Odor Plumes and How Insects Use Them

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Annu. Rev. Entomol. 1992. 37:505-32
Copyright © 1992 by Annual Reviews Inc. All rights reserved
ODOR PLUMES AND HOW
INSECTS USE THEM
John Murlis
Department of the Environment, London SW1, United Kingdom
Joseph S. Elkinton and Ring T. Card~
Department of Entomology, University of Massachusetts, Amherst, Massachusetts
01003
KEY WORDS: pheromones, odor dispersion, orientation, anemotaxis
INTRODUCTION
Odor plumes form as the wind disperses odor molecules from their source.
Their structure is complex and is much like that seen in smoke plumes. The
plume as a whole wanders, apparently randomly, over a wide area. Many
species of insects, however, have behavior that enables them to follow odor
plumes to their source and in this way to find mates or distant resources.
Research on odor communication has important practical implications. The
pheromones of many important pest species have been identified, syn-
thesized, and formulated for use in pest-management schemes, and they are
widely used in traps for population monitoring. Several pheromone formula-
tions are marketed, and many more are under development. They are widely
used in crop fields to disrupt insect mating (70, 103).
Despite considerable research, however, pheromones have not been uni-
versally successful in these applications (-32). Pheromone traps have been
used to detect insects at remarkably low population densities, but numbers
caught often do not correlate well with density of these insects. Catch is
affected by features of population ecology (86), and various factors modify
505
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506 MURLIS, ELKINTON & CARDI~
trap efficiency, including trap shape, placement, and weather (79). Even
more variables influence the success of mating disruption (9, 22).
Entomologists recognize the need for more fundamental understanding of
the factors affecting pheromone communication. They seek answers to sever-
al practical questions concerning, for instance, the effective range of pher-
omone traps or the strength and positioning of sources for mating disruption.
To provide answers, both the odor plume and the insects’ response to it need
study. In this review, we summarize the current knowledge on plumes and
how insects orient to them.
PLUMES IN THE ATMOSPHERE: OBSERVATIONS AND
THE MECHANICS OF DIFFUSION
Everyday observation of smoke plumes from chimneys, stacks, and bonfires
provides insight into their structure. Seen from a distance, smoke from an
elevated source appears as a discrete undulating cloud. In a brisk wind, the
cloud seems to widen rapidly close to the source, after which it expands
steadily at a lesser rate. It rises and falls as it leaves the chimney, but, soon
after, the shape becomes frozen into a sinuous pattern that changes little as it
moves with the wind. From a closer vantage, the cloud contains considerable
fine-scale structure, wispy in its center and ragged at the edges. Filaments of
dense smoke intertwine with regions of clean air. The range covered by a
discrete source is indicated, for example, by the deposits of ash on the ground
downwind of a bonfire. These observations suggest three levels of odor plume
structure:
1. Large-scale structure--the shape and average odor strength of the body .
of the plume affect the orientation strategy of insects.
2. Small-scale structure--the fluctuating odor concentrations within the
plume body affects the input to insects’ central nervous systems and
hence their instantaneous response to the plume.
3. Time-averaged structure-~determines the probability that an insect will
contact the odor plume at different locations downwind of the source.
Odor-plume structure is determined by the physics of atmospheric disper-
sion. Odor plumes are created when odor molecules are released from their
source and are taken away in the wind. As the cloud of molecules moves away
from the source, it expands and the mean concentration of molecules within it
falls. Two processes are at work: (a) molecular diffusion in which random
motion of the molecules causes them to move gradually apart and (b) turbu-
lent diffusion in which the cloud of molecules is physically torn apart by air
turbulence. The temporal and spatial scales of the two processes are very
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ODOR PLUMES AND INSECTS
507
different. Molecular diffusion is a slow and small-scale phenomenon. Turbu-
lent diffusion, by contrast, is vigorous and covers a wide range of temporal
and spatial scales. It dominates plume development.
Several authors have summarized the mechanics of turbulent diffusion in
the atmosphere (57, 99, 109). Turbulence arises from the asymmetry of forces
in the earth’s boundary layer, which causes large air masses many hundreds of
meters across to tumble as the wind drives them along. Its production and
maintenance depend on a balance of inertial and buoyancy forces known as
atmospheric stability. When the atmosphere is stable (typically at night under
clear skies), buoyancy forces dampen down turbulence and inhibit its produc-
tion, but in an unstable atmosphere, buoyancy forces encourage the genera-
tion of turbulence. Unstable conditions occur on sunny days when the ground
absorbs heat from the sun’s rays. This heat is transmitted to the air at ground
level and convective updrafts ensue. Under neutral conditions (heavy over-
cast), turbulen~ generated by nonbuoyancy forces is sustained. The energy
contained in the giant vortices or eddies is transferred to smaller vortices that
in turn transfer it to yet smaller vortices. As the vortices become smaller, they
become more randomly oriented until they show no preferred direction. The
result is that the wind speed measured in a given direction fluctuates con-
tinually. The energy injected into the turbulence by the largest eddies is
finally removed by viscous dissipation in the smallest eddies. The size of the
dissipation range of eddies is determined by viscosity of the air and characte-
rized by a parameter known as the Kolmogoroff length. The Kolmogoroff
length is a measure of the size of the smallest turbulent motions. In the
atmosphere, it is roughly a function of wind speed and height (88) and
typically a centimeter or so. Therefore, turbulent eddies have a minimum
size. Instruments used to measure turbulence are stationary and record wind
speed as a function of time. They register the frequency of wind speed
fluctuations or their period rather than the length scales of the eddies that
create them. Conversion from frequency or period to a length scale can be
made using the approximations: L = U/n = Up, where L is the length scale, n
is the frequency, p is the period (time scale), and U is the mean wind speed.
