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First published online August 22, 2008
Journal of Experimental Biology 211, 2849-2858 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016394
Antennule morphology and flicking kinematics facilitate odor sampling by the spiny lobster, Panulirus argus
Department of Integrative Biology, University of California, Berkeley, CA 94720-3140, USA
* Author for correspondence at present address: Department of Environmental Sciences, University of Virginia, Charlottesville, VA 22904, USA (e-mail: reidenbach{at}virginia.edu)
Accepted 26 June 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: lobster, olfaction, antennule, aesthetasc, chemoreception, Panulirus argus, Reynolds number, particle image velocimetry
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Koehl, 2006). Both field and
laboratory measurements of odor plumes show that concentrations of odors are
filamentous and highly intermittent, both in space and time, and vary in
systematic ways with distance from the odor source
(Crimaldi and Koseff, 2001;
Rahman and Webster, 2005;
Koehl, 2006;
Moore and Crimaldi, 2004).
These spatial and temporal odor signals are sampled by the olfactory organs
(e.g. noses, antennae, antennules) of animals navigating through the
environment and can provide information about the nature and location of the
odor source (Atema, 1996;
Koehl, 2006;
Moore and Crimaldi, 2004). The
first step in the process of smelling, before neural processing, is the
physical capture of odorant molecules from such plumes in the fluid
surrounding an animal.
Many animals actively sample odor-bearing fluid from their environments,
and such `sniffing' is an important component of the process of smelling
(Schoenfeld, 2006). The
purpose of this study was to examine how the structure and odor-capturing
movements of an active olfactory organ affect how it takes samples of the
fluid around it. Here we focus on the olfactory antennules of the Caribbean
spiny lobster, Panulirus argus (Latreille).
Sniffing by lobster olfactory antennules
Decapod crustaceans have different types of hair-like chemosensory sensilla
on various appendages, including the first antennae (`antennules'), second
antennae, mouthparts, claws and walking legs
(Moore et al., 1991;
Keller et al., 2003). Both
behavioral and neurobiological studies are elucidating various roles that
these diverse sensilla play in odor recognition and tracking
(Steullet et al., 2002;
Johnson and Atema, 2005;
Schmidt and Derby, 2005;
Horner et al., 2007). We used
the lateral flagellum of the olfactory antennule of the spiny lobster,
Panulirus argus, as a system to study how the morphology,
orientation, and motion of sensilla-bearing appendages affects the small-scale
water flow within the hair array.
The olfactory antennules of decapod crustaceans such as lobsters and crabs,
have two branches, called flagella. The lateral flagellum of an antennule
bears rows of chemosensory hairs called aesthetascs
(Fig. 1)
(Koehl, 2006), which contain
chemosensory neurons that project to the olfactory lobes of the brain
(Steullet et al., 2002;
Horner, 2007; Schmidt, 2007).
Both the lateral and medial flagella of an antennule also bear other sensilla
containing chemosensory neurons that project to the lateral antennular
neuropil (Steullet et al.,
2002; Schmidt and Derby,
2005; Horner at al.,
2007). Although a variety of chemosensory sensilla on the
antennules and other appendages are involved in various aspects of food-odor
tracking (Keller et al.,
2003), the aesthetascs alone appear to be involved in processing
odors from conspecifics (Johnson and
Atema, 2005; Horner et al.,
2007).
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;
Koehl, 2006). Dye studies
revealed that water flows through the aesthetasc array during the rapid flick
downstroke, and that this water is retained within the array of aesthetascs
during the slower return stroke (Koehl et
al., 2001). Such intermittent flicking has been suggested both to
enable lobsters to take discrete samples of odor-containing fluid and, between
flick downstrokes, to allow sufficient time for odor molecules trapped in the
aesthetasc array to undergo molecular diffusion to the chemosensory cells in
the aesthetascs (Koehl et al.,
2001). The importance of the dynamics of a flick to how a
turbulent odor plume is sampled has also been studied by Crimaldi et al.
(Crimaldi et al., 2002), who
showed that flicking increases both the number of odor filaments sampled per
time and the probability of sampling an odor filament of high concentration.
