Introductory tail-flick of the Jacky dragon visual display: signal efficacy depends upon duration
Animal Behaviour Laboratory and Department of Psychology, Macquarie University, Sydney, NSW 2109, Australia
* Author for correspondence (e-mail: richard{at}galliform.psy.mq.edu.au)
Accepted 13 August 2003
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Summary |
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Key words: Jacky dragon, Amphibolurus muricatus, signal design, visual ecology, movement-based signals, tail-flick
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Introduction |
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Structural differences between the signal and background noise are not
always sufficient for reliable detection. Many animal signals also have
introductory components, which are designed to alert intended receivers to the
elements that follow (Wiley and Richards,
1982; Fleishman,
1992
). In songs and calls, the attention of conspecifics is
typically engaged by high intensity sounds with simple structure and short
duration (Wiley and Richards,
1982
). The initial portions of some movement-based visual signals
have similar properties (Fleishman,
1988b
). Lizards (Anolis auratus) increase the amplitude
of push-ups in the first part of their display when the intended receiver is
distant and may not be oriented toward them (`assertion displays'). These
initial push-ups have greater velocity and acceleration, but shorter duration,
than those that follow and are not accompanied by dewlap extension and
contraction. When the receiver is close and detection is straightforward,
there is little variation in push-up structure over the course of the display
(`challenge displays'), and the amplitude of these movements is lower than
that in assertion displays (Fleishman,
1988b
).
High amplitude push-ups are required to generate the velocity and
acceleration characteristics necessary to engage a visual grasp reflex
(Fleishman, 1992). In a series
of experiments using artificial lures, Fleishman
(1986
) showed that responses
were sensitive to movement amplitude and that abrupt changes in position
(square waveform) were more effective than smooth sinusoidal waveforms. When
velocity and acceleration were continuously varied, response probability was
greatest to the stimulus that had large values for both of these parameters.
The sensory properties of A. auratus lizards are thus well matched to
display structure, and have likely influenced the design of this signal.
Quantitative analysis of the movement-based visual display of another
lizard, the Jacky dragon Amphibolurus muricatus, suggests an
alternative strategy for attracting the attention of receivers
(Peters and Evans, 2003).
Displays consist of five distinct motor patterns, which are produced in an
obligatory sequence (Peters and Ord, in
press
). The initial component is always a tail-flick. This
achieves lower velocity and acceleration values than the other components, but
sweeps a large region of the visual field and has much greater duration than
the motor patterns that follow it (Peters
and Evans, 2003
). Short displays may be ineffective for attracting
the attention of receivers in this system, regardless of intensity.
Introductory motor patterns with long duration confer the obvious benefit of
increasing the time period available for signal detection. The tail-flick of
the Jacky dragon display, and the assertion display of A. auratus,
may hence be different design solutions to the same functional problem.
Both of these signals are highly conspicuous against their respective
backgrounds of wind-blown vegetation (A. auratus:
Fleishman, 1988a; Jacky
dragon: Peters and Evans,
2003
); however, almost all of the motor patterns in the visual
display of the Jacky dragon have velocity characteristics distinct from those
of background plant movement (Peters and
Evans, 2003
), so conspicuousness alone is not sufficient to
explain why the tail-flick is invariably used as the introductory component.
In the present study, we explore the efficacy of Jacky dragon tail-flicks in
order to identify the additional factors that must be invoked fully to account
for signal design.
To assess signal processing by receivers we used digital video playback,
which has previously been shown to be highly effective in this system
(Ord et al., 2002b). Increased
control over stimulus parameters was achieved by using a digitally animated
tail. This approach allows precise mathematical definition of movement and
hence is becoming increasingly popular for work on movement-based signals
(Clark and Uetz, 1993
;
Evans et al., 1993
;
Rosenthal and Evans, 1998
;
Clark and Stephenson, 1999
;
Nicoletto and Kodric-Brown,
1999
; Morris et al.,
2003
). We began by validating the use of the computer-generated
tail, comparing responses to digital video footage of a lizard tail-flick with
those of a precisely matched 3-D animation (Experiment 1). We then examined
the effects of variation in stimulus speed, acceleration, duration and period
by expanding and compressing the time scale of the sequence (Experiment 2).
The results of this experiment identified several variables that might mediate
recognition. These were varied systematically in two follow-up playback
studies that assessed the importance of tail-flick amplitude (Experiment 3)
together with movement speed and signal duration (Experiment 4).
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Materials and methods |
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All experiments were carried out between July 2002 and January 2003. Twenty lizards were used in each of the four experiments, although any individual animal was used in no more than two. Subjects will eventually be released at the site of capture. Housing and experimental procedures were approved by the Macquarie University Animal Care and Ethics Committee (Protocol No. 2001/014) and the NSW National Parks and Wildlife Service (License No. B2125).
Design
Our general approach was based upon a long tradition of successful playback
experiments in bioacoustics (reviewed by
Gerhardt and Huber, 2002). To
obtain sufficient control over the tail-flick motor pattern, it was necessary
to use a completely synthetic stimulus in which all of the aspects of
morphology and movement could be defined precisely. First, we tested the
effectiveness of this computer-generated animation against that of the
representative digital video sequence upon which it was modelled (Experiment
1). Note that this comparison does not involve pseudoreplication
(Kroodsma, 1989
), in the sense
of using a sample size inappropriate to the hypothesis being tested
(McGregor et al., 1992
),
because our question was precisely framed: we wished to determine whether a
particular animation was matched in effectiveness to a natural exemplar,
rather than to establish that all stimuli drawn from these two populations
would evoke indistinguishable responses. In this case, adding exemplars would
actually have degraded the experimental design by increasing the probability
of Type II error (i.e. we would have been more likely to fail to detect a
subtle deficiency in the animation). This initial `calibration' test was
followed by a series of three further playback experiments (24), all
using synthetic sequences only. The issue of pseudoreplication does not arise
in these experiments because the populations of interest are each fully
characterised by the single stimulus used to represent them (i.e. there was
zero variance in parameters other than those manipulated).
We varied tail-flick duration, speed, amplitude, number of direction changes (reversals), period (time elapsed between the beginning of successive flicks) and duty cycle (proportion of the stimulus containing movement). Changes in tail-flick speed for stimuli of equal duration necessarily produced corresponding changes in acceleration. The tail-flick is a complex movement, and several properties are highly correlated in natural sequences. Our strategy was hence to manipulate a different subset of motion variables in each experiment (Table 1), so as to isolate the feature(s) responsible for evoking an orienting response.
