Aaron P. Cook, Jeffrey D. Triblehorn, Aaron Lorsong, Marc Lennon

#28
Praying Mantis Evasive Response: Descending Control and Context Gating.
Aaron P. Cook, Jeffrey D. Triblehorn, Aaron Lorsong, Marc Lennon, and David D. Yager.
Dept. of Psychology and Neuroscience Program, University of Maryland, College Park, 20742.
1 . Mantids hear ultrasound
5 . The head is necessary for the in-flight evasive response
Most praying mantids have sensitive hearing via a single
ear in the ventral midline of the posterior metathorax. Like
vertebrates and some other insects, the ear uses tympana
to detect sound. The ear’s sensitivity is highest to ultrasound at 30-120 kHz depending on species. Because the
ear is in the midline, mantids are unable to determine the
direction a sound is coming from. Approximately 65% of
the 2000 mantis species have hearing, but there is a secondary hearing loss in many taxa with shortened wings.
We used male Parasphendale agrionina for the experiments
described here. The responses are similar for >20 other
species that have been tested.
The most direct way to test whether or not processing in the brain is necessary for the evasive
response is to compare the behavior of normal and headless mantids. In some insects, e.g crickets,
the head is necessary for evasion, but it is not necessary for ultrasound-triggered evasive steering
in noctuid moths and defensive clicking in arctiid moths.
A male decapitated during flight sometimes continued flying
and sometimes stopped. Renewed flight could be triggered by
tactile stimuli, and, once started, headless males tended to fly
longer and more consistently than normal animals. As shown in
the photos, headless males performed no obvious response to
ultrasound. This was true for all sound frequencies presented at
sound pressure levels up to 95 dB SPL (25-30 dB over the normal
behavioral threshold).
Ear
location
Without ultrasound
Hearing
mantids
Deafened
mantids
79.1%
30.2%
Escapes
53
29
Captures
14
67
Total trials
67
96
Escapes
The numbers
3 . A complex, multi-component response to ultrasound causes
the evasive dives
Mantids will fly readily when suspended in an anechoic chamber by a
stiff wire attached to their pronotum with dental wax. A fan blows a
gentle wind from the front to simulate forward motion. Speakers at
the ends of the chamber can produce stimuli at any frequency with
any temporal pattern.
Mantids in normal flight hold all their legs folded against the body,
abdomen level, and the head facing straight ahead. The wingbeat frequency in stable flight is 20-25 cycles/s, and the hindwing stroke
leads the forewing stroke by approximately 30°.
Within 50-100 ms after the onset of a 300 ms train of 10 ms, 35 kHz
pulses, the flying, tethered mantis begins a full extension of the
prothoracic legs, a strong head roll, wing beat rate and phase changes,
and dorsal flexion of the abdomen. The full behavior takes 200-300 ms
to develop, and it continues long after the stimulus has ended.
4 . The neural control system for evasion includes ascending
and descending components
ganglion
connective
The central nervous system of mantids consists of a ganglion in each body segment
for local sensory and motor processing. Information travels between ganglia via two
connectives. The brain (supraesophageal ganglion) contributes to complex behaviors. The tympanal nerve enters the metathoracic ganglion. Within that ganglion
there are > six pairs of auditory interneurons, some of which send axons toward the
brain. One of these, 501, has a high conduction velocity and has been implicated as a
trigger neuron for initiating the evasive response. However, 501 does not appear to
control the timing and coordination of the response components.
to brain
The ultrasound-triggered evasive response utilizes muscles in
every body segment acting in a coordinated fashion. Escape
behaviors require short latencies, and thoracic control of evasion
without the extra time for brain processing (like a reflex) would
be fastest. The complexity of the behavior, however, suggests
that descending control from the brain may be required.
6 . Component latencies during the evasive behavior suggest
multiple descending commands.
The role of the brain in ultrasound-triggered evasive behavior could be:
a) a single descending signal that sequentially activates the four components of the response
b) multiple descending signals that separately control each component
c) a descending signal that activates control circuitry in the thorax
In the first case, the latencies of the components should increase from head roll to foreleg extension
to wing beat changes to abdomen flexion. The other two possibilities predict a sequence dictated,
presumably, by aerodynamic demands.
92 ms
High-speed video (1000 fps) provided latency measurements
for each behavioral component for males in tethered flight. The
stimuli were 300 ms trains of 10 ms, 35 kHz pulses separated
by 10 ms at 85-90 dB SPL, which resembles a bat in mid-phase
attack and is highly effective in eliciting evasive behavior.
