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First published online February 13, 2009
Journal of Experimental Biology 212, 693-703 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.019380
Behavioral responses of big brown bats to dives by praying mantises
1 Neuroscience and Cognitive Science Program and Department of Psychology,
University of Maryland, College Park, MD 20742, USA
2 Department of Psychology, University of Maryland, College Park, MD 20742,
USA
* Author for correspondence at present address: Harvard Medical School, Neurobiology, 220 Longwood Avenue, Boston, MA 02115, USA (e-mail: kaushik_ghose{at}hms.harvard.edu)
Accepted 1 December 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: bat, echolocation, evasion, insect, predator–prey
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Miller and Surlykke, 2001),
avoiding flying at times when bats are also likely to be in the air, flying
erratically, and flying at low altitude
(Lewis et al., 1993). Some
insects also produce sounds that may serve to jam bat sonar or startle bats
(Miller, 1991;
Møhl and Miller, 1975).
The best known specific strategies are dives and erratic loops performed in
response to the ultrasonic signals of bats
(Roeder and Treat, 1961;
Triblehorn and Yager, 2005a;
Yager et al., 1990).
It is possible that bats have, in turn, developed counter-measures to
insect defenses, though evidence for this has been controversial. Some studies
have suggested that bats counter hearing insects by gleaning instead of
hawking (Fenton and Fullard,
1979), and by shifting the energy of their echolocation calls out
of the insect's hearing range (Neuweiler,
1989). Other proposed strategies include shortening calls,
reducing call intensity or going silent altogether, although these changes
also occur during bat attacks on non-hearing prey
(Miller and Surlykke, 2001).
There are studies, however, which call into question the effectiveness of such
call adaptations (Russo et al.,
2007; Schmidt et al.,
2000).
Previous observations of echolocating bats chasing insects in erratic but
level flight have shown that bats employ a strategy well suited to the
unpredictable maneuvers of their prey. This strategy, in which the bat
maintains a constant absolute target direction (CATD), differs from classical
pursuit (Rushton et al., 1998)
and constant bearing strategies (Fajen and
Warren, 2004), and allows the pursuer to minimize the time
required to make contact with an erratically moving target
(Ghose et al., 2006). It is,
however, not known what kind of adjustments bats make to their flight strategy
to deal with rapid vertical plane maneuvers such as ultrasound-triggered
dives. In this study we investigate the responses bats make to defeat
last-second evasion by diving insects.
Mantises are an excellent example of insects that use a specific anti-bat
defense. Many mantises posses a single (cyclopean) ear on the midline of the
thorax that is most sensitive to ultrasonic sounds between 25 and 45 kHz (for
a review, see Yager, 1999). In
response to bat vocalizations, mantises perform turns, turns with dives and
power dives. Turns are elicited when the ultrasonic stimulus is weak,
corresponding to a distant bat, and turns with dives are observed with
stronger ultrasonic stimuli. Power dives, in which the mantis directs the
thrust from its wings downward to add to gravitational acceleration, are
elicited by more intense vocalizations, corresponding to a nearby, perhaps
attacking bat (Yager et al.,
1990).
In this study we examined vocalization patterns, flight strategies, and
sonar beam aim adjustments of big brown bats, Eptesicus fuscus
Beauvois, in response to sudden dives initiated by praying mantises
[Parasphendale agrionina Mantidae: Miomantinae: Miomantini
(Ehrmann and Roy, 2002)] that
served as potential prey in a laboratory flight room. This is the first study
to look at short term responses of bats to ultrasound-triggered evasive
maneuvers by insects. Studying such reactions helps us understand bat
insect-capture behavior and may lead to a more complete understanding of the
dynamic interactions between echolocating bats and nocturnal insects.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) and
at least one species of mantis (Sontag,
1971) are insensitive. Images from two high-speed video cameras
(Kodak MotionCorder, CCD-based infrared sensitive cameras, running at 240
frames per second, synchronized to 1/2 frame accuracy) were used to
reconstruct the three-dimensional flight paths of the bats and the trajectory
of the prey in a calibrated region of the flight room. Two ultrasonic
microphones (Ultrasound Advice SM2 microphones and SP2 amplifiers) were placed
30 cm above the floor to record bat vocalizations. A custom-built, U-shaped
array of 16 microphones (Knowles FG3329, with custom-built amplifying and
filtering circuits) recorded horizontal cross sections of the sonar beam
pattern emitted by the bats. This microphone array was used previously to
study bat sonar beam directing behavior during target interception
(Ghose and Moss, 2003).
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Experimental protocol
We designed our experiments to evaluate the behavioral responses of big
brown bats when their pursuits were interrupted by the mantis' evasive dive
maneuver. We examined flight kinematics, vocalization patterns and sonar beam
aim direction close to the time of the mantis dive, focusing on how these
quantities changed immediately after the mantis dive. Bat responses to mantis
dives were compared with a control group of trials in which the mantis'
ultrasound-triggered dive was suppressed and the bat chased non-diving but
otherwise erratically flying mantises.