The instantaneous recorded wind speed, U, can be resolved into two
components, a mean component, ti (the overbar denotes a time mean quant-
ity), and a fluctuating component, u’, so that U = a + u’. The strength of
fluctuating quantity is often expressed as the root mean square (rms)
deviations from the mean; for example, the strength of an alternating current
(AC) power supply is given as the rms voltage. The rms of a fluctuating signal
is the equivalent of the standard deviation of samples of a distributed quantity.
The rms of the fluctuating wind speed is a good measure of the intensity of the
turbulence. By convention, the intensity is given as a nondimensional quant-
ity by dividing the rms by the mean wind speed.
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508 MURLIS, ELKINTON & CARDI~
The energy contained in a unit volume of a flow is given by a product of
density and half the square of the speed. In the case of turbulence, the
variance of the fluctuating component, fi’ 2, gives a measure of the turbulent
energy. The fluctuations that contribute to the turbulent energy come from a
wide range of different frequencies. The convention is to present measure-
ments of turbulent energy as a spectrum showing how much of the turbulence
energy is contained in each frequency band (84) (Figure 1, top). Currently,
energy spectra are usually derived from anemometer records through digital
processing (12), but the idea is more simply explained by considering the
a
n
Frequency
dominant frequency,
b
Frequency
Figure I (Top) Energy spectrum showing the energy contained in the frequency band centered
on n. (Bottom) Normalized energy spectrum, showing the dominant frequency.
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ODOR PLUMES AND INSECTS
509
analog methods used originally (69). The fluctuating part of the signal
played into a series of band pass filters, each of which allows only frequencies
in a narrow range to pass through. The energy content of each band, derived
from the square of the amplitude of the signal passed (with suitable scaling
factors), is plotted against the center frequency of the band (Figure 1, top).
make spectra measured in different atmospheric conditions comparable, they
can be normalized by dividing by the total variance (Figure 1, bottom).
Spectra contain information about the relative importance of different
turbulence scales. They relate directly to the form taken by dispersion and
hence to the structure of plumes (60). Normalized spectra of turbulence
measured in the open atmosphere have a characteristic shape. The energy
peak, corresponding to the dominant frequency, occurs at time scales of some
hundreds of seconds. Allen (1) measured turbulence spectra in a forest and
reported a progressive change in the spectra from above the forest through the
canopy to ground level. Trees removed energy from the largest and smallest
eddies, leaving a more peaky spectrum dominated heavily by eddies of a size
comparable to the tree spacing. Measurements by Wang (121) show a similar
form with a strongly dominant turbulent scale of a few meters. Turbulence in
the forest is organized into a narrower range of eddy sizes than in the open
atmosphere.
In the following sections we summarize what is now known about the
different levels of structure in an odor plume, the influences of habitat and
atmospheric conditions, and how insects respond to them.
THE STRUCTURE OF ODOR PLUMES
If an odor source is smaller than the Kolmogoroff scale, odor molecules
released into the wind form a filament that expands slowly by molecular
diffusion until it reaches the size of the smallest eddies, when the rapid and
vigorous process of turbulence diffusion takes over. During the period of
molecular diffusion, the development of the plume depends on the character-
istics of the odor molecules. Plumes of different materials may behave
differently.
The length of this molecular-diffusion stage of plume growth depends on
source size and wind speed. Miksad & Kittredge (88) calculated its length
the case of a small source and concluded that the length could be some meters.
Aylor et al (4), however, argued that for most odor plumes to which insects
respond, for example, pheromone emitted by a female insect perched on a
leaf, the source aerodynamically includes both leaf and insect and compares
in size to the smallest eddies. If so, this first stage would probably not exceed
a centimeter or so.
Beyond this point, the plume structure becomes practically independent of
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510
MURLIS, ELKINTON & CARDt~
the properties of the material within it and resembles the familiar form seen in
a smoke plume. Thus a variety of tracers, chosen for visibility or ease of
measurement, may be used to study plume structure. Observations with
tracers show the progressive influence of larger turbulence scales on a de-
veloping odor plume (58). Eddies in the size range from the Kolmogoroff
length up to some hundreds of millimeters determine the small-scale structure:
they stretch and stir the filaments in the plume (66). Those of some meters
size influence the large-scale structure; they cause the fluctuations in the
initial direction of the plume that create the undulating and meandering
patterns. Eddies on the scale of hundreds to thousands of meters give rise to
long-term changes in plume direction.
Pasquill & Smith (99) describe the effect of atmospheric stability on the
large-scale structure of a smoke plume. In unstable conditions, one sees
vigorous vertical and horizontal undulation, which is reduced in neutral and
almost absent in stable conditions. In stable conditions, the continual chang-
ing of wind direction causes the smoke to fan out widely horizontally. A
plume generated in typical daytime conditions will therefore be of a very
different form from one generated at night. Understanding of plume structure
has been advanced by making direct measurements and by the development of
mathematical models based on the physics of diffusion. Recent progress is
summarized below.
Time-Averaged Plume Structure
The first models to be developed provided estimates of mean concentration of
odor downwind of a point source based on studies of the dispersion of
battlefield gases following World War I (104). Sutton (112) developed
semiempirical equation for a plume generated from a point source at ground
level. Sutton’s model assumed a Gaussian (normal) distribution of mean
concentration in all directions perpendicular to the plume center line and a
simple power law to describe the fall in the mean concentration along the
plume center line at increasing distances from the source (Figure 2, top). The
equation included constants known as dispersion coefficients that were de-
termined by the level of turbulence or atmospheric stability.
Wright (126) and Bossert & Wilson (15) applied the Sutton model
estimate concentrations of insect pheromones downwind of a source. They
used typical values for the dispersion coefficients suggested by Sutton for
neutral atmospheric conditions. Numerous subsequent applications of the
Sutton and related models to estimate pheromone concentrations are reviewed
elsewhere (41).
