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First published online March 30, 2006
Journal of Experimental Biology 209, 1430-1440 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02132
Wind generated by an attacking bat: anemometric measurements and detection by the praying mantis cercal system
Department of Psychology, University of Maryland, College Park, MD 20742, USA
* Author for correspondence at present address: Department of Biology, Georgia State University, Atlanta, GA 30303, USA (e-mail: jtriblehorn{at}hotmail.com)
Accepted 30 January 2006
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Summary |
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Key words: mantis, bat, escape, wind, insect, cercal
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Hennig,
1981; Edwards and Reddy,
1986; Boyan and Ball,
1990). The cerci are two posterior appendages that contain many
hair types, including filiform hairs that are sensitive to air currents.
Afferents from these hairs project to the terminal ganglion where they synapse
with ascending interneurons that carry the sensory information rostrally in
addition to local interneurons (Burrows,
1996). In many species, the ascending interneurons have large axon
diameters and are classified as giant interneurons (GIs). The cercal-GI system
mediates terrestrial escape responses in several insects including cockroaches
(Camhi, 1984;
Ritzmann, 1984), crickets
(Tauber and Camhi, 1995) and
firebrats (Edwards and Reddy,
1986). However, other functions for the GIs have also been
identified. These include providing sensory feedback during cricket song
production (Kämper and Dambach,
1981; Kämper,
1984; Kämper and Dambach,
1985), serving as the detectors of wind-generated social signals
in non-singing crickets (Kämper and
Dambach, 1979), and playing a role in flight initiation and
maintenance (Fraser, 1977;
Altman, 1983;
Boyan et al., 1986;
Libersat et al., 1987;
Libersat and Camhi, 1988).
In flying insects possessing cercal systems, another hypothesized role for
the GIs is mediating aerial evasive responses to avoid bat predation,
triggered by detecting wind generated by an approaching bat
(Ganihar et al., 1994).
Although some insects possess auditory systems sensitive to the ultrasonic bat
echolocation calls and perform evasive maneuvers effective in eluding these
predators (Miller and Surlykke,
2001), most nocturnal flying insects lack these specialized active
defenses. However, many of these insects do possess a cercal-GI system and
could potentially benefit from engaging in evasive maneuvers triggered by the
wind generated by an approaching bat.
Ganihar et al. (Ganihar et al.,
1994) described cercal-mediated wind-evoked responses during
tethered flight in the cockroach Periplaneta americana, an insect
that lacks sensitivity to ultrasound. Side-directed wind initiated movements
consistent with turns away from the source of the stimulus in free flight. The
investigators concluded this turning away behavior suggested an escape
function whereas a turn toward the stimulus would suggest a flight correction
function.
One of the issues with the bat-generated wind hypothesis is timing; does an
insect have enough time between detecting the bat and being captured to
perform an effective evasive maneuver? Based on the fastest behavioral
component of the P. americana aerial response (wing phase change, 38
ms) and a detection time based on a moving predator simulation (54 ms),
Ganihar predicted that a cockroach has 16 ms to evade the bat
(Ganihar et al., 1994).
Although some escape responses occur in this amount of time, i.e. crayfish
tailflip <20 ms (Krasne and Wine,
1984) and fish Mauthner-mediated C-start 14 ms
(Eaton et al., 1991), many
responses have latencies of 40 ms or more, i.e. cricket terrestrial response
87 ms (Tauber and Camhi,
1995), locust jump up to 1100 ms
(Heitler, 1974), insect flight
responses 40–240 ms, depending on insect and response type
(Nolen and Hoy, 1986;
Yager et al., 1990). However,
Ganihar et al. (Ganihar et al.,
1994) noted that their simulated predator lacked certain
characteristics of an actual attacking bat. For example, their simulated
predator moved at a constant velocity throughout an attack while a bat
decelerates before it captures a target
(Schnitzler, 1987;
Jones and Rayner, 1988). Also,
a bat flapping its wings might generate more wind than their model. Both of
these factors suggest that the amount of wind generated by an actual attacking
bat and the amount of time between detection and capture were underestimated.
Finally, instead of using the cockroach's cercal system to detect the wind
generated by the simulated approaching predator, the investigators substituted
smoke or Lycopodium spores. When the simulated predator's approach
disturbed the continuous smoke/Lycopodium stream determined the
detection time. However, the smoke/Lycopodium stream may not
accurately reflect the actual physiological cercal response of the
cockroach.
