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First published online February 1, 2008
Journal of Experimental Biology 211, 555-562 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.005736
Free-flight encounters between praying mantids (Parasphendale agrionina) and bats (Eptesicus fuscus)
1 Department of Psychology, University of Maryland, College Park, MD 20742,
USA
2 Neuroscience and Cognitive Science Program, University of Maryland, College
Park, MD 20742, USA
3 Institute for Systems Research, University of Maryland, College Park, MD
20742, USA
* Author for correspondence at present address: Department of Biological Sciences, University of Missouri-Columbia, Columbia, MO 65211, USA (e-mail: triblehornj{at}missouri.edu)
Accepted 29 November 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: escape, hearing, insect, echolocation, predator–prey
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Schnitzler and Kalko,
2001). However, not all insects are defenseless against attacking
bats as some insects possess ultrasound-sensitive auditory systems and perform
ultrasound-triggered behaviors while flying
(Hoy and Robert, 1996;
Miller and Surlykke, 2001). To
date, ultrasound-sensitive auditory systems and in-flight evasive behaviors
triggered by ultrasonic stimuli have been identified and characterized in
several insects that fly at night. These insects include species within the
Lepidoptera, including several moth species as well as some butterflies
(Rydell et al., 1997;
Yack and Fullard, 2000;
Göpfert et al., 2002;
Rydell et al., 2003), the
Orthoptera [locusts (Robert,
1989), crickets (Moiseff et
al., 1978), katydids (Libersat
and Hoy, 1991; Schulze and
Schul, 2001)], the Dictyoptera [praying mantids
(Yager and Hoy, 1989;
Yager and May, 1990;
Yager et al., 1990)], the
Coleoptera [tiger beetles (Yager and
Spangler, 1997), scarab beetles
(Forrest et al., 1995)] and
the Neuroptera [green lacewings (Miller,
1971; Miller and Olesen,
1979)]. Since bat predation has been suggested to be one of the
major selective forces driving auditory evolution in insects, along with
intraspecific communication and parasitism
(Hoy and Robert, 1996;
Conner, 1999), the coincidence
of an ultrasound-sensitive auditory system and ultrasound-triggered in-flight
evasive behaviors in any given nocturnal flying insect indicates that the
system evolved as a defense against bat predation.
Although the conclusion that insects have evolved ultrasound hearing to
avoid bat predation is widely accepted, determining the actual advantage
conveyed by this auditory function is very difficult and has been attempted in
only a few cases. These include noctuid moths
(Roeder and Treat, 1962),
arctiid moths (Acharya and Fenton,
1992; Dunning et al.,
1992) and green lacewings
(Miller and Olesen, 1979).
These studies found that ultrasound-sensitivity and corresponding evasive
maneuvers provided a 40–60% advantage over deafened individuals that did
not perform evasive maneuvers.
This leads to an interesting question: what factors contribute to the
success or failure of evasive responses? Insects may be able to assess the
degree of danger based on the stereotyped pattern of echolocation calls during
attacks. As aerial foraging bats detect, approach and attempt to capture
insect prey, they increase the rate of their emissions from a low rate
[10–15 pulses s–1 (p.p.s.)] to very high rates (>100
p.p.s.). Triblehorn and Yager (Triblehorn
and Yager, 2005) hypothesized that gradual transitions from low to
high rates provide more time for the mantis to respond to the bat and escape,
while rapid transitions may allow a bat to get closer to the mantis before it
can respond, providing less time for the mantis to perform an effective escape
behavior.
Based on these previous findings, insects could benefit from having a
`backup' system mediated by another sensory modality to trigger `last chance'
escape responses. Wind generated by attacking bats has been proposed as a
possible stimulus for mediating such `last chance' responses (Baronestsky and
Møhl, 1987; Ganihar et al.,
1994). Many insects possess a wind-sensitive cercal system capable
of detecting the air currents generated by an approaching bat. However, there
is some question whether an insect would have enough time after initially
detecting the wind generated by an approaching bat to perform an effective
evasive response [around 75 ms for mantids
(Triblehorn and Yager,
2006)].
