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First published online June 27, 2008
Journal of Experimental Biology 211, 2317-2326 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016006
Effects of altering flow and odor information on plume tracking behavior in walking cockroaches, Periplaneta americana (L.)
Department of Biology, Case Western Reserve University, Cleveland, OH 44106, USA
* Author for correspondence (e-mail: maw27{at}case.edu)
Accepted 10 May 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: orientation, pheromone, wind, behavior, cockroach
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Cardé and Minks, 1997;
Weissburg, 2000;
Vickers, 2000). The structure
of plumes means that animals tracking them are not exposed to smooth
concentration gradients. Therefore, they cannot rely on the simple orientation
rules of chemokinesis or chemotaxis
(Frankel and Gunn, 1961;
Schöne, 1984) to orient
toward and efficiently locate the odor source. In fact, it is not clear that
the intermittent structure of an odor plume can provide the
directional information necessary to locate its source unless an organism can
develop a statistical impression of the plume
(Webster and Weissburg,
2001).
If no chemical gradient exists, how do plume tracking organisms orient and
steer toward the source? To perform this task most animals require two pieces
of information: (1) the presence of attractive chemicals and (2) the
direction of the flow carrying the attractants
(Arbas et al., 1993;
Weissburg, 2000;
Webb et al., 2004;
Willis, 2008). The preferred
orientation with respect to flowing air or water steered by plume tracking
organisms appears to be modulated by the presence of an attractive odor
(Baker et al., 1984;
Johnsen and Teeter, 1985;
Emmanuel and Dodson, 1979; Grasso and
Atema, 2002; Kennedy and
Moorehouse, 1969; Kennedy and
Marsh, 1974; Mafra-Neto and
Cardé, 1994; Vickers
and Baker, 1994; Willis and
Avondet, 2005). For example: male cockroaches and immature locusts
prefer to walk downwind (i.e. with the flow) in the absence of an attractive
odor, but reverse this preference and turn and walk upwind when an attractive
odor is present (Kennedy and Moorehouse,
1969; Rust and Bell,
1976; Rust et al.,
1976; Willis and Avondet,
2005).
Whether tested in the laboratory (Baker
et al., 1984) or observed in the field
(Elkinton and Cardé,
1983), flying male moths seem to have no preferred orientation to
the wind direction prior to detecting their sex-attractant pheromone. After
encountering a wind-borne plume of their species' sex pheromone, responsive
males all turn into the wind and fly upwind while in contact with the plume
(Baker and Haynes, 1987;
Baker et al., 1984;
Kennedy and Marsh, 1974). In
addition, insects tracking attractive odors upwind, whether walking or flying,
continuously re-orient to the dynamically changing wind direction as long as
they are in contact with, or have only recently lost contact with the odor
(Baker and Haynes, 1987;
David et al., 1983;
David and Kennedy, 1987;
Wolf and Wehner, 2000;
Vickers and Baker, 1997).
To further understand how walking organisms use information on flow direction and odor to track odor plumes, we recorded the responses of virgin male American cockroaches, Periplaneta americana, to the loss of either odor or wind information while they were tracking a plume of their species' sex pheromone upwind.
The goal of the work presented here is to expand our knowledge of the orientation mechanisms used by walking animals to track odor in terrestrial environments, and to explicitly compare them to the more extensively studied examples of odor plume tracking by flying insects, especially moths. By comparing the performance of the same task by similar organisms using different modes of locomotion we hope to better understand the environmental constraints and biological adaptations that underlie odor plume tracking.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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50% relative humidity on a 12 h:12 h light:dark cycle.
Wind tunnel
The experimental arena was a flat aluminum platform (1.52mx0.92m)
held 25.4cm above the floor of the working section of our laboratory wind
tunnel (1 mx1mx2.5 m). Light levels were 3–5 lux. The
pheromone source was held at the upwind end of the aluminum platform, 1 cm
above the surface. An exhaust duct at the downwind end of the wind tunnel
removed the pheromone plume from the building. For a more detailed description
please see Willis and Avondet (Willis and
Avondet, 2005).
We recorded the cockroaches' movements with a Burle TC355AC B/W video camera (Lancaster, PA, USA) positioned above the wind tunnel. The field of view of this camera encompassed the entire experimental arena. Trials were recorded at 30 frames s–1.