The present study addresses these issues using two methods. First, using hot-wire anemometry, we describe and quantify the wind generated by a flying bat attacking a target. Second, electrodes implanted in the abdomen recorded ascending wind-evoked neural activity from an insect that served as the target during the attack of a flying bat. Both methods provide actual measurements, rather than predictions, to evaluate the bat-generated wind hypothesis, via better understanding of both the wind stimulus generated by a bat when capturing a target and the reception of this wind by the cercal system.
This experiment used the praying mantis Parasphendale agrionina as
a target. Mantids possess an ultrasound-sensitive auditory system
(Yager and Hoy, 1989) and
perform evasive maneuvers effective for eluding bats
(Yager et al., 1990). However,
they could also benefit from evasive responses triggered by bat-generated wind
that are independent of the ultrasound-mediated responses. First, Triblehorn
and Yager (Triblehorn and Yager,
2002) demonstrated that 501-T3, the ultrasound-sensitive
interneuron likely involved in triggering mantis evasive responses, shuts down
during the last 200–300 ms of a bat attack. Furthermore, activity from
other ultrasound-sensitive neurons was not observed during this period. These
results indicate that ultrasound will not trigger any `last-ditch' evasive
responses in mantids. Second, as bats capture insects, their vocalization
emission rate increases from a very low (10–15 pulses
s–1) to very high rates (over 100 pulses
s–1). Rapid transitions from low to high rates can
potentially circumvent the mantis ultrasound defenses, either by not
triggering an evasive response or by triggering the response too close to the
capture point so that the mantis may not have enough time to perform its
evasive response (Triblehorn and Yager,
2005). In both cases, mantids could potentially benefit from a
`last-ditch' response mediated by bat-generated wind cues.
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Materials and methods |
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) raised in our colony maintained at 25–30°C and
30–50% relative humidity with a 13 h day length. Mantids were housed
individually as adults and fed flies twice a week. Testing occurred 7–21
days after the final molt. All experiments used the big brown bat
(Eptesicus fuscus L.) trained to capture tethered mealworms
(Tenebrio monitor L.). Bats were collected locally in Washington, DC,
USA and surrounding Maryland suburbs.
Flight room
All experiments were conducted in a carpeted, acoustically lined (Sonex I,
Illbruck, Minneapolis, MN, USA) flight room (6.4 mx7.3 mx2.5 m) at
the University of Maryland, College Park, USA, under low-light level
conditions (Fig. 1A). Two
synchronized high-speed video recorders (Kodak MotionCorders) recorded the bat
flight and capture behavior at 240 frames s–1. A 25-point
calibration frame (2.2 mx1.9 mx1.6 m; Peak Performance
Technologies, Centennial, CO, USA) placed in the center of the room was filmed
in both camera views. Both the three-dimensional position of the bat and the
target (either the mantis for physiology experiments or the anemometer probe)
as well as the distance between them were analyzed using these images and
commercial motion analysis software (Motus, Peak Performance Technologies).
The mantis was placed near the edge of the calibrated space farthest from the
release site (indicated by a filled circle on
Fig. 1A). This positioning
provided the bat with the greatest amount of time and distance to orient
itself after leaving the perch and accelerate to attack velocity before the
capture attempt.
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Mantis implanted electrode procedure
Each mantis was slightly chilled until immobile. After removing the legs
and wings, the dorsal abdominal cuticle was removed, exposing the gut. The
caudal and rostral ends of the gut were tied off and the gut removed to expose
the ventral nerve cord. The abdominal connectives were cut between A1–T3
to record only ascending activity. Recording from the connectives between
A1–A2, the left connective was placed in one hook while the right
connective was placed in the other. A mineral oil–Vaseline mixture
isolated the recording from the body cavity while preventing the connectives
from drying out. After replacing the dorsal cuticle, an application of agar
(Fisher Science, Hampton, NH, USA) held the cuticle in place and prevented the
electrodes from slipping out. Placement of the indifferent wire in the
prothoracic cavity held the mantis in a `flight-like' posture. The prothoracic
connectives were removed beforehand to prevent the indifferent electrode from
recording the electrical activity from large units (such as mantis auditory
interneuron 501–T3) that would mask activity from wind-sensitive units
in the abdomen.