The praying mantis Parasphendale agrionina possesses both an
ultrasound-sensitive auditory system
(Yager and Hoy, 1987;
Yager and Hoy, 1989;
Yager, 1999) and a
wind-sensitive cercal system (Triblehorn
and Yager, 1999; Triblehorn,
2003). P. agrionina's auditory system, located ventrally
between the metathoracic legs, consists of two tympana within the midline
chamber that function as a single ear. The ear is broadly tuned to ultrasonic
frequencies, with greatest sensitivity (59–61 dB SPL) between
25–50 kHz. In P. agrionina, ultrasound triggers a
multicomponent response (Yager and May,
1990) that produces a rapid power dive in free flight [172 ms
latency for first change in flight path and 242 ms latency for first
indication of power dive (Yager et al.,
1990)]. Although the power dive can have a directional component,
directionality is independent of an attacking bat's approach, since all
behavioral and physiological tests indicate that the mantis ear is
nondirectional (Yager and Hoy,
1989; Yager et al.,
1990). The cercal system consists of the cerci (two posterior
appendages) that contain approximately 100 wind-sensitive hairs each
(Triblehorn, 1997). The
afferents project to at least six ascending wind-sensitive interneurons
(Triblehorn and Yager, 1999;
Triblehorn, 2003). Stimulation
of the cercal system does not evoke terrestrial escape responses, but could be
involved in aerial evasive responses
(Triblehorn and Yager, 1999;
Triblehorn, 2003).
The current study stages free-flight encounters between P. agrionina and big brown bats Eptesicus fuscus. Here we test the efficiency of ultrasound-mediated evasive power dive responses of P. agrionina initiated as the bat pursues the mantis and examine whether the transition rate of the bat's echolocation emission pattern during an attack influences the mantid's probability of surviving We also test the effectiveness of potential wind-mediated escape responses as a secondary/backup `last ditch' response.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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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 their final molt to adult. Big brown bats Eptesicus fuscus
L. were collected locally in the surrounding Maryland suburbs. Bats were
housed individually in cages and fed daily on a diet of mantids (P.
agrionina, Creobroter pictipennis or Miomantis abyssinica),
crickets (Acheta domestica) and mealworms (Tenebrio
monitor). Bats flew 5 days a week for 30–60 min and were fed in the
flight room on those days. Otherwise, they were fed in their cages. Bats were
weighed and examined on days that they flew. Experiments were conducted between May and October across several years (1999, 2000 and 2002) using new, freshly captured bats from the field each year. After each season, the bats were retired from the experiment. They remained in the laboratory with other bats in a cage large enough for flight and provided with food ad libitum. Bats were examined once a week for continued good health.
Training
At least two bats newly brought in from the field were trained and accepted
for experiments each summer using the following procedure prior to data
collection. First, new bats were acclimated to the flight room by allowing
them to fly for at least 30 min. It typically took 2 or 3 days for the bat to
fly smoothly within the flight room. Bats that did not fly continuously for
several minutes after 2 or 3 days were excluded from the experiment. After
acclimation, we released individual deafened mantids (P. agrionina,
Miomantis natalica or Creobroter pictipennis) not only to
determine whether the bat would pursue free-flying mantids within the flight
room, but also to examine the bats' proficiency for capturing, handling and
consuming the mantids. Bats that did not pursue or efficiently capture and
consume mantids during the screening process were excluded after a week. Since
the bats screened had been freshly caught in the field and should already be
proficient aerial foragers, we avoided specifically training the bats to
capture free-flying insects. The screening process ensured that these
abilities remained intact, without impairment, within the flight room.
However, bats were trained to capture hanging mealworm targets. This was
useful for keeping bats motivated during the experimental trials as well as
for feeding the bats on non-data collection days when the bats flew in the
flight room. The bats that captured free-flying mantids in the flight room
required very little training to capture readily hanging targets.
Eleven bats participated in the experiment. Three of the bats accounted for 70.5% of the data trials, another four for 24.9% of the trials, and the remaining four for 4.6% of the trials.
Free-flight room
All experiments were conducted in a carpeted, acoustically lined (Sonex I,
Illbruck, Minneapolis, MN, USA) flight room (6.4x7.3x2.5 m,
Fig. 1) at the University of
Maryland, College Park. We kept the visible light at the lowest levels
possible that still allowed the observers to view the encounters. Lighting
conditions were the same for all trials. Although the flight room is smaller
than some natural foraging sites used by E. fuscus, the room is large
enough for the bats to maneuver vertically and horizontally and allowed
2–3 m distance between the bat and the mantis before the bat attacked
its prey. Although the room has more clutter than an open space around a pond,
E. fuscus does forage near vegetation
(Simmons et al., 2001).
Previous studies of tethered insect capture within this same flight room have
shown that the echolocating bat's pursuit behavior in the laboratory closely
resembles that observed in the field
(Surlykke and Moss, 2000).
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Experimental groups
Mantids were divided into four different experimental groups: (1) hearing
and cercal hairs functional (control group); (2) hearing, but cercal hairs
deactivated; (3) deafened, but cercal hairs functional; (4) deafened and
cercal hairs deactivated.
