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First published online November 19, 2007
Journal of Experimental Biology 210, 4083-4091 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.008664
The flow generated by an active olfactory system of the red swamp crayfish
1 Fluid Dynamics Laboratory, University of Hull, HU6 7RX, UK
2 Department of Biology, University of Hull, HU6 7RX, UK
* Author for correspondence (e-mail: p.denissenko{at}gmail.com)
Accepted 3 September 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: chemical sensing, crayfish, PIV, flow measurement, biomimetics
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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) but is
inefficient at transporting olfactory information to animals over distances
longer than a few millimetres (Dusenbery,
1992; Weissburg,
2000). Large aquatic animals such as crayfish rely on the
information extracted from macroscopic odour plumes. These plumes form
downstream of the odour source by advection and turbulent diffusion (Balkovsky
and Shraiman, 2002).
Animals can orientate towards an odour source by following the mean
direction of the flow carrying odour molecules (odour-gated rheotaxis) or by
evaluating parameters of the turbulent odour plumes
(Vickers, 2000;
Weissburg, 2000). Lobsters,
crabs and crayfish have been shown to navigate towards odour sources using a
combination of these strategies (Atema,
1996; Moore and Grills,
1999; Weissburg and
Zimmer-Faust, 1994; Grasso and
Basil, 2002).
Animal orientation under still water conditions such as in ponds, lakes, caves, or during slack tide, has been less studied. In aquatic environments with little or no ambient water movement, the flow created by an animal itself could help in odour acquisition and orientation. Understanding the active olfactory mechanisms of crayfish inhabiting stagnant waters requires consideration of the flow patterns created by an animal and the transport of odour stimulus to the chemoreceptors. This knowledge can be applied to the design of a robot searching for chemical sources under stagnant water conditions.
Crustaceans are well known for their ability to create directed water
currents by pumping and fanning appendages
(Herberholz and Schmitz, 2001;
Atema, 1985;
Budd et al., 1979;
Burrows and Willows, 1969;
Brock, 1926). Different
appendages can create distinct currents. For example, gill currents ventilate
the gills, abdominal swimmeret currents aid in locomotion, and it has been
suggested that currents created by the anterior fan organs can be used for
odour acquisition and chemical signalling
(Breithaupt, 2001).
The fan organs of a crayfish consist of the flagellae of the three
bilateral maxillipeds. As shown in Fig.
1A, fan organs are located below the frontal sensory organs
including the antennules, which constitute the major chemoreceptors in decapod
crustaceans. The distal part of the multi-segmental flagella bears a dense,
single-layered array of feathered hairs emerging on either side of the stem
(Fig. 1B). During a power
stroke the hairs are erect; during a recovery stroke the hairs are tilted and
the stem is flexed in order to reduce the drag
(Fig. 1C). The fan organs can
be used for chemical communication by generating a forward directed jet
(Breithaupt and Eger, 2002;
Bergman et al., 2005), or for
odour acquisition by drawing water towards the head region
(Breithaupt and Ayers, 1998;
Breithaupt, 2001). In decapod
crustaceans, odour stimulation generally initiates fanning activity
(Atema, 1985;
Brock, 1926). Crayfish
(Astacus leptodactylus) were observed to increase the time spent
fanning from about 50% to more than 90% of their time when encountering an
odour plume (T.B., unpublished data). Inactivating the fan organs causes a
dramatic decrease in their success in finding an odour source, indicating that
fan organs are essential for chemo-orientation in still waters (T.B.,
unpublished data).
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In order to test a proposed mechanism for active odour acquisition we
designed a mechanical model, an assembly of nozzles, simulating the flow
pattern by producing the jets. The model enabled us to reproduce various
velocity fields observed in crayfish. Behaviour of crustaceans has been used
to develop algorithms for autonomous robots searching for chemical sources
(Grasso, 2001;
Ayers, 2004;
Ishida et al., 2006;
Martinez et al., 2006). Active
generation of flow might help to locate chemical sources in a still
environment. Our model can be used as a prototype design of robots orienting
by chemical cues.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Edwards, 1984) photoreceptors
were stimulated by the light scattered by the animal's translucent body. To simulate the flow generating mechanism involved in chemoreception of the crayfish we designed a mechanical model, a closed loop pump–nozzle assembly with one inlet and two outlets, as sketched in Fig. 4B. The assembly mimics the far field flow, initiated by the jets that are generated by the fan organs, preserving the amount of water involved in the motion. Fluid mass conservation is achieved by feeding the outlet nozzles with the fluid pumped from the sink via a closed loop. As in live crayfish, an inflow replaces the fluid drawn in by the sink and subsequently ejected as jets, and the fluid entrained by the jets. The nozzle assembly allows generating horizontal sideward jets, jets directed 45° backwards and jets directed 45° upwards, and was built to match the size scale of a crayfish. Velocity of the flow induced by the model was measured using the same PIV arrangements as for the crayfish and the flow rate through the nozzles was adjusted to make the magnitude of the inflow velocity close to that observed in experiments with live animals.