We divided the mantises into two groups. Mantises in the first group were
untreated, and mantises in the other group were deafened by applying
Vaseline© to the ear
(Triblehorn et al., 2008). The
deafening treatment suppressed ultrasound-triggered escape responses in 19 out
of 22 flights. A given trial randomly involved a deafened or hearing mantis
and the experimenters were blind to the condition of the mantis prior to
release. Bats would chase both hearing and deafened mantises.
Each bat was tested as it chased a single flying mantis in the room. The bat was first released from its temporary cage and allowed to fly in the room for a variable period (10–30 s) while one experimenter (J.D.T.) stood on a step-ladder and kept the mantis concealed in his hand. The mantis was then released into the room from a height of about 2 m, starting the experimental trial. The trial ended when the mantis was captured or when it landed on the floor or walls of the flight room. Only trials in which the mantis attained stable flight were included in the data set. It is probable that the bats learned the release point of the mantis. However, if the bat hovered or circled near the release point, mantis release was delayed until the bat continued to fly around the room. In most cases the mantis was released when the bat was at the far side of the room, requiring the bat to complete at least a half circuit of the room in order to reach the mantis, by which time the mantis had flown to another point in the flight space. The data analysis required three-dimensional reconstruction of both the bat and mantis flight paths. Therefore, only trials in which the encounter occurred in view of both video cameras and within the camera calibrated space of the flight room were used.
Flight path analysis
The flight paths of the bat and mantis were reconstructed using
commercially available motion analysis software (Motus, Peak Performance
Technologies Centennial, CO, USA, now merged to form Vicon Peak). Data
analysis was done using scripts written in MATLAB (MathWorks, Natick, MA,
USA). The digitized flight track data points were smoothed using a rectangular
sliding window 125 ms long. Flight velocities were obtained using Newton's
difference quotient method (Thompson,
1919) to compute time derivatives of position for each time
step.
Flight strategy quantification
In previous work it has been shown that bats pursue non-diving insects
using a constant absolute target direction (CATD) strategy
(Ghose et al., 2006), also
known as parallel navigation in the missile guidance literature
(Yuan, 1948). In this strategy
the bat maneuvers such that bearing lines drawn from the bat to its target
appear parallel when viewed from an external reference frame
(Fig. 1B). A pursuer and evader
pair can maintain parallel navigation (or CATD) both when the distance between
them decreases, as well as when it increases. A pursuer will attempt to
maneuver so that distance decreases. Conversely, an evader that is aware of
its pursuer's position could maneuver to increase distance. In both cases,
when the CATD condition is attained, the rate of change in distance between
pursuer and evader is the maximum that can be obtained, given the current
speed of the pursuer and the evader. The CATD strategy, therefore, enables a
faster pursuer to minimize the time it takes to intercept a slower,
unpredictably moving target. This is in contrast to other common pursuit
strategies reported in the literature such as `classical pursuit'
(Rushton et al., 1998) and
`constant bearing' (Fajen and Warren,
2004).
We computed an index (
) of how close the bat's pursuit approached
the ideal (CATD) condition (Justh and
Krishnaprasad, 2006) and used this to determine the quality of the
bat's pursuit. is the cosine of the angle between the bat-target
separation vector and the vector representing the rate of change of this
separation. A value of –1 indicates the bat is adhering
perfectly to a CATD strategy while closing in at a maximum rate (the
separation between them is directly decreasing). By contrast, a value
of +1 indicates that the target and the bat, while adhering to CATD, are
separating at a maximum rate. Intermediate values of indicate partial
convergence to the CATD strategy. Random motions of two actors that are not
reacting to each other would cause random fluctuations of between +1
and –1, leading to a time averaged value of =0. In our
experiments we consider sustained periods of =–1 or =+1
(combined with specific bat vocal behavior – see next section) as
evidence of a systematic interaction between the bat and insect.
Vocalization pattern analysis
Vocalization times were selected by displaying the time-waveform and
spectrogram of each call and marking the start and stop times of the
fundamental of each bat call. Pulse repetition rate (PRR) was computed from
the time interval between the start of successive calls. We used the PRR to
identify the beginning and end of periods when the bat was actively pursuing
the insect. Typically, when searching or cruising, bats produce calls at low
PRR (<20 Hz). Upon detecting and then pursuing prey, bats raise the PRR to
100 Hz, and conclude with rates as high as 150 Hz, referred to as the `buzz'.
The vocalization pattern can, therefore, be used to index the behavioral state
of the bat (Griffin, 1953;
Griffin et al., 1960;
Surlykke and Moss, 2000).