Mantids were deafened by filling the ear with vaseline, essentially deactivating the ear without adding any significant mass. This method was preferable to other deafening procedures (i.e. puncturing the tympana) since it prevented possible collateral damage. We estimated the volume of the auditory chamber in five mantids by measuring the dimensions of a cast of the chamber made with Mercox (Ladd Industries, Kettering, OH, USA), an ultra-low viscosity casting medium. This was 2.2x10–4 ml. Considering the density of vaseline (0.935 g ml–1), the mass of the vaseline was 2.1x10–4 g at most (very unlikely that the chamber was completely filled). The mass of a male P. agrionina is 0.281±0.008 g (N=10). Therefore, the mass of the vaseline was about 0.1% of the mantis mass. The mantis ear is located at the mantid's center of mass, so any added weight would have no effect on maneuverability.
Mantis ears were filled 1 day prior to testing to avoid stressing the animal immediately before the experiment. Physiological recordings from two mantids before and after filling the ear demonstrated that the vaseline conveyed a hearing loss of at least 40 dB for frequencies between 20 and 60 kHz (no response to 70 ms tones <100 dB SPL). In two other mantids, the ear was filled with vaseline and tested the following day (following the procedure used in preparing mantids for the free-flight experiments). Physiological recordings confirmed that the vaseline plug eliminated responses to frequencies between 20 and 60 kHz (no responses to 70 ms tones <100 dB SPL). Vaseline plugs were inspected in deafened mantids that escaped and the trial was excluded if a hole existed.
Burning the filiform hairs using a fine soldering iron deactivated the cercal wind response. The procedure left the cerci otherwise intact (compared to cercal ablation) without significantly altering the load on the cerci (compared to covering the cerci with vaseline).
Experimental procedure
Each trial consisted of a single free-flight encounter between one bat and
one mantis. Since only one bat was in the flight room at any time, other bats
could not eavesdrop on the echolocation calls emitted by the bat pursuing the
mantids. Three observers, blind to the condition of the mantis, scored each
encounter. A code on the housing cup designated its condition and these codes
were not checked until all trials were collected for the day. The releaser
stood on a stepladder while the other two observers sat on the floor against
the wall in two different configurations, depending on the release point (see
Fig. 1). One observer monitored
bat echolocation vocalizations using a bat detector and headphones. Increases
in the bat's pulse repetition rate (PRR) confirmed that the bat detected and
pursued the mantis using echolocation under the low light level
conditions.
The bat circled the room continuously before mantis release. Release occurred when the bat was at a point in its flight path that would likely give the mantids enough time to fly away from the release location yet give the bat enough time to detect, track and possibly capture the mantis. Using a conservative approach, the experimenters accepted an encounter as a data trial only if the following conditions were met:
The experimenters observed and scored each trial as a successful escape (bat did not capture the mantis), a capture (bat captured the mantis) or a dropped mantis (bat made contact with the mantis, but the mantis immediately dropped to the ground). Mantids dropped in this manner that survived for 24 h counted as successful escapes while those that died during this period counted as unsuccessful escapes (i.e. captures from the mantis point of view). Experimenters also noted the behavior of the mantis (evasion vs no evasion).
After an encounter, the bat was caught to prevent it from tiring or becoming unmotivated while recording the results, downloading video data to tape, and setting up for the next trial. Repeatedly landing on the walls and showing a reluctance to fly was characteristic of a fatigued or unmotivated bat. Bats exhibiting such behavior were first given a tethered mealworm to renew their motivation. If this failed to encourage the bat, we switched to another trained bat. To avoid satiation effects, we limited bats to four captures a day. Bats continued to pursue flying mantids under this procedure and four mantids was sufficient to sustain the bat's body weight.
Transition periods
As described previously (Triblehorn and
Yager, 2005), the transition period was defined as the period of
increasing PRRs from 20 to 100 p.p.s. and the slope of the transition period
(p.p.s. 10 ms–1) provides a measure of how quickly the bat
switches from low to high PRRs during an attack
(Triblehorn and Yager, 2005).
Increasing transition slopes indicate more rapid transitions. In the
free-flight encounters, bats circling the room in the absence of a mantis
echolocated with PRRs under 20 p.p.s. During capture attempts, PRRs increased
over 20 p.p.s. and exceeded 100 p.p.s. PRRs under 20 p.p.s. or over 100 p.p.s.
do not elicit evasive responses in tethered flying P. agrionina
(Triblehorn and Yager, 2005).