Recording procedure
The hook electrodes and indifferent wire were connected to a 32-gauge
braid-shielded stereo cable (Belden, Richmond, IN, USA) that served as the
tether. In the flight room, the cable tether connected to shielded coaxial
cable that carried the neural signals to the amplifier (A-M systems model
1700). Once in place, the mantis was 90–100 cm from the ceiling of the
flight room. The bat's perch was 1.5 m high and 3.37 m away from the hanging
mantis. The mantis cerci were pointed directly at the bat's perch since bats
approached and captured mantids from behind during free-flight encounters
conducted in the same flight room (J. D. Triblehorn, personal
observations).
After hanging and positioning the mantis in the flight room, but prior to releasing the bat, neural responses to a gentle wind stimulus (the experimenter blowing) were recorded. These wind-evoked responses were compared to neural responses elicited during the bat attack to verify that the activity came from wind-sensitive interneurons (based primarily on spike height). Fig. 2 shows an example of neural activity evoked by blowing on the cerci before the trial began with activity recorded from the same mantis just before capture by the bat. The similarity between some of the individual units indicates that both stimuli evoked responses from wind-sensitive interneurons. Signal-to-noise ratios for the largest units were 5 or better in 85% of the trials (71% of these were over 10) and their appearance indicated the beginning of a response. A bat detector (Pettersson model 100, Uppsala, Sweden) placed on the floor below the mantis recorded timing information of the bat vocalizations. Neural data were stored on DAT (Sony PCM-R500) after digitization (BioLogic DRA-400) and analyzed offline using Superscope II (GW Instruments, Somerville, MA, USA) after digitization (instruNet, Model 100B, Somerville, MA, USA) on a Macintosh G3 computer.
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Anemometer wind measurements
Wind generated by a flying, attacking bat was characterized using a single
axis hot-wire anemometer (Model 1700 constant temperature anemometer, Model
1210-60 hot-film probe; TSI, Inc., Shoreview, MN, USA). For one trial, the
sensor was placed 2 cm below the target to record bat-generated wind as the
bat successfully captured the mealworm target. Although the bat only tapped
the sensor when capturing the target, this contact damaged the anemometer
probe. To obtain a larger set of bat-generated wind velocity measurements, the
anemometer was placed at a distance from the target. A small cage (17
cmx13 cmx13 cm) protected the sensor by dissuading the bat from
attacking the probe instead of the mealworm target. The cage was constructed
from wire mesh (wire thickness=1 mm; mesh holes=1 cmx2 cm). The sensor
extended 5 cm beyond the top of the cage. This protective cage, however,
limited how close the sensor could be to the target and still have the bat
capture the mealworm (23 cm below the target was the closest distance the bat
would readily approach). Fig.
1B shows a photo from the high-speed video camera of the
experimental setup during one of these trials.
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Results |
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The wind-sensitive interneurons generally have a low level of spontaneous activity in the absence of a stimulus (indicated by the activity to the left of the arrow in each trace). Therefore, the point at which the wind-sensitive interneurons began responding to bat-generated wind (the detection time, marked by the arrow) was clear.
The neural responses across trials all consisted of a multiunit response that included both large and small amplitude units. Each response continued from the point of detection until the bat contacted and consumed the mantis (broken line). However, detection times varied across trials as did the spike train patterns.
On average, the mantis cercal system detected bat-generated wind during an attack 73.9±18.8 ms (median: 77.5, range: 38–109 ms) before contact when the bat was 27.5±7.69 cm (median: 27.5 cm, range: 14–40 cm) away. Fig. 4 shows the distribution of detection times (Fig. 4A) and distances (Fig. 4B) for the 18 trials. The bat's behavior could influence when the cercal system detects the bat's approach during an attack. One potential factor is the bat's flight velocity as it approaches the target. In these trials, the bat's velocity in the last 200 ms before the response ranged from 292–363 cm s–1. Within this range, there was no relationship between flight speed and detection time or distance (velocity vs time: r=–0.04, t(16)=–0.1763, n.s.; velocity vs distance: r=+0.36, t(16)=1.5523, n.s.; data not shown). Another potential factor is the changes in flight posture a bat performs to reduce its velocity, which could potentially increase wind production suddenly, marking the point when the mantid's cercal system detects the bat's approach. For individuals where data from only one trial was collected, the neural responses began within 70 ms of the time that the bat decelerated in 94% of the trials (15 out of 16). However, the response began before the bat decelerated in 50% of the trials (8 out of 16) and after the response began in 44% of the trials (7 out of 16). In one trial, the response coincided with the bat's deceleration. For the two mantids where data from two trials were collected, responses began with 70 ms of the time the bat decelerated in all four trials. However, for both mantids, responses occurred before deceleration in one trial and after deceleration in the other trial.