Sonar beam direction analysis
Sonar beam directions were computed from sound intensities measured across
the array of microphones (Ghose and Moss,
2003). The experimenters were not in control of where the
encounter between the bat and mantis took place, and in many of the encounters
when video data were available microphone array data were not suitable for
sonar beam computation. For this reason, examples of sonar beam directing
behavior are presented, but without statistical analysis. In addition, only
the horizontal direction of the bat's sonar beam aim is available from the
linear microphone array, so we were unable to investigate the vertical
tracking behavior of the bat's sonar beam.
Identification of mantis dives
Each mantis trajectory was categorized as `dive' or `no-dive' based on the
vertical speed and distance dropped. Fig.
2 shows mantis vertical speed plotted against vertical distance
traveled. In this figure negative vertical speed indicates downward motion
towards the floor and negative vertical distance indicates a drop in height. A
dive was considered to have taken place if a flight segment was found where
the mantis' vertical speed always exceeded –1.0 m s–1
and during which the mantis lost more than 0.5 m in height. The mantis dive
initiation point was defined as the start of such a segment. Even in level
flight, mantises were sometimes observed to make bobbing movements, known as
the `goldfinch flight' (Yager et al.,
1990). Our criterion was chosen to prevent selection of such
bobbing as dives as well as to reject slow descents.
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).
Caveats related to room height
The height of the flight room was 2.5 m. Bat–mantis interactions in
the field have been observed from ground level to tree-top heights
(Yager et al., 1990). The
comparatively low height of the flight room most probably resulted in the bats
not attaining as fast a dive speed as they would in the wild (and in general
not flying as fast as they would in the wild). The flight room ceiling height
also means our experiments form a sample of interactions within a limited
range of elevation above the floor, whereas in the wild such interactions
would occur over a much broader range. In this study we focused on the
response of the bat immediately after the mantis dive. This part of the bat's
response should be minimally affected by the constraints imposed by the
dimensions of the room.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
The bat–mantis interactions were categorized into four classes, based
on the flight behavior of the mantis, the flight responses of the bat, and the
vocal patterning produced by the bat. All mantis captures occurred during
flights when the mantis did not dive (`captures'). All mantises that executed
dives escaped from the bat. After the mantis dived, the bat would sometimes
follow the mantis into the dive (`follows'), abort its pursuit (`abort'), or
display other behavioral responses (`other'). When pursuing mantises that did
not dive, the bats employed a CATD strategy
(Ghose et al., 2006). We found
that during `aborts' the bat's convergence to a CATD pursuit was broken by the
mantis dive. During some `follows' the bat maintained the CATD pursuit for
about 400 ms into the dive, before breaking off. During some follows, however,
the bat did not manage to converge on a CATD pursuit either before of after
the dive.
Four classes of bat-mantis interactions
Captures
In trials when the mantis did not dive, the bat would execute a typical
attack sequence (Griffin, 1958)
an example of which is shown in Fig.
3. In this trial the bat initially approached the mantis head-on,
at a relative horizontal speed of about 7.5 m s–1
(Fig. 3C; sum of speeds, since
bat was approaching the mantis) producing sonar vocalizations at a high PRR,
indicative of pursuit. The bat was unable to maneuver fast enough to capture
the mantis on the first pass [time (t)=t1] and
made a `U-turn' to reposition itself. The U-turn was accompanied by braking
(dip in horizontal speed in Fig.
3C; t>t1) and a drop in PRR
(Fig. 3A;
t>t1). After completing the U-turn, the bat
accelerated and resumed its pursuit of the mantis, once again increasing its
PRR. The bat locked its sonar beam onto the target during the entire maneuver,
starting with the U-turn and continuing up to capture
(Fig. 3H, black lines drawn
from bat trajectory; and Fig.
3I), consistent with a previous study of bats capturing tethered
prey (Ghose and Moss, 2003).
The bearing lines (Fig.
3E–G, light gray lines) drawn from bat to target were
parallel to each other during the final phase of capture. The parallel nature
of the bearing lines shows that during target interception the bat adopted a
constant absolute target direction (CATD) strategy
(Ghose et al., 2006). Right
after capture the bat abruptly dropped its PRR
(Fig. 3B; t>0 s).
During this encounter, neither the mantis nor the bat made large maneuvers in
the vertical plane (Fig.
3D,F,G). The bat's vocalization pattern resembles that reported
for aerial hawking sequences in the lab and field
(Griffin, 1958;
Surlykke and Moss, 2000), as
does its sonar beam tracking behavior
(Ghose and Moss, 2003). Such
interactions were classified as `captures'. In our experiments, whenever the
mantis did not dive, the bat was successful in capturing the mantis.
