Seismic signals in a courting male jumping spider (Araneae: Salticidae)
1 Department of Neurobiology and Behavior, Cornell University, Seeley G. Mudd Hall, Ithaca, NY 14853, USA,2 Division of Life Sciences, University of Toronto at Scarborough, 1265 Military Trail, Toronto, Ontario, Canada M16 1A4 and3 Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
* Author for correspondence (e-mail: doe2{at}cornell.edu)
Accepted 30 July 2003
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Summary |
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Key words: seismic signal, courtship, behaviour, visual signal, thump, scrape, buzz, signal ablation, jumping spider, Habronattus dossenus, vibration.
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Introduction |
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Jumping spiders (Family: Salticidae) are unique among spiders in that they
are visual `specialists', having two large, prominent frontal eyes that are
specialized for high spatial resolution, as befits their predatory habits as
stalker-hunters (Forster,
1982a; Land,
1985
). Not surprisingly, vision also plays a prominent role in
their signalling behaviour. Males, unlike females, have evolved conspicuously
ornamented and coloured appendages that they wave like semaphores during
courtship, producing stereotyped, species-specific visual displays that unfold
over periods of seconds to minutes (Crane,
1949
; Forster,
1982b
; Jackson,
1982
). These displays function in species isolation, species
recognition and female choice (Clark and
Morjan, 2001
; Clark and Uetz,
1993
; Jackson,
1982
) and are specific enough to be useful as taxonomic characters
(Richman, 1982
). These
displays are textbook examples of visual communication
(Bradbury and Vehrencamp,
1998
). While visual signals are well established, seismic signal
production by stridulation (Edwards,
1981
; Gwynne and Dadour,
1985
; Maddison and Stratton,
1988
), percussion (Noordam,
2002
) and tremulation (Jackson,
1977
,
1982
) has been proposed in a
few species of jumping spiders.
Within the jumping spiders, members of the genus Habronattus are
known for extraordinary diversity - especially of the complex, colourful
ornaments used in their multifaceted visual displays
(Griswold, 1987;
Maddison and McMahon, 2000
;
Peckham and Peckham, 1889
,
1890
). Over 100 species have
been described, with most of them occurring in North America, especially in
arid regions of the southwest. Among these species, many exhibit striking
morphological and geographical variation
(Maddison and McMahon, 2000
;
Masta, 2000
;
Masta and Maddison, 2002
). We
focused on one particular species that has multiple, complex visual ornaments:
Habronattus dossenus. We recorded male courtship behaviour in H.
dossenus by using video and laser vibrometry and found that the complex
visual displays of signalling males represent only one component of an
extremely elaborate multi-modal display. Male H. dossenus signal to
prospective mates using a repertoire of seismic signals coordinated with
specific visual signals. In order to investigate these phenomena, we (1)
characterized seismic and visual signals in detail using synchronous
high-speed video and laser vibrometry and (2) examined possible seismic signal
production mechanisms by performing several experiments where we attempted to
manipulate seismic signals. We manipulated abdominal (opisthosoma) movements
and contact with the cephalothorax (prosoma) because previous experiments in
another Habronattus species suggested that seismic signal production
originated there (Maddison and Stratton,
1988
).
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Materials and methods |
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Recording procedures
We anaesthetized female H. dossenus with CO2 and
tethered them to a wire with low melting point wax. We held females in place
with a micromanipulator on a substrate of stretched nylon fabric (25
cmx30 cm). Males were then dropped onto this substrate 15 cm from the
female and allowed to court freely. Females were rotated to face the male
until he oriented to her; recordings began when males approached females. We
recorded substrate vibrations produced during courtship using a laser Doppler
vibrometer (LDV; Polytec OFV 3001 controller, OFV 511 sensor head; Waldbronn,
Germany) (Michelsen et al.,
1982). Laser Doppler vibrometry is a non-contact method of
recording vibrations that measures the velocity of a moving surface by
detecting the Doppler shift of a reflected laser beam. Pieces of reflective
tape (approximately 1 mm2) were attached to the underside of the
courtship substrate 2 mm from the female to serve as measurement points for
the LDV. The LDV signal was synchronized with two concurrent methods of video
recording: (1) the LDV signal was recorded on the audio track during standard
video taping of courtship behaviour (Navitar Zoom 7000 lens; Panasonic
GP-KR222; Sony DVCAM DSR-20 digital VCR; 44.1 kHz audio sampling rate) or (2)
the LDV signal was digitized (PCI-6023E; National Instruments, Austin, TX,
USA; 10 kHzsampling rate) simultaneously with the capture of digital
high-speed video (500 frames s-1; PCI 1000; RedLake Motionscope,
San Diego, CA, USA; Nieh and Tautz,
2000
), using Midas software (Xcitex, Cambridge, MA USA). All
recordings were made on a vibration-isolated table. In some recordings, we
also captured air-borne sound on a second channel using a probe microphone
(B&K Type 4182, B&K Nexus amplifier; Nærum, Denmark).
