Response of western diamondback rattlesnakes Crotalus atrox to airborne sounds
Department of Biology, Lafayette College, Easton, PA 18042, USA
* Author for correspondence (e-mail: youngab{at}lafayette.edu)
Accepted 27 June 2002
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Summary |
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Key words: acoustic, communication, reptilia, squamata, hearing, behaviour, western diamondback rattlesnake, Crotalus atrox
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Introduction |
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Wever conducted a series of experiments in which he recorded the cochlear
potentials of snakes exposed to controlled tones
(Wever and Vernon, 1960;
Wever, 1978
). These studies
demonstrated that snakes can perceive airborne vibrations at a higher
sensitivity than groundborne stimuli. Wever
(1978
) presented a series of
auditory sensitivity curves, demonstrating that perception of airborne
vibrations occurred within a rather narrow frequency range (approximately
200-400 Hz), with some species maintaining high sensitivity for approximately
100 Hz either side of this range. Wever's findings were confirmed by Hartline
and Campbell (1969
) and
Hartline
(1971a
,b
),
who used intracellular recordings from auditory neurons to document the
acoustic sensitivity of snakes exposed to airborne sounds. Though aspects of
snake bioacoustics remain poorly known (B. A. Young, manuscript submitted for
publication), there is clear evidence that snakes can perceive airborne
sounds.
Previous physiological studies of snake audition were performed on
immobilized anesthetized snakes, and thus provided no evidence of a
behavioural response to airborne sounds. Manning
(1923) used a telephone
receiver to present airborne stimuli to rattlesnakes. Few variables were
controlled in this study and though Manning
(1923
) concluded that snakes
are deaf, he reported that some rattlesnakes exhibited consistent responses to
airborne stimuli. Other studies of airborne hearing in snakes have been more
anecdotal and largely devoid of controls (e.g.
Davenport, 1934
;
Klauber, 1956
). Several
studies (e.g. O'Reilly, 1894
;
Werner, 1999
) have shown that
snake `charming' is not dependent on the snake hearing airborne sounds.
Several recent studies have explored the behavioural response of snakes to
groundborne vibrations (e.g. Randall and
Matocq, 1997
; Burger,
1998
; Shivik et al.,
2000
; Young and Morain,
2002
). The purpose of the present study was to explore the ability
of snakes to respond behaviourally to airborne sounds presented within a
controlled context.
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Materials and methods |
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An acoustic chamber was constructed out of an old environmental chamber. This chamber had internal dimensions of 91.5 cm wide x 123 cm tall x46 cm deep and was constructed of an inner metal shell separated from the outer metal frame by a 5 cm layer of insulation. All electronic and movable parts were removed from the environmental chamber, then the inner surface was covered with acoustic dampening insulation. Auralex LENRD Bass trap (noise criteria, NC rating at 250 Hz=1.28) was installed in the corners, and all other inner surfaces were covered in Auralex 7.5 cm wedge foam (NC rating at 250 Hz=0.49). Three portals were made in the chamber. On one wall a fluorescent 40 W bulb was installed; given the low heat produced by this light, the bulb was recessed slightly into the acoustic foam. The socket for the bulb was located between the inner and outer shells of the chamber; the portal through which the cord penetrated the outer shell was packed with acoustic foam. An Optimus speaker (frequency response 50-15 000 Hz) was installed in the upper corner of the chamber opposite the light. The speaker was not hard-mounted to the chamber, but was held in position by the surrounding acoustic foam. The portal through which the speaker wire exited the outer shell of the chamber was packed with acoustic foam. A large portal was cut in the top of the chamber to accommodate a Sony Video8 videocamera. Only the lens of the video camera extended through the inner foam shell of the chamber where the adjacent acoustic foam was trimmed to provide a view of the interior of the chamber.