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Aborts
In contrast, for some trials when the mantis dived, the bat would abruptly
terminate its pursuit shortly after mantis dive initiation, as illustrated in
Fig. 4. Here the bat performed
an almost complete horizontal loop to maneuver itself into a `tail-chase' with
the mantis. The bat's horizontal speed dropped during the initial loop
(Fig. 4C; dip at
t=–1.5 s), after which it accelerated and approached the mantis
from directly behind. During the loop and right up to the mantis dive the bat
kept its sonar beam locked onto its target
(Fig. 4H,I). There was little
change in the vertical (Fig.
4C) or horizontal (Fig.
4D) speeds of the mantis until t=0 s, at which point the
mantis dived. Up to this point the bat had matched or exceeded the mantis'
horizontal speed and was about to capture the mantis. The dive, indicated by a
sudden increase in downward vertical speed in
Fig. 4C (t=0 s),
caused the mantis to drop away rapidly from the bat just before capture. In
response to this maneuver the bat dropped its PRR and continued on a level
course without attempting to compensate for the mantis dive. The bat's vocal,
flight and sonar beam behavior was typical for insect captures right up to the
mantis dive point, after which the bat stopped responding to the mantis. Such
interactions were classified as `aborts'.
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Summary of data in the four classes
We analyzed a total of 35 trials of which 18 (51%) were no-dive and 17
(49%) were dive trials. In the dive category we made further subdivisions
based on the bat's behavior – abort, follows and other – as
described in the examples above. In two trials (2/17, 12%) the bat aborted its
pursuit, by abruptly terminating its high PRR, within 50 ms of the mantis dive
(`abort'). In six trials (6/17, 35%) the bat continued producing high PRRs at
least 200 ms into the mantis dive, indicating continued pursuit even after the
dive (`follow'). In nine trials (9/17, 53%) the mantis dive occurred at a time
when the bat was not producing high PRRs (`other'). A detailed count of
behavioral responses across bats is provided in
Table 1.
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Evasive behavior of the mantis
Mantis dive initiation was triggered by a wide variety of bat vocalization
patterns and occurred at a wide range of distances from the bat.
Fig. 7A shows the pulse rate of
the bat just prior to mantis dive, plotted against bat–mantis range at
dive initiation, and Fig. 8A
(trials in the `dives' section) shows the pulse pattern produced by the bat
plotted with respect to the mantis dive time (t=0). In some trials
the bat never vocalized at a rate above 20 Hz in a 1 s window preceding the
dive (seventh trial from top under `other') while in other trials the bat
persistently pursued the insect, producing high PRR calls for almost 1 s prior
to the dive (second trial from top under `follows').
Fig. 7B is a histogram of the
distance between the bat and the prey at the time when the mantis dive
occurred. Mantis dives were initiated more frequently at closer ranges, with
70% (12/17) of dives occurring within 1.0 m from the bat.
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), we
observed that mantis dives were not directional relative to the position of
the bat near dive time (Fig.
7C,D). Fig. 7C
shows top-views of the 17 mantis trials in which we observed a dive. Each line
shows mantis flight trajectory data up to 400 ms before and after the dive.
Each trajectory is a different colour and line thickness, and the start
position is indicated by a circle. The trajectories themselves have been
translated to place the dive point at the center of the axes (0,0) and rotated
so that the position of the bat relative to the mantis heading at dive time is
along the black dotted line directed along co-ordinates 0,–1.
Fig. 7D is a larger scale view
of the boxed region in Fig. 7C.
In such a representation, if the mantis dive was directionally dependent on
the bat position, then each trajectory, around the time it crossed the origin
of the axis (near dive point), would deflect in a systematic way with
reference to the black dotted line (direction to the bat).
Fig. 7C,D shows, however, that
in almost all cases the mantis continued flying in the same horizontal
direction before and after the dive. Post-dive turning rate traces rose 3
standard deviations above the mean pre-dive turning rate for only two trials
(equivalent to a P value of 0.001).
Vocalization behavior of the bat
The vocalization behavior of the bats across 35 trials is summarized in
Fig. 8. Trials are classified
as `captures', `follows', `aborts' and `other', based on the mantis and bat
behavior as described above. Vocalization rasters for the trials are shown in
Fig. 8A, grouped by category.
In this panel each row represents a single trial, with time on the x-axis
relative to capture or the mantis dive initiation. Each dot represents a
vocalization emitted by the bat and a high density of dots indicates a high
PRR. The mean and standard deviation of the PRR plotted against time for all
trials in a particular behavioral category is shown in
Fig. 8B.
Fig. 8C shows an expanded view
of the PRR profile ±200 ms around dive (or capture) time. Captures,
follows and aborts are characterized by having a high PRR just prior to
dive/capture time. During captures, the PRR dropped just prior to
capture-point, for aborts the PRR dropped just after dive initiation, whereas
for follows, a high value for PRR persisted even 200 ms into the dive.
`Others' are characterized by a low PRR (typical of the post-capture,
post-abort periods) over a ±200 ms window around the dive. There was,
however, a bump in PRR ending just 200 ms prior to the dive point. This
indicates that, typically, the bat probed the mantis at some point earlier in
the trial (exceptions can be seen in Fig.
