body weight within individual males.
in which changes in weight but not TFL were significantly related to
changes in the low-frequency spectral component (Figure 5).
The high-frequency spectral component was also size and condition dependent. The multiple regression models incorporating
TFL, condition, and temperature to explain variation in the value
of the high-frequency spectral component were statistically significant in all 3 years (1999: R2 = 0.44, F3,47 = 12.34, P < 0.0001;
2000: R2 = 0.41, F3,41 = 9.33, P < 0.0001; 2002: R2 = 0.35,
F3,67 = 12.29, P < 0.0001). Condition exhibited a significant negative linear relationship in 2 out of the 3 years, TFL exhibited a significant negative linear relationship in all 3 years, and temperature
exhibited a significant positive linear relationship in 2 out of the 3
years (Table 2). The condition dependence of the high-frequency
spectral component was supported by the multivariate within-male
analysis of calls produced on 2 nights (R2 = 0.53, F3,37 = 14.07,
P < 0.0001), with changes in weight significantly related to changes
in the high-frequency spectral component (Table 3).
The relative amplitude of the 2 spectral components was condition
dependent but not size dependent. Although a relationship between
length, condition, and relative spectral amplitude was found in
the larger population during 1 year (1999: R2 = 0.16, F3,47 = 2.88,
P = 0.045), none of the predictor variables was significant. However,
condition dependence of this call characteristic was detected within
the subset of males observed on 2 nights (R2 = 0.30, F3,37 = 5.33,
P = 0.004; Table 3). An increase in weight corresponded to an increase
in the proportion of energy in the low-frequency spectral component.
Behavioral Ecology
864
Table 2 Effects of condition, length, and temperature on characteristics of the advertisement call Call characteristic
βCONDa
Low frequency (Hz)b
1999
−58.5
2000
−54.2
2002
−35.6
High frequency (Hz)
1999
−35.3
2000
−85.8
2002
−112.5
Relative peak amplitude (dB)
1999
−1.12
2000
−0.94
2002
−0.74
Duration (s)
1999
0.003
2000
0.0002
2002
0.003
Period (s)
1999
−0.010
2000
−0.039
2002
0.016
Call effort (s/min)
1999
0.527
2000
0.867
2002
0.232
Amplitude (dB)
2000
0.12
2002
0.33
P
βTFL
P
βTEMP
P
R2
0.0005
0.00001
0.00001
−25.2
−26.0
−21.5
0.0002
0.00001
0.00001
13.3
9.9
6.5
0.007
0.004
0.17
0.58
0.59
0.56
0.15
0.001
0.00001
−68.8
−47.0
−32.5
0.00005
0.0003
0.01
31.3
18.9
16.3
0.013
0.025
0.30
0.44
0.41
0.35
0.19
0.38
0.99
0.16
0.06
0.01
0.12
0.38
0.40
−0.56
0.64
−0.11
0.17
0.34
0.88
0.42
0.40
0.01
0.15
0.84
0.09
0.001
0.004
0.0004
0.39
0.022
0.71
−0.005
−0.004
−0.006
0.00001
0.0004
0.0001
0.44
0.32
0.23
0.40
0.030
0.67
0.007
0.0001
0.0007
0.15
0.99
0.96
−0.028
−0.031
−0.018
0.00001
0.00001
0.27
0.59
0.49
0.02
0.53
0.10
0.57
0.231
0.365
−0.121
0.020
0.024
0.67
0.18
0.24
0.02
0.0001
0.013
−0.01
−0.23
0.95
0.33
0.33
0.16
0.037
0.067
0.33
−0.08
0.386
0.125
0.62
0.15
1.09
0.49
Multiple regression of body condition, TFL, and temperature on advertisement-call characteristics recorded from males in the field (1999: N = 55; 2000:
N = 50; 2002: N = 74). Significant regression coefficients are indicated in bold.
aThe condition index was calculated using log-transformed variables, but the partial correlation coefficient attributable to condition is shown using
nontransformed data to aid in interpretation (i.e., magnitude of signal change in response to 1.0 g change in mass).
bLog-transformed low-frequency data were used in the multiple regression analysis, but regression coefficients from untransformed data are presented.