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The sacrifice of one anemometer probe allowed the collection of a velocity–time waveform and peak velocity measurement at the point of the attack. Fig. 5 shows the anemometer voltage output leading up to the point when the bat contacted the probe. The bat-generated wind had a high acceleration (800 cm s–2) and reached a peak velocity of 175 cm s–1. The fact that the wind velocity continued increasing until the point of contact suggests that the wind may not have reached its peak before the bat arrived at the target. The anemometer probe detected the bat-generated wind 75 ms before contact when the bat was 18 cm away. The rest of the anemometric data were collected with the anemometer protected and placed near (but not at) the target (see Materials and methods).
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The anemometer waveforms in Fig. 6 illustrate these changes in the bat-generated wind during attacks. All of these examples come from trials where the anemometer was 20–30 cm directly below the target. Since the anemometer was at a distance from the target, the capture time cannot be determined exactly from the anemometer. However, the experiment above demonstrated that the bat's approach was characterized by a sudden voltage increase in the anemometer trace prior to contact. Therefore, a sudden voltage increase served as a marker to indicate the bat's approach (indicated by the arrow for traces with peak velocities of 56 cm s–1 or greater) for the anemometer waveforms collected when the anemometer was near the capture point.
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Peak velocity and peak acceleration measurements of bat-generated wind
A large sample of peak velocity measurements of bat-generated wind were
collected with the anemometer probe placed close to the target (but not
directly at the target). Fig.
7A shows the peak velocities of bat-generated wind for 94 samples
as a function of the anemometer distance. The highest wind velocity recorded
was 326 cm s–1 (28 cm from the target) while the lowest was 6
cm s–1 (27 cm from target). The distance between the
anemometer and the target accounts for some of the variation seen in the data.
However, even when the anemometer was between 18–30 cm from the target
(representing 77% of the trials; shaded area in
Fig. 7A), bat-generated wind
velocity measurements still exhibited substantial variation unrelated to
distance. In 38.5% of the trials, the measured peak wind velocities were below
50 cm s–1. In 31% of the trials, bat-generated wind contained
peak velocities between 50–100 cm s–1 and peak
velocities exceeded 100 cm s–1 in the remaining 30.5% of the
trials.
In the other 23% of the trials, the probe was 30–50 cm away from the
target. In these cases, the anemometer probe was below the target, but off to
the side and not directly below. This setup simulated situations where a
mantis evades capture by performing a power dive and determined how much wind
would reach the mantis as the bat flies by. Since the mantis auditory system
lacks the ability to localize sound (Yager
and Hoy, 1989; Yager et al.,
1990), bat-generated wind could indicate the location of the bat
to the mantis. Mantids could then potentially incorporate this new sensory
information into the power dive response to direct the mantis further from the
bat's location and increase its chances of survival. At these distances, the
anemometer probe still detected bat-generated wind, but the peak velocities
were lower, ranging between 20–60 cm s–1 peak velocity
(Fig. 7A).
The bat-generated wind had a high acceleration component, shown in Fig. 7B. Although the measured peak accelerations spanned a wide range, measurements exceeding 200 cm s–2 account for over one-third of the data. Peak acceleration was significantly correlated with peak velocity (r=+0.92, t(64)=18.7794, P<0.001), increasing exponentially with peak velocity (Fig. 7C).
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Physiological recordings of wind-sensitive interneuron activity during bat attacks provide good measurements of detection times and possess three distinct advantages over the hot-wire anemometric measurements: (1) they provide the most accurate information about bat-generated wind (although uncalibrated regarding the wind's magnitude) since the `sensor' serves as the target, (2) they provide the most relevant information for evaluating the possible success of wind-evoked responses (by providing detection time and distances) since the natural receiver detects the stimulus from the natural producer, and (3) they allow the collection of multiple trials without risking the bat or expensive equipment.
Hot-wire anemometry provided calibrated measurements of bat-generated wind not available in the physiological recordings. The measurements include the magnitude of the wind generated as well as how the generated wind pattern changes at a single point over a period of time.