8A), but was not pursuing it just before dive initiation.
From Fig. 4A and
Fig. 5A we note a saw-tooth
pattern in the PRR profile before the bat produced the terminal buzz,
characterized by a stable PRR of about 150 Hz. This saw-tooth pattern,
indicating clusters of pulses produced at a high rate separated by silent
periods, has been referred to in previous work as `sonar strobe groups'
(Moss et al., 2006;
Moss and Surlykke, 2001). We
observed strobe groups in all four classes of bat–mantis interactions
(Fig. 8A, islands of dots
separated by larger gaps).
Bat flight strategy during pursuit
Bats have been shown to pursue both tethered and free flying insects using
a CATD flight strategy (Ghose et al.,
2006). Under conditions when an evader is moving unpredictably,
the pursuer can minimize, on average, the time it takes to catch the evader by
adopting a CATD strategy. In this sense, the CATD strategy is time optimal for
chasing unpredictably moving prey, and may explain why bats adopt such a
pursuit strategy.
A CATD strategy can be informally inferred by inspecting plots of the flight trajectories of the bat and insect and noting whether bearing lines drawn from the bat to the insect are parallel to each other. Such a strategy is evident in the bat flight trajectory plots in Figs 3 and 5. In Fig. 4, we cannot determine whether the bat used a CATD strategy since the bearing lines overlap with each other since the pursuit was a tail-chase.
We can compute an index to quantify how close the bat is to the
ideal CATD strategy (see Materials and methods). A value of –1
indicates that the bat is maneuvering to maintain a perfect CATD strategy.
Conversely, a value of +1 indicates that the separation between the
mantis and the bat is increasing at a maximal rate.
Fig. 9 shows summaries of
with time for the different categories of trials. The black line shows
the mean value of with standard deviation depicted as the surrounding
gray band.
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close to –1 and
maintained this value for 200 ms or more until it merged with the mantis at
time t=0. During aborts the bat similarly maneuvered to bring
=–1 (Fig. 9B). Up
to the dive point the profile of was similar to that observed during
captures. After the dive the value of shot up to +1, indicating that
the mantis dive was a very effective evasive maneuver. Such trials serve to
illustrate the effect of the mantis dive in the absence of any compensatory
flight maneuvers by the bat.
In some follows (Fig. 9C,
gray line; N=3), even though the high attack PRR was maintained, the
bat did not succeed in adjusting to –1 before or after the dive.
An example of this is shown in Fig.
10 where the bat pursued the mantis into the dive, maintaining a
high PRR past the dive point (Fig.
10A,B) and adjusting its vertical speed to match that of the
mantis (Fig. 10D; vertical
speed traces around t=0). However, as can be seen from the flight
trajectory plots, the bat did not converge on a CATD strategy
(Fig. 10E; bearing lines are
never parallel) either before or after the mantis dive (indicated by an
arrow).
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hovered around zero within a ±100 ms window around the dive).
The dip in at time t<–200 ms is consistent with the
brief increase in PRR around this time
(Fig. 8B) indicating that, in
some trials, the bat responded to the insect at some point earlier in the
trial, but did not pursue it proximate to the dive.
Although the data described so far seem to indicate the bat's flying skills
are no match for the diving mantis, the situation is not quite so bleak for
the bat. In a subset of follows (Fig.
9C, black line; N=3) the bat not only maneuvered to bring
=–1 before the dive, it maintained this optimal pursuit even when
the mantis dived (plot of stayed near –1 even after the dive at
t=0). Eventually, about 200 ms after the dive, the bat terminated its
pursuit, possibly because the mantis landed on the floor and had disappeared
from sonar, or to avoid hitting the floor at a dangerous speed. Though we did
not record any captures of hearing mantises resulting from follows, such
trials illustrate that the bat can maneuver to counter a mantis dive and the
maneuver maintains the advantageous time-optimal CATD strategy that the bat
adopts when pursuing targets in level flight.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The bat does not adjust its flight path in anticipation of the mantis dive
Echolocating bats have been shown to learn specific motion properties of
targets and adapt their flight patterns accordingly
(Masters, 1988). If the mantis
dive occurred in a stereotyped manner, it is possible that the bat could learn
to anticipate the dive path. For example, a bat could learn to approach from
slightly below the mantis and get a head start on the mantis during a dive.
The data we collected show no evidence of bats adopting such an anticipatory
strategy. We observed great variability in bat–mantis separation
(Fig. 7A) and in bat
vocalization patterns (Fig. 8A)
that preceded a mantis dive, which is consistent with earlier studies showing
dive initiation time varies with the rate and intensity of ultrasonic pulses
delivered to the mantis (Triblehorn et
al., 2008; Triblehorn and
Yager, 2005b; Yager et al.,
1990). The high variability in mantis dive initiation point makes
it difficult for the bat to prepare itself for the mantis dive ahead of
time.