Sound and video analysis
Complete courtships of 20 different males were recorded. The same tethered
female was used for all recordings. Examples were selected for detailed
analysis. Body movements were measured frame-by-frame from digital high-speed
video using Midas software. We calibrated absolute distances by photographing
a 1 mm2 grid before each recording. Power spectra of vibratory
signals were calculated using Matlab software (The Mathworks, Natick, MA,
USA). Spectrograms were made using Canary (Cornell University, Lab of
Ornithology).
Seismic signal production mechanisms of H. dossenus
Experimental manipulations
For the signal manipulation experiments, the arena substrate floor for
courtship was a sheet of graph paper attached to a square cardboard frame (60
cmx45 cm). Females were tethered as above, and the male's seismic
signals recorded using a piezo-electric sensor placed directly underneath the
tethered female. We calibrated the response of the piezo-electric sensor using
a vibration source (B&K Type 4810 Mini-shaker) and LDV (OFV 3001
controller, OFV 511 sensor head). Although low-frequency responses (<150
Hz) were relatively attenuated by the piezoelectric sensor, the male's signals
were not significantly altered (data not shown). All experiments were
conducted in a sound-attenuated chamber. Seismic signals were amplified (Nikko
NA790) and recorded on the audio track of a video recording as above (44.1 kHz
audio sampling rate). All recordings were also videotaped (Navitar Zoom 7000
lens; Panasonic GP-KR222; Sony DVCAM DSR-20 digital VCR). Recordings of
signals were made from each male prior to experimental manipulation. Classical
spider anatomy has recognized two body segments in spiders: the prosoma and
opisthosoma (Barth, 2002;
Foelix, 1996
). We use the
alternative nomenclature, cephalothorax (prosoma) and abdomen (opisthosoma) to
describe the spider's body segments
(Maddison and Stratton, 1988
).
We manipulated males by (1) preventing abdominal movements by attaching the
abdomen to the cephalothorax using wax (Kerr Sticky Wax; Cenco Scientific,
Chicago, IL, USA; Fig. 3) and
(2) preventing contact between the cephalothorax and abdomen by attaching a
small piece of aluminium foil to the cephalothorax with wax; this formed a
flap that could be inserted at the junction between the abdomen and the
cephalothorax (Fig. 5). To
ensure that these treatments did not affect normal locomotory activities, we
waited two days following these manipulations and observed whether or not the
spiders were able to successfully capture prey. Both manipulations were
reversible. Two days following reversal by removing the wax or the foil flap,
we recorded courtship signals again. We used only males that were able to
capture prey during both intervals.
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Power spectra analysis
Within a treatment set (control, experimental treatment, recovery) from an
individual animal, individual signals (see below) were identified using
videotaped data, and a random selection of each seismic signal type acquired.
The power spectra of the noise floor, acquired before the start of every
recording, was subtracted using Matlab software. Power spectra of different
signals were then calculated and averaged using Matlab. This shows how, within
an individual, the entire power spectrum of a signal changes according to
experimental treatment.