Furthermore, if flicking does not disrupt the filament structure of an odor
plume, it also permits sampling of the spatial structure of the plume along
the antennule (Koehl et al.,
2001), which may permit animals to use that information in
determining the location of the odor source
(Webster and Weissburg,
2001).
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Approximately 1000–2000 aesthetascs form a dense hair tuft along the
distal portion of the lateral flagellum of each antennule of a P.
argus lobster (Gleeson et al.,
1993). These aesthetascs are attached to the lateral flagellum in
transverse rows, but their distal tips are arranged in a zig-zag pattern along
the antennule (Grunert and Ache,
1988; Gleeson et al.,
1993; Goldman and Koehl,
2001). Each aesthetasc, which is about 0.8mm long, contains
approximately 320 sensory neurons whose dendrites project as a bundle into the
hair shaft (Grunert and Ache,
1988). Olfaction occurs when odor molecules, carried by molecular
diffusion, diffuse through the cuticle into the lumen of the aesthetasc, and
bind to receptors on the outer dendritic segments of an olfactory neuron. The
distal 80% of the length of the aesthetasc, which has a thin cuticle, contains
only the dendritic segments of receptor cells, and should provide a `pure'
membrane for chemosensory transduction
(Grunert and Ache, 1988). When
enough odor molecules bind to the receptors on a neuron, the neuron
depolarizes (i.e. `spikes') and the signal is transmitted to the olfactory
lobe of the brain (Schmitt and Ache,
1979). How does antennule flicking affect the movements of
odor-bearing water around these chemosensory aesthetascs?
The relative importance of viscous to inertial forces in determining flow
around a biological structure, such as an aesthetasc, is defined by the
Reynolds number (Re) as:
 | (1) |
is the kinematic viscosity of the fluid (e.g. sea water).
Aesthetascs of P. argus operate at low Re
(Goldman and Koehl, 2001;
Koehl et al., 2001), hence the
flow is dominated by viscous interactions in the fluid and is laminar. In such
flow, there is no turbulent mixing between adjacent fluid layers and molecular
diffusion is the only mechanism that transports dissolved substances (e.g.
odorants) across streamlines towards or away from the surface of an
aesthetasc. Therefore, the rate of arrival of odor molecules to the surfaces
of an aesthetasc depends first on the inertially dominated advection of the
fluid to the vicinity of the hair and then on the molecular diffusion of
odorants from the bulk flow to the surface of the hair
(Stacey et al., 2002).
When fluid moves relative to a solid surface, the fluid in contact with the
surface does not slip with respect to that surface (i.e. the no-slip
condition). Owing to no-slip and to viscous interactions between the fluid
molecules, a velocity gradient develops in the fluid between the surface and
the freestream flow, forming a boundary layer. The slower the flow, the
thicker the boundary layer that forms. Typically, the larger the Re,
the thinner the velocity boundary layer is relative to the size of a structure
(Schlichting and Gersten,
2000), such as a hair. Therefore, the higher the Re of
the hairs within an array of hairs, the greater the fluid transport through
the gaps between hairs in that tuft (e.g.
Cheer and Koehl, 1987). The
advective transport in the vicinity of each hair is a function of how much
fluid passes through, rather than around, the array
(Loudon et al., 1994). Gleeson
et al. (Gleeson et al., 1993)
proposed that the zig-zag arrangement of the aesthetasc tips on the antennules
of P. argus allows fluid to be channeled between neighboring
aesthetascs.
Kinematics of antennule flicking
Lobsters typically flick the lateral flagellum of their antennule several
times in a row and then pause for a short time period (usually a few seconds
or less) before executing another series of flicks. Average flicking
frequencies measured for undisturbed lobsters were between 0.4 and 1.5 Hz
(Gleeson et al., 1993;
Goldman and Koehl, 2001). When
odors from food were present, the lobsters flicked much quicker, with measured
flicking frequencies up to 3.5 Hz. Velocities and Re of the
aesthetascs during the flick downstroke and upstroke were measured by Goldman
and Koehl (Goldman and Koehl,
2001). For both undisturbed lobsters and those that smelled food
odors, average peak velocities were measured at
0.09±0.01ms–1 during the downstroke flick, with a mean
velocity of 0.06±0.01ms–1. During the upstroke return,
mean velocity was 0.02±0.01 m s–1 (N=15
individuals). The average duration of the downstroke flick was 0.10 s, while
the upstroke was more variable in duration, but on average lasted 0.34 s.