In some trials, bats increased their PRRs to over 20 p.p.s. during pursuit but
broke off their attack before reaching 100 p.p.s. (due to the mantis diving
response). In those cases, the transition slopes were calculated using the
maximum PRR the bat reached during the pursuit.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
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Effectiveness of mantis ultrasound-triggered evasive responses
The results for all 173 free-flight encounters are shown in
Fig. 3 (137 individual mantids:
119 single-trial individuals, 28 multi-trial individuals, each trial occurring
on a different day). Hearing mantids successfully escaped bats in 76% of the
trials (55 out of 72 trials) whereas deafened mantids only escaped in 34% of
the trials (34 out of 101 trials; Fig.
3A, combining active and deactivated cercal groups for hearing and
deaf conditions). These results were statistically significant (two-tailed
Fisher's Exact Test, P<0.0001). For hearing mantids, 91% of the
escape trials (50 out of 55) involved the mantis performing a power dive. In
the other 9% of the trials, the bat made contact with the mantis, but
immediately mishandled the insect and dropped it. Deafened mantids never
performed power dives in response to bat attacks. For trials resulting in a
deafened mantis escape, 41% of the trials (14 out of 34 escapes) involved the
bat contacting the mantis and the mantis immediately tumbling to the
ground.
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). To determine whether attack sequences with faster
transitions allowed bats to get closer to hearing mantids that successfully
escaped, we performed a second analysis.
Fig. 5 compares the slope of
the transition period and the closest distance between the bat and the mantis
during the transition period for 15 trials involving hearing mantids that
escaped. No relationship was found between the closest distance and transition
slope (Pearson's correlation coefficient: r=0.059; t-test:
t(13)=0.213; P=0.8346).
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).
Removing the cercal hairs can affect flight performance, primarily in the yaw
direction (Altman, 1983).
Results from the free-flight studies indicate that cercal hair removal does
not, however, affect the performance or effectiveness of the mantis power
dive. Mantids without their cercal hairs were just as successful at escaping
from bats (79% success, 27 out of 34) as mantids with cercal hairs (74%
success, 28 out of 38; two-tailed Fisher's Exact Test, P=0.5926;
Fig. 3A). For hearing mantids
with functioning cerci, 93% of the escapes were due to power dives (26 out of
28) while 89% of escapes were due to power dives in hearing mantids with
deactivated cerci (24 out of 27; see Fig.
3B).
Effects of cercal hair deactivation on wind-mediated evasive responses
For deafened mantids, those with functioning cerci escaped in only 35% of
the trials (18 out of 52) while those with deactivated cerci escaped in 33% of
the trials (16 out of 49; see Fig.
3A). This difference was not statistically significant (two-tailed
Fisher's Exact Test, P=1). Deafened mantids never exhibited power
dives. Bats mishandling and dropping the mantids accounted for 56% of the
survivals in the deafened mantids with functioning cerci group (10 out of 18)
and for 25% survivals in the deafened mantids group with deactivated cerci (4
out of 16; see Fig. 3B).
However, this difference in survivals due to drops between the two deafened
groups was not statistically significant (two-tailed Fisher's Exact Test,
P=0.0921). The failure to find a statistically significant difference
in the escape percentages between the two hearing groups as well as the two
deafened groups justifies combining the four groups into two in the previous
section. In these cases, one dropped mantis appeared `frozen' or in a
thanatotic state, but the rest appeared unharmed. All dropped mantids
(including the `frozen' mantis) survived for at least 24 h.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)
demonstrated that mantids performing dives eluded capture (100% success, five
total encounters), while those that did not dive escaped in only 17% of the
trials (1 out of 6 trials). These results indicate the power dive response
conveyed an 83% advantage. Utilizing a larger data set, the current results
confirmed that mantids entering power dives always escaped from the bats (100%
effective).
In the other study, Cumming (Cumming,
1996) found that Miomantis natalica also performed
evasive maneuvers when attacked by the bat Rhinolophus clivosus.
Instead of measuring escape rate, Cumming counted how many attempts the bats
made before capturing the mantis. Bats had a more difficult time capturing
M. natalica that could hear compared to those that were deafened
(three times as many passes for hearing vs deafened mantids) and
determined that hearing conveyed a 32% advantage to mantids.
The current study (using different methods, bat species and mantis species)
gave similar results, as hearing conveyed a 42% advantage to mantids (hearing
mantids survived 76% of all encounters vs 34% for deafened mantids).
The effectiveness of the mantis power dive response is similar to that found
in moths [40% advantage (Roeder and Treat,
1962), 48% (Acharya and Fenton,
1992), 50% (Dunning et al.,
1992); latter two studies were conducted under bright light
conditions] but less than green lacewings [60% advantage
(Miller and Olesen,
1979)].
The 42% advantage accounts for the effectiveness of ultrasound-sensitivity
and the power dive response, the primary foci of this study. However, mantids
also exhibit an `early' evasive turning behavior when detecting a bat that is
far away (Yager et al., 1990),
which can prevent a bat from detecting and pursuing the mantis. Therefore,
this 42% advantage is likely a minimum estimation of the actual advantage
conveyed by hearing in the field.