Figure 4 The low-frequency spectral peak is condition dependent. Shown in this
figure is the simple linear regression of low frequency on body condition
(residual condition indices using nontransformed data) for data pooled
across the 3 years in which recordings were made in the field.
Temporal characteristics. Temperature, but not body
length or condition, had significant effects on temporal call
characteristics. The multiple regression models used to explain
variation in call duration (1999: R2 = 0.44, F3,47 = 12.11,
P < 0.0001; 2000: R2 = 0.32, F3,41 = 6.40, P = 0.001; 2002:
R2 = 0.23, F3,67 = 6.50, P = 0.001) and call period (1999:
R2 = 0.59, F3,47 = 22.44, P < 0.0001; 2000: R2 = 0.49,
F3,41 = 12.916, P < 0.0001; 2002: P = 0.70) were statistically
significant. However, examination of the individual regression
coefficients showed that air temperature was the only consistent
explanatory variable (Table 2). Similarly, in analyses of data
from males observed twice, the multiple regression models
were statistically significant (duration: R2 = 0.37, F3,37 = 7.25,
P = 0.0006; period: R2 = 0.30, F3,37 = 5.20, P = 0.004), but
temperature alone explained the changes in these temporal call
characteristics (Table 3). Because frogs exhibited a trade-off
between call duration and call period (i.e., males with shortduration calls tended to produce them more frequently; Table 4;
r = 0.30, P = 0.001), I conducted an analysis on calling effort
per unit time (the product of call duration and call rate). The
multiple regression models used to explain variation in calling
effort were significant in 2 years (1999: R2 = 0.18, F3,47 = 3.35,
P = 0.027; 2000: R2 = 0.24, F3,41 = 4.42, P = 0.009). Temperature
exhibited a significant positive linear relationship both years,
whereas condition exhibited a significant positive relationship in
1999 and a similar tendency in 2000 (Table 2).
Repeated-measures feeding experiment
Long-term feeding regime. Forty-two males produced advertisement calls during this
experiment. The experimental protocol resulted in body weight
decrements over the course of several nights; however, males in
the 2 treatment groups did not initially differ in length and weight
(1-way MANOVA, Rao’s R2,39 = 1.94, P = 0.16), or body weight
decrements over several nights of calling (repeated-measures
Humfeld • Condition-dependent signaling and mating-tactic adoption
865
Table 3 Effects of changing weight, length, and temperature on changes in advertisement call from males recorded more than once Call characteristic
βWEIGHT
P
βTFL
P
βTEMP
P
R2
Low frequency (Hz)
High frequency (Hz)
Relative peak amplitude (dB)
Duration (s)
Period (s)
Call effort (s/min)
−43.0
−124.8
−4.6
0.005
−0.010
0.65
0.0003
0.0001
0.002
0.30
0.69
0.23
−15.9
−66.7
−2.1
−0.008
−0.015
−0.66
0.47
0.25
0.45
0.37
0.75
0.54
1.7
32.6
−0.2
−0.006
−0.031
0.25
0.63
0.001
0.72
0.0001
0.0004
0.16
0.38
0.53
0.30
0.37
0.30
0.08
Multiple regression of changes in body weight, TFL, and air temperature on changes in advertisement-call characteristics from males recorded twice in the field
(N = 41, pooled across years). On average, recordings were separated by 6 nights (range 1–18). Significant regression coefficients are indicated in bold.
correlated with changes in call interval (R2 = 0.57, F1,7 = 9.39,
P = 0.018) and tended to correlate with changes in call duration
(R2 = 0.44, F1,7 = 5.49, P = 0.052); loss of body weight corresponded with production of short advertisement calls at a high rate.
I analyzed the advertisement-call characteristics from the 2 nights
when a male’s body weight was at its maximum and minimum,
independent of time (average interval = 2 nights). In this sample
of 30 males, those that lost weight produced shorter duration calls
(R2 = 0.30, F1,28 = 11.82, P = 0.002) with a higher low-frequency
component (R2 = 0.11, F1,28 = 3.48, P = 0.072).
Figure 5 Within-male changes in the low-frequency spectral component correlate
with changes in body weight (N = 44 males). The average number of days
between observations is 6. Weight loss is associated with production of
higher-frequency advertisement calls.