Using the dimension of the aesthetasc hair as the length-scale, the Reynolds
number for the maximum speed during the downstroke was
Re=2±0.4, with a mean Re=1±0.5. During the
upstroke, the mean Re=0.5±0.3. These Re values did
not vary significantly with carapace length. Since the aesthetascs of the
antennules operate at a range of Re values of order 1, the amount of
fluid passing through the array of aesthetasc hairs should be sensitive to
speed and hair spacing and may enhance their ability to take discrete water
samples with each flick (Koehl,
1995).
Morphology of antennule
The morphology of the P. argus antennule has been described in
detail for both adults and juveniles in Goldman and Koehl
(Goldman and Koehl, 2001). The
scaled model used in our study was based on the characteristics of a flicking
adult lobster whose mean antennule width is 1 mm and aesthetasc hair diameter
is 22 µm. The rows of aesthetasc hairs are characterized by having an
average density of 10 hairs per row and aligned in a zig-zag pattern at the
tips of the aesthetascs. The aesthetascs do not point directly into the flow
but are oriented at a mean angle of 32°±4° to the flow during
the downward flick, and during the upward return stroke are at an obtuse angle
of 148°±4° to the flow as the antennule moves in the opposite
direction from that of the flick (shown in
Fig. 2B). For all measured
antennules in Goldman and Koehl (Goldman
and Koehl, 2001), the morphologic parameters such as aesthetasc
size, spacing and orientation did not vary significantly with respect to
carapace length, suggesting that these parameters were maintained over a range
of body sizes.
Dynamically scaled physical models
Dynamically scaled physical models are useful tools for studying fluid flow
around biological structures that are too large or small to be easily measured
in the laboratory. If the biological structure and model are geometrically
similar and their motion is characterized by the same Reynolds number, then
the ratios of the velocities and the forces in the fluid around the model and
the real structure are the same (Loudon et
al., 1994; Mead et al.,
1999). Physical models also permit the morphology and the
kinematics of the structure to be modified so that their consequences to fluid
flow around the structure can be explored.
Objectives
We used large dynamically scaled physical models of the lateral flagellum
of the olfactory antennule of a spiny lobster, Panulirus argus, to
determine how the kinematics of flicking and the morphology of the antennule
affect flow patterns through the array of chemosensory aesthetascs on the
antennule. The specific questions we addressed were:
These fluid flow data not only enable us to assess ways in which antennule
morphology and motion affect how such an olfactory organ samples the
surrounding water, but also provide the flow velocity fields necessary for
future development of a three-dimensional mathematical model of odor transport
via advection and molecular diffusion to the surfaces of aesthetascs
(e.g. Stacey et al., 2002) to
determine how flicking affects the kinetics of odorant arrival at these
chemosensory hairs.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Relevant morphological and kinematic parameters of the
model and real antennule are compared in
Table 1. The antennule model
was made out of modeling clay (Sculpey© compound, Polyform Products Co.,
Estes Elk Grove Village, IL, USA), while the aesthetasc and guard hairs were
made out of borosilicate glass (Pyrex©, Corning Inc., Lowell, MA, USA) by
heating and then shaping the glass to the correct geometry. Once shaped, the
hairs were embedded into the clay compound and then kiln dried. For real
antennules, no flexing of the guard hairs have been reported during a flicking
sequence, whereas for the aesthetascs, Gleeson
(Gleeson et al., 1993) reported
that only a very slight deflection occurs at the tip (
2.5%) during a
flick. Therefore, we constructed our model from materials that are
structurally rigid and do not flex during typical flicking behavior.