Statistical analysis
For each signal, peak intensities were recorded. For thumps, peak
intensities below and above 500 Hz were recorded. For scrapes, the peak
intensity was recorded. For buzzes, the intensities of the first three
harmonics were recorded. Within treatment sets for each individual,
intensities were normalized to the highest intensity produced for all of the
signal components. Normalized intensities were then averaged and the relative
dB difference between the treatments calculated. The normalized intensities
for different individuals were then pooled into their treatment categories and
averaged. Differences between treatments were tested for significance
(P<0.05) using a repeated-measures analysis of variance (ANOVA)
procedure and a post-hoc Tukey test with Bonferonni corrections.
Scanning electron microscopy (SEM)
Specimens were fixed, dried and gold coated and then viewed with a Philips
SEM 505 microscope.
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Results |
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Thumps
Thumps (Fig. 2A) occur at
the beginning of a sequence of seismic signals. They can precede a sequence of
scrape groups or buzzes in phase 3 of courtship
(Fig. 2A; see below) or occur
simultaneously with buzzes in phase 4 (Fig.
1). The front legs and abdomen both produce the thump
(Fig. 2A). First, the forelegs
are raised high above the body and are then rapidly slapped down onto the
substrate (1-2 in Fig. 2A),
producing a percussive impulse (2 in Fig.
2A). This percussive component was the only display that produced
a detectable air-borne component (data not shown). Approximately 8 ms later,
the forelegs return to a nearly vertical position (2-3 in
Fig. 2A) and the abdomen is
pulled back and released (4-5 in Fig.
2A), causing it to `ring' at a frequency of 58.3±7.5 Hz
(mean ± S.D., N= 5;
Fig. 2Ai). This movement
produces a brief, high-intensity broadband signal
(Fig. 2Aiv). Movements of the
forelegs and abdomen are highly coordinated, with delays of 86.1±32.0
ms (N=27) for lone thumps and 46.0±8.0 ms (N=30) for
thumps preceding buzzes. Both of these categories of thumps also differ in
duration and envelope shape (data not shown). Thumps consist of unique foreleg
movements (Fig. 2Aii) and two
seismic components: a percussive component caused by the front legs contacting
the substrate and a more-intense component caused by the oscillation of the
abdomen (Fig. 2Aiv).
Scrapes
Scrapes (Fig. 2B) are
emitted in groups lasting 5.3±1.1 s(N=10) (Sc G in
Fig. 1C). Within these groups,
scrapes occur at a frequency of 5.7±1.2 Hz (N=15 scrape
groups; Fig. 2Bi). One to four
scrape groups occur between thumps and these occur only in phase 3 of
courtship (Fig. 1). Individual
scrapes (Sc in Fig. 1C) are
associated with movements of the forelegs and abdomen
(Fig. 2Bi). An up-and-down
movement of the foreleg tips (2-3 in Fig.
2B) is followed by a dorso-ventral oscillation of the abdomen (1-2
in Fig. 2B). This `rocking
motion' produces an underlying low-frequency oscillation (5.7 Hz) that is
evident in the oscillogram (Fig.
2Biii). Abdominal and foreleg movements are highly coordinated,
with delays of 32.3±7.0 ms (N=409). In adjacent scrape groups,
the forelegs alternate coming together and moving apart laterally. Two types
of movements can occur between scrape groups: (1) when scrape groups follow
thumps, the 3rd legs are repositioned against the body as the male moves
forward incrementally, and (2) when scrape groups precede a thump, the
pedipalps are moved rapidly up and down prior to the thump. Individual scrape
seismic signals are produced only during abdominal movements
(Fig. 2B) and not during
characteristic foreleg movements (Fig.
2Bii). Within groups, individual seismic scrapes are short,
broadband signals (Fig. 2Biv).
The frequency of abdominal movement is much lower than the frequency of
vibrational signal produced (Fig.
2Bi,iv).
Buzzes
Buzzes (Fig. 2C) occur alone
in phase 3 of courtship or simultaneously with thumps in phase 4
(Fig. 1). Buzzes in phase 3 are
always preceded by 2-5 thumps. The number of thumps occurring increases
linearly as courtship progresses (Fig.