A `hanging basket' was constructed using 1.25 cm steel mesh. The steel mesh was attached to a frame constructed of 2 cm-wide aluminum, which gave the hanging basket final dimensions of 46 cm wide x 30 cm tall x 25 cm deep. The top of the basket was attached using a long stiff hinge, which was the only movable part on the basket. The basket was designed to contain the rattlesnakes while providing minimal surface area for transmitting substratum vibrations. Eyebolts located on the upper corners of the basket and in the roof of the chamber were linked with plastic-coated steel cable to hang the basket within the chamber. When suspended, the bottom of the basket was approximately 90 cm from the top of the chamber and did not touch any of the acoustic insulation lining the inner surface of the chamber.
The entire outer surface of the chamber was covered in Auralex Sheetblok
sound dampening insulation (sound transmission class, STC at 250 Hz=19). The
chamber rested upon a layer of Auralex Platfoam acoustic platform designed to
minimize vibration transmission between the floor and the chamber. The chamber
was located within a laboratory designed for acoustic experiments. Wever
(1978) used cochlear
microphonics to generate acoustic sensitivity curves to airborne sounds from a
number of snakes, including Crotalus viridis. We converted Wever's
intensity data over to sound pressure level (SPL) with a reference of (dB re
2x10-5 Pa) and averaged all of the airborne sensitivity
curves that he published (Fig.
1). 20 sounds were synthesized using SoundEdit 16 (MacroMedia) on
a PowerBook G4 (Apple); each sound had a unique combination of frequencies and
frequency modulation patterns, but all concentrated their acoustic energy
within the range 150-450 Hz (Fig.
1). The amplitude of the 20 sounds was standardized. Each sound
had a duration of 150 ms and was separated from the next sound by 50 ms of
silence. The end product was a 4 s acoustic stimulus which was temporally
patterned and included a variety of frequencies and frequency modulations.
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The computer was coupled to a GRASS AM8 audio monitor that routed the
stimulus to the speaker. A SPER 840029 sound meter was placed within the
hanging basket. With the hamming filter window of the GRASS AM8 set at 30 and
1000 Hz, the amplitude of the stimulus was adjusted (using both the computer
and the GRASS AM8) to a range of 65-75 dB (the variation in acoustic
properties of the component sounds results in a slight variation in
amplitudes). This acoustic intensity, measured at the bottom of the hanging
basket, meant that the stimulus would be presented at 5-10 dB over the
threshold determined by Wever
(1978)
(Fig. 1).
A GRASS SPA1 accelerometer was used to determine the resonance, and thus the likelihood of substrate transmission of the stimulus, of the hanging basket. The accelerometer was wedged into the steel mesh of the hanging basket (which contained a dead specimen with a SVL of 89 cm), in different directions, and connected to a GRASS P511 AC amplifier. The GRASS P511 was coupled to an Instrunet 100B A/D converter and ultimately to a G4 computer (Apple) running Instrunet data acquisition software (GW Instruments). Newly synthesized sounds (frequency range 50-2000 Hz) were presented at the same amplitude range (65-75 dB) determined for the trial stimulus, but with no filtering from the GRASS AM8 audio monitor. With the GRASS P511 amplifier set to a gain of 50 000, clear resonance (signals over 1 V) was detected from the hanging basket upon presentation of the sound (Fig. 2). When the trial stimulus was presented, with the hamming filter set to 30 and 1000 Hz, no resonance signature was recorded (Fig. 2). Our analyses suggested that the hanging basket had a resonance frequency of approximately 600 Hz, which was well above the acoustic range of our trial stimulus.
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For the behavioural trials the laboratory was heated, using portable
electric heaters, to 28°C. The snakes were placed individually within the
hanging basket and the acoustic chamber sealed. The florescent light and video
camera remained switched on throughout the trials. The behaviour of the snake
was monitored with the video camera until the snake was judged to have assumed
a relaxed or investigative behaviour (defined by a lack of rattling, slow
movement and no defensive tongue flicks; for suites of behaviours in
Crotalus, see also Kardong,
1986; Hayes and Duvall,
1991
; Young et al.,
2002
). Once a minimum of 30 continuous seconds of relaxed or
investigative behaviours were observed the trial was initiated. For each trial
we recorded 104s of videotape consisting of an initial 30s control period, the
4s of stimulus presentation, and a final 30s recovery period. Each specimen
was used for three trials, with a minimum time of 90 min between trials.