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Experimental apparatus
The tow tank in which experiments were performed was a 250 l tank (100 cm
long, 50 cm wide, and 50 cm tall) filled with mineral oil
(Fig. 4). The mineral oil had a
viscosity of 0.049 Pa s, measured to the nearest 0.002 Pa s with a viscometer
(Brookfield Inc., Middleboro, MA, USA) at 25°C. The density of the mineral
oil was 840 g l–1. The mineral oil was seeded with 11 µm
silver-coated hollow glass spheres (Potter Industries, Malvern, PA, USA),
which were slightly denser than the mineral oil, but sank at a velocity less
than 1 mm s–1. Since most of the experiments lasted less than
30 s, the sinking of particles did not have any measurable effect on the
velocity calculations. The model was towed along the long axis of the tank
using a programmable stepper-motor (Daedal Inc., Irwin, PA, USA single-axis
microstepping positioning system MC6023) attached to a rail traverse (for
details, see Loudon et al.,
1994). The speed of the stepper-motor, and thus the towing speed
of the model could be controlled by voltage signals sent from a computer. A 20
cm wide by 3 mm thick laser sheet was generated using an array of seven 670 nm
laser diodes with an output power of 7 mW each (World Star Tech, North York,
ON, Canada). Attached to each laser was a 30° cylindrical beam expander to
create the 3 mm thick light sheet. These lasers were aligned horizontally
along a rigid plate and mounted to an adjustable microscope stand which could
be adjusted vertically to an accuracy of 0.2 mm. The tank of mineral oil was
located in a temperature-controlled room away from windows and the temperature
was monitored each day to ensure that the density and viscosity of the oil
remained constant. Before each experiment, the oil in the tank was stirred to
ensure an even suspension of particles, and the fluid was allowed to come to
rest so that no fluid motion in the tank occurred before the start of the
experiment.
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Since this experiment was conducted within an enclosed tank, side walls can
affect the flow around low Reynolds number objects even when they are many
diameters away from the side walls (Loudon
et al., 1994). To ensure minimal interaction with the walls of the
tank, particle velocities next to the wall were imaged during the forward and
return strokes of the model. No flow interaction with the wall was observed
indicating that wall interaction with the model was minimal. As a further
test, a rule of thumb for estimating when wall effects can be ignored
(Vogel, 1994) is:
 | (2) |
is the kinematic viscosity of the fluid. For our
experimental setup, L=0.04 m (diameter of the antennule),
U=0.058 m s–1 (slowest towing speed of model, during
the return stroke), and =5.8x10–5 m2
s–1. For the diameter of the antennule, the model needs to be
2 cm away from the wall for wall effects to be safely ignored. Our model was
at a minimum y=15cm away from either wall, indicating that wall
effects were negligible. In order to make velocity measurements within the aesthetasc hair array using particle image velocimetry it was essential to have a direct line-of-sight from the laser light sheet to the camera. To obtain this, the aesthetasc and guard hair array of the model was constructed specifically from Pyrex® glass because it has an index of refraction of 1.47. This matches the index of refraction of mineral oil (1.46) which made the model fully transparent within the mineral oil such that no refraction of emitted light from the laser beams between the oil and glass model occurred. The guard and aesthetasc hair arrays were essentially `invisible' within the mineral oil.
The model was towed at a velocity to match the Re of the real
antennule during the flick and return strokes (with a mean peak
Re=2.0 during the flick and Re=0.5 during the return). The
mean aesthetasc diameter of the model was 1 mm, which was used as the
characteristic length-scale for Re scaling
(Eqn 1). The model was towed at
14.5 cm s–1 in the forward motion to obtain a Re=2.0
for the flick stroke, and at 3.5 cm s–1 for the return stroke
to obtain Re=0.5. Image recordings were only made when the model was
towed within the center of the tank, minimizing the effects of the end wall
(Loudon et al., 1994).
Images were obtained at 60 frames per second using a Redlake MotionScope
PCI 1000s camera (Redlake Inc., Tucson, AZ, USA) mounted directly above the
tank and attached to a motorized traverse. Each image had a resolution of 480
by 420 pixels. Images were processed using particle image velocimetry (PIV)
software (MatPIV 1.6.1) written for Matlab®
(Sveen, 2004) from a PIV
method developed by Cowen and Monismith
(Cowen and Monismith, 1997).