In all of the experiments described here the pheromone source was a 0.7 cm
diameter disk of filter paper (Whatman No.1, Eastbourne, East Sussex, UK)
containing 0.10ng of (–)-periplanone-B
(Kitahara et al., 1987;
Kuwahara and Mori, 1990). All
solutions of (–)-periplanone-B were made with 95% n-hexane
(Acros Organics, Geel, Belgium). To generate a turbulent plume, the source was
oriented perpendicular to the airflow in the wind tunnel. In all experiments
in which wind was present, the fan generated a constant 25 cm
s–1 flow.
Experimental procedures
Series 1 experiments
To determine the effect of the sudden loss of either odor or wind
information on plume tracking behavior we compared the responses of males to
the experimental treatments detailed below. Treatment order and the
introduction of individual animals were randomized and each animal was used
only once.
Wind and plume (N=14)
In this treatment, the wind and the pheromone source remained constant and
therefore the plume was stable and continuous. We placed individual
cockroaches into the plume on the downwind edge of the experimental arena in
coarse meshed aluminum window screen (holes=2 mm) cages (3 cmx10 cm;
height x diameter) and allowed them to acclimate for 1 min before
releasing them into the plume by manually removing the top of the cage from
the arena. [Prior to experimentation, smoke plume flow visualization (titanium
tetrachloride) showed that a windborne plume flowed through the cage
unhindered.] This treatment served as a control for the two following
experimental trials, `wind stop' and `plume pull'.
Wind stop (N=16)
Individual P. americana males were presented with the same initial
conditions as described above. However, once they had initiated tracking
behavior, we abruptly stopped the wind in the tunnel, leaving only a slowly
expanding plume hanging in a zero wind environment. The cockroach's behavior
was recorded until he reached the odor source. During practice sessions prior
to data recording, we used a piece of filter paper of the same size and shape
dosed with titanium tetrachloride (TiCl4), a source of dense white
smoke, to visualize the wind stopping event. The wind stopping procedure
involved three parts performed in rapid sequence: (1) the fan generating the
flow through the wind tunnel was turned off, (2) a sliding door rapidly closed
the air intake of the wind tunnel, and (3) the exhaust fan was turned off. The
three steps were coordinated to produce a consistent, abrupt and complete
cessation of the wind. The duration of the wind stopping procedure from
initiation to total wind stop (as measured from TiCl4 smoke) was
approximately 1 s. We found that the expanding plume reached the lateral edges
of the aluminum platform roughly 45 s after the wind stopped. The moment of
completion of the wind stopping procedure was marked by illumination of an
infra-red light emitting diode (LED) in the field of view of the camera. The
LED was triggered automatically as the sliding door at the tunnel's air intake
closed.
Plume pull (N=17)
For this treatment the pheromone source was mounted on nylon fishing line
that formed a continuous loop from the floor to the ceiling and connected
outside the wind tunnel. As a cockroach approached the center of the arena,
the source was removed from the arena by pulling it rapidly to the ceiling of
the wind tunnel. Rapidly removing the pheromone source truncated the plume,
and its remains were carried down the wind tunnel and out the exhaust, leaving
the cockroach walking upwind in clean air
(Kuenen and Baker, 1983). We
tested this by using TiCl4 to visualize the smoke plume in the same
manner that we used it to test the wind stop as described above. We recorded
each individual's response to odor loss until it left the experimental arena.
Knowing the wind speed and the average walking speed of a cockroach enabled us
to time the removal of the pheromone source so that the cockroach lost the
plume in the field of view of the camera. The exact moment of odor loss was
determined for each individual later. We calculated the plume to move downwind
2.075 cm in the interval between each digitized cockroach position. When the
truncated end of the pheromone plume passed the male cockroach as he walked
upwind, we declared that to be the moment of odor loss.
Series 2 experiments
To determine whether prior exposure to wind, with or without odor, could
support plume tracking in zero wind, we exposed the cockroaches to the
following four different combinations of wind and odor prior to release into
the pheromone plume: (1) continuous pheromone plume in wind, (2) pre-exposure
to pheromone plume and wind, (3) pre-exposure to wind only, and (4) no
exposure to wind or pheromone plume (see
Table 1 for more details).