The Sutton model lacks flexibility, however, as the dispersion coefficients
do not adequately reflect the physical processes they describe. The Gaussian
plume models currently used to predict mean concentrations for air pollutants
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ODOR PLUMES AND INSECTS 511
(29, 117) or radioactive materials (63) are more general and empirically based
(Figure 2, top). The basic equatign for a Gaussian plume is:
- Q exp
exp- -~ +
C(x,y,z) 2 7r UrO.yO.
z
~ff y2
where C~x,y,z) is the mean concentration at any position (x,y,z) with the x axis
aligned with the mean horizontal wind direction, the y axis aligned horizontal-
ly cross-wind, and the z axis representing height above ground (Figure 2,
top). Q is the release rate of the material in the plume, and Ur is the mean wind
speed at a standard reference height (10 m is usual). The coefficients O’y, trz
are standard deviations of the concentration distributions in the respective
horizontal and vertical directions, and h is the height of the source of emission
above ground. The equation also contains a constant, a, the proportion of
material reflected back into the plume when it reaches ground level.
The coefficients, ~ry, Crz, are analogous to the dispersion coefficients of the
Sutton model. They are not constants, however; instead they vary with
distance from the source in addition to atmospheric stability and wind speed.
They are derived from trials such as the US Prairie Grass project (31, 59).
practice, estimating the atmospheric stability is difficult. The Richardson
number, a function of the rates of change of temperature and wind speed with
height, is commonly used (99), but it is not convenient to measure. Pasquill
(98) proposed a classification system for stability based on observations
wind speed and cloud cover. The resulting dispersion coefficients can be
obtained from charts (29, 117). A more quantitative method based on surface
measurements of heat flux and wind speed was recently proposed by Hunt et
al (62).
Elkinton et al (42) tested a range of Gaussian plume models in analysis
gypsy moth response to pheromone. The moths, in field cages, were exposed
to pheromone from a distant point source roughly upwind and the onset and
duration of wing fanning was recorded. The time-averaged plume models
tested did not predict where wing fanning took place in relation to the mean
wind direction. The work revealed two main kinds of difficulty with time-
average plume models:
1. Insects do not respond to mean concentration as calculated by these
models (over an averaging time of 3 min in the case of the Sutton model).
Instead, insects respond to instantaneous concentrations that are frequent-
ly many-fold higher than mean concentrations (91).
2. The averaging times implied by the model are themselves physically
unrealistic in the atmosphere where, because of the influence of continual
shifting in the mean wind direction, stable means do not form.
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512
MURLIS, ELKINTON & CARD~,
Time-averaged plume
The filamentous structure of a real plume
Figure 2 (Top) Time-average Gaussian plume model, showing the principle axes and the source
positioned at height h. (Middle) A meandering plume model with concentration in each disc
distributed normally about the meandering center line. (Bottom) The structure of a real plume.
Models of this type cannot provide a general framework for the analysis of
insect odor communication (41), but they may be useful in specific cases, for
example, where there is significant contamination of vegetation by an odor
source (120). Gaussian plume models could be used to map the contaminated
area downwind.
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ODOR PLUMES AND INSECTS 513
Large-Scale Structure: Meandering Plumes
The most obvious feature of a plume is that it meanders (Figure 2, bottom)
and insects will encounter much higher levels of odor than the time mean.
Predicting concentration in the meandering plume is therefore of great prac-
tical importance, but concentration is difficult to assess. In the absence of
helpful experimental data, the problem was first tackled theoretically.
Gifford (51) suggested a meandering plume model in which Gaussian
functions described the distribution of material across the plume, but the
position of the plume center was free to move. He assumed that the plume was
made up of a series of disks in a plane perpendicular to the mean wind
direction, the centers of which were displaced around the mean wind axis
according to the displacement of the meandering plume (Figure 2, middle).
The overall variance of the concentration fluctuations is a combination of the
variance of the concentration fluctuations with respect to the center of each
disk and the variance of the position of each disk relative to the mean wind
axis:
where
1 is the overall variance,
2 is the variance of concentration across the disk, and
3 is the variance of the position of disk centers.
If the odor is normally distributed along any axis perpendicular to the
plume centerline, the ratio of peak to mean concentration on the mean wind
axis is:
peak
_ cV2i q- CV2M
mean
c ! 21
More general equations for the ratio of the instantaneous concentration to the
local mean concentration can be obtained. Venkatacham (118) proposed
simple model based on the assumption that small parcels of material from an
elevated source are carried downwind at the mean wind speed along straight
lines that deviate vertically and horizontally from the mean wind direction.
The deviations give the parcels a vertical and .horizontal speed component,
and by making assumptions about the distributions of these, one can calculate
the distribution of concentration across the plume downwind. Models of this
kind are known as PDF (probability density function) models.
A plume meandering in roughly sinusoidal form spends most of its time
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514
MURLIS, ELKINTON & CARDI~
around the edges of its range. Ride (102) predicted that the cross-wind
distribution of mean concentration from a narrow plume subject to wide
meandering should be bimodal with peaks towards the edges of the plume’s
cross-wind range. Studies with smoke plumes by Hanna (55) illustrate this
bimodal cross-wind distribution. Calculations predict that the degree of
bimodality would depend on the ratio of plume body width to the width of
meandering, r. Bimodality in Ride’s model starts to appear at r = 0.50 and
becomes well developed at r = 0.75. Hanna’s data correspond to r = 0.65.
For pheromone plumes in unstable or neutral conditions, the source is usually
small compared to the size of the eddies responsible for meandering, and r
will be well above 0.5. Ride’s model suggests that the edges of the envelope
in which an odor plume meanders contain higher mean concentrations. These
findings contradict the earlier assumptions of normal distributions of odor
embodied in Gaussian plume models.
Models of these types are simple but powerful. They fit the experimental
data well (46) and have considerable potential for further development (54).