Although the experimental conditions included low-level visible light, the light conditions were the same for both hearing and deafened mantids, as well as the bats hunting them. Therefore, any additional advantage using vision by the bats or mantids would be equivalent across all experimental conditions designed to test the effectiveness of either the ultrasound- or the wind-mediated responses discussed below.
Effect of transition rate on mantis escape responses
The transition rate hypothesis proposed
(Triblehorn and Yager, 2005)
suggests one potential explanation why insect ultrasound-mediated evasive
behaviors are not 100% effective. Using pulse trains simulating the PRRs and
pulse durations of several actual bat attack sequences, they found sequences
with rapid transitions elicited escape responses closer to the time of
`contact' compared to sequences containing gradual sequences. Therefore, a bat
could potentially circumvent the mantis (or other insect) auditory defense by
rapidly increasing from low to high PRRs during an attack echolocation
sequence. The results of Triblehorn and Yager
(Triblehorn and Yager, 2005)
indicated that attack sequences containing gradual transitions would provide
mantids with more time to escape while sequences with rapid transitions would
provide less time. However, they did not directly test whether the bat's sonar
signal transition rate actually reduced the mantid's chance of escaping or
what transition rates decrease the number of successful escapes.
The results from this study showed that mantids escaped from bats 80% of
the time when transition rates were less than 16 p.p.s. 10
ms–1 (84% for 0–4 p.p.s. 10 ms–1; 64%
for 4–8 p.p.s. 10 ms–1; 90% for 8–12 p.p.s. 10
ms–1; 100% for 12–16 p.p.s. 10 ms–1),
but fell to 37.5% for transition rates over 16 p.p.s. 10 ms–1
(Fig. 4). The simulated
sequences in the previous study
(Triblehorn and Yager, 2005)
contained transitions between 1–14 p.p.s. 10 ms–1, all
of which fall within the range where mantids escaped 80% of the time. These
results support both hypotheses that mantids can successfully escape from bats
producing echolocation sequences containing gradual transitions and that bats
can improve their chances of capturing mantids (and possibly other insects
with ultrasound-sensitive auditory systems) by employing faster transitions in
their attack sequences. Based on these results, the advantage switches to the
bats when their attack sequences contain transitions over 16 p.p.s. 10
ms–1. In our study, however, bats produced attack sequences
containing rapid transitions in only 15% of the trials. In fact, bat attack
sequences contained gradual transitions with slopes <4 p.p.s. 10
ms–1 in one-third of the encounters.
Attack sequences containing gradual transitions typically did not include a
continuous increase in PRR, but rather incorporated clusters of sonar sound
groups with stable PRRs. Bats would emit two or three vocalizations at a
stable PRR (known as a sonar strobe group)
(Moss and Surlykke, 2001),
followed by a gap (indicated by the alternating high and low PRRs in
Fig. 2, escape example).
Although the function of sonar strobe groups is still unclear, they may
facilitate analysis of sonar scenes by the bat during complicated acoustic
tasks such as capture attempts (Moss and
Surlykke, 2001; Moss et al.,
2006). However, the fact that bats produce these strobe groups,
and not how bats utilize them, is what is relevant from the mantis point of
the view for three reasons. First, echolocation attack sequences containing
strobe groups had longer transition periods, which provide the mantis with
more time to escape. Second, these echolocation sequences provide more
information (via the auditory system) that the mantid's nervous
system can use to determine the appropriate time to initiate a power dive
response. Third, the production of strobe groups could strongly activate the
mantis auditory system through temporal integration at the level of auditory
interneurons and/or higher centers.
The results from this study did not support the hypothesis that using
faster transition rates would allow bats to get closer to the mantids
(Fig. 5). This indicates that
other factors in the bat's echolocation behavior, such as sound frequency or
intensity, likely contribute to how close the bat can get before the mantis
dives. The simulated sequences in Triblehorn and Yager
(Triblehorn and Yager, 2005)
did not vary in frequency or intensity, as occurs in actual bat attack
sequences (Griffin, 1958;
Simmons et al., 1979;
Kick, 1982;
Surlykke and Moss, 2000;
Boonman and Jones, 2002). Of
these two parameters, intensity is likely to have a greater influence over
triggering the mantis power dive response. The mantis auditory system is
broadly tuned and lacks frequency discrimination
(Yager and Hoy, 1989;
Triblehorn and Yager, 2001).