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The simplest description of tail-flick structure is obtained by tracking
the position of the tail tip in each frame, and then calculating the Euclidean
distance between these coordinates and the corresponding values in the first
frame of the sequence. These data define a display action pattern (DAP;
Fig. 1A), which has
traditionally been used to depict display structure
(Carpenter et al., 1970). The
number of reversals is reflected in the number of peaks in the DAP, while the
duty cycle describes the proportion of frames containing motion.
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Playback procedure
Our test setup was based upon one used in a recent video playback study
(for a detailed description, see Ord et
al., 2002b). All stimuli were presented on a Sony PVM-14M2A colour
monitor (resolution >600 lines; screen size 34 cmmeasured diagonally). In
Experiment 1, sequences were stored on an Apple PowerBook G3 running Final Cut
Pro 2 (Apple Computer Inc.). Video was streamed as a digital signal to a Sony
GV-D300E mini-DV deck, using an IEEE 1394 Firewire interface. The S-video
analog output from the deck was then connected to the Sony monitor. The
digital video sequences for Experiments 2, 3 and 4 were too large to store on
the computer, so these were played from digital videotape (Sony DVM60EX2)
using the same deck as in Experiment 1. In both of these techniques, stimulus
resolution was limited only by the PAL DV standard (5:1 compression;
horizontal resolution 550 lines; 25 frames s1).
Lizard responses were recorded using a Panasonic WV-CP240 CCTV camera with
a WV-LZ62/2 lens, connected to a VHS video deck. All stimuli were presented
with the soundtrack muted, but a marker tone (inaudible to the subject lizard)
was dubbed directly to the VHS deck so that responses could later be scored
relative to stimulus onset. We conducted all playback tests between 08:00 h
and 12:00 h, which corresponds to the period of peak activity in our captive
population (Ord, 2001).
Presentation time was standardised within each lizard, so that the
inter-playback interval was always approximately 24 h.
The movie sequences are available in the Supplementary material to this paper and also at: http://galliform.bhs.mq.edu.au/lizard/supplement.html.
Statistical analysis
Our dependent measure was the orienting response, which we operationally
defined as an observable movement of the head toward the monitor. For each
stimulus presentation, we scored whether or not an orienting response occurred
and latency to the nearest frame (temporal resolution 40 ms).Lizards that
failed to respond to any of the stimuli in an experiment were excluded from
analyses.
We used Friedman's analyses of variance (ANOVAs) to assess variation in the probability of response over all stimuli, followed by Wilcoxon signed-ranks tests for pairwise comparisons between conditions. Formal analyses of response latencies could only be conducted for Experiments 1 and 3. The stimuli used in Experiments 2 and 4 varied in duration, and this would have introduced a systematic bias in response latencies if we had considered the whole stimulus presentation. To overcome this, we windowed responses, and considered only those that occurred within a period equivalent to the duration of the shortest sequence (42 frames in both experiments). In addition, only lizards that responded to all stimuli in our repeated measures design could be included in standard statistical models. With both of these constraints in place, our effective sample size for latency analysis was reduced to two animals in Experiment 2 and zero in Experiment 4.
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Results |
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Stimulus sequences
Videorecorded tail-flick
We randomly selected a digital video sequence from an archival collection
that depicted a Jacky dragon tail-flicking on a wooden perch
(Fig. 2). Full details of
recording procedure are presented in Ord et al.
(2002b). Footage was edited,
using Final Cut Pro 2 software on a Macintosh G4/500 computer (Apple Computer
Inc.), to isolate the tail-flick motor pattern. We added fade transitions
before and after the tail-flick to avoid spurious orienting responses that
might be caused by an abrupt change in the displayed image. The final stimulus
(LIVE) consisted of 10 s of an empty perch before the lizard's tail faded into
view (1 s), and then remained stationary for a further 1 s before a single
bout of continuous flicking (162 frames, 6.5 s). The tail then faded away (1
s), and an empty perch was presented for a further 10 s. A black mask was
added to the right side of each video frame to conceal the lizard's body
(Fig. 2).
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Animated tail-flick
Construction of the 3-D computer-generated tail-flick sequence (ANIMATED)
involved the following steps: (1) building a model with appropriate shape and
surface markings, (2) manipulating the model to match the live sequence, (3)
adjustments to lighting to match the natural exemplar, followed by sequence
rendering and (4) final editing to overlay the synthetic tail on the same
digital video background as in the LIVE tail-flick sequence, and also to add
identical fades and mask. The following description provides a brief overview
of procedure; recent reviews provide additional background on the use of
computer animation to create visual stimuli
(Kunzler and Bakker, 1998;
Clark and Stephenson, 1999
;
Nicoletto and Kodric-Brown,
1999
; Rosenthal,
1999
).
Model construction. Measurements of tail morphology from the time of recording were not available, so current measurements were used as an approximation (other physical data showed only moderate growth: 3 mm increase in snoutvent length and 3 g mass increase). We measured overall tail length, as well as diameter at equally spaced points along the tail. Digital photographs of the tail were taken from above and from the sides, using a Panasonic NV-DS15 digital video camcorder, and then transferred to computer for editing.
We used the modeller module of LightWave 3D v6 (NewTek Inc. 2001, San Antonio, TX, USA) to construct the synthetic tail. Briefly, we began with a cylindrical object scaled to match the length of the real tail, and then modified this using shaping functions to match the circumference at each point. We then used the digital photographs of real tail skin to create a texture map of the tail in Adobe Photoshop v6 (Adobe Systems Inc.), which was overlaid onto the 3-D wire-frame model. This process produced a tail structure with shape and surface characteristics that closely resembled those of the original.
Animating the 3-D model. We used the animation module of LightWave
to define changes in position over time, so that the movement of the synthetic
tail matched precisely that of the original. To assist in this process, we
added a skeleton, made up of 24 artificial `bones'. These are invisible
elements that facilitate adjustment of a model in which there is both global
displacement and local movement of some sectors, relative to others. To
animate the tail, we used a technique known as `rotoscoping'
(Gatesy et al., 1999). This
involved superimposing the computer-generated model over sequential frames
from the original sequence, and then adjusting the model to match each
one.
