Behavioral
Ecology
The official journal of the
ISBE
International Society for Behavioral Ecology
Behavioral Ecology (2014), 25(3), 520–530. doi:10.1093/beheco/aru016
Original Article
Behavioral strategies and signaling in
interspecific aggressive interactions in gray
tree frogs
Michael S. Reichert and H. Carl Gerhardt
Division of Biological Sciences, University of Missouri, 215 Tucker Hall, Columbia, MO 65211, USA
Received 24 September 2013; revised 16 December 2013; accepted 16 January 2014; Advance Access publication 17 February 2014.
Interspecific aggression has important consequences for ecological processes and the evolution of behavioral strategies. We examined interspecific aggressive interactions in the 2 gray tree frog species, Hyla chrysoscelis and Hyla versicolor. These species call
side by side in the same ponds, and acoustic interference occurs because of the similar spectral characteristics of their vocalizations.
The aggressive calls of these 2 species, although very similar, were statistically distinguishable: calls of H. chrysoscelis were more
strongly amplitude modulated than those of H. versicolor. We used playbacks and staged interactions to characterize the behaviors of
males exposed to heterospecific competitors or their signals. Males readily responded with aggression to heterospecific individuals
and playbacks of their calls. These behaviors were qualitatively similar in both intraspecific and interspecific interactions, but there
were some significant differences. First, males of H. chrysoscelis were more aggressive toward playbacks of conspecific advertisement calls than toward those of H. versicolor. There were no significant differences in this respect in H. versicolor. Second, interspecific interactions were usually more escalated than intraspecific interactions and more likely to end with the loser moving away from
its opponent. Although neither species had an advantage in staged interactions, behavioral responses were asymmetrical because
H. versicolor was more likely than H. chrysoscelis to initiate physical contact. Previous studies showed that H. versicolor suffers from
a greater reduction in attractiveness than H. chrysoscelis in the presence of heterospecific call overlap. Thus, the asymmetries in
aggressive behavior between the 2 species may be related to differential costs of heterospecific competition.
Key words: acoustic communication, aggression, anuran, interspecific competition, playback.
Introduction
Competition is a major channel through which selection operates
because the outcomes of competitive interactions determine the
distribution of resources among individuals (Milinski and Parker
1991). In general, competition among conspecifics is common
because of high overlap in resource use (Peiman and Robinson
2010). Nonetheless, under certain ecological conditions, individuals of different species may also engage in competitive interactions with one another (Orians and Willson 1964; Ebersole 1977;
Mikami and Kawata 2004). When, for example, 2 species compete
for a common food resource or display territory, individuals of different species may exert indirect negative effects on one another
(i.e., exploitative competition; Schluter 2000) or directly interfere
with one another via aggressive behavior (i.e., interference competition or heterospecific aggression; Peiman and Robinson 2007).
Address correspondence to M.S. Reichert, who is now at Institut für Biologie
der Humboldt-Universität zu Berlin, Abt. Verhaltensphysiologie, Invalidenstr.
43, 10115 Berlin, Germany. E-mail: [email protected].
© The Author 2014. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved. For
permissions, please e-mail: [email protected]
Although heterospecific aggression is apparently widespread in
animals, it has received less attention than other forms of interspecific competition and both the mechanisms and consequences of
this behavior remain poorly understood (Grether et al. 2009, 2013;
Peiman and Robinson 2010). Because animal contests are often
mediated by signaling interactions (Maynard Smith and Price 1973;
Maynard Smith and Parker 1976), the study of the aggressive signals used in interspecific contests is likely to be a fruitful approach
to addressing the major outstanding questions in the understanding
of heterospecific aggression. A longstanding question of interest is
whether heterospecific aggression affects patterns of signal evolution. Cody (1969, 1973) proposed that when animals display interspecific territoriality, there should be selection for the convergence
of aggressive signal characteristics to facilitate heterospecific aggressive interactions. This hypothesis was disputed, however, and other
researchers proposed that patterns of similarity in aggressive signal
characteristics across species may be related to common ancestry,
perhaps with selection for conservation of similar signal properties where species’ ranges overlap (Gerhardt and Schwartz 1995).
Alternatively, selection might disfavor heterospecific aggression so
Reichert and Gerhardt • Interspecific aggression in tree frogs
that most observed instances are caused by receivers’ inabilities to
discriminate conspecifics from heterospecifics (Murray 1971, 1976,
1981). Despite this controversy, several studies have now documented interspecific aggressive interactions and provide evidence
that such behavior is adaptive and influences the evolution of signal
structure (e.g., Martin and Martin 2001; Adams 2004; Peiman and
Robinson 2007; Tobias and Seddon 2009; Laiolo 2012).
The occurrence of heterospecific aggressive interactions also
raises important questions for the understanding of strategic contest behavior. This topic has received a great deal of recent attention in the literature on studies of intraspecific contests (reviewed
by Arnott and Elwood 2009) but is largely unexplored for interspecific contests (Tanner and Adler 2009; Lehtonen et al. 2010;
Green and Field 2011). Species that engage in both intraspecific
and interspecific contests provide ideal study systems to understand
the mechanisms that shape the dynamics and outcome of contests.
First, as noted above, selection may favor certain aggressive signal characteristics to facilitate or reduce heterospecific aggression.
However, selection from conspecific aggressive interactions also will
act on aggressive signals, and the strength and direction of these
2 sources of selection may not be equivalent. A reduction in overall levels of heterospecific aggression might result if competitors’
signals are unrecognizable (e.g., Tynkkynen et al. 2004), but an
increase might equally well be predicted if these signals are recognizable but less efficient as a means of contest assessment than the
corresponding conspecific signal. Second, even if 2 species utilize
identical aggressive signals, the means by which these signals are
assessed may differ for each species and therefore limit the utility
of interspecific aggressive communication. For instance, the same
signal may be used in one species to signal a low level of threat and
in another to signal a high level of threat. Thus, it is important to
measure variation in not only the structure of signals of interacting
heterospecifics but also the responses of receivers to conspecific and
heterospecific signals. Finally, individuals of the different species
may differ in characteristics that determine the outcome of contests, which offers opportunities to test theoretical models of contest
behavior. For instance, the negative consequences of the presence
of a heterospecific may be asymmetric between the 2 species’
studied. This pattern may generate an asymmetry in costs, which,
according to many models, could lead one species to be more likely
to win contests (Maynard Smith and Parker 1976; Hammerstein
and Parker 1982). All of these questions can be addressed by examining the dynamics of contests and response to signals of individuals engaged in intraspecific and interspecific aggressive interactions.
In this study, we examined aggressive signals and behaviors of 2
cryptic species of gray tree frogs, Hyla chrysoscelis and Hyla versicolor,
in staged and simulated heterospecific and conspecific interactions.
As in many anurans, mate attraction and reproduction takes place
in or near ponds and other small bodies of water, where individuals
of different species often gather in large numbers at the same time
during the breeding season (Duellman and Pyles 1983; Schwartz and
Wells 1983a; Donnelly and Guyer 1994). Competition between species may occur over physical space needed to attract mates and raise
offspring, and interspecific aggressive behavior has been documented
frequently in anurans (Wells 1980; Brzoska 1982; Schwartz and Wells
1984, 1985; Given 1990; Gerhardt and Schwartz 1995; Shimoyama
1999). Male gray tree frogs do not defend territories but nonetheless
engage in aggressive interactions with other males to defend a calling
space, a buffer between itself and nearby males, which reduces acoustic interference in that area and presumably increases its chances of
female attraction (Wells and Schwartz 2007). Importantly, acoustic
521
interference from not only conspecifics but also heterospecifics can
reduce a male’s chances of attracting a mate (Marshall et al. 2006).