HOgstrOm (61) used Gifford’s model for predicting fluctuating odor con-
centrations, and this model seems an ideal basis for the analysis of trap
interaction (17). These models are still designed to give averaged con-
centrations, however, and do not address the question of the small-scale
structure of a plume. For this, experimental data remain the most reliable
source of information.
Small-Scale Structure
Odors insects use, for example pheromones, cannot at present be measured
with sufficient time resolution to allow the fine-scale structure of odor plumes
to be assessed directly. We rely on data from trials with tracers for this
information.
Concentrations in a smoke plume can be measured over short averaging
periods with photometers [6 s (108), 1 s (55), < I s (37)]. Other studies
53) obtained resolutions better than 30 ms using sulphur dioxide and phos-
phorus pentaflouride tracers with fast flame photometric detectors. Studies
with propylene (93, 94) obtained resolution to better than one second
distances up to 1000 m from source: digital processing improved this figure to
approximately 0.1 s. Fackrell (44, 45) obtained response times of a few
milliseconds in a wind tunnel with methane and propane.
Jones (64) and Jones & Griffiths (67) described a simple and robust system
for generating and detecting unipolar ions in the atmosphere. Ion plumes can
be used to model plumes of odor provided that repulsion between ions and
deflection of the plume (resulting from image forces in the ground) are
minimized or allowances are made for them in analysis (27). Both unipolar
(68) and bipolar (13) ion tracers have also been used in wind-tunnel work
diffusion.
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ODOR PLUMES AND INSECTS
515
Analysis of Small-Scale Plume Structure
High-resolution tracer detectors produce a signal consisting of a series of short
bursts of activity, separated by periods of zero signal (Figure 3). At the
leading and trailing edges, the signal amplitude rises sharply. Bursts some-
times consist of one clearly defined spike but more often they have consider-
able structure within them. Murlis & Jones (91) defined the burst length as the
time between leading and trailing edges and the burst return period as the time
between the leading edge of one burst and the next.
As with instantanerus recorded wind speed (U), one can resolve the
instantaneous concentration, C, into two components, a mean concentration ~
and a fluctuating component, c’, such that: C = ~ + c’. The intensity of
concentration fluctuations is given by the rms of the fluctuating component
divided by the mean concentration. The variance in the fluctuating component
can be broken down into contributions from the range of frequencies and
formed into a spectrum. Hanna & Insley (58) showed that smoke-plume data
from large-scale field trials produce well-defined spectra but the dominant
scales of concentration fluctuations are considerably shorter than the domi-
nant turbulence scales.
VOLTS
EAG potential
Burst length
VOLTS
S~CONOS
Figure 3 Fluctuating signal from an ion concentration sensor showing burst length and burst
return period. Electroanntenogram (EAG) signal recorded from a gypsy moth antenna responding
to pheromone at the same time and in the same position as the ion sensor. Taken from Murlis et al
(92).
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516 MURLIS, ELKINTON & CARDI~
Time Dependency of Concentration Fluctuations
The few published measurements of the temporal structure of plumes show
that the burst lengths and burst return periods at a fixed position range widely
with an approximately log-normal distribution. Bursts last from less than 10
ms to over a second and burst return periods from 500 ms to several minutes
(66, 90-92). If the turbulence scales responsible for the large-scale structure
of the plume as a whole were distinct from those responsible for the small-
scale structure within the plume (56), then the distributions of burst return
period would be bimodal. Evidence of bimodality, however, can only be
found in distributions of return period measured at great distances from the
source (66) and where the criterion for positioning leading and trailing edges
of bursts was set at higher concentration values (90). The large- and small-
scale structure is not therefore easily separable. A continuum of scales
corresponds to the continuum of eddy sizes. Typical values for burst length
and burst return period (the value of the mode of their distributions) are,
respectively, a few hundreds of milliseconds and a second or so.
As conventionally measured, distributions of neither burst lengths nor burst
return period show significant trends related to source-to-receptor distance
(66). Murlis et al (92), however, took an ensemble mean of both return period
and length measured over short sections of active signal 90 s and 180 s long.
Mean burst length and mean burst return period measured in this way in-
creased as source-to-receptor distance increased from 2.5 m to 20 m; mean
burst length increased by a factor of 2, and burst return period increased by a
factor of >7.
Intermittency of Fluctuating Concentration
Intermittency is defined as the proportion of time when the signal is absent.
Because it is also sometimes defined as the proportion of time when the signal
is present (the one being 1.0 minus the other), we have converted where
necessary.
Intermittency, arising from zero concentrations inside the plume and the
meandering of the plume as a whole, considerably affects concentration
measurements. Zero values can, however, be rejected through a procedure
known as conditional sampling (108). Conditionally sampled means are
formed from ensembles containing only values that meet some set con-
dition--for example, that they are nonzero.
Jones (65) measured intermittency over successive 1-h samples of an ion
detector signal. He found it varied widely and concluded that intermittency is
a highly unreliable signal characteristic because long period events have a
disproportionate effect on samples. The wind may shift away from the
measurement point, for example, for minutes at a time. Murlis et al (92)
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ODOR PLUMES AND INSECTS 517
estimated intermittency from short samples of active signal (90-s and 180-s
durations) to remove the influence of long periods of zero concentration.
Intermittency estimated in this way increased systematically with increasing
distance from the source, from over 60% at 2.5 m to 90% or more at 20 m.
Much intermittency comes from movements of the plume as a whole, but a
significant part is derived from patches of clean air inside the plume (Figure 1,
bottom). Fackrell & Robins (47) show that intermittency depends on
turbulence structure of the air flow and the source size. Intermittency inside
their wind-tunnel plume decreased as the distance from the source increased,
until at large distances downwind it became close to 0% (no patches of
uncontaminated air left). In the atmosphere, however, where source size is
comparable to that of the smallest eddies, Mylne & Mason (93, 94) found that
the minimum intermittency in the center of a plume reaches an asymptotic
value significantly greater than zero. In the atmosphere, some patches of
odor-free air are apparently always inside a plume from a small source--the
smaller the source relative to the smallest turbulence, the more significant the
patches are.