The LIVE sequence was exported as a series of still images using MovieShop v 5.2 software, on a DraCo nonlinear video editing workstation (MS MacroSystem Computer GmbH). The first frame was then used to determine the appropriate position of the animation `camera' in three-dimensional space, so that the artificial tail would be rendered from the same perspective as the real one. LightWave allows manipulation of the spatial location of each bone in three planes (x, y and z), as well as orientation and range of movement. To achieve a match, it was necessary to utilise this level of control, making judgements about how the tail would move that took into account both the shape required in future frames and the mechanical constraints of the bones. Once the model matched the background image, a `key-frame' was used to save the location of all bones. We then advanced to the next animation frame, imported the next image in the video tail sequence, and repeated the process for the whole sequence. Although LightWave has powerful interpolation algorithms, manual definition of tail location in each of 162 frames ensured the closest possible match between the VIDEO and ANIMATED tail-flicks.
Lighting and sequence export. The last stage in the animation process was to add `lights' to the scene in locations that matched those used in the original videorecording setup. We selected a random frame in the original sequence and measured Red, Green and Blue values at three different points on the tail using Photoshop. We then adjusted light specifications (angle, intensity and hue), rendered a single frame to compare model and original values, and iterated this process. The animated tail was then exported as a digital video (DV) stream with a homogenous black background.
Final editing. The DV stream was imported into Final Cut Pro 2 and then combined with background video footage from the original lizard filming setup, so that the only difference between the two finished sequences was that the tail was recorded in one case and animated in the other. We used a chroma-key effect to make the black region of each frame transparent and then combined these with video recordings of the empty perch, so that the animated tail was superimposed on the same structure and background as the video exemplar (Fig. 2). A black mask was then added to the right-hand side of each frame.
Quantitative comparison of movement
In a recent paper (Peters et al.,
2002), we describe our strategy for exploring the design of
dynamic visual signals and show that local changes in image intensity can be
used to measure the direction and speed of motion (see also
Zeil and Zanker, 1997
). A
summary estimate for speed over time can be calculated by averaging velocity
magnitude (i.e. vector length) over the whole sequence
(Peters et al., 2002
;
Peters and Evans, 2003
). We
compared movement in the two sequences using DAP profiles
(Fig. 1A), and average speed
and acceleration (Fig. 1B,C).
These complementary analyses reveal that the video and animated sequences were
closely matched on all parameters. Full details of analysis procedures can be
found elsewhere (Peters et al.,
2002
; Peters and Evans,
2003
).
Playback
We presented tail-flick sequences twice each to 20 lizards, over 4
successive days. The first frame of the stimulus depicted an empty perch in
both cases; this appeared on the monitor from the start of the session. We
waited until the lizard was oriented away from the front before cueing the
stimulus (mean 255±75 s, mean ± S.D.). We used a
randomised block design in which half of the lizards were shown the stimuli in
the order VIDEOANIMATION and the other half ANIMATIONVIDEO. Each
group was then retested with the reverse sequence. Order effects were thus
controlled both by random assignment at the group level and by
counter-balancing within individual. Two lizards were excluded from the
analysis because they did not respond to any of the stimuli.
Results
Both stimuli were highly effective; 68 of the 72 presentations evoked an
orienting response. There was no difference between VIDEO and ANIMATED in the
proportion of sequences that evoked a response (Friedman's
2=2.000; d.f.=3; P=0.572). The mean latency to
respond was also very similar (Fig.
3), and did not differ between the two stimulus types
(t=0.66, d.f.=17, P=0.515). We used power analysis (Power
& Effect 2.0.3) to assess the probability of Type II error; this revealed
a very small estimated effect size (
2=0.016).
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Experiment 2
Experiment 1 showed that computer-generated and video tail-flicks are
equally effective in eliciting orienting responses. This finding validated the
use of animated stimuli for the remaining experiments of this series, each of
which required a highly controlled manipulation of movement characteristics
(see Introduction). In Experiment 2, we manipulated the duration of the
ANIMATED tail-flick used in Experiment 1. This produced sequences in which the
tail moved through a nearly identical series of x, y, z coordinates,
but over varying time periods (Fig.
4), with concomitant differences in speed and acceleration.
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Stimulus sequences
The response latencies for the ANIMATED tail-flick used in Experiment 1
indicated that when orienting responses were evoked, these occurred well
before the end of the sequence. To avoid a ceiling effect, we only used the
first half of the original sequence (82 of 161 frames), and scaled the tail to
half its original size. This represents an apparent distance of 1.50 m from
the observer. The time scale was then systematically varied using LightWave,
without changing other parameters that define movement, such as amplitude and
plane of motion (Fig. 4).
Increased duration was achieved by interpolating between the key-frames
defined in the original sequence. This technique ensures smooth slow motion
and produces much better results than the algorithms available in
video-editing software, which simply repeat frames, producing discontinuous
motion.
The time base was expanded to create sequences that were longer than the
original, and compressed to produce shorter ones. We selected three stimuli
that sampled the natural range observed in our captive population. In addition
to the original sequence (NORMAL), we used sequences that were 0.5x
(FAST) and 5.0x (SLOW) the duration of NORMAL. We also included a
sequence 7.5x the original duration (SLOWER), which is probably outside
the natural range. This design allowed us to test whether lizard responses are
approximately matched to the distribution of conspecific tail-flick durations,
and also to evaluate the alternative possibility that exceptionally long
signals might prove more effective (i.e. supernormal;
Tinbergen, 1951).
In Experiment 1, we used a homogenous background to maximise stimulus
conspicuousness. However, Jacky dragon displays will usually be seen against
wind-blown vegetation (Peters and Evans,
2003), which acts as background noise. We reasoned that lizards
are likely to habituate to the movement of wind-blown plants
(Fleishman, 1992
) and that
signal efficacy would therefore best be assessed in terms of ability to engage
visual processing after a period spent viewing irrelevant background motion.
This general approach of using background footage videorecorded in the
animal's natural habitat has recently been advocated by Rosenthal
(1999
).
Tail-flick animations were overlaid onto footage of wind-blown plants
(Fig. 5), recorded at the site
where the subject lizards had been caught. A continuous 15 min plant sequence
was used, during which wind speed had varied between 0.7 and 2.2 m
s1. Recording procedure and vegetation movement
characteristics have recently been described
(Peters and Evans, 2003). The
animations and vegetation sequences were combined using a chroma-key effect in
Final Cut Pro, in the same way as the model tail-flick and background in
Experiment 1. The tail appeared at the twelfth and fourteenth minute of each
sequence, and commenced flicking immediately. To assess whether there was an
effect of the tail structure appearing, independent of movement, we added a
control sequence that depicted a stationary tail of the same duration as the
original stimulus (82 frames).
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The five stimuli were presented to 20 lizards on successive days. We used the stationary tail stimulus to obtain a baseline score on the first day. Each lizard was then shown the four animated tail-flick stimuli in a unique random sequence.