1). Both abdominal and leg movements accompany the signal. The
front legs come down in a slow continuous movement (1-2 in
Fig. 2C), while the abdomen
produces a sustained, rapid, low-amplitude oscillation at a frequency of 65.0
Hz (Fig. 2C). Abdominal
movements are precisely synchronized with the vibratory signal, while
distinctive foreleg movements (Fig.
2Cii) occur at variable delays (180±644 ms, N=14;
Fig. 2C). Buzz seismic signals
are long in duration, with a fundamental frequency of 65.0±2.9
Hz(N=12) plus higher harmonics
(Fig. 2Civ). Frequencies of
seismic buzzes are temperature dependent (data not shown). Abdominal
oscillations are at the same 65 Hz frequency as the fundamental frequency of
the buzz seismic signal (Fig.
2C).
Seismic signal production mechanisms of H. dossenus
Experimental manipulations
Abdominal movement. Analysis of high-speed videos, along with
observations suggesting that abdominal movements are not visible to a female
while the male is courting, suggests that most seismic signals are produced by
abdominal movements and not by movements of the legs. To investigate whether
seismic signals are produced by any of the observed body movements, we
performed a series of experiments where we tried to eliminate signals. We did
this by immobilizing the abdomens of males by fixing them with wax to the
cephalothorax (Fig. 3). This
treatment was fully reversible. Males were recorded prior to treatment, then
with abdomen immobilized and finally after removal of the wax. We could
readily identify the occurrence of each signal type by the stereotypic leg
movements and postures characteristic of each signal from videotapes
(Fig. 2ii). Only the abdominal
and not the weak percussive component of the thump was analyzed
(Fig. 2A). All three seismic
signals were greatly attenuated when the abdomen was immobilized (Figs
3,
4). All frequencies were
attenuated in all signal types (Fig.
3). Experimental treatments were significantly different
(P<0.001) from both control and recovery treatments
(Fig. 4). All signals recovered
following removal of the wax, and no significant differences were observed
between the control and recovery treatments
(Fig. 4). Thus, abdominal
movements are necessary for seismic signalling.
|
Abdomen-cephalothorax contact. Observations using synchronous high-speed video and vibrational recordings revealed that the power spectrum of a buzz exactly matched the oscillation frequency of the abdomen, while the power spectra of thumps and scrapes included much higher frequencies than the oscillation frequency of the abdomen. This hinted that buzz, scrape and thump signals are produced by different mechanisms. Hence, in a second set of experiments, we prevented direct contact between the cephalothorax and abdomen but did not prevent abdominal movements (Fig. 5). We prevented abdomen-cephalothorax contact by placing a small barrier of aluminium foil between the cephalothorax and abdomen. Recovery treatments consisted of removing the barrier (Fig. 5). Buzzes were unaffected at all frequencies (Figs 5A, 6C); no significant differences were observed between the control, experimental and recovery treatments (Fig. 6C). Both scrapes and thumps, however, were affected. Scrapes were attenuated significantly at all frequencies (Figs 5B, 6B). For thumps, low-frequency components (<500 Hz) were unaffected but high-frequency components of the thump (>500 Hz) were attenuated (Figs 5C, 6A). Experimental treatments for the scrape and high-frequency components of the thump were significantly different (P<0.05) from both control and recovery treatments (Fig. 6). Control and recovery treatments were similar for all components (Fig. 6). Thus, including the percussive component of thumps, at least three separate mechanisms are used in the production of vibrational signals. Buzz signals are produced by abdominal oscillations and do not require contact between the abdomen and cephalothorax. Scrape and thump signals, on the other hand, require abdomen-cephalothorax contact to produce the high frequencies evident in both of these signals.
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Scanning electron microscopy
The observation that high-frequency signal components require direct
contact between body parts that move relative to each other suggests a
stridulatory mechanism (Dumortier,
1963). Therefore, we examined, using SEM, the
cephalothorax-abdomen junction of both male and female H. dossenus
for evidence of a stridulatory apparatus, as observed in males of another
Habronattus species (Maddison and
Stratton, 1988
). Female H. dossenus do not produce
seismic signals in any context. SEMs revealed the presence of a file on the
male cephalothorax (Fig. 7Bi)
but not on the female (Fig.