On the other hand, emission intensity, the distance between the bat and
mantis, and the bat's head position relative to the mantis
(Ghose and Moss, 2003) all
affect the intensity of the sound reaching the mantid's ear. We could not
determine the intensity of the echolocation the mantis received during attack
sequences or across attack sequences and cannot account for this effect.
However, it is an area that warrants future investigation.
Since pulse trains with single PRRs can trigger mantis power dive responses
(Yager and May, 1990;
Yager et al., 1990), it is
clear that mantids do not require a rate of change in the echolocation pulses
to perform a response. However, it is equally clear that the transition period
in bat echolocation sequences contains rapid changes in the intervals between
successive vocalizations. Other phases of the echolocation sequence do contain
relatively consistent PRRs, such as the low PRRs (<15 p.p.s.) emitted prior
to the transitions period and the high PRRs (>100 p.p.s.) after the
transition period. However PRRs <15 p.p.s. and >100 p.p.s. do not evoke
mantis power dive responses while the changing PRRs during the transition
period do (Triblehorn and Yager,
2005). Therefore, changing PRRs are the reality that the mantis
nervous system (via auditory input) must respond to in the natural
predator–prey situation. This not only affects when power dive responses
occur, but also could influence the magnitude (i.e. increase in flight speed,
steepness of dive) of the response. Future experiments will examine how the
mantis nervous system incorporates this variable incoming information and
produces a subsequent power dive response.
Effectiveness of the mantis wind-evoked response
Previous studies by two of the current authors
(Triblehorn and Yager, 2002;
Triblehorn and Yager, 2005)
have provided reasons why mantids could benefit from a backup escape system.
The current finding that hearing mantids sometimes failed to perform power
dives effective at evading capture supports this idea. Wind-evoked aerial
evasive responses, mediated by bat-generated wind acting on the cercal system,
could potentially serve as this backup system. For flying insects unable to
hear echolocating bats (i.e. cockroaches), these responses may serve as the
only protection against bat predation. However, the current study shows that
deafened mantids with functioning cerci were not better at evading capture
than deafened mantids with deactivated cerci. This finding indicates that
wind-evoked evasive responses in mantids do not serve as a beneficial backup
system in the event that the auditory system fails, possibly because the
wind-evoked in-flight responses observed under experimental simulation
conditions (Triblehorn, 2003)
either do not occur or are ineffective in the free-flight situation.
One interesting observation does warrant further investigation, however.
Quantitatively, bats dropped twice as many deafened mantids with functioning
cercal systems compared to deafened mantids with deactivated systems. Mantids
have, on average, 75 ms between detection of bat-generated wind and capture to
escape from a bat (Triblehorn and Yager,
2006). It is unlikely that this is enough time for the mantis to
perform a maneuver that will cause the bat to completely miss its target, but
may allow the mantis to alter its flight path sufficiently to cause the bat to
drop the mantis without damage, resulting in a successful escape. Bat wing
stretch receptors, sensitive to membrane deformations, overlap to form regions
of high sensitivity where bats prefer to capture insects on the wing
(Zook, 2005). Last-ditch
wind-mediated responses could cause the mantis to move away from these regions
of high sensitivity as the bat attempts a capture, causing the bat to contact,
but not capture, the mantis. Based on this hypothesis, deafened mantids with
functioning cercal systems should be dropped more often. This was the trend,
but it was not statistically reliable, most likely due to the small sample
size (deafened mantids only escaped capture 29 times). The larger sample size
required to properly address the issue of dropped mantids was beyond the scope
of the current study. The finding that most dropped mantids appeared unharmed
immediately after the encounter and that they all survived for at least 24 h
demonstrates that being dropped is an effective escape strategy. Even if a
larger sample size revealed that some dropped mantids do not survive 24 h 100%
of the time, it is possible that these mantids could mate prior to dying and
being dropped would still be an effective strategy.
Other insects, such as crickets and cockroaches, have more developed cercal
systems than P. agrionina. These insects possess more wind-sensitive
hairs on their cerci, the hairs are longer (and, thus, more sensitive), and
they have larger ascending wind-sensitive neurons, resulting in faster neural
conduction velocities (reviewed in Boyan
and Ball, 1990). Wind-mediated in-flight evasive responses could
be more effective in crickets and cockroaches since these factors allow these
insects to detect bats earlier (via wind cues) alone and respond
faster. The dropping phenomenon observed in this study may also occur more
often in these insects and may be a general escape strategy for flying insects
possessing cercal systems.