This software divided each frame of each run into an array of `interrogation
sub-windows' and calculated the most probable displacements of particles in
successive pairs of frames using cross-correlation analysis. The final output
from the software produced a horizontal and vertical velocity estimate for
every 8 by 8 pixel sub-window, giving 59 by 51 velocity measurements per image
pair. For each towed experiment we collected 31 images across a transect,
generating 30 image pairs. Each experiment was repeated three times for a
total of 90 distinct image pairs in which velocities were computed. Means and
standard deviations are reported using these 90 independent velocity
measurements. To determine spatial variability of velocities within the
aesthetasc array, multiple transects were made by adjusting the location of
the laser sheet relative to the model in 1 mm increments. In total, 20
transects were conducted spanning a 20 mm distance along the length of the
aesthetasc model.
Accuracy of the PIV measurements was estimated by towing the camera at known speeds with no antennule model attached. For the framing rate used, the accuracy of the velocity measurements were found to improve with slower particle motions. Overall, the relative accuracy of reported velocities, U, are ±6%. Velocities were obtained scaled to the antennule model. All velocities and size scales reported herein have been re-scaled to match the actual velocities and dimensions of a real flicking lobster antennule.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Within the zig-zag pattern of the aesthetasc hair array, the highest flow occurs near the tips of the hairs, with peak velocities of 1.4 cm s–1. Further within the aesthetasc array, the magnitude of the flow depends upon the proximity to the rows of aesthetasc hairs. Averaged over the entire length of the hair array, the mean flow is 0.24±0.06cms–1. During the return stroke (Fig. 5B) the average flow within the aesthetasc hair array is 0.01±0.005 cm s–1, allowing for essentially zero net transport of fluid out of the hair array during the time period of the return stroke. No net flow occurs along the ventral side of the guard hairs due to the combined effect of flow blocking by the antennule and guard hairs. The only flow within the region encompassed by the guard hair array occurs along the dorsal edge, with a magnitude of 0.9±0.1 cm s–1.
Owing to the zig-zag pattern of the aesthetasc hair array, the velocity structure during a flick appears non-uniform along a transect that is perpendicular to the antennule (Fig. 6). The 3D geometry is angled, however, such that the pattern of the zig-zag alternates from the base to the tip, i.e. the zig-zag pattern is arranged so that locations with open gaps at the base of the hairs have closed gaps at the tips, and vice versa. Fluid flow within the hair array forms a boundary layer with highest flow that coincides along the center of the gaps and the slowest flow coincides with regions that are adjacent to the rows of hairs (Fig. 7). Within the interior of the aesthetasc array, a uniform velocity of 0.24±0.1 cm s–1 occurs at the center of the gaps between the rows of hairs, whereas adjacent to the hairs viscous interaction reduces the magnitude of flow to 0.10±0.06cms–1. Near the tips of the hairs, flow increases both along the gaps and adjacent to the hairs.
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), a
simple multiplication of the mean flick speed by the duration of the flick
indicates that this flick duration would need to be 1.9 s for a
Re=0.5 and 0.8 s for a Re=1.0 flick to fully exchange the
water mass contained within the hair array. This compares with 0.1 s for a
natural flick at Re=2.0. The distance over which the antennule would
need to flick over this time period to completely exchange the entrained fluid
would be 4.1 and 3.5cm for the Re=0.5 and 1 flick, respectively.
Using a value of 0.24±0.06 cm s–1, measured for the
natural flicking Re=2.0, an excursion length of 0.8 cm is needed.
This is similar to the actual measured flick distance of P. argus of
between 0.7 cm (Goldman and Patek,
2002) and 0.87±0.05cm
(Gleeson et al., 1993). For
flicking speeds faster than Re=2, flow within the hair array
increases dramatically, more than doubling the within-array velocity to
>0.5 cm s–1 for Re=2.5. For a flicking regime of
Re=2.5, if the antennule were to hold constant the distance over
which it flicked its antennule, more than twice the amount of fluid exchange
would occur within the array than would be necessary to capture a distinct,
new parcel of water.
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The return stroke occurs at a Re of 0.5 and produces a mean flow within the aesthetasc array of 0.01±0.005 cm s–1. If the return stroke occurs at the same velocity as the flick, at Re=2.0, the mean flow is 0.06±0.005cms–1. This signifies that the flick generates four times the flow through the aesthetasc hair array than does the return stroke at the same Re=2. The difference is primarily due to the orientation of the hair array during the forward and return strokes. During the flick, the hairs are oriented towards the flick direction into the flow, whereas during the return stroke, the hairs are sheltered behind the antennule.