7Ai). In the apposing abdominal areas, we noted the presence of
hardened sclerotized scrapers on the male
(Fig. 7Bii) but not on the
female (Fig. 7Aii). Thus,
scrape and thump signals appear to be produced by stridulation.
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Discussion |
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Three different mechanisms are responsible for the different signals: (1)
the first thump component is produced from percussion with the forelegs and
the ground, (2) scrapes and the second thump component are produced from
abdominal movements coupled to a frequency multiplier (stridulation) and (3)
buzzes are produced from abdominal oscillations alone (tremulation). Selective
elimination of only the high frequencies of thump signals suggests that both
vibratory mechanisms (stridulation and tremulation) contribute to thumps or
possibly that low frequencies in thumps are produced using a different area on
the scraper, one where contact was not prevented. The entire diversity of
substrate-borne vibration-production mechanisms described to date in spiders
(Uetz and Stratton, 1982) is
seen here in one species: H. dossenus. To our knowledge, no other
spider described exhibits such complexity in seismic signal production. This
is surprising since it occurs in a family in which signalling is thought to be
predominantly visual (Foelix,
1996
). This raises the question of why H. dossenus has
evolved multiple seismic signals in addition to its repertoire of visual
signals.
Two major `quality-based' hypotheses have been proposed for the evolution
of multiple signals: `backup signals' and `multiple messages'
(Johnstone, 1996;
Moller and Pomiankowski,
1993
). The backup signals hypothesis states that different signals
provide the same information about a sender but allow for a more accurate
assessment of condition, while the multiple messages hypothesis states that
different signals code for different aspects of a senders condition. The
backup hypothesis, in this context, would predict that visual and seismic
signals are alternative media for the same signal information and that seismic
signals may be most important when visual signals are obscured. This seems
unlikely for several reasons. H. dossenus courtship only occurs
diurnally. Visual courtship starts at ranges up to 60 mm away while seismic
courtship signals only occur at close ranges (5-8 mm). The start of courtship
appears to be visually mediated since males orient and court to tethered
females in the absence of any chemical cues produced, for example, by the
female's drag line. Sometimes, however, males will display when the female is
looking in the opposite direction. Regardless, courting males are usually in
the female's line of sight and in close proximity when seismic signals are
produced. This still leaves the question of whether the three different
seismic signals are acting as `backups' to each other. H. dossenus
can be collected on various substrates; leaf litter, sandy soil or rocks. Each
of the different substrates has very different transmission properties (D. O.
Elias, R. R. Hoy and A. C. Mason, manuscript in preparation) and it is
possible that some signals propagate better in some substrates than others.
The difference at short distances is minimal however. Also, the most common
substrate (leaf litter) transmits all signals equally well. Again, because all
signals are produced at very close distances, where signal attenuation is
presumably negligible, it seems unlikely that the three signals are redundant
backups. Another possibility is that the different seismic signal production
mechanisms may act to backup one another. This is unlikely due to the large
temporal and spectral differences between the signals.
A better alternative is that seismic signals are used as multiple messages
for sender condition. Male H. dossenus have multiple visual
ornaments. Males, but not females, are strikingly ornamented, especially the
body parts that are used in courtship. The forelegs, for example, are bright
green with a dark brown border and a fringe of white hair, while the tips of
the legs are a deep black. The pedipalps, third pair of legs and face are also
ornamented (Griswold, 1987).
One problem that may be encountered by having multiple signals in a single
modality is the amount of information that can be effectively detected and
discriminated (Rowe, 1999
).
Within a discrete signal modality, habituation, adaptation and transduction
mechanisms in sensory neurons, as well as memory capabilities of receivers,
may set limits to signals that animals are able to effectively detect and
process. Complex signals with many different characteristics in a single
modality, for example, are often perceived as one unified stimulus
(Honey and Hall, 1989
;
Rowe, 1999
), while information
transmitted in multiple modalities is not
(Hillis et al., 2002
). The
evolution of seismic signals could therefore be a way to add multiple messages
when there is selection for multiple avenues of information for females and
the evolution of further signals in the visual modality is limited by
physiological or economic constraints. The three different seismic signals
could also be used to relay multiple messages. The occurrence of three
different seismic signal production mechanisms that involve different motions
and anatomical structures suggests the possibility that each different signal
could relay very different information about the male's condition.