After being exposed to an experimental treatment for 1 min, the cockroaches
were released from screen cages in the center of the experimental arena,
rather than at the downwind end as above. This allowed them to orient to the
experimental environment and leave the release point in any direction. When
applicable, we stopped the wind in the same manner as detailed above, prior to
releasing the cockroach. In all pre-exposure experiments the males were placed
into the plume with their longitudinal body axes aimed in random directions to
eliminate bias in the individual's walking direction. Pilot studies showed
that males detect and orient to air flow while in the screen release cages
(M.A.W. and J.L.A., unpublished). Each individual's response was recorded
until it located the odor source.
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Continuous exposure to wind and odor (N=15)
Each individual was placed in the plume at the longitudinal midpoint of the
experimental arena, providing a continuous exposure to wind and odor. In this
treatment the wind was not stopped, serving as the control.
Pre-exposure to odor and wind (N=16)
Each individual was placed into a wind-borne pheromone plume in the center
of the experimental arena for 1 min, the wind was then stopped and the
cockroach was released from the screen cage into the stationary plume.
Pre-exposure to wind only (N=16)
The cockroach was placed at lateral edge of the experimental arena, exposed
to wind, but 40 cm outside the time-averaged plume boundary. After 1 min,
the wind was stopped and the cockroach was slowly released from the screen
cage into the now stationary pheromone plume.
No exposure to wind or odor (N=15)
The cockroach was placed at the same point as those in the pre-exposure to
wind only treatment, but in a sealed plastic container approximately the same
dimensions as the screen cages used for the other treatments. Then, the wind
was stopped and the cockroach was released.
Data analysis
We manually digitized the walking paths of male cockroaches using a
computerized motion analysis system (Motus 7.1TM, Vicon Inc., Centennial,
CO, USA). We then digitized the position of the cockroaches' heads every 83
ms. The response variables measured from the video-recorded tracks were: track
angle (orientation of the movement vector from one cockroach position to the
next with respect to the wind direction – due upwind is 0°), body
yaw angle (angle of the longitudinal body axis with respect to the wind),
track width [distance between sequential turn apices measured perpendicular to
the wind direction, as per Kuenen and Baker
(Kuenen and Baker, 1982)],
groundspeed (walking speed of cockroaches measured from point to point along
its track), inter-turn duration (time between the apices of sequential turns),
net velocity (speed in the upwind direction from the beginning to the end of
each walking track), the number of times each individual stopped during an
odor-tracking performance, the duration of each stop, and the linearity index
(degree of straightness of the walking track).
In order to examine different sections of the cockroach's tracking behavior, each individual's response to the plume pull, wind stop and wind and plume treatments were split into two parts: (1) prior to the experimental manipulation, known hereafter as pre-plume pull and pre-wind stop, and (2) after experimental manipulation, known hereafter as post-plume pull and post-wind stop (Fig. 1). To control for any bias in position in the wind tunnel, the responses of males tracking the point-source plume were divided into two segments (split after 3 s. which was the mean pre-plume pull and pre-wind stop duration) termed wind and plume beginning half and end half (Fig. 1). These sub-divisions yielded a total of six different treatments for analysis.
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) to test
for differences among treatments (plume pull and wind stop: N=6, wind
and odor orientation: N=4), day (plume pull and wind stop:
N=4, wind and odor orientation: N=5), and day by treatment
interactions. Treatments and individuals were randomized daily. Each day the
number of individuals available for experimentation was divided evenly across
the treatments. Individuals from the first group were introduced sequentially
to the first treatment, the next group to the second treatment, and so on.
When an ANOVA revealed significant effects in the experiment, we applied
Tukey's multiple comparison test to determine which variables differed
significantly among the experimental treatments. We considered test statistics
with a probability of less than 0.05 (P<0.05) unlikely to be
obtained by chance, and thus statistically significant. |
RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Wind stop
After the wind was stopped, the cockroaches continued to track the now
stationary plume with few changes in behavior detectable by eye
(Fig. 1Bi–iii).
Eighty-seven percent of the males walked directly to the source
(Fig. 1Bi,ii), whereas 13%
briefly lost and then found the plume and located the source
(Fig. 1Biii; average total
tracking time: 9.64±8.38 s, N=16). Few quantifiable changes in
the behavior of males were detected from before to after the wind stopped
(Fig. 1Bi–iii,
Table 2). However, they did
increase the width of their tracks and steered their track angles more across
the previous wind direction after the wind stopped
(Table 2). The behavior of the
males tracking the continuous plume in continuous wind was not different from
the males that experienced the wind stop. (Average total tracking time:
9.52±5.93 s, N=14.)