Effects of orientation angle of the aesthetasc array on flow
The aesthetascs are aligned in a ventrolateral position along the antennule
at an angle 32° to the main flick direction (schematic shown in
Fig. 2B). This angle has been
hypothesized to direct fluid flow into the aesthetasc array during the flick
(Gleeson et al., 1993). The
effect of this angle on flow penetration into the array was quantified by
changing the angle of the antennule to 0° with respect to the flick
direction (Fig. 9). The peak
flow at the center of the gaps within the hair array is 0.07±0.03 cm
s–1, with an average flow of 0.03±0.01 cm
s–1 near the rows of aesthetascs. This is a 3.5-fold
reduction in velocity through the aesthetasc hair array compared to the
realistic 32° orientation. At a 0° orientation, flow along the tips of
the aesthetasc array is of similar or slightly greater magnitude than the
32° orientation, but the flow does not penetrate into the interior of the
array and no flow occurs along the distal end of the hairs where they attach
to the antennule.
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Effects of guard hairs
To determine the effect of guard hairs on flow within the aesthetasc array,
the hairs were removed from the model and towed in the flick and return
orientation. During the downward flick, the mean peak velocity through the
aesthetasc hair array without the guard hairs is 0.89±0.12 cm
s–1. This is a 3.7-fold increase in velocity compared to when
the guard hairs are in place. Outside of the aesthetasc array but within the
region that the guard hairs would normally occupy, the velocity increases from
4.2 to 8 cm s–1 by removing the guard hairs. During the
return stroke, the mean peak velocity through the aesthetasc array is
0.025±0.001 cm s–1 without the guard hairs, an
increase of 2.5 times compared to flow when the guard hairs are present. The
smaller increase in flow during the return versus the flick stroke
without the guard hairs is probably due to the blocking effect that the
antennule has when the aesthetascs are in the downstream wake of the antennule
during the return.
Flow dynamics at mechanosensors
Mechanosensory hairs (labeled `2' in
Fig. 1B) line laterally along
the antennule, along both the ventral and dorsal outer edges of the guard
hairs. PIV analysis of the flow along the ventral side (near location `1' in
Fig. 5A) indicates that the
mechanosensory hairs are exposed to a mean velocity of 3.9±0.3 cm
s–1 during a flick, while during the return the mean velocity
is 0.04±0.01 cm s–1. Thus, a tenfold variation in flow
occurs at the mechanosensory hairs lining the ventral edge of the antennule.
Along the dorsal side (near location `2' in
Fig. 5A) during the forward
flick, the mechanosensory hairs are exposed to a velocity of
0.8±0.2cms–1, whereas during the return, a mean
velocity of 1.0±0.1 cm s–1 is encountered. These
velocities act in opposite direction depending on the direction of antennule
movement, but the magnitude of the velocity is essentially the same at this
dorsal location. This is due to the offset orientation of the aesthetascs,
which shelters the mechanosensory hairs from the main flow during the downward
flick, but exposes the mechanosensors to flow during the upstroke phase.
If comparisons are made along the opposite dorsal–ventral sides of the antennule where mechanical sensors are located, the kinematics of the flick creates a fivefold difference in the flow rate. If the Re of the downward flick stroke is changed from a Re=2 to Re=1, the flow rate on the ventral side is 1.15±0.1cms–1, while on the dorsal side, the velocity is 0.1±0.03cms–1. This increases the relative difference between the two locations to almost 12 times. Therefore, because of the orientation of the aesthetasc array, variations in flick speed not only create differences in flow along the aesthetasc array, but also cause changes in flow gradients across the aesthetasc array.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Crimaldi et al., 2002;
Koehl et al., 2001). This
uniform flow distribution is significantly different from that found in
stomatopods (Mead and Koehl,
2000), whose antennules consist of four rows of three aesthetascs
aligned at a 45° angle to the antennular flagellum. During a stomatopod
flick, the main flow penetration into the aesthetasc array occurs at the tip,
while a substantial reduction of flow occurs near the base of the aesthetasc
array. The majority of dendritic segments where the chemoreceptors reside on
the stomatopod aesthetascs are found along the distal portion of the
aesthetasc near the tips, in the region where largest flow occurs
(Mead and Weatherby, 2002).