During `aborts' the mantis dive causes the bat to suddenly diverge from a CATD pursuit
Abort trials give us insight into the effects the mantis dive has in the
absence of any counter-measures by the bat. As expected, after a dive the
vertical distance between the bat and the mantis suddenly increased
(Fig. 4F,G). Interestingly, the
value of , carefully brought near –1 by the bat, shot up to +1
(from Fig. 9B). This indicates
that the bat initially maneuvered itself into a time-efficient CATD pursuit
( close to –1), but the mantis dive (resulting in a value
close to +1) completely turned the tables on the bat, and resulted in a
`perfect get-away' for the mantis, mirroring the bat's own time-optimal
approach to an erratically moving insect
(Ghose et al., 2006).
The bat needs to sense the bearing and possibly the range to its target to
maintain a CATD flight path during its approach. The bat is most certainly
using its echolocation to determine the position of the mantis during the
chase and make adjustments to its flight path with that information. Such
continual adjustments based on sensory feedback enable the bat to maintain its
CATD strategy ( close to –1) in the face of erratically flying
prey.
The mantis, however, is unlikely to be able to locate the bat using either
vision or audition. Spectral sensitivity measures of another mantis species
(Tenodera sinsesis) suggest that the prey in this study would not be
able to rely on vision under the long wavelength lighting conditions in our
flight room to track the bat position
(Sontag, 1971), and its
cyclopean ear is non-directional (Yager,
1999) (Fig. 7C).
Despite not having access to the bat's position, the mantis still generates an
effective maneuver to escape in a time-optimal fashion. The effectiveness of
the response probably relies on the fact that, prior to the dive, both the bat
and the mantis were maneuvering mainly in the horizontal plane. During this
phase the velocity vectors of the bat and mantis were directed largely
parallel to the horizontal. At the start of the dive (a sudden out of plane
maneuver) the velocity vector of the mantis is directed downwards, while the
bat's velocity vector is still horizontal. This sudden large angle between the
two vectors results in a large value of , indicating that, for a given
mantis speed, this vertical maneuver results in the fastest increase in
distance between bat and mantis, at least, until the bat reacts to add a
vertical component to its motion.
Separation between bat and mantis at dive
In these experiments the bats only followed the mantis when it initiated a
dive within a range of 0.6 m. Interestingly, mantis dives occurred at a mean
range of 0.9 m (with a skew towards shorter ranges). It is possible that, for
dives initiated at further or closer ranges, the mantis runs a higher risk of
being captured. If the mantis dives when the bat is further away and does not
dive all the way to the ground, the bat could have time to adjust its approach
to a lower altitude and attack the mantis after the dive. If, however, the
mantis dives when the bat is close, it would risk being captured by the bat
more often, either because the bat catches it before dive initiation, or
because it has not built up sufficient dive speed.
We note that the encounters we studied took place in a confined space where the bat probably has made various adjustments such as slowing flight speed and lowering vocalization intensity. Such adjustments may affect mantis dive initiation, though in different ways. Lower intensity vocalizations might move the dive initiation point closer to the bat, while a slower flight speed means the bat will take longer to close the distance to a mantis about to dive.
Vocalization behavior of the bat and its pursuit behavior
The PRR profiles for `captures' and `aborts'
(Fig. 8) look qualitatively
similar to typical insect capture profiles recorded from bats pursuing insects
under field and laboratory conditions
(Surlykke and Moss, 2000). The
high PRR phase in `aborts' has a shorter duration and sharper transition time
than the other two categories. From the viewpoint of the bat, the mantis dived
earlier in the chase during `abort' trials compared with `capture' trials
based on the observation that the bat spent less time in the high PRR phase
during `abort' trials. Sonar strobe groups were observed in all classes of
bat–mantis interactions. The functional role of such strobe groups for
the bat is unknown but may facilitate target localization and tracking
(Moss et al., 2006). The bat's
production of such vocalization patterns may, however, benefit the mantis in
bat evasion (Triblehorn et al.,
2008; Triblehorn and Yager,
2005b).
The persistent bat
In 75% (6/8) of the dives that occurred when the bat was pursuing the
mantis, the bat maintained a high PRR after the mantis dived, indicating it
followed the mantis into the dive. All follows occurred when the mantis was
within 0.6 m of the bat at dive initiation and the bat was already attacking
it. The bats were never observed to commence an attack on an already diving
mantis.