Thus, individuals are likely to respond aggressively to both conspecifics and heterospecifics that intrude on their calling space.
The ranges of our study species include large areas of sympatry.
Our choice of the 2 species of gray tree frogs was in part based on
their frequent activity in mixed species choruses. Although there is
some evidence that males of the different species occupy slightly
different microhabitats within mixed choruses (Ptacek 1992), there
is nonetheless considerable overlap within ponds, and males of
the 2 species often call side by side (Gerhardt et al. 1994; see also
Marshall et al. 2006).
These 2 species also have a close evolutionary relationship;
H. versicolor is a tetraploid species that is thought to have arisen by
allopolyploidy from ancestral H. chrysoscelis and 2 extinct, closely
related lineages (Holloway et al. 2006). A few interspecific hybrids
have been found even though hybrid offspring have reduced viability (Gerhardt et al. 1994). The 2 species of gray tree frogs also
offer an interesting contrast in their signal repertoires. Although
their advertisement calls are distinctive and there is evidence for
how these differences evolved (e.g., Keller and Gerhardt 2001),
the aggressive calls of the 2 species are much more similar to one
another. If this similarity facilitates interspecific aggressive behavior, then future comparisons of allopatric and sympatric populations may allow us to determine if conservation or convergence is
the cause for aggressive-call similarity.
Here, we provide data that address 3 important aspects of interspecific aggressive behavior. First, we analyzed the characteristics
of the aggressive calls of both species to determine if there are any
differences between the 2 species’ aggressive calls for the populations under study. Second, we used playbacks to determine whether
males were more likely to respond aggressively to a simulated conspecific or heterospecific competitor. Third, we staged interactions
between heterospecifics to determine if they would interact aggressively with one another, and if so, if their behavior in these interactions differed from that observed in previous studies of intraspecific
aggressive interactions in H. versicolor.
Methods
Aggressive-call analyses
We recorded and analyzed the aggressive calls of males of each
species to determine if there were species differences in aggressivecall characteristics. This study was not designed as an exhaustive
survey of geographic variation in aggressive calls and hence we
assert that the differences we observed may be due both to differences between the species and differences in the geographic location and species composition of the recorded individuals’ natural
habitats. Nevertheless, these analyses are valuable because they provide an initial overview of the potential for variation in aggressive
calls in these 2 species. Male H. versicolor were captured from local
ponds in Boone County, MO; these populations are currently allopatric with respect to H. chrysoscelis although isolated populations of
the latter species occur within 20 km. Male H. chrysoscelis were captured from sympatric populations located in Phelps County, MO.
Additional H. chrysoscelis were captured from an allopatric population from Liberty County, FL. Calls to be analyzed were selected
from a subset of recordings of males calling during the staged
interactions described in Experiment 2, along with recordings of
males that were prompted to give aggressive calls in response to the
522
playback of a conspecific advertisement call. When males gave sufficient numbers of aggressive calls, we analyzed the first 10 such
calls given during the recording that were sufficiently free from
background noise interference to permit the analysis of fine-temporal structure. Not all males gave 10 aggressive calls, but all recordings included in the data set contained measurements from at least
3 calls per male.
We analyzed temporal and spectral characteristics of each
aggressive call using the Raven Pro sound analysis program (V 1.3,
Cornell Laboratory of Ornithology) and custom-designed software
(Signan, created by G. Klump and modified by D. Poleet). We were
particularly interested in fine-temporal differences in call structure. Thus, in addition to measuring call duration, we measured
rise times (the time from the start of the call to its peak amplitude)
and fall times (the time from peak amplitude to the ending of the
call) of each call. Because absolute rise and fall times depend on
Behavioral Ecology
the total duration of the call, a characteristic that varies between
individuals, we converted these into the percentages of the total call
duration in which the call was rising and falling, respectively. These
measures allowed us to compare overall differences in call shape
between the 2 species in a standardized manner. In addition, we
examined the possibility that the pattern of amplitude modulation
may differ in the aggressive calls of these 2 species. Aggressive calls
are usually not composed of clearly separate pulses; nonetheless,
there is substantial variation between calls in the depth of amplitude modulation (Figure 1). Because we could not count pulses in
most cases, we quantified amplitude modulation by measuring the
number of times the amplitude of the call dropped below 50% of
the peak amplitude. By definition, all calls drop below 50% of the
peak amplitude at their beginning and end, thus we subtracted one
from this number to obtain a quantity somewhat comparable to the
pulse number that is often measured for advertisement calls.
Figure 1
Waveform displays of typical aggressive calls. All calls were recorded from individuals engaged in staged interspecific interactions. (a) Hyla chrysoscelis, (b)
Hyla versicolor, and (c) a pair of calls given by H. chrysoscelis. Note that the calls of H. chrysoscelis have much greater amplitude modulation than the call of
H. versicolor. In H. chrysoscelis, this amplitude modulation is usually incomplete, as in (a). However, in some cases, as in (c), the amplitude modulation is of
sufficient depth that the aggressive call is composed of clearly separate pulses.
Reichert and Gerhardt • Interspecific aggression in tree frogs
In addition to these temporal characteristics, we measured the
values of the 2 major frequency peaks in the call, the low-frequency
peak and the (dominant) high-frequency peak. For those male
H. chrysoscelis that were recorded in staged interactions, we determined the extent to which they reduced the frequency of their
aggressive calls relative to that of their advertisement calls. Such
behavior has already been shown to be an important component
of aggressive interactions in H. versicolor (Reichert 2013a; Reichert
and Gerhardt 2013a). Thus, we also measured the frequency peaks
of advertisement calls of these males and subtracted the average
frequency value for the aggressive call from that of the advertisement call to obtain an average amount by which males adjusted
their aggressive-call frequencies.
Our primary aim was to determine if the aggressive calls of the 2
species are acoustically distinct. To this end, we entered the call characteristics into a discriminant function analysis (DFA) that determined the
extent to which the 2 species’ calls were statistically distinguishable from
one another. We performed separate DFAs for all possible combinations of the 3 populations under study. Thus, our analyses also allowed
us to assess whether there were any differences in aggressive-call characteristics between H. chrysoscelis from 2 widely separated populations.
Independent samples t-tests were then used to determine which of the
individual call characteristics included in the DFA were significantly
different. In addition, we performed a principal components analysis
to reduce the number of variables and then plotted the first 2 components against one another to illustrate differences in call characteristics
between the 2 species. The latter 2 analyses were only performed with
males from Missouri because the recordings from Florida H. chrysoscelis
males could not be corrected for body mass (see below).
The H. chrysoscelis males included in this analysis from the Phelps
County, MO, population were on average heavier than the H. versicolor
males from the Boone County, MO, population. Both the frequency
characteristics and the duration of aggressive calls are correlated with
body mass (Reichert 2013a; Supplementary Table 1). Thus, except
where noted below, prior to statistical analyses, we adjusted these
characteristics to the average body mass (6.35 g) of the individuals
included in this analysis. To do this, we calculated linear regressions
for each call characteristic on body mass for each species and used the
parameters of the regression equation to adjust each individual’s call
characteristics relative to its body mass to that expected for an average-massed individual (Platz and Forester 1988). This ensured that
our comparisons reflected differences between the species that were
not biased by the mass differences between the samples. Mass data
were unavailable for H. chrysoscelis from the Florida population; thus,
we present only uncorrected data for these individuals and limit the
extent to which they were included in analyses. Although many characteristics of the advertisement calls of these 2 species are influenced
by temperature, such effects are much weaker or nonexistent in the
aggressive-call characteristics we measured in this study (Gayou 1984;
Reichert 2013a; unpublished data). For this reason, we did not adjust
call characteristics for temperature in our analyses. Recordings of 25
male H. chrysoscelis from Missouri, 14 males from Florida, and 34 male
H. versicolor from Missouri were used for these analyses.
Behavioral experiments
Frog capture and experimental setup
All males used in behavioral experiments originated from Boone
County, MO (H. versicolor) or Phelps County, MO (H. chrysoscelis);
males from the Florida population were not used in these experiments. In all cases, males were housed in an animal care facility in a
523
greenhouse located near the campus of the University of Missouri.