The nature of wind generated by an attacking bat and its measurement
The wind stimulus created by an approaching bat should be very complex and
will vary with the angle of approach, initial bat flight speed, wing stroke
angle and frequency, rate and timing of deceleration, and the effective area
of the bat facing the anemometer probe. The air motion will be turbulent,
hence varying unpredictably in velocity and direction. The complexity and
variability of the wind produced by an attacking bat makes the measurements of
the bat-generated wind using a single-axis hot-wire anemometer probe with a 2
mm sensor surface difficult. In addition to the factors mentioned above, the
probe only samples a small region of the entire wind stimulus. However, these
are the same difficulties faced by an insect's cercal system when detecting
the wind from an approaching bat. P. agrionina's cerci occupy as much
space as the anemometer probe and, therefore, sample only a small portion of
the bat-generated wind. Furthermore, cercal systems are directionally
sensitive (Palka et al., 1977;
Dagan and Camhi, 1979;
Westin, 1979), similar to the
anemometer probe. Therefore, certain characteristics of the data collected
using the anemometer, such as the large variation in the data when the probe
was within 20–30 cm of the target, fully represent and describe the
situation involving the cercal system.
Despite the predicted and observed variation in the wind stimulus, the
anemometer data consistently show an initial peak with a high acceleration and
the maximum velocity for the trial. The early appearance of these components
represents the insect's first indication of a bat's approach based solely on
wind. Furthermore, the anemometer data unquestionably underestimate the
maximum velocity and probably the acceleration, since the probe was not
directly at the target for the majority of the measurements. Variation in
maximum velocity may be relatively unimportant to the insect, because even our
underestimates are orders of magnitude above detection threshold for the
cercal system (Triblehorn,
1997). The physiological recordings confirm that such a
bat-generated wind stimulus sufficiently excites several wind-sensitive
interneurons.
Wind stimulus acceleration, not peak velocity, may be the more important
parameter for triggering an evasive response. This is the case in
cercal-mediated terrestrial responses and is important for the animal
distinguishing between wind generated from a predator (with high
accelerations) that trigger an escape response vs changes in ambient
wind conditions (with low accelerations though potentially high velocities)
that do not trigger escape responses
(Plummer and Camhi, 1981). For
cercal-mediated aerial responses, the acceleration component may be even more
important since flight provides continuous wind stimulation on the cerci with
relatively high velocities (around 180 cm s–1 in mantids and
cockroaches) but with low accelerations during stable flight.
In cockroaches, wind stimuli with high accelerations (60 cm
s–2 or higher) evoke escape running, while stimuli with
accelerations around 30 cm s–2 evoke a pause in walking
(Camhi and Nolen, 1981). The
peak acceleration of the bat-generated wind often exceeded 200 cm
s–2, more than three times the acceleration necessary to
evoke escape running in cockroaches. The peak accelerations measured in our
experiments using stationary targets (both the anemometer and mantis
physiological preparation) may be overestimates compared to the natural
situation where the mantis would be flying. As mentioned previously, however,
the anemometer probe was not located directly at the target and, therefore,
likely underestimates the actual peak acceleration. Even so, the peak
accelerations measured were very high (a large proportion were >200 cm
s–2). Furthermore, the peak acceleration was 800 cm
s–2 for the one trial where the anemometer was located at the
target.
Evaluating the bat-generated wind hypothesis: is there enough time to escape?
The physiology results showed that the mantis cercal system detected the
bat an average of 74 ms before contact, when the bat was 27.5 cm away. Since
the electrodes were implanted to record from the connectives between
A1–A2, these detection times actually incorporate the detection of the
bat-generated wind by cercal hairs, afferent neural conduction, processing and
information transfer to ascending interneurons in the terminal ganglion, and
conduction time to reach the electrodes. These results correlate well with the
detection time measured by the anemometer placed within 2 cm of the target (75
ms), but not as well with the detection distance measurement (18 cm). Still,
18 cm is within the range of detection distances from the physiological
measurements. It is interesting that this detection time matches the cockroach
cercal system's detection time of the wind produced by the tongue strike of an
attacking toad, a natural predator that evokes the terrestrial wind-evoked
response (Camhi et al., 1978).
Based on the wind cue alone, cockroaches escaped 55% of the time (47%
advantage over cockroaches with cerci covered and unable to detect wind).
Therefore, it is not unreasonable that using the wind cue may improve the
mantid's odds at escaping when the auditory defense fails.