In three of the pursuits where the bat followed the mantis into the dive
(3/6, 50%) the bat did not succeed in converging to the time-optimal CATD
strategy during the attempted capture ( hovered around 0;
Fig. 9C, gray line). In such
cases, although the mantis dive did not lead to a sudden spike in to
+1 (as happened in aborts) the bat did not manage to maneuver to reduce
to –1 during the dive. In such trials, the bat responded to the
mantis dive (e.g. Fig. 10),
but did not achieve CATD pursuit. One possibility is that such incomplete
follows were due to the mantis executing a dive before the bat had a chance to
converge on a CATD pursuit (mantis dived early into pursuit). All trials
tended to start out with a high value of
(Fig. 9) and the bat had to
maneuver to reduce to –1. If the mantis executed a dive when the
bat was still early in the pursuit the bat did not have enough time to
converge on a CATD strategy ( remained high).
In the other three trials (3/6, 50% of follows;
Fig. 9C, black line) the bat
pursued the mantis with a CATD strategy both before and after the dive. In
such trials the bat maneuvered into a favorable situation before the dive.
This is indicated by the similarity between the curves in
Fig. 9A,C (and B) up to
t=0, where was close to –1. At the point of the dive
(t=0) rather than shooting up (as did for aborts;
Fig. 9B) remained close
to –1, indicating that the bat had adjusted its flight well to
compensate for the sudden vertical maneuver by the mantis. An example of this
is seen in Fig. 5. This example
illustrates how the bat maneuvered into position, adopted a CATD strategy
(observable from the parallel nature of the bearing lines) and maintained it
even after the mantis dived (t=0, black arrow). Presumably, the bat
pulled out of the dive at the end in order to avoid hitting the floor and
injuring itself, or because the mantis had become acoustically `invisible' at
the moment it landed on the floor. We are unable to say definitively how
beneficial the bat's ability to follow the mantis dive is, since all our
encounters were staged in a flight room only 2.5 m high, and the bats aborted
their chases as the mantis got close to or hit the floor. In the field,
however, bats and mantises can fly anywhere from ground level to treetop
height (Yager et al., 1990)
and depending on the height of the initial encounter, the bat may have enough
time and space to overtake a diving mantis and capture it.
These experiments suggest that mantis dives are not always sufficient to deter the bat in its pursuit. Previous work with deafened mantises has shown that bats adopt a time-optimal strategy to capture non-diving but otherwise erratically moving prey. The experiments reported here show that in several encounters the bat maneuvered and maintained such a time-optimal pursuit strategy even when chasing the mantis into a dive. This time-optimal strategy is likely to increase the bat's chances of catching up with and capturing diving prey in the field, perhaps providing the bat with an effective counter-measure to the insect's ultrasound-triggered dive.
|
Footnotes |
|---|
), which laid the foundation for flight trajectory
analyses in this paper. We also thank the three anonymous reviewers for their
comments and suggestions. In addition, we wish to express our appreciation to
Melinda Byrns and Amaya Perez, who assisted with the flight experiments, Ann
Planeta, who helped with video data analysis, and Sachin Vaidya for his help
raising the mantises. This work was supported by a UMD-CP
Psychology Dept. Jack Bartlett fellowship (K.G.),
NIMH (National Research
Service Award) Grant F31 MH12025 (J.D.T.),
NSF grant IBN-9808859
(D.D.Y.), NSF grant
IBN-0111973 (C.F.M.), and
NIH grant R01
MH56366 (C.F.M.). Deposited in PMC for release after 12
months.
Present address: Department of Biological Sciences, University of
Missouri-Columbia, Columbia, MO 65211, USA 
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Ehrmann, R. and Roy, R. (2002). Systematische aufstellung der gattungen. In Mantodea: Gottesanbiterinnen der Welt (ed. R. Ehrmann), pp. 374-378. Munich: Natur und Teil-Verlag.
Fajen, B. R. and Warren, W. H. (2004). Visual guidance of intercepting a moving target on foot. Perception 33,689 -715.[CrossRef][Medline]
Fenton, M. B. and Fullard, J. H. (1979). Influence of moth hearing on bat echolocation strategies. J. Comp. Physiol. 132,77 -86.[CrossRef]
Fullard, J. H. and Napoleone, N. (2001). Diel flight periodicity and the evolution of auditory defences in the Macrolepidoptera Anim. Behav. 62,349 -368.[CrossRef]
Ghose, K. and Moss, C. F. (2003). The sonar beam pattern of a flying bat as it tracks tethered insects. J. Acoust. Soc. Am. 114,1120 -1131.[CrossRef][Medline]
Ghose, K. and Moss, C. F. (2006). Steering by
hearing: a bat's acoustic gaze is linked to its flight motor output by a
delayed, adaptive linear law. J. Neurosci.
26,1704
-1710.
Ghose, K., Horiuchi, T. K., Krishnaprasad, P. S. and Moss, C. F. (2006). Echolocating bats use a nearly time-optimal strategy to intercept prey. PLoS Biol. 4, 865-873.
Griffin, D. R. (1953). Bat sounds under natural conditions, with evidence for echolocation of insect prey. J. Exp. Zool. 123,435 -466.[CrossRef]
Griffin, D. R. (1958). Listening in the Dark: The Acoustic Orientation of Bats and Men. New Haven, CT: Yale University Press.