On each day of testing, we released males in the afternoon into an
indoor artificial pond that had environmental conditions (simulated
rainfall, artificial chorus noise) conducive to male chorusing (see
also Schwartz et al. 2001). Experiments were performed at night
during the peak period of chorusing activity (2000 to 0200 hours;
tests were carried out from April to July, 2008–2011). Males that
called well in the artificial pond were placed in cages atop platforms
scattered about the pond. Males selected for testing could then be
transported on these platforms to testing arenas located outside
of the pond. Once males were placed in the arena, the cage was
removed. Thus, males were potentially free to move off of the platform. Nonetheless, males generally remained in place while calling
except when challenged by another nearby male (see Experiment 2:
staged aggressive interactions).
Experiment 1: aggressive-threshold measurements
We tested whether male H. versicolor and H. chrysoscelis differed in
their aggressive responses to a playback simulating an approaching
conspecific or heterospecific male. Our experimental design followed
the approach of Rose and Brenowitz (1991) to measure aggressive
thresholds, defined as the lowest amplitude at which a male gave
an aggressive response to the playback stimulus. Thus, lower aggressive thresholds indicated an increased aggressive responsiveness to
the playback stimulus. Our playback stimuli were 1) a synthetic
H. versicolor advertisement call with call characteristics (pulse number: 18; call duration: 0.9 s; frequency of the low-frequency peak:
1100 Hz; frequency of the high-frequency peak: 2200 Hz; call
repetition rate: 5 s) based on averages obtained from field recordings of calling males from our study population and 2) a synthetic
H. chrysoscelis advertisement call with a pulse rate (approximately
40 pulses/s) somewhat lower than the average (pulse number: 34;
call duration: 0.9 s; frequency of the low-frequency peak: 1100
Hz; frequency of the high-frequency peak: 2200 Hz; call repetition
rate: 5 s). Synthetic calls were used rather than natural exemplars
to ensure that differences in males’ responses were not related to
any idiosyncratic characteristics of the particular stimuli chosen but
rather can be interpreted as a difference in response to calls with
typical characteristics of the 2 species (McGregor et al. 1992). We
recorded the stimuli to a compact disk and broadcast them through
a Mineroff SME-AFS speaker. The sound pressure level (SPL) of
the loudest playback stimulus was set to 107 dB SPL at 10 cm from
the speaker using a digital sound level meter (Radio Shack 33-2055).
This amplitude approximates that expected between males interacting at a typical distance (10 cm) at which aggressive interactions take
place (Gerhardt 1975; Reichert and Gerhardt 2011). This was also
the highest amplitude at which our playback system emitted undistorted signals. We placed the platforms of individual males so that
they would be positioned approximately 10 cm from the speaker, but
small movements by the frogs prior to testing sometimes prevented
us from exposing males to exactly the same maximum SPL. The
playback stimulus was designed such that it began at an SPL 30 dB
below the maximum. The SPL of the playback was increased by
3 dB every minute until it reached the maximum SPL at the 10th
minute. Playback tests took place approximately 6 m away from
the artificial pond and thus the background chorus was audible
throughout the playbacks, although at this distance, it was substantially quieter than the playback (see also Christie et al. 2010).
The background chorus noise fluctuated often. Although we did
not attempt to control for this or measure absolute amplitudes, we
randomized the playback stimulus, and during time periods when
Behavioral Ecology
524
both species were available, the species of the focal male, in order
to ensure that chorus background noise amplitude did not bias our
results. The randomization also ensured that results were robust to
any changes in aggression over the course of the season, although
no such changes have been observed (Marshall VT and Gerhardt
HC, unpublished observations).
We began playbacks once the frog resumed spontaneous calling
after being transported from the artificial pond. We recorded males’
calling responses throughout the playback onto a digital-audio
recorder (Tascam DR-680) with a microphone (Sennheiser ME-67)
suspended directly above the calling male. We continued playbacks
until either the male gave an aggressive call or until the 11-min
playback period had elapsed. For males that gave an aggressive
call, we measured the SPL of the playback stimulus at the male’s
position at the time they first gave an aggressive call to determine
the aggressive threshold. Thus, males that did not give an aggressive call at any point during the playback did not contribute to our
measurements of aggressive thresholds. We compared aggressive
thresholds for each species using nonparametric Wilcoxon–Mann–
Whitney tests and also compared the proportion of individuals of
each species that gave an aggressive call at some point during the
playback using chi-square tests. We emphasize that these threshold estimates are not equivalent to those that would be obtained
with psychophysical procedures, which would take into account the
effects of subthreshold playbacks. Rather, our playbacks simulated
the approach of 2 calling individuals to one another. We obtained
responses from 61 male H. versicolor and 38 male H. chrysoscelis for
this experiment.
Experiment 2: staged aggressive interactions
We used the techniques described by Reichert and Gerhardt
(2011) to stage interactions (n = 20) between male H. versicolor and
H. chrysoscelis. We selected a male of each species that was calling
well in the artificial pond and brought them to an arena located
approximately 3 m away from the pond. Each male was placed on
a wheeled platform on opposite ends of a 1.8-m long runway. Once
both males resumed calling, we gradually pulled the platforms
toward one another by means of ropes attached to each platform
until the platforms abutted one another. At this point, males were
calling at extremely close range, which, in interactions between
2 conspecific H. versicolor, would often lead to contests involving
aggressive calling and in some cases, physical combat (Reichert and
Gerhardt 2011). We considered an interaction to have taken place
when both males called at least once after the platforms had been
pulled toward one another. In these competitive interactions, there
was always a clear winner and loser. We defined losers as individuals that either escaped from the interaction by moving at least 1
platform length away while their opponent (the winner) remained
in place and called or remained in place but stopped calling for
at least 5 min while their opponent (the winner) continued to call.
We recorded audio and video throughout the interaction using
digital-audio recorders (Marantz PMD-660 and PMD-661), directional microphones (Sennheiser ME-66, ME-67 and ME-80), and a
digital camcorder (Sony DCR-SR85). All staged interactions were
performed at night (2000 to 0200 hours) under ambient light conditions within a glass-roofed greenhouse from May to June 2010.
After each interaction had taken place, we measured the mass of
each male.
We tested several hypotheses with these data. First, we tested
whether one species had an advantage over the other in contests.
Second, we tested whether one species was more likely to instigate
aggressive behaviors. That is, we examined the recordings of each
interaction and determined which individual was the first to give
an aggressive call, and, when physical combat took place, which
individual initiated physical contact. Third, we made several comparisons of contest characteristics between these interspecific interactions and intraspecific interactions between male H. versicolor
(n = 173) that had been recorded for previous studies using the same
methodology described here (Reichert and Gerhardt 2011, 2012,
2013b). We compared the proportions of intraspecific and interspecific contests that terminated at each of 4 mutually exclusive stages,
listed here in order of increasing escalation: both males only gave
advertisement calls, only 1 of the 2 males gave aggressive calls, both
males gave aggressive calls, and males engaged in physical fighting.
Likewise, we compared average contest duration between interspecific and intraspecific interactions. Contest duration was defined as
the amount of time between the point at which both males had first
called after their platforms were pulled toward one another and the
time at which the loser gave its final call; we were unable to measure interaction duration for one interspecific interaction because
of an equipment malfunction. Finally, we compared the behavior
of losers of interspecific and intraspecific interactions. At the conclusion of the interaction, losers either moved away from the contest winner or remained in place but ceased calling. Thus, we tested
whether there were differences in the occurrence of these behaviors when the competitors were of the same or different species.