ANOVA, F2,14 = 1.56, P = 0.24), so males were grouped for further
analyses. In the 30 males that called on more than 1 night, the
percentage change in body weight was significantly related to the
number of intervening nights (R2 = 0.53, F1,28 = 31.85, P < 0.0001).
On average, males lost 4.6% of their body weight per night.
Changes in body weight were correlated with changes in call
characteristics when observations were separated by at least 2 intervening nights. In these 9 males, simple linear regression revealed
that the percentage change in body weight was significantly
Nightly feeding regime. Males assigned to the 2 feeding regimes in 2003 did not
initially differ in length and weight (1-way MANOVA, Rao’s
R2,23 = 1.22, P = 0.3), and the feeding treatments had the
desired effect of causing differential decrements in body weight.
Over the course of 5 nights, males lost body weight (2-way
repeated-measures ANOVA, night main effect, F4,84 = 13.83,
P < 0.0001), and males that were fed nightly lost weight at a
slower rate than males that were not fed (food × night interaction effect, F4,84 = 5.31, P = 0.001). Males fed nightly maintained their body weight at roughly 97% of initial body weight,
whereas males that did not feed dropped to 87% of their initial
body weight.
Seventeen males called on at least 3 nights (fed = 9, not fed = 8).
The only call characteristic that changed conditionally over the
course of these 3 nights was the low-frequency spectral component
(Figure 6); males that were fed nightly maintained constant low-frequency values, whereas males that were not fed experienced a gradual increase in the value of the low-frequency spectral component
(2-way repeated-measures ANOVA, food × night interaction effect,
F2,30 = 4.91, P = 0.014). By the third night of calling, some males
produced advertisement calls up to 22.8% higher in frequency than
those they produced on the first night.
Table 4 Correlations among advertisement-call characteristics Call characteristic
High frequency
Relative amplitude
Duration
Period
Amplitude
Low frequency
High frequency
Relative amplitude
Duration
Period
0.49 (0.000)
1.00
0.11 (0.249)
0.23 (0.012)
1.00
−0.23 (0.013)
−0.19 (0.044)
−0.08 (0.384)
1.00
−0.07 (0.476)
0.05 (0.627)
0.00 (0.982)
0.30 (0.001)
1.00
−0.35 (0.000)
−0.21 (0.025)
0.15 (0.117)
0.14 (0.139)
−0.02 (0.798)
Pearson product–moment correlations for 6 advertisement-call characteristics recorded in the field (N = 117). P values are presented in parentheses. Significant
correlations (P < 0.05) are indicated in bold type.
866
Figure 6 Weight loss results in production of higher-frequency advertisement calls
during the short-term feeding experiment. Males that were not fed nightly
produced higher-frequency calls over time. Open markers = high-food
treatment; solid markers = low-food treatment. Changes in frequency are
shown as a percentage of the value recorded on the first night (dot = mean;
whiskers = SE).
Discussion
Conditional mating strategies have been described in a wide variety
of taxa (Oliveira et al. 2008), but less frequently in lekking species
with high energetic investments in mating displays. In this study,
I demonstrated that body condition can change substantially over a
short period of time and affect the adoption of alternative mating
behaviors. These condition-dependent decisions are likely to result
from corresponding short-term changes in characteristics of advertisement calls that are important for intra- and intersexual competition for mates. Development of vocal fatigue (e.g., Vannoni and
McElligott 2009) may help provide a proximate explanation for the
surprising condition-dependent changes observed in the spectral
content of advertisement calls. Taken together with previously published research describing the acoustic preferences of females, these
results support the hypothesis that short-term mating-tactic decisions are mediated, in part, via the effects of size and condition on
a male’s ability to compete acoustically for access to mates (Henson
and Warner 1997; Alonzo 2008).
Condition-dependent tactic switching
My data support the hypothesis that condition influences matingtactic choice in male H. cinerea. I had previously reported that satellites are smaller and weigh less for a given body size than calling
males (Humfeld 2008). However, the resumption of calling by satellites shows that these frogs can still produce advertisement calls.
Instead, the caller-removal experiment supports my conclusion
that, when a male experiences a change in competitive status, condition is a more salient short-term determinant of mating-tactic use
than absolute body size.