For analysis, the videotape record of each trial was divided into a control period (the 10s immediately prior to the presentation of the stimulus), a stimulus period (the 4s of the stimulus and the subsequent 6s), and a recovery period (10s in duration, beginning 20s following the onset of the stimulus). For each period we quantified the number of tongue flicks, the number of head jerks (rapid lateral movements of the head independent of directed movement of the body), and the number of seconds during which the snake was moving within the hanging basket. We determined (using both visual and audio information) whether or not the snake rattled. Quantitative data from the video records were processed using Systat 5.2.1 and analyzed using ANOVA.
The protocols used for this experiment conform to guidelines for research on reptiles and venomous snakes, and were approved by the Institutional Animal Care and Use Committee of Lafayette College.
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Results |
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Total response
Presentation of the airborne stimulus resulted in a suite of four
significant responses: decreased tongue flicking, a freeze behaviour, head
jerks and rattling. At least one of these four behavioural responses was
observed in 22 of the 24 trials (Fig.
4). Two of the four responses were observed in six of the trials,
while three of the four responses were recorded from five trials
(Fig. 4). The four behaviours
were observed concurrently in only two of the trials
(Fig. 4). At least one positive
response was obtained from each specimen, and four of the eight specimens
responded positively to sound during each trial.
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Intraspecific variation
An examination of the distribution of positive responses for each
behavioural variable among the eight specimens reveals little evidence of
trends with increasing body size (Fig.
5). Changes in tongue flick rates and body movement showed a
similar pattern among the species. There is clearly interspecific variation in
the responses, particularly with the 76 cm and 96 cm SVL specimens
(Fig. 5).
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Discussion |
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Crotalus atrox was used for this study due to its reputation as an
irritable species (e.g. Ernst,
1992; Tennant and Bartlett,
2000
) and the presence of overt suites of defensive and predatory
behaviours found in Crotalus sp. Previous studies have characterized
defensive behaviour in Crotalus sp. as including rattling, limited
body movement (due to maintained elevated coiling), and a decrease in
tongue-flick rate (Kardong,
1986
; Hayes and Duvall,
1991
; Young et al.,
2002
). This study relied exclusively on these overt behaviours to
gauge the response to the stimulus; inclusion of more physiological responses,
such as heart rate or hormone levels (e.g.
Moore et al., 2000
;
Secor et al., 2000
;
Mathies et al., 2001
), would
probably increase the number of positive responses. Lastly, though steps were
taken to increase the potential information content of the stimulus tone (by
using multiple unique tones with temporal patterning and frequency
modulation), they remained artificial tones played to specimens in an
isolation chamber. Presumably a biological sound, especially one coupled with
other biological stimuli, would be more likely to evoke a behavioural
response.
Wever (1978) and Hartline
(1971a
,b
)
both documented that snakes are capable of perceiving airborne vibrations, and
that they are more sensitive to airborne than groundborne vibrations (see
Young, 2002). Despite these findings, many works still describe snakes as
hearing only groundborne or substratum vibrations (e.g.
Bauchot, 1994
). This study was
designed to use unrestrained and unanesthetized snakes while restricting, if
not eliminating, the potential for groundborne vibration detection. Combining
the low frequency sound-dampening insulation with a freely suspended `hanging
basket' greatly reduced the likelihood that an acoustic bounce from the inside
of the chamber would be absorbed by the hanging basket. The open mesh design
of the hanging basket reduced the transmission of acoustic energy from the air
to the basket. The data from the accelerometer trials indicate that
transmission of sufficient acoustic energy to induce vibrations of the hanging
basket was not occurring within the frequency range of the behavioural trials.