Differences in qualitative behavioral measurements were compared
using Fisher’s Exact tests because of the small sample size for some
categories of interspecific interactions.
Results
Aggressive-call analyses
Descriptive statistics for the characteristics of aggressive calls for
each species are given in Table 1. Aggressive calls of both species
showed a broadly similar structure. In both species, the calls consist
of a brief burst of sound with 2 major frequency peaks, and calls
are organized into bouts in which several calls are given in rapid
succession followed by a relatively longer pause. As in H. versicolor
(Reichert and Gerhardt 2013a), the frequency peaks of the aggressive calls of H. chrysoscelis were lower than the respective peaks in
their advertisement calls (mean ± standard deviation [SD] difference between the frequency peak for advertisement calls and the
frequency peak for aggressive calls, uncorrected for body mass; lowfrequency peak: 229 ± 69 Hz; high-frequency peak: 242 ± 99 Hz;
n = 14 males from the Phelps County population calling in staged
interactions). Nonetheless, the DFA revealed that the aggressive
calls of the 2 species could be distinguished quite well: in comparisons between the 2 Missouri populations, 96.0% of H. chrysoscelis aggressive calls and 97.1% of H. versicolor aggressive calls were
assigned by the analysis to the correct species (canonical correlation:
0.90; Wilks’s lambda: 0.19; χ26 = 89.4 , P < 0.001). The amplitude
modulation of the calls had the largest influence on the discriminant function (Table 2). The aggressive calls of H. chrysoscelis were
much more likely to contain amplitude modulation than were those
of H. versicolor. Indeed, in exceptional cases, the aggressive calls of
H. chrysoscelis were composed of distinct pulses (Figure 1c); this was
never the case for H. versicolor. Nonetheless, when we removed this
variable from the DFA, the classification success was again high
(84.0% correct classifications for H. chrysoscelis and 88.2% correct
classifications for H. versicolor; canonical correlation: 0.77; Wilks’s
Reichert and Gerhardt • Interspecific aggression in tree frogs
525
Table 1
Descriptive statistics and t-tests comparing the call characteristics of each species
Call characteristic
Mean (SD) Hc-MO
Mean (SD) Hc-FL
Mean (SD) Hv-MO
t
P
Amplitude modulation
Call duration—uncorrected (s)
Call duration—mass corrected (s)
Low-frequency peak—uncorrected (kHz)
Low-frequency peak—mass corrected (kHz)
High-frequency peak—uncorrected (kHz)
High-frequency peak—mass corrected(kHz)
Proportional rise time
Proportional fall time
6.2 (2.3)
0.12 (0.04)
0.10 (0.03)
1.02 (0.07)
1.06 (0.04)
2.08 (0.17)
2.17 (0.10)
0.67 (0.14)
0.24 (0.11)
6.3 (2.1)
0.12 (0.04)
1.7 (1.1)
0.15 (0.04)
0.16 (0.04)
1.06 (0.07)
1.02 (0.04)
2.12 (0.17)
2.03 (0.11)
0.73 (0.13)
0.19 (0.08)
9.98
3.94
6.84
2.41
3.49
0.90
5.20
1.54
2.28
<0.001
<0.001
<0.001
0.02
0.001
0.37
<0.001
0.13
0.03
1.04 (0.07)
2.15 (0.18)
0.69 (0.11)
0.22 (0.11)
Mean and SD of each of the 6 measured call characteristics for Hyla chrysoscelis from a sympatric population in Phelps County, MO (Hc-MO; n = 25),
H. chrysoscelis from an allopatric population in Liberty County, FL (Hc-FL; n = 14), and Hyla versicolor from an allopatric population in Boone County, MO (Hv;
n = 34). Definitions of call characteristics are given in Methods. The proportional rise and fall times represent the proportion of the call duration from the
beginning of the call to its peak amplitude and from the peak amplitude to the end of the call, respectively. Because the peak amplitude of some calls was a
plateau rather than a single point, the sum of the proportional rise and fall times does not add up to 1. The values for call duration and both frequency peaks
are presented both as the original measurements and as values after a correction for male body mass (see Methods). Body mass measurements were not made
for the Florida males and therefore only raw values of calls from this population are presented. Also shown are test statistics and P values for independent
samples t-tests comparing the mean value of each call characteristic between the Missouri populations of the 2 species. Degrees of freedom = 57 for all tests.
lambda: 0.41; χ25 = 48.5 , P < 0.001). Here, the magnitude of the
high-frequency peak was the variable that had the largest influence
on the discriminant function, and both the low-frequency peak and
call duration also contributed heavily (Table 2). In fact, when comparisons were made between the species for each individual call
characteristic, all the differences were statistically significant except
for call rise time (Table 1). A DFA with the full set of 6 predictor
variables but with call frequency and duration measurements that
were not corrected for body mass gave qualitatively similar results
(92% and 97.1% classification success for H. chrysoscelis and H. versicolor calls, respectively). However, the uncorrected mean values were
more similar to one another, particularly for the high-frequency
peak, than were those that were corrected for body mass (Table 1).
In the principal components analysis, the first 2 principal components explained 74.6% of the variance in call characteristics. The
first component loaded heavily on all call characteristics except for
rise and fall time, whereas the second component was primarily
influenced by these latter 2 variables (Table 3). A plot of the first 2
principal components against one another clearly demonstrates the
differences between the calls of the 2 species and shows that most
of these differences are accounted for by the first principal component, that is, by the extent of amplitude modulation, call duration,
and call frequency (Figure 2).
Although comparisons could not be made for mass-corrected call
characteristics between populations of H. chrysoscelis from a sympatric Missouri population and an allopatric Florida population, the
uncorrected characteristics were very similar in the 2 populations
(Table 1). A DFA analysis classified only 71.8% of calls to the correct population; this analysis did not reach statistical significance
(canonical correlation: 0.30; Wilks’s lambda: 0.91; χ26 = 3.21 ,
P = 0.78). As with H. chrysoscelis males from the sympatric Missouri
population, the calls of males from the allopatric Florida population were easily distinguished from those of H. versicolor (uncorrected for body mass; 100% correct classifications for H. versicolor
and 92.9% correct classifications for H. chrysoscelis; canonical correlation: 0.89; Wilks’s lambda: 0.22; χ26 = 65.8 , P < 0.001).
Aggressive thresholds
Male H. versicolor did not differ in the likelihood of giving aggressive calls in response to playbacks of conspecific or heterospecific
Table 2
Coefficients from a DFA of aggressive calls
Call characteristic
DFA coefficient
(full)
DFA coefficient
(reduced)
Amplitude modulation
Call duration
Low-frequency peak
High-frequency peak
Proportional rise time
Proportional fall time
0.89
−0.50
−0.27
0.74
−0.12
0.04
—
0.70
0.69
−1.06
0.31
−0.28
These standardized canonical coefficients show the extent to which each
characteristic contributed to the discrimination of the 2 species’ aggressive
calls. The full model included all 6 measured call characteristics. The
reduced model excluded the characteristic with the highest explanatory
power, “amplitude modulation.” Even with the reduced model, the calls
of these 2 species could be discriminated with few errors (see Results). The
values for call duration and frequency peaks were corrected for male body
mass prior to calculating the DFA. Values shown are for an analysis of the
Missouri populations of each species (see Methods).