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Plume pull
Males dramatically changed their plume tracking behavior when they walked
upwind through the truncated end of the pheromone plume after the pheromone
was pulled (Fig.
1Ci–iii). Upon loss of pheromone contact the cockroaches
ceased upwind progress and began to perform behaviors that we interpret as
search strategies aimed at locating the source of the pheromone, or relocating
the plume. The duration of the response to loss of pheromone (from plume loss
until they encountered an edge of the arena) was significantly longer
(P<0.05) than the responses to the wind stopping treatment
(average total tracking time: 30.67±11.04 s, N=17). The
average interval between encountering the truncated upwind end of the plume
and their initial behavioral response [i.e. turning at an angle greater than
90° with respect to the wind direction (N=9) or stopping
for longer than one sampling period and then executing a turn greater than
90° (N=8)] was 1.1±0.4 s. When the cockroaches stopped
upon plume loss, they waited for an average of 0.3±0.2 s before they
re-initiated walking and began turning. In 41% of the cases, upon losing the
pheromone plume the individuals looped across and downwind
(Fig. 1Ci,iii). In 59% of the
cases, the males stopped moving upwind and rather than looping around the
point of behavioral response to odor loss, they retraced their steps downwind,
sometimes walking all the way back to the release point
(Fig. 1Cii). Males apparently
switched their preferred orientation with respect to the wind from upwind to
downwind, and while walking downwind typically turned back-and-forth across
the area of the arena where the plume had been.
In most cases no statistically significant differences were observed
between the average movement parameters measured from the pre-plume pull
walking patterns and the walking tracks generated by males tracking the
standardized point-source plume. However, there were several statistically
significant differences between the males' behavior during the pre-plume pull
and post-plume pull condition. The looping maneuvers initiated upon plume loss
caused the linearity index to decrease significantly (i.e. the tracks become
less linear) (P
0.05), and the body yaw angle and track angle
also increased significantly (i.e. oriented more perpendicular to the wind
direction or downwind; Fig.
1Ci–iii). This contrasts dramatically with the typical
straight inter-turn track legs aimed mainly upwind observed prior to the plume
pull (Fig. 1Ci–iii,
Table 2). The track width also
increases, which in turn causes the inter-turn duration to increase and the
net velocity to decrease (Table
2).
To identify behavioral changes at the transitions from wind to no-wind, or pheromone to no-pheromone, and if any observed changes persisted, we then divided each track into three sections labeled as: tracking, event, and post-event. Our analysis was based on a 1.0s sub-sample of data from the center of each of these three sections. The control tracks (wind and plume) were also divided into three track sections in a similar way (0–25% to source, 26–74% to source, and 75% to source; Fig. 1). To make a matched comparison of the three track segments across the treatments, we divided the pre-plume pull and pre-wind stop track sections described above (Fig. 1, Table 2), as well as the section where the cockroach, responding to the wind and plume, was approximately 25% of the way down the wind tunnel floor. We then took a 1s. sample of data from the event (initiation of the plume pull odor loss ±500ms, initiation point where the wind was stopped ±500ms), and from the center section of the wind and plume track. We compared these to a 1s sample of data from the center section of the post-plume pull and post-wind stop data sets, as well as from the section where the cockroach was approximately 75% of the way down the wind tunnel floor.
In this experiment, the only aspect of the cockroaches' behavior that changed significantly when tracking an odor plume in wind was the groundspeed (Table 3). Cockroaches tracking wind and plumes walked significantly faster through the center section of their tracks than the beginning (Table 3). In the plume pull trials the only aspect of the animals' performance that changed significantly was their track angles. Once they lost contact with the plume, the cockroaches began to circle, resulting in a significant increase in the track angles measured (Table 3). The only aspect of the cockroaches' behavior that changed significantly in the wind stop experiment was the track width. During the event period in the wind stop treatment, the track width increased slightly and then continued to increase, becoming significantly wider than the pre-wind stop tracks, as the time post-wind stop increased (Table 3). At the spatial and temporal resolution of the video that we used we were unable to detect an identifiable transient change in behavior associated with the rapid cessation of wind.
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Series 2
Orientation to wind and odor after pre-exposure treatments
We observed a wide variety of behavior from the males exposed to the
different combinations of wind and odor before they were released into a plume
in zero wind (Fig. 2).
All cockroaches eventually found the source, some more rapidly than
others.