Results
There was significant variation in the probability of an orienting response
to the first trial in each sequence (Fig.
6; Friedman's 2=35.415; d.f.=4; P=0.000).
To ensure that this was not simply attributable to a difference between the
four moving stimuli and the non-moving control sequence, we repeated the
analysis with data from the stationary condition excluded. This revealed that
response probability varied significantly as the time base for the tail-flick
was expanded and compressed (Friedman's
2=12.636; d.f.=3;
P=0.005). Pairwise comparisons indicate that the FAST sequence was
significantly less effective than each of the other sequences (NORMAL:
Z=1.667, P=0.048; SLOW: Z=2.828,
P=0.0025; SLOWER: Z=2.449, P=0.007).
Responses to NORMAL were also significantly different from those to the SLOW
stimulus (Z=1.732, P=0.0415). None of the other
comparisons was significant.
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Formal analysis of response latencies was not possible (see Materials and methods). However, examination of the distribution of latencies, relative to tail position, in plots of amplitude over time reveals a marked correspondence between mean response time and the DAP profile (Fig. 4).
Experiment 3
It has been shown previously that lizard responses to moving stimuli are
sensitive to amplitude (Fleishman,
1986). Experiment 3 was designed to test this idea. We
systematically varied tail-flick amplitude, while controlling stimulus
duration. Speed, acceleration, total sweep area and number of reversals also
varied systematically across the stimulus set. Response to these parameters
was assessed by planned comparisons across the amplitude series, and also by
including an additional control sequence.
Stimulus sequences
The modelling process for Experiment 1 produced an animation precisely
matched to a real tail-flick, and Experiment 2 stimuli were created by
expanding and compressing the time scale of this sequence. In this experiment,
it was necessary to manipulate tail-flick parameters in a way that would have
been impractical with the original complex movement, as this included
excursion into the z (depth) plane. Instead, we created a simplified
tail-flick, which was constrained to the xy plane
(i.e. all movement was orthogonal to the camera). The modelling process used
bones as invisible elements that controlled the configuration of the tail
model as before (see methods for Experiment 1), but took advantage of the
structural relationship between these components to better define movement.
Each bone was connected to the next in the series and was set up to have a
restricted range of motion and relative stiffness; bones further from the base
of the tail had a greater range of motion and were lower in stiffness. The
last bone in the series was linked to an invisible target, which allowed us to
manipulate the entire chain by setting a single coordinate location.
LightWave's powerful inverse kinematics algorithms (NewTek), which take into
account each bone's range of motion and stiffness, then calculated the shape
of the tail in each frame, producing realistic flicking movements
(Fig. 7).
|
Stimulus sequences depicted elevation of the tail from its resting position
to one of three maximum amplitudes (measured from the tip of the tail): SMALL,
MEDIUM and LARGE, followed by return along the same path
(Fig. 7). The motor pattern was
then repeated, such that each tail-flick animation swept across the same
number of total pixels (distinct from the number of unique pixels swept, which
covaried with amplitude). Animation DAPs are presented in
Fig. 7. To assess whether there
was an effect of variation in the number of direction changes across the
sequences (24 SMALL to 6 LARGE), we constructed a fourth tail-flick sequence
(CONTROL) that had the same number of reversals as the MEDIUM sequence (12),
but the same amplitude as the LARGE sequence. Velocity estimates
(Peters et al., 2002) were
calculated for each of the tail-flick animations. Mean acceleration did not
differ across the stimuli. The SMALL and MEDIUM animations were matched for
speed, but were faster than the LARGE sequence. The CONTROL sequence matched
the LARGE sequence for average speed.
The tail-flick animations were overlaid onto footage of wind-blown plants, as in Experiment 2. A fifth sequence (BLANK), which depicted the background only, was added to examine spontaneous response to wind-blown vegetation. Stimuli were presented on five successive days. The order of presentation of SMALL, MEDIUM and LARGE tail-flick sequences was randomised across lizards; these stimuli were presented on the first, third and fifth days. The CONTROL and BLANK sequences were then randomly allocated to either the second or fourth day of testing.
Results
No spontaneous orienting responses occurred during the BLANK stimulus
sequence, so we excluded data for this treatment from the analysis
(Fig. 8A). In this experiment,
in which stimuli were matched in duration, differences in tail-flick amplitude
did not affect the probability of an orienting response
(Fig. 8A; Friedman's
2=1.077; d.f.=2; P=0.584), or the latency to respond
(Fig. 8B; F2,12=1.234; P=0.326). Sequences matched for the
number of reversals, but differing in amplitude, also did not differ in
response probability (MEDIUM vs. CONTROL: Z=0.333,
P=0.739), or latency (t=0.801; d.f.=8;
P=0.446). Similarly, increasing the number of reversals, while
maintaining the same amplitude, did not affect response probability (LARGE
vs CONTROL: Z=1.134, P=0.257), or latency to
respond (t=0.361; d.f.=9; P=0.726).
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Experiment 4
In this final experiment, we considered the interaction between duration
and speed in a 2x2 Latin Square design. Amplitude was held constant.
Based on the results of Experiment 2, together with previous work on
movement-based signals (Fleishman,
1992), we predicted that longer signals would be more effective
than short ones, and that the most effective signal would be a long duration
tail-flick at fast speed. We also wished to establish whether continuous
movement was necessary for optimal tail-flick efficacy. Natural tail-flicks
typically have pauses after each sweep, so we added a fifth stimulus designed
to test whether such discontinuous motion has a cost in terms of reduced
receiver response.
Stimulus sequences
Sequences were constructed using the same procedure as in Experiment 3. The
LARGE amplitude tail-flick formed the basis for five new stimuli that varied
in speed of movement and sequence duration. Display action patterns for these
stimuli are presented in Fig.
9A. We began with a tail-flick that had slow speed and short
duration (SLOW,SHORT), and then increased speed fourfold, while keeping
duration constant (FAST,SHORT); this change produced a corresponding increase
in the number of reversals. To assess whether any change in response was
caused by the number of reversals, rather than speed, we created a longer
version of the SLOW,SHORT stimulus (SLOW,LONG) with a matched number of
reversals. To test the combined effect of speed and duration, we created a
stimulus (FAST,LONG) which matched the duration of SLOW,LONG, but had a
fourfold increase in both speed and number of reversals.