This is in contrast to the lobster aesthetasc, where the dendritic segments
are found over 80% of the length of the hairs. Our measurements on the
dynamically scaled model indicate that the morphology of the P. argus
antennule allows for increased fluid flow near the base of the hairs,
essentially allowing for a greater surface area available for chemoreception.
The added benefit of this uniform flow is that the physical and temporal
structure of the filaments of odor formed during turbulent transport within
the ambient fluid is not altered significantly when encountered by a flicking
antennule (Koehl et al.,
2001).
Gleeson et al. (Gleeson et al.,
1993) measured the mean duration of a flick to be 113±3 ms,
with the mean excursion distance (as measured from the center of the
aesthetasc tuft) of 8.7±0.5 mm. Measurements obtained on the scaled
model indicate that average distance over which fluid travels in the
aesthetasc array is 0.27 mm if one multiplies the average velocity of the
water within the hair array by the duration of a flick. This value is just
larger than the average width of the aesthetasc row measured at both the base
and the tip of the hair array, of 0.23±0.02 mm and 0.22±0.03 mm,
respectively (Goldman and Koehl,
2001), indicating that during each flick, the entirety of the
fluid held within the hair is exchanged with new fluid. Kinematic variation of
the model has shown that flicking faster or longer exchanges appreciably more
fluid than is necessary to obtain a discrete new sample of fluid, whereas a
slower or shorter flick would not allow for a complete exchange of fluid
within the array.
Since a flicking flagellum rotates relative to a fixed point at the base of
the antennule, the velocity of the flick will vary linearly along the length
of the flagellum. Our model was towed at a velocity and Re
encountered at the midpoint of the aesthetasc hair-bearing region along the
antennule. Locations distal from this location should experience relatively
faster flicking speeds, while locations closer to the base of the antennule
should experience slower speeds with respect to the ambient flow. Goldman and
Koehl (Goldman and Koehl, 2001)
also reported that the tip of the antennule bends as it is moved through the
water such that the relative speed may be faster or slower than the mid-point
of the antennule at a given instant during the flick. They measured peak
speeds of the tip of the antennule to be 0.12 m s–1, compared
with peak speeds at the mid-point of 0.09 m s–1. This
increase in speed will increase the Re for a constant aesthetasc hair
array geometry. However, the antennule tapers near the tip. Although
measurements have not been performed to determine if changes in antennule
diameter also scale with changes to the morphology of the aesthetasc hair
array near the tip, Gleeson et al. (Gleeson
et al., 1993) found that the guard hair spacing does scale
geometrically with antennule width across a range of P. argus
carapace sizes. Whether the increase in flicking speed at the tip is offset by
a decrease in antennule width and thus a corresponding change in aesthetasc
hair geometry to keep Re constant is still unknown.
Importance of morphology to odor sampling
We tested the effects of the guard hairs on fluid transport by removing the
hairs from the antennule model. When this was done, the transport of water
through the aesthetasc array increases to 3.7 times higher than when guard
hairs were present. The guard hairs apparently have the dual role of
protecting the aesthetasc array from damage as well as conditioning the flow
to allow for the correct `leakiness' during a flick and return sequence.
During the return stroke, with the absence of guard hairs the mean flow
through the aesthetasc array increases 2.5 times. The less pronounced increase
during the return is due primarily to the sheltering of the aesthetasc hairs,
which are oriented downstream in the wake of the antennule during the return
stroke.
Altering the orientation of the hair array from a 32° to a 0° offset orientation with respect to flick direction increased flow along the tips of the aesthetascs, but reduced flow penetration into the array. With the 32° orientation, flow along the ventral side of the array was diverted to penetrate perpendicularly into the zig-zag orientation of the aesthetascs, allowing fluid to infiltrate more uniformly along the length of the aesthetasc hairs. At a 0° orientation, flow was diverted around the aesthetascs near the tips and never penetrated appreciably into the inner region, reducing the ability for odor molecules entrained in the fluid to come into contact with the chemosensory surfaces of the hairs.