In the treatment where cockroaches were pre-exposed to wind and pheromone prior to odor tracking, 40% walked relatively directly to the source (Fig. 2Ai), 33% walked in looping maneuvers covering much of the area of the arena, eventually making it to the source (Fig. 2Aiii), whereas 27% displayed an intermediate amount of looping before locating the source (Fig. 2Aii). For the cockroaches with no prior wind or odor information before being released into the plume, 25% walked relatively directly to the source (Fig. 2Bi), 50% generated looping tracks that, in many cases covered much of the arena before finally locating the source (Fig. 2Biii), and 25% showed an intermediate level of searching before locating the pheromone source (Fig. 2Bii). In the treatment where cockroaches were exposed to wind only before the wind was stopped, 31% went relatively directly to the source (Fig. 2Ci), 38% looped searching across both ends of the floor until finally reaching the source (Fig. 2Ciii), and 31% displayed some looping before finding the source (Fig. 2Cii). In the standardized treatment where odor and wind were continuously present, 80% of the cockroaches walked directly to the source (Fig. 2Di), whereas 20% of them looped before reaching the source (Fig. 2Dii).
Cockroaches responding to the continuous wind and odor treatment, in which the wind and pheromone stimulus was continuously present, behaved in a significantly different way from those exposed to the other treatments (Table 4). The cockroaches that had no pre-exposure to either wind or odor had longer inter-turn durations than those in the other three treatments, but the cockroaches pre-exposed to odor and wind did not have significantly shorter times between their turns (Table 4).
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Did exposure to odor or wind information, in any combination, prior to
release in the pheromone plume without wind affect the initial walking
direction of the cockroaches? The mean leaving direction of cockroaches that
were not pre-exposed to wind or pheromone was 91.3° and was not
significantly different from a random distribution according to Rayleigh's
test (z=0.34, P>0.05;
Fig. 3)
(Fisher, 2000). Cockroaches
that were pre-exposed to wind and pheromone prior to release in the plume with
no wind showed no preference in the direction they left the release point
(mean direction of leaving=151.7°). This orientation was not significantly
different from a random distribution (z=2.56,
0.05<P<0.10) (Fisher,
2000). The cockroaches pre-exposed to wind alone had a mean
leaving direction that was 24.9°, on average, but the distribution of
leaving directions was not significantly different from random
(z=0.16, P>0.05)
(Fisher, 2000). Only the
cockroaches that were continuously exposed to wind and odor generated a
distribution of leaving directions that was significantly different from
random (z=3.75, P<0.05)
(Fisher, 2000), with a mean
direction of orientation of 37.7°.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Under these
conditions few males moved further upwind than the point at which they lost
the plume. When we removed the plume most of the cockroaches turned and walked downwind, while maintaining their tracks roughly within the boundaries of the previously existing time-averaged plume. Upon reaching their starting point or the downwind end of the arena, they turned and walked back upwind and often repeated this behavior even though the odor plume had been gone for many seconds (Fig. 1Cii). Two possible explanations for this behavior are: (1) that they were orienting to and tracking residual pheromone molecules deposited on the floor of the `plume area' of the arena, and (2) they had associated the pheromone plume, and then pheromone loss, with specific locations in the experimental arena. (According to our TiCl4 smoke visualizations, the plume was in contact with the floor from a few centimeters downwind of the source to the downwind end of the arena.)
Orientation to residual pheromone deposited on the floor would require the
cockroaches to switch from pheromone-modulated orientation to wind direction,
to a mechanism used by insects like ants that track trails deposited on the
ground [i.e. turning toward the antenna that detects the highest odor
concentration (Hangartner,
1967)]. It is clear from other observations that their antennae do
contact the floor during antennal movements performed continuously during
plume tracking (M.A.W., unpublished data).
Previous experiments have all shown that attractive chemical cues can alter
the preferred orientation to flow in walking insects
(Bell and Kramer, 1980;
Kennedy and Moorehouse, 1969;
Rust and Bell, 1976;
Rust et al., 1976;
VanVorhis Key and Baker, 1982;
Willis and Avondet, 2005). If
our males are using chemical cues deposited on the floor of the arena when
they turn down wind, they seem to ignore the wind direction. Thus, they have
apparently `disconnected' the typical linkage between the pheromone inputs and
directional cues provided by the wind direction
(Rust and Bell, 1976;
Rust et al., 1976;
Willis and Avondet, 2005). If
they are following a trail of pheromone deposited on the floor of the arena,
then the link between pheromone detection and preferred orientation to wind
direction may be context dependent. Loss of contact with a source of female
pheromone is an ecological context that may demand the chemical signal receive
increased weight, and wind direction decreased. Detection of the pheromone on
the local substrate may be a more relevant stimulus.