Concentration Fluctuations in a Plume
Probability distributions of concentration fluctuations are highly skewed
towards high values, low concentration values being disproportionately
numerous. Functions proposed for the distributions include exponential, log
normal, and clipped normal (52, 55, 65, 66, 114). The intensity of concentra-
tion fluctuations decreases with increasing distance from source more rapidly
than mean concentration. The intensity seems eventually to reach some
approximately constant (nonzero) value dependent on source size and the
turbulence scale (46, 47, 93, 94).
Mylne & Mason (93, 94) found that the distribution of mean concentration
across the plume, obtained by conditional sampling, corresponded to a rough-
ly Gaussian form. However, intermittency showed a complementary trend,
and these authors concluded that the lower conditional mean concentrations
found at the edges of the plume were produced by the higher intermittency,
the concentration in odor bearing filaments remaining unchanged.
Aylor (3) recognized the probable behavioral importance of extreme values
in pheromone plumes. Hence, an alternative way of assessing odor concentra-
tion is to focus on peak values in bursts. Storeb0 et al (111) found patches
undilute material 100 m and more from its source. Murlis & Jones (91)
measured probability distributions of peaks of concentration. They were
skewed to higher values, but less so than mean concentrations in bursts.
Distributions of burst-peak concentrations from signals recorded at different
positions overlapped significantly, even when they were as much as 5 m
apart.
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518
MURLIS, ELKINTON & CARD~
One can estimate the strength of odor in a plume in’other ways. In
experiments with smell in the atmosphere (10, 61), observers found that smell
arrived in short bursts, both because the plume switched back and forth and
because the human nose is itself a sampling organ, with an averaging period
of a few seconds. Similarly, an insect flying in an odor plume samples
(though over shorter times). Because of its movement through the plume and
because the plume is being driven past it by the wind, the concentration in the
plume has less direct impact on the insect than the flux of material past it (41).
Murlis et al (92) measured the mean flux, the dose (the quantity of ions
contained in each burst), the peak value of flux in each burst, and the
maximum peak recorded in each 90-s or 180-s sample of active dignal using
Langmuir ion probes (13, 14) (Figure 3). Strength as assessed in all these
ways decreased systematically as source-to-receptor distance increased
according to simple power laws, but the mean flux and dose decreased more
rapidly than the peak values.
Effects of Habitat and the Size and Position of an Odor
Source
In an open habitat, dominant turbulent scales are some hundreds of meters and
energy is progressively transferred from large to small scales. There is
considerable energy at small scales, and mixing is vigorous. David et al
showed that, for smoke puffs released from a low source over open ground
(36), each followed (different) linear trajectories for at least 20 m, showing
that individual segments of a plume travel long distances in straight lines
despite differences in original orientation as they leave the source. Meander-
ing is produced as successive plume segments set out in a slightly different
direction from their immediate neighbors.
In a forest, however, where small-scale turbulence is relatively less energe-
tic and the dominant scale is only a few meters, mixing is far more leisurely
and the directional sense of plume segments is less well sustained. The
structure in a forest smoke plume seems almost frozen as it is carried
downwind on a path winding on the scale of the dominant eddy size. Elkinton
et al (43) showed that individual puffs of pheromone beneath a forest canopy
would follow highly nonlinear trajectories even within a few meters of the
source. Under light wind conditions in a forest, tracers (smoke puffs or
bubbles) are frequently observed to change direction by more than 180
°
over a
distance of 20 m or so. Consecutive puffs follow similar paths to about 20 m
where they frequently become very different, sometimes one in a sequence
doubling back on its trajectory. Brady et al (18) also recorded trajectories
this kind in studies of tsetse response to host odors in African bush (low
shrub).
Recordings of tracer signals made in a forest (92) had longer bursts than
an equivalent trial in an open field. Flux decreased as source-to-receptor
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ODOR PLUMES AND INSECTS 519
distance increased less rapidly than in the field. Peak-to-mean ratios were
lower close to the source and increased less rapidly in a forest.
The size of the source has a considerable effect on plume structure (47, 88);
in general, the smaller the source, the higher are the intermittency and the
intensity of concentration fluctuations. An odor source’s size depends on the
size of the insect’s perch rather than the size of the insect or its odor-emitting
gland (4). The size of the perch clearly depends on the habitat. Even in
forest, where the typical source is about the size of the diameter of the tree
trunks, the effective source size is small compared with the energetic turbu-
lent scales and corresponds to the smallest source sizes considered in the wind
tunnel trials of Fackrell & Robins (47).
Fine-scale structure in plumes is also affected by height of the source. From
sources at ground level, it is dominated by intense mixing at the surface (101)
and is independent of source size (47). Hanna & Insley (58) found
systematic data on elevated sources. It is generally assumed (91, 111) that
greater heights than about 1.5 m above ground, the structure of plumes from
sources whose effective size is a few centimeters is affected little by the
surface for distances of tens of meters from the source.
Models for Predicting Concentration Fluctuations
Experimental data of the kind detailed above has enabled modelers to test a
range of different approaches to the prediction of fluctuating concentration.
Hanna (54) reviewed such models and tested them against field data.
concluded that simple analytical formulae derived from such models fit the
data well, but that considerable potential for further development remained.
The most common output from these models is a distribution of concentra-
tion fluctuation intensity, which can be considered as a property to be created,
removed, and transported. For an idealized plume with its center line on the x
axis, the conservation equation for the fluctuating concentration (c’) is given
by Pasquill & Smith (99) as:
where
1 is an advection term (transport of c’ along the x axis),
2 is a production term,
3 is a diffusion term (transport of
’2
by the cross-wind gradients
of c’), and
4 is a dissipation term (loss of
’2
by molecular diffusion).