Table 3
Component matrix for the first 2 principal components (PC1
and PC2) of the aggressive-call characteristics
Call characteristic
PC1
PC2
Amplitude modulation
Call duration (s)
Low-frequency peak (kHz)
High-frequency peak (kHz)
Proportional rise time
Proportional fall time
0.580
−0.795
0.826
0.868
−0.164
0.331
−0.416
−0.111
0.312
0.368
0.898
−0.841
Values for call duration and the frequency peaks were corrected for male
body mass prior to the principal components analysis. This analysis included
males from the Missouri populations of the 2 species.
advertisement calls (13 of 28 males gave aggressive calls in response
to the H. versicolor playback; 14 of 33 males gave aggressive calls
in response to the H. chrysoscelis playback; χ21 = 0.1 , P = 0.75). In
contrast, male H. chrysoscelis were more likely to give aggressive
calls in response to the conspecific playback than to the heterospecific playback (12 of 17 males gave aggressive calls in response to
526
Behavioral Ecology
Figure 2
Plot of the first 2 principal components of aggressive-call characteristics against one another. Closed circles: Missouri Hyla versicolor; open circles: Missouri
Hyla chrysoscelis.
the H. chrysoscelis playback; 7 of 21 males gave aggressive calls in
response to the H. versicolor playback; χ21 = 5.2 , P = 0.022). For those
individuals that gave aggressive calls, there were no differences
in aggressive thresholds when comparisons were made between
responses to the 2 stimuli within each species (Figure 3; Wilcoxon–
Mann–Whitney test, H. chrysoscelis: n = 19, U = 23, P = 0.11; H. versicolor: n = 27, U = 72.5, P = 0.37). However, male H. chrysoscelis had
lower aggressive thresholds in response to the H. chrysoscelis stimulus
than did male H. versicolor (Figure 3; Wilcoxon–Mann–Whitney test,
n = 26, U = 26.5, P = 0.003). Because of movements on the platform, not all males were tested at an identical maximum playback
SPL. Nonetheless, there was no evidence that males that failed to
respond aggressively to the playback did so because these playbacks
were less intense than those in which males responded aggressively.
The range of maximum SPLs of playbacks in which males did not
give aggressive calls (103–115 dB SPL) overlaps with and extends
beyond the distribution of SPLs at which aggressive calls were elicited in other males (Figure 3).
Staged aggressive interactions
Males interacting at close range with a heterospecific readily
responded with aggressive behavior, and the structure of aggressive interactions between a male H. versicolor and H. chrysoscelis was
qualitatively similar to the structure of interactions between 2 male
H. versicolor. As in interactions between conspecifics, interactions
between heterospecifics involved 4 distinct levels of escalation, and
the types of behaviors exhibited by winners and losers were similar
(Reichert and Gerhardt 2011). Nonetheless, there were some differences between intraspecific and interspecific aggressive interactions.
Interspecific interactions were significantly longer in duration than
intraspecific interactions (mean ± SD; interspecific: 163.0 ± 135.3
s, n = 19; intraspecific: 121.4 ± 151.8 s, n = 173; t-test on ln-transformed interaction durations: t190 = 2.2, P = 0.03). This result
probably is explained by a tendency for interspecific interactions to
reach higher levels of escalation, although distributions of levels of
escalation in the 2 types of interaction were not significantly different from one another when all 4 levels of escalation were considered separately (Figure 4; Fisher’s Exact test, P = 0.13). Sample
sizes were small for some levels of escalation of interspecific interactions. When we pooled the 2 lowest and 2 highest levels of escalation together, the difference in escalation between interspecific
and intraspecific interactions approached significance (Fisher’s
Exact test, P = 0.056).
Neither species had a clear advantage in interspecific interactions; 12 of 20 interactions were won by H. versicolor. Also, neither
species was more likely to be the first to give aggressive calls in the
interaction; in 10 of 19 interactions, the H. chrysoscelis male was the
first to give aggressive calls. However, when interactions escalated
to physical fighting, males of H. versicolor were much more likely to
initiate physical contact; this was the case for 8 of the 9 physical
fights between the 2 species. There was a difference in the behavior
of losers when comparisons were made between interspecific and
intraspecific interactions. In interspecific interactions, losers nearly
always moved away from the winner rather than remaining in place
and not calling, whereas in intraspecific interactions, losers were
more likely to remain in place than to move away (proportion of
losers moving away at the end of the contest: interspecific interactions, 18/20; intraspecific interactions, 56/173; Fisher’s Exact test,
P < 0.0001). Losers of physical fights in intraspecific interactions
are more likely to move away from the winner than losers at other
levels of escalation (Reichert and Gerhardt 2011). Nonetheless, the
differences between interspecific and intraspecific interactions in
loser behavior were not explained by the increased likelihood of
interspecific interactions escalating to physical fighting. When physical fights were excluded from the analysis, losers of interspecific
interactions were still more likely to move away from their opponent than losers of intraspecific interactions (proportion of losers
moving away at the end of the contest: interspecific interactions,
Reichert and Gerhardt • Interspecific aggression in tree frogs
527
10/11; intraspecific interactions, 21/119; Fisher’s Exact test,
P < 0.0001). Heavier individuals did not have an advantage in
interspecific interactions (n = 10 of 20 interactions won by the
heavier male; mean ± SD mass: H. chrysoscelis losers: 6.45 ± 1.05 g,
n = 12; H. versicolor winners: 6.31 ± 0.67 g, n = 12; H. chrysoscelis winners: 6.90 ± 1.30 g, n = 8; H. versicolor losers: 6.90 ± 0.47 g, n = 8).
Individuals of neither species were significantly heavier than those
of the other species in these contests (paired t-test: t19 = 0.38,
P = 0.71). Likewise, for those interactions in which aggressive calls
could be recorded from both males, there were no differences in
aggressive-call frequency between winners and losers (frequencies
uncorrected for body mass: low-frequency peak: t13 = 0.49, P = 0.6;
high-frequency peak: t13 = 0.94, P = 0.36).
Discussion
The results of this study clearly show that males of the 2 species
of gray tree frog are responsive to one another’s signals and that
behavioral contexts that would elicit aggressive behavior in intraspecific interactions also elicit aggressive behavior in interspecific
encounters. The acoustic recognition space of males of each species for aggressive signals remains to be determined, but the results
obtained here suggest that males will be largely responsive to signals of both species across their range of variation. This similarity
in responsiveness contrasts with our finding of acoustic differences
between the aggressive calls of the 2 species and in general raises
intriguing questions about the strength and direction of, and forces
responsible for, changes in aggressive signal characteristics of these
species relative to each other. Despite broad similarities between
intraspecific and interspecific aggressive interactions, there were
some subtle differences that suggest that the consequences of
engaging in these 2 types of interactions differ for the participants.
Differences in aggressive-call structure
Figure 3
Aggressive thresholds of male Hyla versicolor (Hv) and Hyla chrysoscelis (Hc)
in response to advertisement call playbacks of each species. (a) Playback
of H. versicolor stimulus. (b) Playback of H. chrysoscelis stimulus. Asterisk
indicates a significant difference (P < 0.05) between the 2 species in response
to the playback stimulus (see Results).
Figure 4
Proportions of interactions that terminated at each level of escalation
(ADV: both males only gave advertisement calls, AG1: only 1 of the 2 males
gave aggressive calls, AG2: both males gave aggressive calls, PF: physical
fight). White bars: intraspecific interactions (n = 173; data from Reichert
and Gerhardt 2011); gray bars: interspecific interactions (n = 20).
Previous studies have described numerous differences in the advertisement calls of H. chrysoscelis and H. versicolor (Gerhardt 2001).