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A fifth stimulus (INTERMITTENT) tested the effect of naturalistic motion, while controlling duration, matched to that of the two long stimuli, speed, matched to the two fast stimuli, and number of reversals, which matched FAST,SHORT and SLOW,LONG (Fig. 9B). This was achieved by removing flicks from the FAST,LONG sequence and spacing the four remaining movements at equal intervals so that the stimulus began and ended with movement like the others (Fig. 9B). The five tail-flick animations were then overlaid onto footage of wind-blown plants, in the same way as in the previous experiments.
Stimuli were presented on successive days using the same test procedure as Experiments 2 and 3. Each lizard was assigned a unique random sequence of the five stimuli.
Statistical analysis
We compared the frequency of response in several ways. First, we determined
if there was a main effect for either speed or duration using Wilcoxon
signed-ranks tests on the pooled data from pairs of stimuli differing on these
parameters. Next we performed an overall Friedman's test of the four
speed/duration sequences (Fig.
9A), and conducted planned pairwise comparisons. We asked if
increased signal duration affected responses within a speed class (SLOW,SHORT
vs SLOW,LONG; FAST,SHORT vs FAST,LONG). These sequences also
differed in number of reversals, so we compared the SLOW,LONG and FAST,SHORT
sequences, which were matched on this parameter. We then compared responses to
the FAST,LONG sequence with those to the two slow sequences. Finally, we
compared responses to the INTERMITTENT stimulus with those to the other long
duration sequences, and with the FAST,SHORT sequence. The latter comparison
tests for a difference between stimuli with an equal number of reversals, as a
consequence of adding pauses to increase duration.
Results
Consistent with results of Experiment 2, response probability increased
with stimulus duration (Fig.
10). The largest values were obtained with the INTERMITTENT
stimulus. Faster signals did not improve response probability
(Z=0.943, P=0.346), but longer duration signals were
more effective than short ones (Z=2.556,
P=0.011).
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An overall Friedman's test revealed sufficient variation in response to the
four continuous sequences (Fig.
9A; Friedman's 2=9.778, d.f.=3, P=0.021).
Comparisons between short and long durations within each speed class suggest
that the duration main effect above was largely due to differences in response
to the two fast signals (Z=2.530, P=0.011);
differences in duration between the slow signals did not affect orienting
probabilities (Z=1.414, P=0.147). The comparison
between the FAST,SHORT and SLOW,LONG sequences revealed that the increased
effectiveness of long signals is unlikely to be a consequence of correlated
increase in number of reversals (Z=1.265, P=0.206).
The FAST,LONG stimulus evoked more orienting responses than SLOW,SHORT
(Z=2.53, P=0.011), but was comparable in
effectiveness to the SLOW,LONG sequence (Z=1.414,
P=0.147). The INTERMITTENT stimulus was as effective as the FAST,LONG
sequence (Z=0.378, P=0.705), but significantly more
effective than the other three sequences (SLOW,SHORT: Z=3.00,
P=0.003; FAST,SHORT: Z=3.00, P=0.003;
SLOW,LONG: Z=1.890, P=0.059).
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Discussion |
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In Experiment 2, we performed straightforward manipulations of the time scale of a tail-flick sequence, keeping the motor pattern otherwise unchanged. The appearance of a stationary tail was relatively ineffective (Fig. 6), which emphasises the importance of movement for reliable signal detection. Response probabilities also suggested that longer duration tail-flicks were more likely to evoke an orienting response than shorter ones (Fig. 6), even though speed was progressively reduced.
In Experiment 3, we manipulated maximum flick amplitude, while keeping
sequence duration constant and controlling other parameters (speed,
acceleration and total sweep area). Amplitude increases did not increase
response probability or reduce latency under our testing conditions. Clearly,
all tail-flicks used in this experiment exceeded the amplitude threshold
required for detection. It is, however, likely that amplitude interacts with
distance, such that an efficacy benefit of higher amplitudes might only be
apparent at longer range. If so, the principal advantage gained from having
large amplitude motor patterns would be increased signal active space (i.e.
visibility to more distant opponents;
Fleishman, 1988b). Additional
playback experiments are planned to test for this predicted effect.
In the final experiment, we explored the interaction between tail-flick speed and duration (Fig. 9). Results suggest that this latter parameter is particularly important (Fig. 10). The probability of a response was unaffected by speed, but increased significantly when signal duration was extended. Furthermore, longer signals were equally effective, irrespective of speed. Nevertheless, there was some evidence for a subtle interaction between these two variables because the effect of duration, within speed class, was only significant for the fast tail-flick sequences.
Comparison between the INTERMITTENT stimulus, which depicted realistic pauses between tail-flicks, and the FAST,SHORT stimulus, which presented the same number of movements without breaks, suggests that pauses increase the probability of receiver response. In addition, the INTERMITTENT stimulus was as effective as the matched-duration FAST,LONG stimulus, suggesting that large differences in period do not affect response probability, and that there does not seem to be a cost associated with reduced duty cycle. Taken together, these results are consistent with the idea that intermittent movement is an energetically cheap strategy for achieving the efficacy benefit of increased duration.
The propensity of a signal to attract attention is an important
consideration for understanding design. Some animals achieve this goal using
high intensity, short duration, alerting components
(Richards, 1981;
Fleishman, 1992
). However,
both quantitative analyses of display structure
(Peters and Evans, 2003
), and
the results of the present series of playback experiments, indicate that Jacky
dragons may have evolved an alternative approach. The most effective stimulus
for eliciting orienting responses was a long duration signal with low duty
cycle. This finding suggests that there may be several possible solutions to
the problem of engaging the intended receiver, and invites comparative study
to identify the ecological and physiological factors responsible for this
variation (e.g. Ord et al.,
2001
; Ord and Blumstein,
2002
; Ord et al.,
2002a
).
Tail-flick design: a working hypothesis
In Fig. 11 we present a
preliminary model of the interactions between factors that are likely to have
shaped the structure of this introductory display component. Movement-based
signals are constrained by the sensory capabilities of receivers
(Fig. 11A). The evolutionary
significance of perceptual processes is well documented
(Endler, 1991;
Guilford and Dawkins, 1991
;
Pagel, 1993
;
Dawkins and Guilford, 1996
;
Endler and Basolo, 1998
). For
example, female butterflies in the Genus Lycaena ensure recognition
by having visual-pigment absorbance characteristics that are well matched to
the wing reflectance spectra of conspecific males
(Bernard and Remington, 1991
).