The terms v’ and w’ are the fluctuations of wind speed in the y
and z directions, respectively.
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520 MURLIS, ELKINTON & CARDI~
The equation can be solved only by making several assumptions and
simplifications. Csanady (33, 34) made the major simplifying assumption that
the cross product terms involving w’, v
v
, and c’ could be represented by the
product of the mean gradient and a coefficient of diffusivity, K. The conserva-
tion equation then becomes:
where Ta is a time constant for the decay of concentration fluctuations and is a
function of x. Ky and K~ are the coefficients of diffusivity in the y and z
directions, respectively, and are also functions of x.
Although this equation still appears somewhat intractable, all the terms can
be estimated or derived from experiments, and a solution can be found for c’
as a function of downwind position for a specified mean concentration
distribution, C = f(x,y,z). Further simplifications are possible. For example,
far downwind, the production term is small. If it is neglected and Ky = K~ =
K, a constant, the distribution of variance is Gaussian and the equation for
cross-wind distribution of intensity becomes:
~
~ exp
exp
C
Cy,z=
0
4~y ~
where y,z=O refers to values on the plume centerline. As a consequence of
this relationship, intensity of concentration fluctuation is greatest at the edges
of the plume body.
Wilson et al (124) proposed an empirical Gaussian model for c’ 2, assuming
it is produced from point sources positioned independently of the source of the
plume. The cross-wind profiles were similar at each position down wind and
were scaled on plume-body widths. The parameters describing position and
strength of the variance sources, the form of cross-wind profiles, and other
input needed were chosen to fit the wind tunnel data of Fackrell & Robins (46,
47). The parameters themselves have a sound physical basis, and the model
therefore has potential for general application. Wilson et al (125) modified
to predict conditionally sampled concentrations and intermittency.
Models of both these kinds predict fluctuations in the plume, but they can
be combined with meandering plume models to predict the overall fluctuation
(54).
Two kinds of advanced models have been developed: (a) mathematical
models that solve equations for fluctuation variance directly, such as the
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ODOR PLUMES AND INSECTS 521
second-order closure models of Sykes and coworkers (113, 114), and (b)
statistical models, such as random walk models (107, 115, 116) or large eddy
simulations (85, 97). Second-order closure methods use more physically
defensible means of calculating the difficult cross-product terms in the con-
tinuity equation for c
’2.
Numerical simulations of dispersion calculate large
numbers of trajectories of particles or particle pairs. Single particle models
yield mean concentrations, but by considering particle separation in parti-
cle-pair models, one can also obtain a statistical description of concetra-
tion fluctuations. Once fully developed, numerical simulations should offer
significant new possibilities. By tracing paths of populations of particles,
they could provide a unique realization of the fluctuating concentrations
in a plume. A model of this kind could be used in combination with a
model of insects’ instantaneous response to odor to evaluate theories about
orientation.
Mason (85) noted that the influence of large-scale motions responsible for
movements of the plume as a whole are often neglected in dispersion model-
ing. He proposed a model in which the movements of large eddies are
simulated by a numerical scheme and the small-scale motions are paramete-
rized. The model produced results that agreed well with experimental data but
was costly in computer resources.
Therefore, one has several options for modeling the distribution of fluctuat-
ing concentration in a plume. The concept of active space could be revived
with the mean concentration replaced with one or other measure of fluctuating
concentration.
BEHAVIORAL IMPLICATIONS
With an understanding of the generation and structure of odor plumes, we
may now ask what features of the plume are detected and used by insects in
walking and flying toward the odor’s source. This line of inquiry requires
knowledge of the mechanisms of insect orientation to odors (73) and the
sensory inputs that mediate them.
Insects produce and respond to odor plumes that differ markedly. Bark
beetles (Scolytidae) can generate a large plume with an effective source the
size of an entire tree trunk with hundreds of odor-emitting beetles. Arctiid
moths may release pheromone as both a vapor and an aerosol (76), and
because the pheromone gland is rhythmically protruded, the plume is released
as a series of pulses (30). Parasitoid wasps following a plume to a prospective
host may need to navigate a narrow plume of host-released kairomone within
a larger diffuse plume of odor from the plant harboring the host. Such
different plume structures certainly exert different selective pressures. Insects
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522
MURLIS, ELKINTON & CARDI~
with differing phylogenies and therefore independently evolved orientation
mechanisms assure multiple solutions to the location of odor sources (21).
Most of our examples are of orientation to odors by flying insects, which
entails the difficult navigational task of detecting wind direction while air-
borne. Most of the evidence on this phenomenon has been accumulated on the
attraction of male moths to a female.
Search Strategies
Which attributes of the plume’s structure and an insect’s pattern of movement
with respect to the wind’s direction are important to the initial contact with an
odor source? Most insects actively move about before entering the plume, and
several modeling studies have asked: are there optimal strategies for contact-
ing the plume?
This approach requires assumptions about plume structure. Some have
suggested that the optimal strategy for the animal is to fly cross-wind if the
plume length exceeds its width and up or downwind otherwise (20, 83).
Sabelis & Schippers (106) provided mathematical expressions of this idea.
Dusenbery (38, 39) developed similar predictive models that incorporated the
cost of moving with or against the air stream. These treatments assumed
simplistic time-average plumes. For instance, plume width has been defined
by the range of the wind direction (106); when the range exceeds
°
, th e
plume is wider than long. However, the range of the wind direction depends
on the time interval over which it is measured (41). These studies further
assumed that the insect can estimate the mean (as opposed to instantaneous)
wind direction and can fly at some fixed angle with respect to it. They also
assumed that the insect would inevitably contact the plume and locate the
source once within the time-average boundaries. However, much evidence is
to the contrary (e.g. 43).