Lastly, the airborne stimulus was designed to be 5-10 dB above the threshold
response determined by Wever
(1978
). Given the necessary
loss of energy if these vibrations were transmitted to the hanging basket, and
the findings of both Wever
(1978
) and Hartline
(1971a
,b
)
that snakes are less sensitive to groundborne vibrations, it seems unlikely
that our trial stimulus was of an amplitude sufficient to evoke a response as
a groundborne vibration.
Few studies have attempted to place vibration detection in snakes within
the context of behavioural ecology. Randall and Matocq
(1997) showed that
Pituophis melanoleucus was attracted to the sounds produced by a
buried `artificial thumper', which was used to represent the defensive foot
drumming of kangaroo rats (Dipodomys spectabilis). Burger
(1998
) modeled the footfalls of
a potential predator by dropping a rock (behind a screen) and reported that
hatchling P. melanoleucus retreated when exposed to the resulting
vibrations. Shivik et al.
(2000
) claimed that Boiga
irregularis responded in a predatory fashion to vibrational stimuli
(though in this study the snake may have been responding to motion). Young et
al. (2000
) used geophones to
model the snake ear and recorded the groundborne vibrations produced by
potential predators and prey; their results suggested that groundborne
vibrations could prove an effective detection system against potential snake
predators, but probably only valuable for predation under special
circumstances (Young et al.,
2000
). Young and Morain
(2002
) documented that Saharan
sand vipers (Cerastes cerastes) were capable of using groundborne
vibrations to target prey items. Though only anecdotal, there are additional
claims for vibration detection being used for prey capture (e.g.
Wharton, 1969
) and defense
(e.g. Klauber, 1956
). The
present study is the first evidence from controlled experimentation of a
behavioural response to airborne sound in snakes.
The head jerks that were observed in 33% of the trials
(Fig. 3B) appeared to be a
startle response rather than an orientation behaviour, in that the head was
not jerked in the direction of the speaker. Though we saw a positive response
in 92% of the behavioural trials, we saw no evidence of acoustic orientation
or even that the Crotalus atrox could spatially localize the sound
source. In sharp contrast, Young and Morain
(2002) found that C.
cerastes could localize small, free-moving mice spatially using
groundborne vibrations. No experimental work has been done on the ability of
snakes to localize airborne sound stimuli spatially, and there are several
reasons to suspect that this ability may differ from what is known in other
reptiles (Young, 2002). The results of the recent study of C.
cerastes (Young and Morain,
2002
) audition, combined with those of the present study, suggest
that snakes are capable of contextualizing vibratory information. Both C.
cerastes and Crotalus atrox have distinct suites of predatory
and defensive behaviours (e.g. Young et al.,
1999
,
2002
). In these studies C.
cerastes never exhibited defensive behaviour when presented with a small
live mouse, and Crotalus never exhibited predatory behaviour when
presented with synthesized tones.
As Hartline (1971b)
discussed, there are effectively two different pathways for hearing in snakes:
an auditory pathway, involving the stapescochlear complex, and a poorly
understood somatic pathway, involving cutaneous vibration receptors. Both
pathways can perceive both airborne and groundborne vibrations
(Hartline 1971b
). It seems
unlikely that one pathway preferentially responds to groundborne vibrations
through specific neural pathways that lead to predatory behaviour. Instead, we
believe that snakes are able to extract enough information from the
vibrational stimuli to contextualize the sounds accurately, though the
mechanism for these contextualizations remains unknown. If snakes can extract
information from vibrational stimuli, they could possibly recognize prey- or
predator-specific signatures from these signals, which is the converse of the
interesting system detailed by Rowe and colleagues (e.g. Rowe and Owings,
1990
,
1996
), in which ground
squirrels were shown to extract biologically useful information from the sound
produced by rattling rattlesnakes. Whatever the extent of contextualization of
the perceived vibrations, the results of the present study indicate that the
sensory ecology of rattlesnakes, and presumably all snakes, is more complex
than previously realized.
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Acknowledgments |
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