In nature, fluctuations in body condition are potentially significant sources of short-term behavioral variation. In displaying amphibians, mammals, and birds, body weight losses of up
to 20% are not uncommon, potentially limiting the proportion of
the breeding season during which a male can compete for females
Behavioral Ecology
(Andersson 1994). In my field study, I documented significant shortterm fluctuations in body weight but not size; males suffered total
weight losses of up to 15%. However, I also observed individual
gains of 25% and no relationship between observation intervals
and amount of weight lost, indicating that males probably forage
intermittently during the breeding season. In the laboratory, my
experimental treatments clearly demonstrated that both feeding
and calling effort affected body weight. Spatial or temporal variation in foraging opportunities might impact the expression of satellite behaviors in a given population.
In species in which males produce expensive mating displays
for several days or weeks, energetic reserves are likely to be an
important determinant of a male’s ability to successfully compete for access to females. Males can potentially allocate energy
to mate acquisition on 3 timescales: 1) the instantaneous rate or
intensity; 2) the amount of time within a day; or 3) the number
of days (Halliday 1987; Castellano 2009). In a wide variety of lekking species, including green tree frogs, male mating success is positively correlated with the number of nights a male participates in
the breeding aggregation (meta-analysis: Fiske et al. 1998; review
anurans: Wells 2007; green tree frogs: Gerhardt et al. 1987). The
satellite tactic may enable males with low energy reserves to allocate energy preferentially to chorus attendance, while periodically
investing in instantaneous mate-acquisition behaviors (calling) when
their competitive status improves in relation to the quality of nearest neighbors’ calls (McCauley et al. 2000; Judge and Brooks 2001;
Lucas and Howard 2008).
Although not yet widely used to explain alternative behaviors
(Brockman 2008; Shuster 2008), the significant logistic relationship
between condition and resumption of calling by satellites provides
preliminary evidence for the existence of a threshold mechanism
regulating the expression of alternative mating behaviors. Assuming
that genetic variation in behavioral switchpoints exists within the
population, individuals are predicted to respond differentially to the
same environmental cues (Shuster and Wade 2003). Investigations
of how thresholds vary among males of different sizes and ages,
at different times during the breeding season, or in different types
of habitats will ultimately further our understanding of the genetic
architecture and evolution of conditional strategies (Shuster and
Wade 2003; Taborsky et al. 2008).
In anuran amphibians, only a few empirical studies have compared body condition of callers and satellites in the same population to test the theoretical prediction that somatic reserves are
an important factor in the short-term mating-tactic decisions of
animals producing expensive sexual displays (Wells 2007). In the
Australian frog Uperoleia rugosa, territorial males were observed to
maintain their territories until they lost 30% of their body weight
(presumably because calling and fighting were energetically costly);
subsequently they stopped calling and became satellites or foraged
(Robertson 1986). After regaining weight as a satellite, some males
resumed calling and regained a territory. In Woodhouse’s toads
(Bufo woodhousii) and Great Plains toads (Bufo cognatus), callers were
in better condition than satellites (Leary et al. 2004). Neither study
examined the relationship between body condition and call production, and surprisingly, there are few studies of condition-dependent
changes in tactics in other taxa (birds, orthopteran insects) that produce energetic acoustic signals.
This study does not rule out a role for body size on a male’s
selection of reproductive tactics. Body size differences among satellites and callers are common in anuran amphibians (Wells 2007;
Zamudio and Chan 2008), and in field observations of green tree
Humfeld • Condition-dependent signaling and mating-tactic adoption
frogs, satellites are often smaller than calling males (Garton and
Brandon 1975; Perrill et al. 1978; Humfeld 2008). A priori, I did
not predict body size to be a strong predictor of tactic switching
because size is not a determinant of reproductive success (Gerhardt
et al. 1987) and males do not engage in high levels of physical
aggression. Moreover, as in other anuran species, chorus participation appears to result in suspension of body growth (Given 1988;
Woolbright 1989; Figure 2a), so it is an unlikely predictor of behavior on a short-term basis. In species with strong intersexual selection, however, the simplest explanation for size-dependent tactic
adoption may be the constraints that body size places on the production of call characteristics preferred by females, like amplitude.
Unlike birds, in which song amplitude can be both size and condition dependent (Brumm 2009), I only demonstrated a positive linear relationship between call amplitude and body size in H. cinerea.