Comparisons between the bat's flight velocity at detection indicated that this parameter was not correlated to either an earlier detection time or distance. However, the tail-flip used by a bat to capture an insect and transfer it to its mouth begins about 65±15 ms before capture (N=10; K. Ghose, personal communication). This value is close to the 74 ms average detection time, suggesting that the tail-flip may be a major contributor to the bat-generated wind that the cercal system detects.
Based on their predator simulations, Ganihar et al.
(Ganihar et al., 1994)
estimated that an insect could detect an approaching bat predator 54 ms before
contact (40–68 msrange). The current assessment of average detection
time (74 ms) based on physiological recordings allows the insect 20 ms more to
escape. The new estimate allows the cockroach a total of 36 ms to evade the
bat (based on the cockroach's 38 ms behavioral response latency;
Ganihar et al., 1994). Even
with the increase in the detection time from Ganihar's estimate, it still
seems unlikely that enough time exists for a cockroach (or any insect) to
detect the bat and perform a response that will cause a bat to completely miss
it. However, there may be enough time for the insect to alter its position
just before capture. Although researchers suggest that echolocating bats
update the target location on an echo-by-echo basis
(Masters et al., 1985;
Masters, 1988), others suggest
that bats plan their capture attempt early by predicting the location of the
insect at the point of capture (Wilson and
Moss, 2002; Ghose et al., in
press). If bats do plan their capture attempt in advance, any
wind-evoked behavior altering the insect's flight would result in a difference
between the bat's prediction and the insect's actual location. This deviation
could cause the bat to mishandle the insect (i.e. drop it) since the bat would
not be able to adjust to the unpredicted change. Earlier wind detection would
give the insect more time to respond, resulting in a larger discrepancy
between the bat's prediction and the mantid's actual location. Therefore,
successful wind-evoked insect evasive maneuvers would likely not cause the bat
to completely miss the insect, but cause the bat to mishandle the target
during capture by tipping the insect with its wing or tail membrane and give
it one final chance to avoid the bat. Such late changes in the insect's
trajectory could also pose problems if bats do update a target's location on
an echo-by-echo basis. Although the bat may detect the change, it may not be
able to act on this information and adjust its capture attempt to compensate
for the alteration of the insect's location in such a short time.
In staged free-flight encounters between mantids and bats, we have observed
bats making contact with deafened mantids (thus eliminating the
ultrasound-triggered evasive response) and dropping them
(Triblehorn, 2003). These
mantids were not bitten, so they were not dropped after the bat transferred
the mantis to its mouth and began eating. Although no behavioral responses
from the mantids were observed, such responses would occur very close to the
time of capture (within 100 ms) and would not likely be seen by the observers
(though the sound of the bat making contact with the mantis was evident).
Although such observations could be coincidental mistakes in the bat handling
the mantis, it is also possible that these dropped, deafened mantids
successfully detected and responded to wind from the approaching bat, enabling
them to survive the attack.
The fragility of the implanted mantis preparation and the nature of the
experiment as a whole prevented establishing, without a doubt, that the
activity recorded during the bat attacks are from ascending wind-sensitive
interneurons. However, in addition to the data presented here (see
Fig. 2 and Results), data from
other studies conducted in our laboratory indicate that this is most likely
the case. First, mantids do possess filiform hairs that are sensitive to wind
stimulation, and removing and/or shortening these hairs increases wind
detection thresholds measured by recording from the cercal nerve
(Triblehorn, 1997). Second,
extracellular recordings from abdominal connectives in P. agrionina
reveal that wind puffs of varying velocities elicit responses from multiple
ascending interneurons (Triblehorn,
2003). These interneurons vary in spike height and firing
properties (i.e. find both phasic and tonic units). Furthermore, covering the
cerci with Vaseline eliminated these wind-elicited responses (J. D.
Triblehorn, personal observation). Finally, in the current study, with the
exception of testing the mantis preparation by blowing on the cerci, neural
responses resembling those elicited by the approach of the bat did not occur,
either spontaneously or as a result of the experimenter's actions while
preparing for the trial.
Using bat-generated wind during escapes
Anemometer measurements show that bats can generate wind detectable at
least 50 cm away from the target. Mantids are unable to localize sound and
cannot determine the approaching direction of the attacking bat
(Yager and Hoy, 1989;
Yager and May, 1990). When the
bat is close, the mantis executes a power dive to evade the bat and does not
necessarily need to know the bat's approach direction. However, the wind
created as the bat passes the diving mantis could serve as a cue to the bat's
location. The mantis could incorporate this new sensory information into its
power dive, giving the dive a directional component allowing the mantis to not
only escape from the bat's initial attack, but also enable it to avoid a
second attack.