Few good field data are available on the actual search strategies employed
by flying insects before they contact odor plumes. Some studies suggest a
cross-wind tactic, whereas others do not (e.g. 40). A deficiency in many field
observations is the anecdotal estimation of the instantaneous orientations of
wind and the organism’s path. Realistic models of optimal foraging for a
plume await construction. Such models would incorporate improved repre-
sentations of plume size and shape based on isopleths that indicate the
probability of contacting the instantaneous plume at each point downwind of
the source (54, 102).
Orientation Toward the Source
HEADING UPV¢IND USING OPTOMOTOR ANEMOTAXIS Walking toward an
odor in wind is a simple task because gauging the wind’s instantaneous
direction only requires mechanoreceptive input (11). Upwind flight, however,
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ODOR PLUMES AND INSECTS
523
requires that the airborne organism determine the wind’s direction by judging
visually how wind has deflected the flyer from its heading. Although an
organism can estimate its airspeed by mechanoreceptive input, the optomotor
reaction (comparing the discrepancy between heading and track over ground
as visually detected drift or side slip) is the only verified mechanism by which
an airborne organism can reckon wind direction (72). When side slip is zero,
the organism is heading due up (or down) wind. The optomotor reaction
wind appears to explain nearly all cases of flying orientation to odor, except
an aim and shoot strategy in which insects determine upwind heading while
perched on a substrate and then fly in that direction (19).
HEADING TOWARD THE PLUME’S SOURCE The instantaneous wind direc-
tion and the plume’s axis are only infrequently coincident, so that simply
heading upwind while in the plume will not routinely lead toward the odor’s
source. In open fields, moving upwind while in a plume should aim the insect
toward the odor’s source, particularly within tens of meters (36), but because
the plume meanders, often an insect heading upwind will exit the plume. In
forests (43) and the African bush (18), the meandering plume can be over-
taken by large-scale eddies traveling in different directions, often producing
highly contorted plume paths. Flight upwind in such plumes often carries an
insect out of the plume. In addition, the upwind direction is only infrequently
aimed toward the odor’s source.
Both of these constraints imply that successful location of an odor over
distances of tens of meters requires a tactic to enable relocation of the plume
when upwind flight carries the insect beyond the plume’s boundary. Casting,
a reiterative zigzag that may progressively widen but does not progress
upwind, enhances the likelihood of directly recontacting the plume as the cast
widens or provides a station-keeping maneuver until the plume shifts back to
the insect’s position (35).
Successful flight toward the source may depend upon sustained (tens of
seconds) intervals when the wind vectors are parallel, such that the directions
along the plume’s axis and upwind are coincident. Such parallel wind fields
within which an insect may successfully follow a plume are more diagnostic
of active spaces than the mere concentration of odor (43). The effective
distance over which insects follow odor sources may be related to the domi-
nant frequency of the large-scale eddies responsible for the major wind shifts.
Models of such large-scale structure might be applicable to insect orientation
strategy.
NONANEMOTACTIC MECHANISMS OF ORIENTATION Although odor-
induced anemotaxis is the primary mechanism for locating a distant odor
source (74), various forms of chemotaxis have been hypothesized to play
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524 MURLIS, ELKINTON & CARDI~
role in orientation. Such a navigational system might rely upon directional
cues extracted from the plume’s structure (such as the position of the bound-
ary) or temporally monitored changes in intensity of the plume’s signal. To
verify that factors other than the optomotor reaction to wind do contribute to
orientation, one experimental scheme is to impose windless conditions. In
their wind tunnel trials, Farkas & Shorey (48) observed that some moths
continued flight along the plume’s axis following a sudden cessation of the
wind. A similar response to a plume in zero wind was verified with Grapholi-
ta molesta (78) and Lymantria dispar (123). Longitudinal klinotaxis (sequen-
tial sampling of concentration) appeared to contribute to flight along the
plume in concert with an initial setting of course polarity, by optomotor
anemotaxis (78). In nature, this maneuver is potentially useful for distances
on the order of meters when wind speed falls below the level needed for the
optomotor reaction.
Wright (126) was the first to point out that the filamentous nature of odor
plumes might provide directional cues. He proposed that flying insects could
measure frequency of bursts to determine source’s direction, but he later
abandoned this idea in favor of anemotaxis (127). Moore & Atema (89)
proposed that lobsters (at relatively close range and in water) extract di-
rectional information from the changes in the rate of increase in concentration
at the leading edges of odor bursts. However, Murlis & Jones (91) concluded
from ion plume trials in the atmosphere that the rates of change in concentra-
tion or other plume characteristics with distance from the source are unreliable
indicators of direction to the source, unless, perhaps, the source was very
close.
Detection of Fine-Scale Structure
Scrutiny of the flight tracks of G. molesta suggests that either contact or loss
of the plume can induce a change in course angle within 0.15 s (5). This
expressed as a surge upwind in pheromone and a tendency toward cross-wind
casting upon loss of the scent. In the silkworm Antheraea polyphemus,
casting latency following odor loss was not as rapid~.3-0.5 s (7). Not only
does the fine-scale structure of plumes alter behavior, it appears to be required
for sustained upwind flight. In wind-tunnel trials with two tortricid moths,
continued upwind progress did not occur in a homogeneous cloud of pher-
omone (75, 122). Rather, a plume or a naturally fenestrated (or
perimentally pulsed) cloud of odor was needed.
Baker et al (8) proposed that cessation of upwind progress, as occurs near
the pheromone source, might be triggered by fusing of the receptor output
when the receptor system could no longer resolve the individual odor pulses.
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ODOR PLUMES AND INSECTS 525
Field and wind-tunnel electroantennogram (EAG) recordings of G. molesta
suggested that peak-to-mean ratio rather than either the peak or mean con-
centrations induced in-flight arrestment (6).