Male cockroaches that generated looping tracks after loss of pheromone
increased the area of the arena that they encountered, presumably in an
attempt to re-contact the pheromone plume. In addition, this looping local
search seemed to be focused on the location where odor contact was lost,
suggesting that they may be incorporating landmark cues into their working
knowledge of their environment. Landmark learning has been demonstrated
previously in P. americana
(Mizunami et al., 1998). This
looping behavior after odor loss may be functionally equivalent to the
side-to-side turning behavior, known as `casting', executed by flying moths
when they lose contact with a pheromone plume
(Kennedy and Marsh, 1974;
Kennedy, 1983). In contrast to
the irregular looping search performed by walking cockroach males, moths
performing casting flight execute temporally regular left–right turns
with the inter-turn legs oriented roughly 90° to the wind
(Kennedy and Marsh, 1974).
These side-to-side turns are continuously re-oriented as the wind direction
changes (Baker and Haynes,
1987), whereas there is no obvious preferred orientation to the
looping search of walking cockroaches (Fig.
1).
At wind-stop, the loss of directional information provided by the wind will
require our cockroaches to switch and use only chemo-orientation mechanisms to
follow the plume. Results from our work
(Willis and Avondet, 2005) and
others (Tobin, 1981), suggest
that the steering maneuvers of plume tracking P. americana males may
result from multiple mechanisms. These include: (1) a temporally regular
internal turn timer, similar to that proposed for plume tracking flying male
moths (Kennedy, 1983;
Tobin, 1981), (2) turns
triggered by bilateral spatial comparisons of concentration detected by the
two antennae (i.e. turn toward the higher concentration)
(Tobin, 1981;
Willis and Avondet, 2005), and
(3) internally generated so-called stochastic turns, or turns not clearly
associated with any obvious external stimulus
(Tobin, 1981). Until we can
know when an individual detects odor and how it subsequently responds, we will
be unable to completely discriminate between these alternatives. However,
results of other work in our lab (Willis
and Avondet, 2005) suggest that bilateral comparisons of
concentrations detected by each antenna are likely to support the successful
plume tracking behavior we observed after wind-stop.
Measurements of time-averaged plume boundaries and antennal locations
during plume tracking by P. americana males suggest that many of the
side-to-side turns are triggered when the cockroach encounters the high
contrast edge between clean air and the plume
(Willis and Avondet, 2005). In
our experiments, the 5 cm average span between the tips of the cockroaches'
antennae (Willis and Avondet,
2005) allows males near the lateral boundary of the point-source
plume to have one antenna near the plume boundary or outside the plume in
clean air while the other is near the zone of highest concentration, near the
midline of the plume. Observations of TiCl4 smoke visualizations of
the plume during practice prior to performing these experiments show that when
the wind stops, the two most obvious changes in the structure of the pheromone
plume are: (1) the high contrast boundaries between pheromone and clean air
move outward laterally, away from the centerline of the arena, and 2) as the
stationary plume expands away from its centerline the space between filaments
increases and the size of each filament also increases. Because the plume
continues to expand after the wind stops, the high-contrast signal provided by
the lateral boundary of the plume recedes away from the tracking cockroach.
Thus, the significant increase in the width of walking tracks after wind stop
may be the result of the males `feeling for the edge' of the plume and using
it as a cue to turn back into the plume.
It is well known that the tracking behavior of flying male moths is
significantly affected by plumes issuing from sources of different
concentrations (Cardé and Hagaman,
1979; Charlton et al.,
1993; Kuenen and Baker,
1982) or with different turbulent structures
(Mafra-Neto and Cardé,
1994; Vickers and Baker,
1994). Therefore it is possible that some of the changes we
observed from our cockroaches could have been caused by the changes to the
structure of the plume after the wind stopped. The fact that it was often
impossible to discriminate between pre- and post-wind stop tracking behavior
suggests that if the changes in plume structure are affecting the cockroaches'
performance, these effects are subtle.