Indeed, other than chromosome number, differences in advertisement-call characteristics are the only way to reliably distinguish
between individuals of these 2 species (Wasserman 1970). Likewise,
we found several differences in their aggressive calls. Intriguingly,
the greatest difference between the 2 species’ aggressive calls was
found for amplitude modulation, which is also one of the most
divergent characteristics of their advertisement calls (Gerhardt
2001). Individuals of H. chrysoscelis tended to have clearly amplitude-modulated aggressive calls, whereas those of H. versicolor rarely
showed any notable amplitude modulation. Nonetheless, although
the aggressive calls of these 2 species were statistically distinguishable, there was some overlap between aggressive-call characteristics
of the 2 species and the calls could not always be unequivocally
classified as belonging to one species or the other. In contrast, at a
given temperature, advertisement calls of these 2 species are apparently always different in pulse rate and fine-temporal structure
(Gerhardt and Doherty 1988; Gerhardt 2001).
That aggressive calls show more structural overlap than advertisement calls may indicate that selection toward species-specific
signal characteristics is stronger in advertisement calls than in
aggressive calls because the costs of mismating are higher than
those associated with misdirected aggression toward a heterospecific. This possibility seems reasonable because interspecific matings
rarely result in viable offspring (Gerhardt et al. 1994) and although
the costs of aggressive interactions in these species are unknown,
528
they are probably minimal given the lack of weaponry and potential for injury (Reichert and Gerhardt 2011). Furthermore, as
hypothesized by Cody (1969, 1973), similarity in aggressive signals may in fact be selected for in some cases when heterospecific
aggression is a particularly important component of a species’ life
history. Our results cannot directly address hypotheses of character
convergence or divergence in aggressive signals because we did not
sample from a large range of populations in both sympatry and
allopatry for each species. Nevertheless, the limited information on
geographical variation in aggressive signals from this study and that
of a previous study of these species (Pierce and Ralin 1972) suggests that the presence of heterospecifics may not have any effects
on aggressive-call structure. There were no obvious differences
between the aggressive calls of male H. chrysoscelis from a sympatric
population in Missouri and an allopatric population in Florida. In
addition, characteristics of the aggressive calls of male H. chrysoscelis measured by Pierce and Ralin (1972) from populations in Texas
that were likely sympatric with H. versicolor are within the range of
variation in aggressive calls for the 2 populations of H. chrysoscelis measured in this study. Pierce and Ralin (1972) also presented
measurements of males from 2 populations of H. versicolor in Texas
that were largely similar to the data we present for H. versicolor
from an allopatric population in Missouri. The only major difference between the 2 studies is that Pierce and Ralin (1972) found
that the aggressive calls of both H. chrysoscelis and H. versicolor were
amplitude modulated, whereas in the present study, H. versicolor was
found to be much less likely to have amplitude-modulated calls than
H. chrysoscelis. However, the conclusions of Pierce and Ralin (1972)
are apparently based on measurements of only 2 male H. versicolor,
and as we noted above, our study found some overlap in the extent
to which the calls of each species showed amplitude modulation.
Thus, there is some evidence for differences at the species level in
aggressive-call structure, although we caution that sampling over a
much larger geographic range using uniform recording techniques
and accounting for variation in mass is necessary before any firm
conclusions can be reached.
A related question is whether the differences in aggressive-call
structure described here are meaningful to receivers. The staged
interactions showed that individuals responded to aggressive signals of heterospecifics, and we can conclude that the differences
between the species’ calls are insufficient to eliminate heterospecific
aggression. Thus, selection for character displacement of aggressive signals is probably weak at best in this system and several alternative hypotheses can be posed to explain species divergence in
aggressive calls. First, there may be differences in the signal characteristics that are important for intraspecific aggressive interactions.
For example, the amplitude modulation of aggressive calls may be
a relevant signal in interactions between male H. chrysoscelis but not
between male H. versicolor. Second, the differences between the 2
species’ aggressive calls may be driven by divergence in advertisement calls that, due to a shared vocal production system, resulted in
correlated changes in aggressive-call characteristics. Evidence consistent with such a process was found in the tree frog Dendropsophus
ebraccatus, in which there were strong positive between-individual
correlations between advertisement and aggressive-call characteristics even though these characteristics tend to vary in opposite
directions within individuals in response to competition (Reichert
2013b). Third, the differences between the aggressive calls of the
2 species could be an incidental consequence of drift since the 2
lineages diverged. These hypotheses can be addressed by playbacks
testing the effects of variation in aggressive-call characteristics on
Behavioral Ecology
the responses of receivers of each species, measurements of correlated selection on advertisement and aggressive-call characteristics,
and a more thorough sampling of geographic variation in aggressive calls. Likewise, comparative studies of aggressive calls across a
range of species could reveal broader patterns in the diversification
of aggressive-signal characteristics. There has been little work to
date on this subject (Owen PC, unpublished data).
Differences in receiver responses and contest
structure
Perhaps the most significant results of this study were the differences
in behavior of males in interactions that were staged either between
2 conspecific H. versicolor or interspecific interactions between a male
H. versicolor and a male H. chrysoscelis. Interspecific interactions tended
to be longer and more escalated than intraspecific interactions.
Predictions for interaction duration and likelihood of aggression
are unclear for heterospecific interactions and depend on not only
the expected degree of resource overlap but also on the response
function of individuals to variation in signals characteristic of conspecifics and heterospecifics (Ord and Stamps 2009). Although the
resource under dispute, the calling space, is presumably identical
in intraspecific and interspecific interactions of these 2 species, the
negative consequences of a nearby competitor may differ, leading
to differences in the predicted behaviors of individuals in these 2
situations. Specifically, a major negative effect of nearby competitors is that overlap from their calls may reduce an individual’s likelihood of attracting a mate because females are more attracted to
calls that are free from overlap or spatially separated from the source
of overlap (Schwartz and Wells 1983b; Schwartz 1987; Schwartz
and Gerhardt 1995). Interestingly, the effects of heterospecific call
overlap are asymmetric in these 2 species. Marshall et al. (2006) presented females of each species with playbacks simulating call overlap between a conspecific and a heterospecific. Surprisingly, female
H. versicolor almost always chose the heterospecific call in this situation, likely because these calls happened to contain more leading
pulses, which are strongly attractive to females (Marshall et al. 2006;
Marshall and Gerhardt 2010). A caveat in the context of this study
is that such masking was contingent on complete overlap of all of
the advertisement calls presented to the females. Although complete
overlap is probably very rare in natural vocal interactions, we note
that the incidence of call overlap increases substantially when males
interact at close range (Reichert and Gerhardt 2013b). In contrast,
females of H. chrysoscelis generally chose the speaker broadcasting
conspecific calls. Thus, a male H. versicolor may have more to lose
by the presence of a heterospecific competitor than would a male
H. chrysoscelis. Because of this, male H. versicolor may be expected to
be more likely to initiate aggressive behaviors in this situation, and
in fact because of the asymmetry in costs, perhaps be more likely to
win interactions against H. chrysoscelis (Maynard Smith and Parker
1976; Hammerstein and Parker 1982). Although the latter prediction was not fulfilled in this study, and for the most part the contestant’s behaviors were relatively evenly matched, it is interesting
in this context that when interactions escalated to the most intense
level, physical fighting, physical contact was nearly always instigated
by H. versicolor. A similar asymmetry was apparent in the aggressivethreshold measurements. Although H. versicolor males were equally
likely to respond with aggressive calls to both conspecific and heterospecific stimuli, H. chrysoscelis males responded less to the heterospecific than to the conspecific stimulus. Asymmetries in the aggressive
responses of members of the 2 species are a typical feature of interspecific aggressive interactions (Schwartz and Wells 1985; Robinson
Reichert and Gerhardt • Interspecific aggression in tree frogs
and Terborgh 1995; Tobias and Seddon 2009; Jankowski et al.
2010). However, it is generally unknown whether such asymmetrical responses are caused by varying costs and benefits of aggressive
interactions among the species involved or if these may simply stem
from unequal divergence of signal recognition mechanisms between
species.