Alternatives to these two quality-based hypotheses have been proposed in
models of the evolution of multiple sexual preferences and ornaments
(Iwasa and Pomiankowski, 1994;
Pomiankowski and Iwasa, 1993
,
1998
). These models are not
necessarily based on mate quality assessment but are instead based on
Fisherian `runaway selection' (Fischer,
1930
) and their interplay with other Fisherian and handicap traits
(Zahavi, 1975
). In these
models, female preferences lead to the elaboration of male display traits, and
multiple male ornaments evolve in spite of the increased cost to males.
Regardless of the evolutionary process that has led to signal elaboration
in this species, a further question is how the addition of a second stimulus
modality contributes to signal content and efficacy. Spiders in the
Habronattus group are known for the complexity of visual displays as
well as their visual ornaments. Habronattus dossenus is no exception
to this pattern. How then does H. dossenus incorporate two separate
but precisely coordinated sets of complex signals? One possibility is that it
is the coordination of visual and seismic signals that relays information.
Especially with thumps preceding buzzes and scrape signals, the coordination
of visual and seismic signals can be very precise and it is possible that
females are using this tight temporal coordination as a measure of male
quality. Another possibility is that either vibratory or visual signals carry
information, and the tight coordination of the alternative modality directs
attention to subsequent signals. In animal signals, signal components that
precede focal informative signals have often been shown to improve signal
efficacy and efficiency by directing attention
(Fleishman, 1988;
Rowe, 1999
). Jumping spiders'
well-developed sense of vision (Blest et
al., 1981
; Eakin and
Brandenburger, 1971
; Forster,
1982a
,b
;
Jackson, 1982
; Land,
1969
,
1985
) could possibly be a good
mechanism to draw attention to seismic signals that may be more difficult to
detect than visual signals. Alternatively, experiments in humans have shown
that when sound stimuli are matched with a corresponding visual stimulus, the
perception of visual temporal rate is improved
(Recanzone, 2003
). A similar
process may be at work in these animals, particularly in the short-duration
thump and scrape signals, where seismic signals could improve the detection of
rapidly occurring visual signals. Similar arguments have been made regarding
the evolution of visual ornaments and visual motion displays in jumping
spiders (Peckham and Peckham,
1889
,
1890
). If visual form and
motion pathways are considered separately
(Barth, 2002
;
Forster, 1982b
;
Strausfeld et al., 1993
), then
it is possible that visual ornaments can focus attention on motions or
vice versa (Hasson,
1991
), hence the tight correlation between ornaments and the body
parts used in displays (Peckham and Peckham,
1889
,
1890
). Attention focusing
via the combinatorial possibilities created by the combination of
multiple modalities or components could therefore be a powerful force driving
the evolution of complex signals.
While much recent work has documented the occurrence of multi-modal signals
in a variety of animals (Fusani et al.,
1997; Hoelldobler,
1999
; Hughes,
1996
; McGurk and MacDonald,
1976
; Partan and Marler,
1999
; Rowe and Guilford,
1999
), including spiders
(Hebets and Uetz, 1999
;
Scheffer et al., 1996
;
Uetz and Roberts, 2002
), the
complexity found in H. dossenus is impressive. Multiple visual
ornaments and visual displays exist together with a complexity of seismic
signals that is unprecedented in spiders. H. dossenus uses three
independent mechanisms to produce three types of signals, which can further be
divided into at least seven categories based on the power spectra, envelope
shape and temporal structure of the signals (D. O. Elias, A. C. Mason, W. P.
Maddison and R. R. Hoy, unpublished observations). Each of these seismic
signals is precisely coordinated with a unique visual display, and some visual
signals (i.e. pedipalp signals) have no corresponding seismic component. We
feel that this signal complexity represents a good system in which to test
competing models of signal evolution. Future studies will examine female
responses to manipulated and control males in an attempt to elucidate the
function of different aspects of the male's complex, multi-modal
multi-component courtship signals.
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Acknowledgments |
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