Griffin, D. R., Webster, F. A. and Michael, C. R. (1960). The echolocation of flying insects by bats. Anim. Behav. 8,141 -154.[CrossRef]
Hope, G. M. and Bhatnagar, K. P. (1979). Electrical response of bat retina to spectral stimulation: comparison of four microchiropteran species. Experientia 35,1189 -1191.[CrossRef][Medline]
Justh, E. W. and Krishnaprasad, P. S. (2006).
Steering laws for motion camouflage. Proc. R. Soc. A
462,3629
-3643.
Lewis, F. P., Fullard, J. H. and Morrill, S. B. (1993). Auditory influences on the flight behavior of moths in a nearctic site. 2. Flight times, heights, and erraticism. Can. J. Zool. 71,1562 -1568.[CrossRef]
Masters, W. M. (1988). Prey interception: predictive and nonpredictive strategies. In Animal Sonar: Processes and Performance (ed. P. E. Nachtigall and P. W. Moore), pp.467 -470. New York: Plenum Press.
Miller, L. A. (1991). Arctiid moth clicks can degrade the accuracy of range difference discrimination in echolocating big brown bats, Eptesicus fuscus. J. Comp. Physiol. A. 168,571 -579.[CrossRef][Medline]
Miller, L. A. and Surlykke, A. (2001). How some insects detect and avoid being eaten by bats: tactics and countertactics of prey and predator. Bioscience 51,570 -581.[CrossRef]
Møhl, B. and Miller, L. A. (1975). Ultrasonic clicks produced by the peacock butterfly: a possible bat-repellent mechanism. J. Exp. Biol. 64,639 -644.
Moss, C. F. and Surlykke, A. (2001). Auditory scene analysis by echolocation in bats. J. Acoust. Soc. Am. 110,2207 -2226.[CrossRef][Medline]
Moss, C. F., Bohn, K., Gilkenson, H. and Surlykke, A. (2006). Active listening for spatial orientation in a complex auditory scene. PLoS Biol. 4, e79.[CrossRef][Medline]
Neuweiler, G. (1989). Foraging ecology and audition in echolocating bats. Trends Ecol. Evol. 4, 160-166.[CrossRef]
Roeder, K. D. and Treat, A. E. (1961). Detection and evasion of bats by moths. Am. Sci. 49,135 -148.
Rushton, S. K., Harris, J. M., Lloyd, M. R. and Wann, J. P. (1998). Guidance of locomotion on foot uses perceived target location rather than optic flow. Curr. Biol. 8,1191 -1194.[CrossRef][Medline]
Russo, D., Jones, G. and Arlettaz, R. (2007).
Echolocation and passive listening by foraging mouse-eared bats Myotis
myotis and M. blythii. J. Exp. Biol.
210,166
-176.
Schmidt, S., Silja, H. and Jurgen, P. (2000). The role of echolocation in the hunting of terrestrial prey-new evidence for an underestimated strategy in the gleaning bat, Megaderma lyra. J. Comp. Physiol. A 186,975 -988.[CrossRef][Medline]
Sontag, C. (1971). Spectral sensitivity studies
on visual system of praying mantis, Tenodera sinensis. J. Gen.
Physiol. 57,93
-112.
Surlykke, A. and Moss, C. F. (2000). Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. J. Acoust. Soc. Am. 108,2419 -2429.[CrossRef][Medline]
Thompson, S. P. (1919). Calculus Made Easy. London: Macmillan.
Triblehorn, J. D. and Yager, D. D. (2005a). Acoustic interactions between insects and bats: a model for the interplay of neural and ecological specializations. In Ecology of Predator-Prey Interactions, pp. 77-104. New York: Oxford University Press.
Triblehorn, J. D. and Yager, D. D. (2005b).
Timing of praying mantis evasive responses during simulated bat attack.
J. Exp. Biol. 208,1867
-1876.
Triblehorn, J. D., Ghose, K., Bohn, K., Moss, C. F. and Yager,
D. D. (2008). Free-flight encounters between praying mantids
(
CO2) and bats
(Eptesicus fuscus). J. Exp. Biol.
211,555
-562.
Yager, D. D. (1999). Structure, development, and evolution of insect auditory systems. Microsc. Res. Tech. 47,380 -400.[CrossRef][Medline]
Yager, D. D., May, M. L. and Fenton, M. B.
(1990). Ultrasound-triggered, flight-gated evasive maneuvers in
the praying mantis Parasphendale agrionina. 1. Free flight.
J. Exp. Biol. 152,17
-39.
Yuan, L. (1948). Homing and navigational courses of automatic target-seeking devices. J. Appl. Phys. 19,1122 -1128.[CrossRef]
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–1 until capture.
Limitations of the video data digitization introduce an artifact in the