Another intriguing result of this study involved the behaviors
expressed by contest losers. Losers of interspecific interactions
usually moved away from their opponent, whereas previous studies of intraspecific interactions in H. versicolor showed that losers
usually remain in place near the winner but cease calling behavior
(Reichert and Gerhardt 2011). The latter behavior is analogous to,
and may in fact be an example of, satellite behavior, an alternative mating tactic in which noncalling individuals position themselves near calling individuals and attempt to intercept approaching
females (Halliday and Tejedo 1995). Interestingly, satellite behavior
has been shown to be a conditional strategy in some species. That
is, individuals can switch between calling and satellite behavior
based on their own condition or competitiveness relative to that of
their nearby competitors (Castellano et al. 2009; Humfeld 2013).
Furthermore, some studies have demonstrated that satellites preferentially associate with more attractive individuals (Humfeld 2008;
Brepson et al. 2012). The losing behavior in the aggressive interactions of gray tree frogs in which individuals stop calling may therefore be a conditional strategy in which less competitive individuals
choose to adopt a satellite strategy rather than move somewhere
else and call. Although this hypothesis remains speculative, the finding in this study that individuals are more likely to move away from
a heterospecific opponent than they are to move away from a conspecific opponent adds weight to this argument. Whether or not
males recognize their opponent as a heterospecific, it is likely that
they are responsive to variation in its calls and that heterospecific
calls are at the extreme low end of the continuum of call attractiveness. In any event, avoidance of satellite behavior near unattractive
males would have the additional effect of avoidance of mismatings
with heterospecific females.
Conclusions
We conclude that interspecific interactions in the 2 species of gray
tree frog are structured similarly to intraspecific interactions but
have some unique behavioral consequences. We must emphasize,
however, that these conclusions are necessarily limited because
we did not sample across multiple sympatric and allopatric populations across the full range of each species. Indeed, we hope the
results of this study will prompt more detailed studies of geographical variation in aggressive behavior and signal characteristics. Our
findings demonstrate that such studies not only should test hypotheses related to patterns of convergence or divergence of aggressive
signals but also should examine variation in receiver responses to
aggressive signals and variation in the structure and dynamics of
contests. All of these factors are likely to be influenced by interactions with heterospecifics and therefore the study of interspecific
aggression should continue to provide many valuable insights relating to topics as diverse as signal evolution, species interaction and
distribution, and the costs and consequences of aggressive behavior.
Supplementary Material
Supplementary material can be found at http://www.beheco.
oxfordjournals.org/
529
Funding
Financial support was provided by a U.S. National Science
Foundation doctoral dissertation improvement grant (IOS
1010791), a Graduate Assistance in Areas of National Need fellowship from the University of Missouri and the U.S. Department
of Education (P200A100178), and grants from the Chicago
Herpetological Society, the Gaige Fund of the American Society for
Ichthyologists and Herpetologists and a Dean E. Metter Memorial
Award from the Society for the Study of Amphibians and Reptiles.
Two anonymous reviewers provided helpful comments on a previous draft
of this article. Members of the Gerhardt lab assisted with frog collection:
M. Tucker, J. Merricks, and P. Moler were especially helpful in the collection of H. chrysoscelis. T. Drew, N. Fowler, D. Gruhn, C. Harjoe, W. Li, and
B. Nickelson assisted with the experiments and call analyses. The experimental procedures were approved by the University of Missouri Animal
Care and Use Committee (ACUC protocols # 1910 and 6546).
Handling editor: Bob Wong
References
Adams DC. 2004. Character displacement via aggressive interference in
Appalachian salamanders. Ecology. 85:2664–2670.
Arnott G, Elwood RW. 2009. Assessment of fighting ability in animal contests. Anim Behav. 77:991–1004.
Brepson L, Troïanowski M, Voituron Y, Lengagne T. 2012. Cheating
for sex: inherent disadvantage or energetic constraint? Anim Behav.
84:1253–1260.
Brzoska J. 1982. Vocal response of male European water frogs (Rana esculenta
complex) to mating and territorial calls. Behav Process. 7:37–47.
Castellano S, Marconi V, Zanollo V, Berto G. 2009. Alternative mating tactics in the Italian treefrog, Hyla intermedia. Behav Ecol Sociobiol.
63:1109–1118.
Christie K, Schul J, Feng A. 2010. Phonotaxis to male’s calls embedded
within a chorus by female gray treefrogs, Hyla versicolor. J Comp Physiol
A. 196:569–579.
Cody ML. 1969. Convergent characteristics in sympatric species: a possible
relation to interspecific competition and aggression. Condor. 71:222–239.
Cody ML. 1973. Character convergence. Annu Rev Ecol Syst. 4:189–211.
Donnelly MA, Guyer C. 1994. Patterns of reproduction and habitat use in
an assemblage of Neotropical hylid frogs. Oecologia. 98:291–302.
Duellman WE, Pyles RA. 1983. Acoustic resource partitioning in anuran
communities. Copeia. 1983:639–649.
Ebersole J. 1977. The adaptive significance of interspecific territoriality in
the reef fish Eupomacentrus leucostictus. Ecology. 58:914–920.
Gayou DC. 1984. Effects of temperature on the mating call of Hyla versicolor. Copeia. 1984:733–738.
Gerhardt HC. 1975. Sound pressure levels and radiation patterns of the
vocalizations of some North American frogs and toads. J Comp Physiol
A. 102:1–12.
Gerhardt HC. 2001. Acoustic communication in two groups of closely
related treefrogs. Adv Study Behav. 30:99–167.
Gerhardt HC, Doherty JA. 1988. Acoustic communication in the gray
treefrog, Hyla versicolor: evolutionary and neurobiological implications. J
Comp Physiol A. 162:261–278.
Gerhardt HC, Ptacek MB, Barnett L, Torke KG. 1994. Hybridization in
the diploid-tetraploid treefrogs Hyla chrysoscelis and Hyla versicolor. Copeia.
1994:51–59.
Gerhardt HC, Schwartz JJ. 1995. Interspecific interactions in anuran courtship. In: Heatwole H, Sullivan BK, editors. Amphibian biology, volume 2:
social behavior. Chipping Norton (Australia): Surrey Beatty. p. 603–632.
Given MF. 1990. Spatial distribution and vocal interaction in Rana clamitans
and R. virgatipes. J Herpetol. 24:377–382.
Green JP, Field J. 2011. Assessment between species: information gathering
in usurpation contests between a paper wasp and its social parasite. Anim
Behav. 81:1263–1269.
Grether GF, Anderson CN, Drury JP, Kirschel AN, Losin N, Okamoto
K, Peiman KS. 2013. The evolutionary consequences of interspecific
aggression. Ann N Y Acad Sci. 1289:48–68.
530
Grether GF, Losin N, Anderson CN, Okamoto K. 2009. The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol Rev. 84:617–635.
Halliday T, Tejedo M. 1995. Intrasexual selection and alternative mating
behavior. In: Heatwole H, Sullivan B, editors. Amphibian biology, volume 2: social behavior. Chipping Norton (Australia): Surrey Beatty. p.
419–468.
Hammerstein P, Parker GA. 1982. The asymmetric war of attrition.
J Theor Biol. 96:647–682.
Holloway AK, Cannatella DC, Gerhardt HC, Hillis DM. 2006. Polyploids
with different origins and ancestors form a single sexual polyploid species.
Am Nat. 167:E88–E101.
Humfeld SC. 2008. Intersexual dynamics mediate the expression of satellite
mating tactics: unattractive males and parallel preferences. Anim Behav.
75:205–215.