In summary, the results from this study demonstrate that the mantis ultrasound-triggered evasive response is very effective for eluding bat predators. However, the response was not 100% effective. Incorporating very rapid transition rates in attack sequences increased the bat's probability of capturing a mantis with functional hearing. Mantids did not gain a significant advantage from the wind-sensitive cercal system serving as a secondary `backup' evasive system, but bats dropped deafened mantids with active cercal systems twice as often as deafened mantids with deactivated cercal systems. Although this difference was not statistically significant, this latter observation was an unexpected result that this study was not specifically designed to evaluate fully, and failure to find a statistical difference was likely due to small sample sizes. As such, this interesting observation warrants further investigation to sufficiently evaluate this result, especially since dropped mantids always survived the encounter.
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Acharya, L. and Fenton, M. B. (1992). Echolocation behavior of vespertilionid bats (Lasiurus cinereus and L. borealis) attacking airborne targets including arctiid moths. Can. J. Zool. 70,1292 -1298.
Altman, J. (1983). Sensory inputs and the generation of the locust flight motor pattern: from the past to the future. In Biona Report 2 (ed. W. Nachtigal), pp.127 -136. Stuttgart: Gustave Fischer.
Baronetzky, E. and Möhl, B. (1987). Afferent input from the cerci on the locust flight motor. In New Frontiers in Brain Research: Proceedings of the 15th Göttengen Neurobiology Conference (ed. N. Elsner and O. Creutzfeldt), p.50 . Stuttgart: Georg Thieme.
Boonman, A. and Jones, G. (2002). Intensity
control during target approach in echolocating bats; stereotypical
sensori-motor behaviour in Daubenton's bats, Myotis daubentonii. J.
Exp. Biol. 205,2865
-2874.
Boyan, G. S. and Ball, E. E. (1990). Neuronal organization and information processing in the wind-sensitive cercal receptor/giant interneurone system of the locust and other orthopteroid insects. Prog. Neurobiol. 35,217 -243.[CrossRef][Medline]
Conner, W. E. (1999). `Un chant d'appel amoureax': acoustic communication in moths. J. Exp. Biol. 202,1711 -1723.[Abstract]
Cumming, G. S. (1996). Mantis movements by night and the interactions of sympatric bats and mantises. Can. J. Zool. 74,1771 -1774.[CrossRef]
Dunning, D. C., Acharya, L., Merriman, C. B. and Dal Ferro, L. (1992). Interactions between bats and arctiid moths. Can. J. Zool. 70,2218 -2223.
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.
Forrest, T. G., Read, M. P., Farris, H. E. and Hoy, R. R. (1995). A tympanal hearing organ in scarab beetles. J. Exp. Biol. 200,601 -606.
Ganihar, D., Libersat, F., Wendler, G. and Camhi, J. M. (1994). Wind-evoked evasive responses in flying cockroaches. J. Comp. Physiol. A 175,49 -65.[Medline]
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]
Göpfert, M. C., Surlykke, A. and Wasserthal, L. T. (2002). Tympanal and atympanal `mouth-ears' in hawkmoths (Sphingidae). Proc. R. Soc. Lond. B Biol. Sci. 269, 89-95.[Medline]
Griffin, D. R. (1958). Listening in the Dark. New Haven, CT: Yale University Press.
Hoy, R. R. and Robert, D. (1996). Tympanal hearing in insects. Annu. Rev. Entomol. 41,433 -450.[CrossRef][Medline]
Kick, S. A. (1982). Target detection by the echolocating bat, Eptesicus fuscus. J. Comp. Physiol. A 145,431 -443.[CrossRef]
Kick, S. A. and Simmons, J. A. (1984). Automatic gain control in the bat's sonar receiver and the neuroethology of echolocation. J. Neurosci. 4,2725 -2737.[Abstract]
Libersat, F. and Hoy, R. R. (1991). Ultrasonic startle behavior in bushcrickets (Orthoptera; Tettigonidae). J. Comp. Physiol. A 169,507 -514.[Medline]
Libersat, F., Levy, A. and Camhi, J. M. (1989). Multiple feedback loops in the flying cockroach: excitation of the dorsal and inhibition of the ventral giant interneurons. J. Comp. Physiol. A 165,651 -668.[CrossRef][Medline]
Miller, L. A. (1971). Physiological responses of green lacewings (Chrysopa, Neuroptera) to ultrasound. J. Insect Physiol. 17,491 -506.[CrossRef]
Miller, L. A. and Olesen, J. (1979). Avoidance behavior in green lacewings. I. Behavior of free flying green lacewings to hunting bats and ultrasound. J. Comp. Physiol. 131,113 -120.[CrossRef]
Miller, L. A. and Surlykke, A. (2001). How some insects detect and avoid being eaten of free flying green lacewings to hunting bats and ultrasound. Bioscience 51,570 -581.[CrossRef]
Moiseff, A., Pollock, G. S. and Hoy, R. R.
(1978). Steering responses of flying crickets to sound and
ultrasound: mate attraction and predator avoidance. Proc. Natl.