Odor transport to chemosensory hairs
Flow adjacent to the rows of aesthetasc hairs was less than half that
measured along the centerline of the gaps found between the hairs. This
reduction of flow caused by frictional interaction with the hairs, forming a
boundary layer, limits odor transport to the chemosensory cells lining the
aesthetascs. However, the slower return stroke, and pause before the next
flick, allows odor molecules time to diffuse to the surfaces of the
aesthetascs. During the return stroke, the average velocity within the hair
array was measured to be 0.01cms–1, and no variation in
velocity was measured with respect to location within the array. Goldman and
Koehl (Goldman and Koehl, 2001)
measured the average duration of a return stroke plus pause period before the
next flick occurs to be much more variable than the downward flick stroke. The
return stroke plus pause period lasted between 0.20 and 0.90 s. Under such low
flow conditions, it is hypothesized that the main mechanism for odor transport
to the sensory cells along the aesthetasc hair array is by molecular diffusion
(Koehl, 2001;
Stacey et al., 2002). Most
odors that attract lobsters are composed of amino acids with a molecular
diffusivity (D) of 10–9 m2
s–1 (Lide,
1991). The average root mean squared distance
(xrms) odor molecules would molecularly diffuse over time
t would be xrms=
2Dt
(Denny, 1993). If 0.5 s is
assumed as the mean duration of the return stroke, an odor molecule travels on
average 32 µm over the time period of the return stroke plus pause. The
average spacing between arrays of aesthetasc hairs of an adult P.
argus lobster (Goldman and Koehl,
2001) was measured to be 53µm at its narrowest and 196 µm at
its widest location, with a mean gap width of 125 µm. This indicates that
given a uniform distribution of odor molecules, up to 25% of the odor
molecules entrained within the hair array should be molecularly fluxed to the
aesthetasc surfaces during the time period of the return stroke.
Lobsters in their natural habitats are exposed to ambient water flow. Although flicking behavior of P. argus exposed to ambient water currents has not yet been quantified, such behavior has been studied in the stomatopod, Hemisquilla ensiguera. Hemisquilla changed the velocity of their flicking so that the net water velocity relative to the tip of their antennule (the vector sum of the ambient current and the water flow past the antennule tip due to flicking) maintained the Re of the rapid stroke of the flick (K. S. Mead, personal communication). Blue crabs, Callinectes sapidus, when exposed to ambient flow that exceeded the speed of their flick, ceased flicking and simply extended their antennules with the aesthetascs facing into the main direction of flow (M. Martinez, U. Lee and M.A.R.K., unpublished).
Integration of hydrodynamic and odorant signals
Crabs, lobsters and crayfish all detect odorants using antennules that bear
both chemoreceptive and mechanoreceptive sensilla
(Steullet et al., 2002;
Mellon, 2005;
Mellon, 2007). Much work has
been done on the neurobiology of chemoreception in lobsters (reviewed by
Schmidt, 2007), and recent
studies have begun exploring how olfactory and hydrodynamic signals are
processed and integrated in the brain
(Mellon, 2007). For example,
research on crayfish has shown that initiation of water movement past the
antennular lateral flagellum evokes responses in the crayfish brain that
enhance the chemosensory signal (Mellon
and Humphrey, 2007), indicating that multimodal integration of
chemical and mechanical information occurs in the neurons of the crayfish
brain. Our measurements of water velocities relative to the mechanosensory
hairs along the sides of the lateral flagellum of the P. argus
antennule show distinct differences between the flow they encounter during the
rapid flick downstroke, and the slower return stroke. Rapid water motion past
the mechanoreceptors on the lateral flagellum of the antennule during each
flick downstroke can serve as an indicator that a new sample of water has just
been taken from the environment. Although hydrodynamic studies make it clear
that flicking (1) increases the rates at which odorant molecules reach
chemosensory sensilla, and (2) permits the animal to take odor samples that
are discrete in space and time, further research is still needed to determine
the extent to which hydrodynamic and olfactory sensory modalities are combined
to affect both the neurobiology and behavior of lobsters when detecting odors
in natural environments.
LIST OF ABBREVIATIONS
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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