Similarly, the auditory periphery of cricket frogs Acris crepitans is
well-matched to the call structure of their own species
(Ryan et al., 1992
), and the
preference of female Túngara frogs Physalaemus pustulosus for
low frequency male chucks reflects the tuning of their basilar papillae
(Ryan et al., 1990b
;
Ryan and Rand, 1990
). Studies
of acoustic communication in insects and anuran amphibians have yielded many
other examples of such detailed correspondence between signal structure and
receiver sensory characteristics (Gerhardt
and Huber, 2002
). In Jacky dragons, the relative ineffectiveness
of a stationary tail in Experiment 2 (Fig.
6) highlights the importance of movement for signal detection, and
suggests that motion-processing constraints will probably have influenced
tail-flick structure in an analogous fashion.
|
Signal design is also a product of the environment
(Fig. 11B;
Endler, 1992). Signals must be
detectable to be effective, and conspicuousness is often a function of habitat
characteristics. Endler (1991
)
demonstrated that the colour patterns of guppies Poecilia reticulata
appear different in varying light environments, and that this affects their
relative conspicuousness to females and predators. Similarly, Leal and
Fleishman (2002
) have recently
shown that two sympatric lizards Anolis cooki and A.
cristatellus occupy different terrestrial microhabitats that ensure
optimal signalling conditions for each. Anolis cristatellus is found
in microhabitats that have low ultraviolet (UV) radiance (background light).
These lizards are sensitive to UV and have UV-reflecting dewlap regions.
Conversely, A. cooki have relatively low UV spectral sensitivity, no
UV-reflecting structures in their dewlap, and occupy microhabitats that are
characterised by high UV radiance. Differences between microhabitats have also
promoted divergence in call structure between subspecies of cricket frogs
Acris crepitanus (Ryan et al.,
1990a
).
Conspicuousness can also be enhanced through temporal adjustments in
signalling behaviour. For example, guppies court early and late in the day
during conditions of low light to enhance their conspicuousness to
conspecifics, while minimizing detection by predators
(Endler, 1991). Similarly,
Panamanian katydids (Genus: Neoconcephalus) adjust their singing
behaviour to avoid interference from sympatric congeners
(Greenfield, 1988
).
Sensitivity to environmental noise also allows for structural change to suit
signalling conditions. Amplitude compensation in noisy environments occurs in
the acoustic signals of zebra finches Taeniopygia guttata
(Cynx et al., 1998
),
white-lipped frogs Leptodactylus albilabris
(Lopez et al., 1988
), and
budgerigars Melopsittacus undulatus
(Manabe et al., 1998
). There
have been no comparable reports for movement-based displays. It is intriguing
to consider whether Jacky dragons might adjust their introductory tail-flicks
(e.g. by increasing duration) on windy days; this is a topic for future
study.
The environment also defines the state of receiver nervous systems at the moment of signal production. Consistent background movement over long periods will cause selective habituation/adaptation. To properly understand signal perception, it is necessary to study receivers in this state, which was the rationale for incorporating a baseline period of moving vegetation playback in Experiments 24. It follows that signal conspicuousness should not be a simple product of the average contrast between structure and background, but rather, will vary with the recent experience of the receiver. For example, tail-flicks may be more easily recognised when recent wind conditions have been stable than when they have been variable. These examples illustrate the way in which the structural correlates of conspicuousness are defined by the interaction between environmental conditions and receiver sensory systems.
A particular problem for communication in the visual domain is that signals
are not omni-directional; the probability of attracting the attention of
conspecifics is constrained by receiver orientation
(Fig. 11C). Physical
adaptations such as laterally placed eyes
(Moermond, 1981), and a high
concentration of motion-sensitive cells in the periphery
(Stein and Gaither, 1983
),
increase the likelihood of detecting salient visual motion. However, constant
scanning of the environment is also necessary to obtain full coverage of the
visual field. This behaviour is necessary, not only for detecting signalling
conspecifics, but also insect prey and aerial predators. The attention of
receivers will hence often be engaged by other functionally critical tasks.
The tail-flick component is typically one or two orders of magnitude longer
than the other motor patterns that comprise the push-up display of the Jacky
dragon, which are very brief (ca. 500 ms;
Peters and Ord, in press
). The
results of our playback experiments suggest that increasing signal duration
will be the most effective strategy for enhancing the probability of an
orienting response.
However, longer signal durations are also likely to impose costs
(Fig. 11D). In many systems,
energetic costs are proportional to signal duration or rate
(Taigen and Wells, 1985;
Ryan, 1988
;
Andersson, 1989
;
Vehrencamp et al., 1989
;
Eberhardt, 1994
;
Mappes et al., 1996
;
Kotiaho et al., 1998
). For
example, oxygen consumption by Carolina wrens Thryothorus
carolinensis increases exponentially with greater singing rates, and is
higher than for other non-flight activities
(Eberhardt, 1994
). Similarly,
Kotiaho et al. (1998
) have
shown that the drumming performed by male wolf spiders Hygrolycosa
rubrofasciata during sexual displays is more demanding than locomotion.
Another important cost of highly conspicuous displays is increased predation
risk (McKinney, 1965
;
Cade, 1975
;
Burk, 1982
;
Ryan et al., 1982
;
Yasukawa, 1989
). For example,
female Túngara frogs are attracted to the low frequency chucks of male
frogs, but so are fringe-lipped bats Trachops cirrhosus
(Ryan et al., 1982
).
It seems likely that the tail-flick is better suited to sustained
signalling than other motor patterns in the Jacky dragon display repertoire.
The tail is a relatively light structure, but nevertheless able to sweep a
large area of the visual field (Peters and
Evans, 2003). The only other display motor pattern with structural
characteristics that suggest equivalent conspicuousness is the body-rock,
which consists of a wave travelling anteriorposterior down the lizard's
body (Peters and Ord, in
press
). However, this involves displacing the whole mass of the
animal off the substrate and is hence likely to be relatively costly. The
strategy of intermittent signalling with the tail-flick clearly achieves
signal efficacy comparable to that of continuous movement
(Fig. 10), so this aspect of
signal structure is consistent with selection for reduced energetic cost
(Fig. 11D). Furthermore,
because Jacky dragons face predation from both terrestrial and aerial
predators in their natural habitat, they must be ready to respond to impending
threats, even while signalling. Unlike other motor patterns, such as push-ups
and body-rocks, which involve the legs
(Peters and Evans, 2003
;
Peters and Ord, in press
),
tail-flicks probably do not compromise the capacity for rapid flight. We plan
to measure both the rate of energy consumption and the changes in
conspicuousness to predators associated with different displays. We anticipate
that the design of this signal, as in many other systems, will reflect a
trade-off between efficacy and cost.