Acad. Sci. USA 75,4052
-4056.
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, 615-626.
Robert, D. (1989). The auditory behavior of
flying locusts. J. Exp. Biol.
147,279
-301.
Roeder, K. D. and Treat, A. E. (1962).The acoustic detection of bats by moths . Proceedings of the 11th Entomological Congress 3,7 -11.
Rydell, J., Skals, N., Surlykke, A. and Svensson, M. (1997). Hearing and bat defence in geometrid winter moths. Proc. Biol. Sci. 264,83 -88.[CrossRef][Medline]
Rydell, J., Kaerma, S., Hedelin, H. and Skals, N. (2003). Evasive response to ultrasound by the crepuscular butterfly Manataria maculata. Naturwissenschaften 90, 80-83.[Medline]
Schnitzler, H. U. and Kalko, E. K. V. (2001). Echolocation by insect-eating bats. BioScience 51,557 -569.[CrossRef]
Schulze, W. and Schul, J. (2001). Ultrasound avoidance behavior in the bushcricket Tettigonia viridissima (Orthoptera, Tettigoniidae). J. Exp. Biol. 204,733 -740.[Abstract]
Simmons, J. A., Fenton, M. B. and O'Farrell, M. J.
(1979). Echolocation and pursuit of prey by bats.
Science 203,16
-21.
Simmons, J. A., Eastman, K. M., Horowitz, S. S., O'Farrell, M. J. and Lee, D. (2001). Versatility of biosonar in the big brown bat, Eptesicus fuscus. Acoust. Res. Lett. Online 2, 43-48.[CrossRef]
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]
Triblehorn, J. D. (1997). Near-field sound reception in the praying mantis Sphodromantis aurea. Masters thesis, University of Maryland, College Park, USA.
Triblehorn, J. D. (2003). Multisensory integration in the ultrasound-triggered escape response of the praying mantis, Parasphendale agrionina. PhD thesis, University of Maryland, College Park, USA.
Triblehorn, J. D. and Yager, D. D. (1999).Wind-evoked neural responses in the praying mantis Parasphendale agrionina . 30th Annual Meeting of the Society for Neuroscience.
Triblehorn, J. D. and Yager, D. D. (2001). Broad versus narrow auditory tuning and corresponding bat-evasive flight behavior in praying mantids. J. Zool. Lond. 254, 27-40.[CrossRef]
Triblehorn, J. D. and Yager, D. D. (2002).
Implanted electrode recordings from a praying mantis auditory interneuron
during flying bat attacks. J. Exp. Biol.
205,307
-320.
Triblehorn, J. D. and Yager, D. D. (2005).
Timing of praying mantis evasive responses during simulated bat attack
sequences. J. Exp. Biol.
208,1867
-1876.
Triblehorn, J. D. and Yager, D. D. (2006). Wind
generated by an attacking bat: measurements and its detection by the praying
mantis cercal system. J. Exp. Biol.
209,1430
-1440.
Yack, J. E. and Fullard, J. H. (2000). Ultrasonic hearing in nocturnal butterflies. Nature 403,265 -266.[CrossRef][Medline]
Yager, D. D. (1999). Hearing. In The Praying Mantids (ed. F. R. Prete, H. Wells, P. H. Wells and L. E. Hurd), pp. 93-113. Baltimore: Johns Hopkins University Press.
Yager, D. D. and Hoy, R. R. (1987). The midline metathoracic ear of the praying mantis, Mantis religiosa. Cell Tissue Res. 250,531 -541.[CrossRef][Medline]
Yager, D. D. and Hoy, R. R. (1989). Audition in the praying mantis, Mantis religiosa L.: identification of an interneuron mediating ultrasonic hearing. J. Comp. Physiol. A 165,471 -493.[CrossRef][Medline]
Yager, D. D. and May, M. L. (1990).
Ultrasound-triggered, flight-gated evasive maneuvers in the praying mantis
Parasphendale agrionina. II. Tethered flight. J. Exp.
Biol. 152,41
-58.
Yager, D. D. and Spangler, H. G. (1997). Behavioral response to ultrasound by the tiger beetle Cicindela marutha Dow combines aerodynamic changes and sound production. J. Exp. Biol. 200,649 -659.[Abstract]
Yager, D. D., May, M. L. and Fenton, M. B.
(1990). Ultrasound-triggered, flight-gated evasive maneuvers in
the praying mantis Parasphendale agrionina. I. Free flight.
J. Exp. Biol. 152,17
-39.
Zook, J. M. (2005). The neuroethology of touch in bats: cutaneous receptors of the wing. 2005 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2005. Online. Program No. 78.21.
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