Humfeld SC. 2013. Condition-dependent signaling and adoption of
mating tactics in an amphibian with energetic displays. Behav Ecol.
24:859–870.
Jankowski JE, Robinson SK, Levey DJ. 2010. Squeezed at the top: interspecific aggression may constrain elevational ranges in tropical birds.
Ecology. 91:1877–1884.
Keller MJ, Gerhardt HC. 2001. Polyploidy alters advertisement call structure in gray treefrogs. Proc Biol Sci. 268:341–345.
Laiolo P. 2012. Interspecific interactions drive cultural co-evolution and
acoustic convergence in syntopic species. J Anim Ecol. 81:594–604.
Lehtonen TK, McCrary JK, Meyer A. 2010. Territorial aggression can
be sensitive to the status of heterospecific intruders. Behav Process.
84:598–601.
Marshall V, Schwartz J, Gerhardt HC. 2006. Effects of heterospecific call
overlap on the phonotactic behaviour of grey treefrogs. Anim Behav.
72:449–459.
Marshall VT, Gerhardt HC. 2010. A precedence effect underlies preferences for calls with leading pulses in the grey treefrog, Hyla versicolor.
Anim Behav. 80:139–145.
Martin P, Martin T. 2001. Behavioral interactions between coexisting species: song playback experiments with wood warblers. Ecology.
82:207–218.
Maynard Smith J, Parker GA. 1976. The logic of asymmetric contests.
Anim Behav. 24:159–175.
Maynard Smith J, Price GR. 1973. The logic of animal conflict. Nature.
246:15–18.
McGregor P, Catchpole C, Dabelsteen T, Falls J, Fusani L, Gerhardt HC,
Gilbert F, Horn A, Klump G, Kroodsma D, et al. 1992. Design and interpretation of playback: the Thornbridge Hall NATO ARW consensus.
In: McGregor P, editor. Playback and studies of animal communication.
New York: Plenum Press. p. 1–9.
Mikami OK, Kawata M. 2004. Does interspecific territoriality reflect the
intensity of ecological interactions? A theoretical model for interspecific
territoriality. Evol Ecol Res. 6:765–775.
Milinski M, Parker GA. 1991. Competition for resources. In: Krebs JR,
Davies NB, editors. Behavioural ecology: an evolutionary approach.
London: Blackwell Scientific. p. 137–168.
Murray B. 1971. The ecological consequences of interspecific territorial
behavior in birds. Ecology. 52:414–423.
Murray B. 1976. A critique of interspecific territoriality and character convergence. Condor. 78:518–525.
Murray B. 1981. The origins of adaptive interspecific territorialism. Biol
Rev. 56:1–22.
Ord TJ, Stamps JA. 2009. Species identity cues in animal communication.
Am Nat. 174:585–593.
Orians GH, Willson MF. 1964. Interspecific territories of birds. Ecology.
45:736–745.
Peiman KS, Robinson BW. 2007. Heterospecific aggression and adaptive divergence in brook stickleback (Culaea inconstans). Evolution.
61:1327–1338.
Peiman KS, Robinson BW. 2010. Ecology and evolution of resource-related
heterospecific aggression. Q Rev Biol. 85:133–158.
Behavioral Ecology
Pierce JR, Ralin DB. 1972. Vocalizations and behavior of the males of
three species in the Hyla versicolor complex. Herpetologica. 28:329–337.
Platz JE, Forester DC. 1988. Geographic variation in mating call among
the four subspecies of the chorus frog: Pseudacris triseriata (Wied). Copeia.
1988:1062–1066.
Ptacek MB. 1992. Calling sites used by male gray treefrogs, Hyla versicolor
and Hyla chrysoscelis, in sympatry and allopatry in Missouri. Herpetologica.
48:373–382.
Reichert MS. 2013a. Sources of variability in advertisement and aggressive calling in competitive interactions in the grey treefrog, Hyla versicolor.
Bioacoustics. 22:195–214.
Reichert MS. 2013b. Patterns of variability are consistent across signal types
in the treefrog Dendropsophus ebraccatus. Biol J Linn Soc. 109:131–145.
Reichert MS, Gerhardt HC. 2011. The role of body size on the outcome,
escalation and duration of contests in the grey treefrog, Hyla versicolor.
Anim Behav. 82:1357–1366.
Reichert MS, Gerhardt HC. 2012. Trade-offs and upper limits to signal
performance during close-range vocal competition in gray tree frogs Hyla
versicolor. Am Nat. 180:425–437.
Reichert MS, Gerhardt HC. 2013a. Gray tree frogs, Hyla versicolor, give
lower-frequency aggressive calls in more escalated contests. Behav Ecol
Sociobiol. 67:795–804.
Reichert MS, Gerhardt HC. 2013b. Socially mediated plasticity in call timing in the gray tree frog, Hyla versicolor. Behav Ecol. 24:393–401.
Robinson S, Terborgh J. 1995. Interspecific aggression and habitat selection
by Amazonian birds. J Anim Ecol. 64:1–11.
Rose GJ, Brenowitz EA. 1991. Aggressive thresholds of male Pacific treefrogs for advertisement calls vary with amplitude of neighbors’ calls.
Ethology. 89:244–252.
Schluter D. 2000. Ecological character displacement in adaptive radiation.
Am Nat. 156:S4–S16.
Schwartz JJ. 1987. The function of call alternation in anuran amphibians: a
test of three hypotheses. Evolution. 41:461–471.
Schwartz JJ, Buchanan BW, Gerhardt HC. 2001. Female mate choice in the
gray treefrog (Hyla versicolor) in three experimental environments. Behav
Ecol Sociobiol. 49:443–455.
Schwartz JJ, Gerhardt HC. 1995. Directionality of the auditory system and
call pattern recognition during acoustic interference in the gray tree frog,
Hyla versicolor. Audit Neurosci. 1:195–206.
Schwartz JJ, Wells KD. 1983a. An experimental study of acoustic interference between two species of neotropical treefrogs. Anim Behav.
31:181–190.
Schwartz JJ, Wells KD. 1983b. The influence of background noise on
the behavior of a Neotropical treefrog, Hyla ebraccata. Herpetologica.
39:121–129.
Schwartz JJ, Wells KD. 1984. Interspecific acoustic interactions of the
Neotropical treefrog Hyla ebraccata. Behav Ecol Sociobiol. 14:211–224.
Schwartz JJ, Wells KD. 1985. Intraspecific and interspecific vocal behavior
of the Neotropical treefrog Hyla microcephala. Copeia. 1985:27–38.
Shimoyama R. 1999. Interspecific interactions between two Japanese pond
frogs, Rana porosa brevipoda and Rana nigromaculata. Jpn J Herpetol. 18:7–15.
Tanner CJ, Adler FR. 2009. To fight or not to fight: context-dependent
interspecific aggression in competing ants. Anim Behav. 77:297–305.
Tobias JA, Seddon N. 2009. Signal design and perception in Hypocnemis antbirds: evidence for convergent evolution via social selection. Evolution.
63:3168–3189.
Tynkkynen K, Rantala MJ, Suhonen J. 2004. Interspecific aggression and
character displacement in the damselfly Calopteryx splendens. J Evol Biol.
17:759–767.
Wasserman AO. 1970. Polyploidy in the common tree toad Hyla versicolor Le
Conte. Science. 167:385–386.
Wells KD. 1980. Behavioral ecology and social organization of a dendrobatid frog (Colostethus inguinalis). Behav Ecol Sociobiol. 6:199–209.
Wells KD, Schwartz JJ. 2007. The behavioral ecology of anuran communication. In: Narins PM, Feng AS, Fay RR, Popper AN, editors. Hearing
and sound communication in amphibians. Springer handbook of auditory research. Vol. 28. New York: Springer-Verlag. p. 44–86.