Because the amplitude of the call is important to attract a female in
a noisy chorus (Gerhardt and Klump 1988; Wollerman 1999) and
because frogs have little scope to modulate their call intensity (Love
and Bee 2010), the only option available to small males might be
to become satellites. Because there were significant differences in
size between years (Humfeld 2008), we might expect that population age structure will affect the behavioral threshold for adopting
satellite behavior. For instance, in years when most males are small,
a small individual may be less likely to switch to the satellite tactic
than in years when most of his competitors are large. Indeed, the
independent effects of size and condition on different call characteristics might explain, in part, the seasonal and geographic variation observed in size-dependent adoption of alternative mating
tactics (Garton and Brandon 1975; Perrill et al. 1978).
Condition-dependent advertisement calls
Indicator models of sexual selection suggest that some characteristics of sexual displays develop in proportion to the condition
of the male (Andersson 1994). However, the inverse relationship
between dominant frequency and body condition is a surprising
and novel finding because dominant frequency is considered an
honest indicator of male body size in a variety of animals (Morton
1977; Davies and Halliday 1978). In some genera, body size correlates highly with morphological traits important for call production: laryngeal size, arytenoids cartilage volume, vocal cord volume,
and laryngeal muscle volume (Titze 1994; McClelland et al. 1996;
Fitch and Hauser 2002). Although male loons (Mager et al. 2007)
and red deer (Reby and McComb 2003) communicate information
about condition through frequency of territorial calls, frogs do not
possess a tubular vocal tract whose length can be modified to adjust
formant frequencies of signals. Indeed, a strong inverse relationship
between body size and dominant call frequency has been documented in numerous anuran species (reviewed in Blair 1964; Wells
2007), suggesting little scope for environmentally induced variation
in this call property.
In species in which males produce energetically costly acoustic
displays (e.g., frogs and toads, birds, cervids) leading to significant
weight loss (reviewed in Andersson 1994; Table 1), we might reassess our assumption that dominant frequency is tightly inversely
correlated to body size and search for proximate causes of condition-dependent calling. I hypothesize, for example, that change in
body weight in green tree frogs results from 2 physiological processes, each of which can impact sound generation. First, anuran
amphibians can experience significant levels of dehydration. For
instance, free-ranging males of Eleutherodactylus coqui may lose 8% of
867
their body mass during a single dry night (Pough et al. 1983), much
of it potentially via the respiratory tract (Geise and Linsenmair
1986). So, even though hylids are more resistant to cutaneous water
loss than E. coqui (Wygoda 1984), significant nightly dehydration is
likely because amphibians greatly increase ventilation rates (Wells
2007), and thus rates of water loss, during vigorous calling. It would
be interesting to explore the relationships between dehydration and
changes in call characteristics over the course of a single night, such
as those observed in H. intermedia (Castellano and Gamba 2011).
Terrestrial amphibians rehydrate rapidly in fresh water (Wells
2007); therefore, changes in signal quality occurring over successive
nights probably require additional explanation.
The second cause of weight loss is probably oxidation of
energetic substrates. Both lipid and carbohydrate reserves in
the sound-producing muscles are important sources of energy
for calling frogs (Wells 2001). Glycogen stores can be depleted
rapidly; species with high calling rates can deplete 60% of
their trunk-muscle glycogen reserves in 2 h (Bevier 1997). Lipid
reserves are depleted more slowly, over the course of a breeding
season (reviewed in Wells 2007), and serve as the main energy
source for species supporting high levels of calling over long
periods (Prestwich 1994).
Several authors (Vannoni and McElligott 2009; Castellano and
Gamba 2011) have begun to suggest that vocal fatigue, the deterioration of vocal quality due to prolonged use, might be a widespread
communication phenomenon among species with high levels of
vocal activity during the breeding season. I hypothesize that dehydration and/or energy depletion leads to vocal fatigue in green tree
frogs via their effects on the rate at which air is expelled through
the vocal apparatus. In frogs, the dominant frequency of the signal is positively correlated with the pressure differentials between
the lungs and buccal cavity; a very forceful expulsion of air results
in a short-duration, high-frequency call (Martin 1971, 1972;
McClelland et al. 1996; Table 4). Within males, lower frequency
calls are produced at lower amplitudes (i.e., less forceful expulsion
of air) (Lopez et al. 1988; Bee and Perrill 1996; Castellano et al.