![]() |
Acknowledgments |
---|
![]() |
Footnotes |
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References |
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Aho, A.-C., Donner, K., Hyden, C., Larsen, L. and Reuter, T. (1988). Low retinal noise in animals with low body temperature allows high visual sensitivity. Nature 334,348 -350.[CrossRef][Medline]
Andersson, S. (1989). Costs of sexual advertising in the lekking Jackson's widowbird. Condor 96, 1-10.
Bernard, G. D. and Remington, C. L. (1991). Color vision in Lycaena butterflies: spectral tuning of receptor arrays in relation to behavioral ecology. Proc. Natl. Acad. Sci. USA 88,2783 -2787.[Abstract]
Burk, T. (1982). Evolutionary significance of predation on sexually signalling males. Fla. Entomol. 65, 90-104.
Cade, W. (1975). Acoustically orienting parasitoids: fly phonotaxis to cricket song. Science 190,1312 -1313.
Capranica, R. R. (1965). The Evoked Vocal Response of the Bullfrog: A study of communication by sound. Cambridge: MIT Press.
Carpenter, C. C., Badham, J. A. and Kimble, B. (1970). Behavior patterns of three species of Amphibolurus (Agamidae). Copeia 1970,497 -505.
Clark, D. L. and Stephenson, K. R. (1999). Response to video and computer-animated images by the Tiger barb, Puntius tetrazona. Environ. Biol. Fishes 56,317 -324.[CrossRef]
Clark, D. L. and Uetz, G. W. (1993). Signal efficacy and the evolution of male dimorphism in the jumping spider, Maevia inclemens. Proc. Natl. Acad. Sci. USA 90,11954 -11957.[Abstract]
Cynx, J., Lewis, R., Tavel, B. and Tse, H. (1998). Amplitude regulation of vocalizations in noise by a songbird, Taeniopygia guttata. Anim. Behav. 56,107 -113.[CrossRef][Medline]
Dawkins, M. S. and Guilford, T. (1996). Sensory bias and the adaptiveness of female preference. Am. Nat. 148,937 -942.[CrossRef]
Eberhardt, L. S. (1994). Oxygen consumption during singing by male caroline wrens (Thryothorus carolinensis). Auk 111,124 -130.
Endler, J. A. (1991). Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. Vision Res. 31,587 -608.[CrossRef][Medline]
Endler, J. A. (1992). Signals, signal condition and the direction of evolution. Am. Nat. 139,S125 -S153.[CrossRef]
Endler, J. A. and Basolo, A. L. (1998). Sensory ecology, receiver biases and sexual selection. Trends Ecol. Evol. 13,415 -420.[CrossRef]
Evans, C. S., Macedonia, J. M. and Marler, P. (1993). Effects of apparent size and speed on the response of chickens, Gallus gallus, to computer-generated simulations of aerial predators. Anim. Behav. 46, 1-11.[CrossRef]
Fleishman, L. J. (1986). Motion detection in the presence or absence of background motion in an Anolis lizard. J. Comp. Physiol. A 159,711 -720.[Medline]
Fleishman, L. J. (1988a). Sensory and environmental influences on display form in Anolis auratus, a grass anole of Panama. Behav. Ecol. Sociobiol. 22,309 -316.
Fleishman, L. J. (1988b). Sensory influences on physical design of a visual display. Anim. Behav. 36,1420 -1424.
Fleishman, L. J. (1992). The influence of the sensory system and the environment on motion patterns in the visual displays of anoline lizards and other vetebrates. Am. Nat. 139 (Supplement),S36 -S61.[CrossRef]
Fleishman, L. J., Loew, E. R. and Leal, M. (1993). Ultraviolet vision in lizards. Nature 365,397 .[CrossRef]
Gatesy, S. M., Middleton, K. M., Jenkins, F. A. and Shubin, N. H. (1999). Three-dimensional preservation of foot movements in Triassic theropod dinosaurs. Nature 399,141 -144.[CrossRef]
Gerhardt, H. C. and Huber, F. (2002). Acoustic Communication in Insects and Anurans: Common problems and diverse solutions. Chicago, IL: University of Chicago Press.
Greenfield, M. D. (1988). Interspecific acoustic interactions among katydids Neoconocephalus: inhibition induces shifts in diel periodicity. Anim. Behav. 36,684 -695.
Guilford, T. and Dawkins, M. S. (1991). Receiver psychology and the evolution of animal signals. Anim. Behav. 42,1 -14.
Harlow, P. S. and Taylor, J. E. (2000). Reproductive ecology of the jacky dragon (Amphibolurus muricatus): an agamid lizard with temperature-dependent sex determination. Austr. Ecol. 25,640 -652.[CrossRef]
Heiling, A. M., Herberstein, M. E. and Chittka, L. (2003). Crab-spiders manipulate flower signals. Nature 421,334 .[CrossRef][Medline]
Kotiaho, J. S., Alatalo, R. V., Mappes, J., Nielsen, M. G., Parri, S. and Rivero, A. (1998). Energetic costs of size and sexual signalling in a wolf spider. Proc. R. Soc. Lond. B 265,2203 -2209.[CrossRef]
Kroodsma, D. E. (1989). Suggested experimental designs for song playbacks. Anim. Behav. 37,600 -609.
Kunzler, R. and Bakker, T. C. M. (1998). Computer animations as a tool in the study of mating preferences. Behaviour 135,1137 -1159.
Leal, M. and Fleishman, L. J. (2002). Evidence for habitat partitioning based on adaptation to environmental light in a pair of sympatric lizard species. Proc. R. Soc. Lond. B 269,351 -359.[CrossRef][Medline]
LeBas, N. R. and Marshall, N. J. (2000). The role of colour in signalling and male choice in the agamid lizard Ctenophorus ornatus. Proc. R. Soc. Lond. B 267,445 -452.[CrossRef][Medline]
Lopez, P. T., Narins, P. M., Lewis, E. R. and Moore, S. W. (1988). Acoustically induced modification in the white-lipped frog, Leptodactylus albilabris. Anim. Behav. 36,1295 -1308.
Macedonia, J. M., Brandt, Y. and Clark, D. L. (2002). Sexual dichromatism and differential conspicuousness in two populations of the common collared lizard (Crotaphytus collaris) from Utah and New Mexico, USA. Biol. J. Linn. Soc. 77, 67-85.[CrossRef]
Manabe, K., Sadr, E. I. and Dooling, R. J. (1998). Control of vocal intensity in budgerigars (Melopsittacus undulatus): differential reinforcement of vocal intensity and the Lombard Effect. J. Acoust. Soc. Am. 103,1190 -1198.[CrossRef][Medline]
Mappes, J., Alatalo, R. V., Kotiaho, J. and Parri, S. (1996). Viability costs of condition-dependent sexual male display in a drumming wolf spider. Proc. R. Soc. Lond. B 263,785 -789.