Latencies were measured as the first observable movement of
the relevant body part after the stimulus onset. Measured in
this way, the latency is a combination of neural and biomechanical delays. Latency measures of wing changes is complicated by the random phase in which the stimulus occurs. We
estimated the latency as the time from the stimulus to the first
cycle showing a change in wing beat frequency.
Extended data:
(in ms.)
Mean
Std. dev.
Min.
Max.
Lucifer yellow stain of
interneuron 501
What are the characteristics of the control
system?
Total trials Animals
71.7
18.0
37.5
120.0
169
17
340.3
57.7
190.0
530.0
167
17
1191.9
387.5
8600.0
123
17
86.9
45.0
30.0
282.5
127
17
Time to Maximum
279.9
129.0
120.0
1347.5
126
17
Duration
748.3
180.8
480.0
1420.0
76
17
Latency
136.8
30.5
67.5
302.5
167
17
Time to Maximum
333.6
69.4
162.5
462.5
166
17
Duration
748.8
155.0
492.5
1675.0
124
17
Forearms
Latency
Time to Maximum
Duration 2132.4
Head
Latency
tarsus
What area(s) of the mantis CNS control
the ultrasound-triggered evasive response?
Several lines of evidence show that the absent response was
not due to loss of sensory input, immediate trauma, or general debilitation.
1) Headless males lived for up to three days after surgery
(22-71 hrs; mean = 33.9 ± 14.7 hrs; n=12) and during that
time were able to walk, fly, and respond to tactile and wind
stimuli. The apparent cause of death was dessication.
2) Headless males tested in flight 24 hours after surgery
showed no evasive behavior (n=5).
3) Intact males whose compound eyes and/or ocelli
were covered with black paint responded normally (n=10).
4) Immobilizing the antennae in intact males did not alter
the response (n=10).
5) Socketed hairs at the neck provide proprioceptive
feedback to the CNS about movements like the head roll.
Intact animals with the head immobilized and/or the hairs
covered continued to respond as before (n=5).
72 ms
87 ms
(estimate)
Brain
Forelegs
Wings
Abdomen
A single command from the
brain sequentially activates the
individual components of the
evasive behavior.
Most mantis species perform a
deimatic display when threatened. Many, like Parasphendale,
fully extend the forelegs. Some,
like Mantis religiosa, raise and
fold their forelegs to flash an
eyespot. The wing and abdomen components are always
present. In M. religiosa, repeated
abdomen flexions produce a
hissing sound.
We suggest that the deimatic display was the
precursor of the evasive maneuver and that they
share the same neural circuits for control.
Not supported
Photo by Rudolf Bischoff
In headless males and females, tactile stimuli can
elicit the full defensive display. The forelegs are
extended as shown above or are both kept near the
midline. The mantis directs the display toward the
side of the ‘attack.’ As with intact animals, the
females display more readily and vigorously, but the
response tends to be more prolonged than normal in
both sexes.
Thus, the defensive display does not require input
from the brain for its complete execution.
9 . Context determines mantids’ response to threat and the
effective stimuli for eliciting that response
Substrate
Hanging
Hanging
with tarsal contact
with no tarsal contact
Sound
V ision
Touch
Sound
V ision
Touch
Sound
V ision
Touch
Sound
V ision
Touch
Head on
E
(E)
(E)
0
D
D
0
0
D
T
T
0
Head off
0
•••••
•••••
0
•••••
D
0
•••••
D
0
•••••
0
1
The table above presents data from tethered mantids in flight or hanging from
the tether without flying, and from mantids standing on a substrate. Tarsal
contact for tethered mantids was a ball of paper held by the walking legs. Tarsal contact inhibits flight, so both cannot coincide. Three conclusions:
2) the defensive display requires tarsal contact
Key:
E = evasive response
(E) = weak, partial
evasive response
D = defensive display
T = non-specific twitch
0 = no response
••• = couldn not test
•••1 = stopped flying
when touched
n = >5 for all conditions
3) sound never triggers a defensive display
The sequence of foreleg joint
extension varied. The bodycoxal joint most often was first.
Forelegs first = 68.3% of 167 trials with 17 males
Head roll first = 29%
Abdomen first = <1%
Head roll second = 64%
Abdomen second = 35.3%
The mean latency for foreleg extension appears shorter
than for the more rostral head roll, but the difference is
not statistically significant. This is due to the high variability, especially in the head roll, which was absent in
25% of trials. However, even if the neural latencies were
identical, the lower mass of the head compared to the
forelegs and the more flexible neck joint would predict
an earlier head roll. Thus, the shorter foreleg latency
takes on more significance.