The ability of an organism to resolve individual bursts of odor and possibly
features of individual bursts rests on the characteristics of the odor-detection
system. In the case of attractant pheromones, odor molecules are thought
(110) to enter pores on the sensilla and bind to receptor proteins on the surface
of the sensory dendrites. The receptor cells themselves, at least in the case of
moth pheromones, appear to have a narrowly tuned specificity. Populations of
such receptors on the antenna respond to a single or perhaps two closely
related compounds in the blend. Other odor receptors many have broad tuning
(2). Graded potentials arising from the dendrite are transduced into trains
action potentials that propagate along the sensory axon to the central nervous
system. The frequency of such action potentials is proportional to the odor
intensity. The odor molecules are rapidly degraded by enzymes (119) so that
receptors are available to respond to a new odor pulse. The latency of axon
response is on the order of 100 ms.
Most receptors exhibit a phasic/tonic response to odor signals of a second
or more duration (71). A strong odor causes an initial high-frequency burst
action potentials (the phasic response), followed by a period of reduced
frequency (the tonic response) that persists for the duration of the odor pulse.
At low odor concentrations, only the tonic phase occurs.
In the receptor cells of A. polyphemus, the two receptor cell types (each
sensitive to a different pheromone component) have different response pat-
terns (105). One cell type can resolve 20-ms pulses at 5 or more stimuli/s,
while another can only distinguish 2 stimuli/s. Thus in A. polyphemus, the
structure of the odor plume might be registered in a different pattern by each
receptor type. At the level of the antenna as a whole, much of the small-scale
plume structure in a plume is reflected in EAG signals (92) (Figure
Central olfactory neurons can detect the pheromone plume’s discontinuous
structure. Christensen & Hildebrand (28) recorded from higher-order in-
terneurones in the deutocerebrum of Manduca sexta and found that pulses
were resolved up to 10/s.
Changes in Behavior as Insects Approach the Source
As flying insects approach an odor source, their flight patterns typically
change, and ultimately landing may ensue. The site of landing may be close to
the odor source, or if the effective source size is large, as occurs for example
when a female gypsy moth calls from a tree trunk, landing may be many
centimeters away from the source. The insect locates the source following
walking orientation (26). Of particular interest are the alterations in the
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526
MURLIS, ELKINTON & CARD~
plume’s signal that influence these behavioral changes. In moths, a typical
change seen in wind-tunnel trials employing lures of varying strength is a
reduction in ground speed and a decrease in the width of the zigzag path, both
of which can be attributed to increases in pheromone concentration because
the plume’s dimensions are ,essentially unaltered (25, 49, 50, 77, 84a). Farkas
et al (50) found that landing was induced by a high concentration of pher-
omone accompanied by an appropriate visual stimulus.
Pheromone Blends and the Role of Indi~vidual Components
Most attractant pheromones (indeed most behaviorally relevant odors) consist
of blends. Much debate has focused on the possibility that in moths a portion
of the blend mediates the earliest behaviors in source location (such as locking
on to a plume), whereas the entire mixture (or the natural component ratio)
evokes later behaviors (such as landing or courtship) (24, cf. 82).
alternative system envisages the complete blend evoking all behaviors at a
lower threshold than partial blends (82). Although several behavioral studies
suggest such a nested active-space system (16, 23, 95, 96), the blends tested
have not always been complete (23), and alternative behavioral interpretations
exist. The complete blend has the lowest concentration threshold for eliciting
all behaviors observed in Argyrotaenia velutinana, Tricoplusia ni, and G.
molesta (80, 81) and thus the entire blend governed the active space.
Support for the potential differences in active spaces of partial and com-
plete blends comes from a study of receptors for Antheraea polyphemus and
Antheraea pernyi. The relative number of cells sensitive to each component of
the pheromone, their relative sensitivity, and the release rates of components
from the female suggest that the active space of the major component could
project farther downwind than that of the blend (87). The dynamics of the
receptor’s response to different components in the blend also play a part. The
rapid cells in A. polyphemus antennae (105) are highly responsive at low
concentrations but would soon be overwhelmed by high stimulus levels. The
slower ceils are less sensitive to low concentrations but continue to function at
high stimulus levels. There may be no generic solution to how moths organize
a system of thresholds for blends.
CONCLUSIONS
Considerable progress has been made in understanding the fine-scale structure
of odor plumes and consequently in unraveling the information available to
insects. Odor signals consist of short bursts of odor of greatly varying
intensity. Farther from the source, bursts are on average weaker (but not
reliably so). They are also slightly longer and there is a lengthened gap
between them. Overall, the intermittency of the signal is higher at greater
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ODOR PLUMES AND INSECTS 527
distances from the odor source. Nearer the source, the peak-to-mean ratio is
considerably reduced, but the rate at which the odor concentration rises at the
leading edge of the bursts increases. How much of this rich array of informa-
tion is used in orientation remains to be established.
Insects can resolve odor bursts at least as fast as 10/s in the peripheral
receptors and in interneurons farther up the afferent pathway. The kind of
information derived from these patterns is not yet clear.
Progress in modeling plumes has also been substantial and a variety of
approaches have emerged to deal with fluctuating concentration and its time
dependency. These models have application in the studies of active spaces.
Determinisitic plume models based on numerical simulation of diffusion
could improve our understanding of orientation strategies.
There is promise in applying advanced plume models and field measure-
ments of simulated plumes in different habitats to define the temporal and
spatial cues available in odor plumes. In turn, such information will engender
the behavioral and neurophysiological experiments requisite to explain the
navigational mechanisms used by insects to locate odor sources.
ACKNOWLEDGMENTS
We thank C. Boettner for editorial assistance and D. Hall, C. Jones, L.
Kuenen, K. Mylne, and D. Ride for helpful discussions. Our studies have
been supported by USDA competitive grants.
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