The use of bat-generated wind in these scenarios only seems reasonable if
the mantis is within 30 cm of the bat (see
Fig. 7). Within this distance,
peak velocities exceed 100 cm s–1 in 30.5% of the trials.
However, beyond this range, peak velocities rarely exceeded 60 cm
s–1. Wind puffs at 60 cm s–1 failed to
elicit strong behavioral responses in flying cockroaches
(Ganihar et al., 1994) or
significant changes in P. agrionina wind-sensitive interneuron
activity in the presence of a flight-simulated headwind
(Triblehorn, 2003). In the
latter experiments, the flight-simulated headwind was set to 180 cm
s–1 (equal to the mantis stable flight velocity). When
executing a power dive, mantids double their flight velocity, which would
potentially make it more difficult for the cercal system to detect the
bat-generated wind. However, this increase is not instantaneous and mantids
should be too far from the bat by the time they reach this velocity for the
bat-generated wind to be a factor. However, even when flying at 180 cm
s–1 at the initiation of a power dive, it seems unlikely that
mantids should rely on bat-generated wind for determining the direction of the
attack and incorporate this information into their response.
Candidates for putative wind-mediated evasive responses
Insects that would benefit from wind-mediated evasive response to avoid bat
predation are those that possess cerci and fly nocturnally. Despite the
prevalence of either of the characteristics across insect species, those that
possess both are in the minority. The majority of insects that possess cerci
are wingless and do not fly. On the other hand, all of the holometabolous
(complete metamorphosis) insects (such as Diptera, e.g. flies; Lepidotera,
e.g. moths and butterflies; Homoptera, e.g. cicadas and aphids; Hymenoptera,
e.g. bees, ants and wasps; and Coleoptera, e.g. beetles) as well as Hemiptera
(e.g. the true bugs) and Neuroptera (e.g. lacewings and caddis flies) have
lost their cerci but have the ability to fly. The main candidates for putative
wind-mediated evasive responses are members of Dictyoptera (e.g. mantids and
cockroaches) and Orthoptera (e.g. crickets, locusts, grasshoppers,
katydids).
Insect `last chance' bat avoidance responses
Late `last-chance' behaviors, mediated by ultrasound-sensitive auditory
systems, have been described in several insects. Green lacewings passively
fall in response to bat vocalizations emitted at low rates, but as the bat
closes in on the capture, the higher emission rates trigger `wing-flips' in
the lacewing that abruptly slow its descent
(Miller and Olesen, 1979).
`Wing-flips' occur about 50–100 ms before capture and this unexpected
alteration in the lacewing's descent occurring late in the bat's capture
attempt causes the bat to miss the insect 70% of the time. Arctiid moths
produce ultrasonic `clicks' that deter bats from capturing the insects as an
acoustic aposematic signal (Dunning,
1968; Dunning et al.,
1992; Hristov and Conner,
2005), by startling the bat
(Möhl and Miller, 1976)
or `jamming' its ability to echolocate
(Fullard et al., 1979). High
bat emission rates trigger arctiid moth `clicks' during the late stage of the
bat attack (Fullard, 1984;
Fullard et al., 1994) and
begin between 142–270 ms before capture, depending on stimulus level.
Acharya and Fenton (Acharya and Fenton,
1992) showed that bats rarely contact `clicking' moths even though
the arctiids show little, if any, evasive behaviors during the attack.
These `last-chance' maneuvers do not require significant alterations in
flight trajectories to be effective, which likely contributes to their high
success rate. The lacewing passive fall relies on gravity and the `wing-flip'
simply alters the velocity of this fall, not its trajectory. Arctiid moth
`clicks' effectively protect the insect without any alteration in its flight
path. However, for the putative wind response, success potentially relies on
how much the insect can alter its trajectory from the bat's prediction during
its capture attempt. This requires time to initiate the response internally
(neuromuscular response) and for the response to take effect (resulting in a
change in flight path). Given the short amount of time for this to occur, the
success rate will likely be much lower than the other `last chance' maneuvers.
Still, very low survival advantages can be very important evolutionarily
(Endler, 1986). Since the
response makes use of the neural, muscular and behavioral elements already
present and in use during normal flight, the cost to the insect is minimal
while providing a slim chance to survive the encounter, which is better than
no chance.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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