2000). Human studies document a similar correlation: vocal fatigue
is characterized by elevated airflow rates, reduced maximum phonation times (reviewed in Welham and Maclagan 2003), and elevation in fundamental frequency (Laukkanen and Kankare 2006).
In frogs, a change in airflow rate may arise because dehydration
(Pough et al. 1983) or depletion of muscle glycogen (Guppy 1988)
reduces muscle performance in the large and highly aerobic trunk
muscles that generate pulmonary pressure. In addition, dehydration
increases the viscosity of the vocal folds in humans (Titze 1994),
increasing the pressure required to initiate vocal fold oscillation
(Welham and Maclagan 2003). Both of these physiological changes
could lead to the fast and forceful expulsion of air, typical of the
calls produced by male green tree frogs in poor condition.
Although I saw some evidence of condition-dependent call
effort, the lack of strong condition dependence in several temporal
call characteristics was surprising (Tables 2 and 3) in light of the
significant correlations between metabolic costs and calling effort
(Halliday 1987; Prestwich 1994; Wells 2001). Because male–male
competition frequently involves increasing calling effort (reviewed
by Wells and Schwartz 1984), temporal call properties may not
exhibit condition dependence at baseline levels of calling (Green
1990). Alternately, males may maintain high levels of performance
for traits under strong sexual selection, while allowing other traits to
reflect fatigue (Castellano and Gamba 2011). And indeed, although
a few studies have documented condition-dependent calling effort
868
in frogs (Zimmitti 1999), several others have shown that body condition is unrelated to variation in duration, pulse rate, call rate, or
nightly calling effort (Green 1990; Docherty et al. 1995; Howard
and Young 1998; Murphy 1999; Morrison et al. 2001). More
repeated observations of individuals in competitive situations are
needed to reveal whether condition dependence of temporal properties is a general phenomenon.
Competitive status in a dynamic social
environment
Size and condition affect the values of call properties in ways
that impact a male’s ability to compete acoustically for mates.
Female green tree frogs from many localities prefer advertisement
calls with lower-than-average low-frequency spectral components
(Höbel and Gerhardt 2003; Humfeld 2008) and calls delivered at
a higher rate (Gerhardt 1987). Male–male acoustic competition frequently involves increasing the rate or duration of acoustic displays
(reviewed by Wells and Schwartz 1984). In terms of these criteria,
small males and males in poor condition will be constrained to produce unattractive advertisement calls (Humfeld 2008).
A male’s competitive status, however, depends on the interplay
between his condition-dependent calling ability and extrinsic factors related to the communication environment itself. Frog choruses
are good examples of dynamic social environments that exhibit
high degrees of variability in density and composition (Parrish and
Hamner 1997; Gerhardt and Huber 2002), in diel and seasonal
activity patterns (Runkle et al. 1994; Oseen and Wassersug 2002),
and the attendance and calling activity of particular individuals
in the chorus (Murphy 1994; Friedl and Klump 2005). Variation
in the number and density of neighbors producing attractive calls
will directly impact a male’s relative attractiveness. Previous field
experiments indicate that male frogs partly base their tactic decisions on the vocal performance of their neighbors, becoming satellites of low-frequency calls simulating a large male (i.e., Davies and
Halliday 1978; Robertson 1986; Wagner 1989). The next step in
linking mating-tactic decisions with a male’s condition-dependent
ability to compete acoustically will be accomplished by directly
testing the influence of local signaling environment using playback experiments in which the stimuli vary in relative intensity, frequency, and calling effort.
Funding
This work was supported by a Doctoral Dissertation Improvement
Grant from the National Science Foundation, The Explorers Club
Exploration Fund, a Student Research Grant from the Animal
Behavior Society, a Grant-in-Herpetology field research award
from the Society for Study of Amphibians and Reptiles, and a
Theodore Roosevelt Memorial Fund grant from the American
Museum of Natural History.
The author wishes to thank H.C. Gerhardt, M.A. Bee, V.T. Marshall,
M. Reichert, and A.M. Welch for helpful comments on earlier versions of
this manuscript.
Handling editor: Sue Healy
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