It has been proposed that flying male moths are able to determine the
correct direction to track pheromone plumes in still air, and possibly in
wind, by comparing the concentration of sequential odor samples (i.e.
increasing concentration across sequential samples indicates that the tracker
is approaching the source, decreasing concentration indicates that the tracker
is moving away from the source) (Baker and
Kuenen, 1982; Kuenen and
Baker, 1983). This information may be available from the plume,
since the probability of encountering odor filaments, and the concentration in
these filaments, decrease predictably with both distance downwind from the
source, and distance from centerline across the plume
(Moore and Atema, 1991;
Murlis and Jones, 1981;
Murlis et al., 2000;
Vickers et al., 2001).
Comparison of sequential samples could enable any plume tracking animal to
continue toward and possibly successfully locate the source during a lull in
wind, especially if it moved fast enough to arrive near the source before the
plume dissipated. Such temporal comparisons along the plume, together with
bilateral spatial comparisons between the antennae, may explain the
performances of our cockroaches that successfully tracked the stationary plume
with no directional information from the wind.
The results of the `Series 2' experiment suggest that the chemo-orientation capabilities of P. americana males vary in different individuals (Fig. 3). In each treatment group where the wind was stopped, between 25–40% of the individuals were able to quickly and efficiently track the stationary plume to the source, whether or not they had been exposed to wind prior to their release into the plume. The proportions of males able to rapidly track the stationary plume to the source decreased from those that had experienced wind and pheromone (40%), to those that had experienced wind alone (31%), to those that had experienced neither (25%), prior to introduction to a stationary plume in still air. Thus, there is some indication that experience with the wind direction immediately prior to release in the plume may have increased the number of individuals able to subsequently track the plume with no directional cues from wind. However, since the number of individuals accounting for this increase is only one or two, this effect seems small. When released into a stationary plume in still air, the majority of our experimental population (60–75% depending on the treatment group) had considerable difficulty locating the pheromone source. Thus, unless the cockroach is already tracking a plume upwind when odor is lost, the directional information available to them from chemical information alone enables only slow, inefficient location of the pheromone source.
Even in the treatment groups that did not experience wind and pheromone together while tracking, all of the individuals located the pheromone source when given enough time. It could be argued that by leaving the males to walk around the surface of our experimental arena we are assuring that they will eventually locate the source. However, during the course of previous experiments we have observed males routinely leaving the experimental arena, sometimes not to return. We interpret the males' persistent search of the experimental arena, and the fact that they never left the arena when they could have, as an indication of continued orientation to the pheromone in the still air above the arena.
The behavior of our cockroaches is broadly similar to that reported for
plume tracking moths challenged with similar experimental conditions
(Baker and Kuenen, 1982;
Baker et al., 1984;
David and Kennedy, 1987;
Farkas and Shorey, 1972;
Kuenen and Baker, 1983;
Willis and Cardé,
1990). Like our cockroaches, male moths that had begun to track
plumes of pheromone before wind was stopped, continued to track the stationary
plume to the source with success rates similar to those in wind
(Baker et al., 1984;
Farkas and Shorey, 1972;
Willis and Cardé,
1990). Furthermore, whether tracking a plume in flight
(Baker et al., 1984) or while
walking (this study), these animals must experience the odor and wind cues
while locomoting in order to orient toward the odor source and locate it
quickly and efficiently. Both moths and cockroaches can track a stationary
plume in still air, but they take much longer to locate the source and fewer
may be able to locate the source (Baker et
al., 1984).
The variety of apparent searching behaviors expressed by our cockroaches upon loss of the plume is somewhat at odds with the consistent descriptions of crosswind casting flight reported for several species of plume-tracking moths upon plume loss. We suggest that the cockroaches may be incorporating a memory of the visual landmarks in its environment during plume tracking to support this olfactory searching, and that the addition of these visual cues may allow the cockroaches to re-prioritize the directional information provided by the wind. Further experiments aimed at characterizing the interplay amongst the various sensory modalities supporting this behavior are necessary before we can draw any conclusions. However, as we compare and contrast the plume tracking task as performed by similar organisms using different modes of locomotion, we expect the differences and similarities to reveal underlying organizational principles critical to understanding control rules and how they are adapted in different environmental and biological contexts.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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, angle of mean
leaving direction; r, length of mean vector. r is
distributed between 0 and 1, with 0 indicating no movement in the mean
direction, and 1 indicating all movements were in the mean direction.