Abdomen
The observations above argue that the contribution
of the brain is not a single descending signal
sequentially activating the components from front to
back.
The brain controls each component
of the evasive behavior separately.
The defensive display is controlled
by a separate circuit.
Both evasive behavior and defensive display are controlled by the
same circuit. Evasion/defense can
be triggered either by a signal
from the brain (requires sound +
flight) or from the thorax (requires
tarsal contact + touch).
Supported
Supported and favored
The defensive display is controlled by a separate circuit.
8 . Headless mantids perform the defensive display
Flight
Evasion/defense
circuit
Neck
1) evasive behavior requires flight
137 ms
Hypotheses for the control of the ultrasound-triggered evasive behavior:
Mantids faced with a sudden visual or tactile
threat perform a defensive ‘deimatic’ display.
The extended foreleg and wings make them
look bigger, and the often colorful underside of
the forewings provide a ‘flash’ component. Eyespots are frequently prominent on the
hindwings. Females, without the options of
flight or speedy retreat, display more readily
and more vigorously.
With ultrasound
The ultrasonic stimuli may have elicited
changes in wing beat rate or phase compared to intact mantids that would be difficult to observe directly. The wingbeat frequency in stable flight for headless males
was lower than that for intact males (20.3 ±
1.3 Hz vs. 19.3 ± 0.9 Hz; 107 trials from 11
animals). The phase lag of the forewings
was the same before and after decapitation
(118.6° ± 44.6°; 80 trials from 8 animals). The
graphs show the patterns of change in these
parameters following a stimulus for intact
and headless males, and confirm that there
are clear changes in intact animals, but no
response to ultrasound by headless animals.
(Asterisks indicate a statistically significant
difference from the pre-stimulus mean.)
1 1 . Summary
resembles the ultrasound-triggered evasive behavior
The defensive display has two characteristics
not shared with the evasive behavior: a gaping
mouth and directionality. Touch and
vision—but not sound—are directional cues for
mantids
When a flying mantis hears the echolocation cries of a hunting
bat (or bat-like 35 kHz pulses in these experiments), it performs
an evasive maneuver within 150-250 ms. At lower stimulus
intensities (right photo), it may be a dive and turn. At higher
intensities, i.e. a closer bat (below), the mantis goes into a steep
spiralling power dive that may exceed twice the normal flight
velocity of 1.5-2.0 m/s. The direction of the turn or dive is random. (The strobe flash interval in the photos was 20 ms. The
white arrow indicates the stimulus onset.)
Is the evasive maneuver effective? We
released mantids into a large flight
room where a bat was hunting. Some
mantids were normal, and others had
been deafened by filling the ear with
Vaseline. The trials were run doubleblind with 2-3 observers. The results
show an advantage of almost 50% for
hearing mantids.
7 . The defensive ‘deimatic’ display to diurnal predators
The primary components of the defensive display are the same as the components of the airborne evasive behavior triggered by ultrasound:
foreleg extension, head turn, wing changes, and
abdomen dorsiflexion.
2 . Hearing helps mantids evade capture by bats
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The twitch in response to ultrasound or a flash of light was a slight, brief flexion of most of the legs.
1 0 . What CNS area(s) control the evasive response?
Our results are consistent with the hypothesis that the brain controls evasive behavior when the mantis
is flying and thoracic circuitry controls defensive display when the tarsi are in contact with the ground.
Hearing is essential in the former case; vision or touch are needed in the latter case.
The necessary CNS circuitry would be reduced, however, if evasion and defense are expressions of
the same basic behavior. In that case, all of the timing and coordinating circuitry for the behavior
would be a ‘module’ located in the thorax. The fundamental behavior is the diurnal defensive display triggered by vision and/or touch. The brain serves simply as an ‘AND gate’ for context and
modality: if flight and ultrasound coincide, a descending signal turns on the thoracic
display/evasion module.
The module model makes sense in an evolutionary perspective as well. The appearance of mantids 170-150 million years ago predates the appearance of echolocating bats by at least 60 million years. During the pre-bat period, a diurnal defensive display would have served the mantids well, and aerial evasive behavior, especially
triggered by sound, would not have been necessary. Bat predation provided impetus for the evolution of ultrasonic hearing and of an effective way to avoid capture by echolocating predators. Rather than evolving new
escape circuitry, it would be more efficient to tap into an existing behavioral module. The only major change
required would be the addition of a switching mechanism to link the new sensory modality and context to the
existing defensive circuitry. According to our data, this switch resides in the brain.