Marshall, N. J. (2000). Communication and camouflage with the same `bright' colours in reef fishes. Phil. Trans. R. Soc. Lond. B 355,1243 -1248.[CrossRef][Medline]
McGregor, P. K., Catchpole, C. K., Dabelsteen, T., Falls, B. J., Fusani, L., Gerhardt, H. G., Gilbert, F., Horn, A. G., Klump, G. M., Kroodsma, D. E. et al. (1992). Design of playback experiments: The Thornbridge Hall NATO ARW Consensus. In Playback and Studies of Animal Communication (ed. P. K. McGregor), pp.231 . New York: Plenum Press.
McKinney, F. (1965). The spring behavior of wild Steller eiders. Condor 67,273 -290.
Moermond, T. C. (1981). Prey-attack behavior of Anolis lizards. Z. Tierpsychol. 56,128 -136.
Morris, M. R., Nicoletto, P. F. and Hesselman, E. (2003). A polymorphism in female preference for a polymorphic male trait in the swordtail fish Xiphophorus cortezi. Anim. Behav. 65,45 -52.[CrossRef]
Morton, E. S. (1982). Grading, discreteness, redundancy, and motivation-structural rules. In Acoustic Communication in Birds, vol. 1 (ed. D. E. Kroodsma and E. K. Miller), pp. 183-212. New York: Academic Press.
Nicoletto, P. F. and Kodric-Brown, A. (1999). The use of digitally-modified videos to study the function of ornamentation and courtship in the guppy, Poecilia reticulata. Environ. Biol. Fishes 56,333 -342.[CrossRef]
Ord, T. J. (2001). The evolution and function of visual communication in lizards. PhD thesis, Macquarie University, Sydney, Australia
Ord, T. J. and Blumstein, D. T. (2002). Size constraints and the evolution of display complexity: why do large lizards have simple displays? Biol. J. Linn. Soc. 76,145 -161.[CrossRef]
Ord, T. J., Blumstein, D. T. and Evans, C. S. (2001). Intrasexual selection predicts the evolution of signal complexity in lizards. Proc. R. Soc. Lond. B 268,737 -744.[CrossRef][Medline]
Ord, T. J., Blumstein, D. T. and Evans, C. S. (2002a). Ecology and signal evolution in lizards. Biol. J. Linn. Soc. 77,127 -148.[CrossRef]
Ord, T. J., Peters, R. A., Evans, C. S. and Taylor, A. J. (2002b). Digital video playback and visual communication in lizards. Anim. Behav. 63,879 -890.[CrossRef]
Pagel, M. (1993). The design of animal signals. Nature 361,18 -20.[CrossRef]
Peters, R. A., Clifford, C. W. G. and Evans, C. S. (2002). Measuring the structure of dynamic visual signals. Anim. Behav. 64,131 -146.[CrossRef]
Peters, R. A. and Evans, C. S. (2003). Design of the Jacky dragon visual display: signal and noise characteristics in a complex moving environment. J. Comp. Physiol. A 189,447 -459.
Peters, R. A. and Ord, T. J. (in press). Display response of the Jacky dragon, Amphibolurus muricatus (Lacertilia: Agamidae), to intruders: a semi-Markovian process. Austr. Ecol.
Richards, D. G. (1981). Alerting and message components in songs of Rufous-sided Towhees. Behaviour 76,223 -249.
Rosenthal, G. G. (1999). Using video playback to study sexual communication. Environ. Biol. Fishes 56,307 -316.[CrossRef]
Rosenthal, G. G. and Evans, C. S. (1998).
Female preference for swords in Xiphophorus helleri reflects a bias
for large apparent size. Proc. Natl. Acad. Sci. USA
95,4431
-4436.
Ryan, M. J. (1988). Energy, calling, and selection. Am. Zool. 28,885 -898.
Ryan, M. J., Cocroft, R. B. and Wilczynski, W. (1990a). The role of environmental selection in intraspecific divergence of mate recognition signals in the cricket frog, Acris crepitans. Evolution 44,1869 -1872.
Ryan, M. J., Fox, J. H., Wilczynski, W. and Rand, A. S. (1990b). Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343, 66-67.[CrossRef][Medline]
Ryan, M. J., Perrill, S. A. and Wilczynski, W. (1992). Auditory tuning and call frequency predict population-based mating preferences in the cricket frog, Acris crepitans.Am. Nat. 139,1370 -1383.[CrossRef]
Ryan, M. J. and Rand, A. S. (1990). The sensory bias of sexual selection for complex calls in the tungara frog, Physalaemus pustulosus (sexual selection for sensory exploitation). Evolution 44,305 -314.
Ryan, M. J., Tuttle, M. D. and Rand, A. S. (1982). Bat predation and sexual advertisement in a neotropical anuran. Am. Nat. 119,136 -139.[CrossRef]
Stein, B. E. and Gaither, N. S. (1983).
Receptive-field properties on reptilian optic tectum: some comparisons with
mammals. J. Neurophysiol.
50,102
-124.
Taigen, T. L. and Wells, K. D. (1985). Energetics of vocalization by an anuran amphibian (Hyla versicolor). J. Comp. Physiol. B 155,163 -170.
Tinbergen, N. (1951). The Study of Instinct. Oxford: Oxford University Press.
Vehrencamp, S. L., Bradbury, J. W. and Gibson, R. M. (1989). The energetic cost of display in male sage grouse. Anim. Behav. 38,885 -896.
Whitehead, J. M. (1987). Vocally mediated reciprocity between neighbouring groups of mantled howler monkeys, Alouatta palliata palliata. Anim. Behav. 35,1615 -1627.
Wiley, R. H. and Richards, D. G. (1982). Adaptations for acoustic communication in birds: sound transmission and signal detection. In Acoustic Communication in Birds Volume 1: Production, Perception and Design Features of Sounds (ed. D. E. Kroodsma and E. H. Miller), pp. 131-181. New York: Academic Press.
Yasukawa, K. (1989). Costs and benefits of a vocal signal: the nest-associated `Chit' of the female red-winged blackbird, Agelaius phoeniceus. Anim. Behav. 38,866 -874.
Zeil, J. and Zanker, J. M. (1997). A glimpse into crabworld. Vision Res. 37,3417 -3426.[CrossRef][Medline]
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