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Results |
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;
Koehl, 2006). Flicking
occurred at multiple heights as the antennules were slowly swept downwards.
Flicking and downward sweeping occurred only rarely when the animals were not
fanning, indicating the close link between fanning and olfactory sampling. The
animals occasionally walked on the treadmill while waving the fan organs, but
most of the time their walking legs were steady. The outward jets induce an inflow converging towards the fan organs and the jets themselves. A typical flow field measured by PIV in the vertical plane is shown in Fig. 5. Note that the antennules are lowered in front of the fan organs, thereby exposing olfactory receptors to the incoming flow. The streamlines in Fig. 5 are more or less horizontal at the level of fan organs, which suggests that one can study the horizontal inflow structure by measuring the velocity field at this height. Examples of the flow field measured in the horizontal plane are shown in Fig. 6. Since the instantaneous velocity field (Fig. 6A) appears too irregular, we use the averages over the 30 sequential images. Visual observation shows that the crayfish changes its fanning behaviour over a timescale of minutes, so we used the 30 s average to illustrate the actual range of the odour attraction. The streamlines leading to the animal chemoreceptors illustrate that the sector of odour attraction may vary. The jets were out of the plane of measurement in most of the experiments with live animals, which may create an illusion of breaking the conservation of fluid mass.
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Since odour tracking is a time-dependent process, we investigated how long it takes for the inflow pattern to adjust to a changed configuration of the jets. Experiments with the flow-through nozzles switched on from rest showed that the steady flow field is stable within several seconds after starting the pump.
To assess the range of odour acquisition, the flow velocity as a function
of distance from the fan organs/sink along the streamlines (broken lines in
Fig. 6A–D and
Fig. 7A–D) is plotted for
the live animal in Fig.
8A–D and the mechanical model in
Fig. 9A–D. The slopes of
the plots show that the flow velocity is somewhat inversely proportional to
the distance from the fan organs, i.e.:
 | (1) |
 | (2) |
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5 mm s–1 at
s010 mm (as in Fig.
8B), we can infer that an odour patch located 100 mm away from the
crayfish fan organs would reach the chemoreceptors in approximately 100 s.
This time interval increases quadratically with L, rising to
approximately 4 min for a distance of 150 mm. For comparison, solution of the
diffusion equation for the point source [(for example, see
Batchelor, 2000), p.187] shows
that the characteristic time of molecular diffusion at a distance of 100 mm is
measured in days.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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The most important fact revealed by the PIV measurements is a surprisingly
slow decay of the inflow velocity with the distance from fan organs, as
plotted in Fig. 8. The slow
decay is explained by a fluid entrainment by jets. Indeed, if the entrainment
were insignificant and the inflow were formed only by a point sink at the
location of fan organs (the origin of jets), one would expect the inflow to be
spherically symmetric [(see Batchelor,
2000), p. 89]. In that case the flow velocity would decrease as
the inverse square of the distance from the fan organs, and the travel time
T for the odour patch to reach the crayfish chemoreceptors
(Eqn 2) would be proportional to
the third power of the distance L to the odour source. This would
increase the travel time to 10 min for the distance of 100 mm and to 40 min
for the distance of 150 mm, indicating efficiency of the jet-based odour
acquisition mechanism used by crayfish.
Fluid entrainment by a single jet has been described theoretically
(Schneider, 1981). Schneider
showed that a turbulent jet acts as a line sink with respect to the
surrounding fluid. This leads to the axial rather than spherical symmetry of
the flow field, hence to a slower decay of velocity with distance. The
velocity decay is now proportional to the inverse distance from the jet axis
(a line) instead of the inverse squared distance from the sink (a point). The
secondary flow induced by a turbulent jet and decay of the jet itself were
described analytically (Kotsovinos and
Angelidis, 1991). However, the results of this paper cannot be
extended to a case of two jets because the Navier–Stokes equations
governing fluid motion are not linear. Moreover, the relatively weak jets
created by a crayfish cannot be considered as fully developed turbulent jets,
and the presence of a rigid boundary, the bottom of the tank, affects the
flow. The above argument suggests employment of direct numerical simulation to
model the flow induced by the jets. However, simulation of a system of jets is
a problem on its own, so in the present study we do not investigate the inflow
structure any further. We merely observe that the range of odour acquisition,
i.e. the range in which the inflow rate decreases slowly with the distance, is
defined by the jet length (Fig.
4A), and that the jet length may exceed 10 cm as the jet
visualization has shown.
To produce continuous jets as visualized in
Fig. 3, a row of the three
exopodites is located on each side waving with the phase shifts of 120°
(Breithaupt and Ayers, 1998).
In contrast, the fanning appendages aimed to produce thrust, the swimmerets,
are arranged to generate a less regular excurrent, which induces suction at
the locus of the appendages and much weaker suction along the extended line
such as the jet axis. Extreme examples of the thrust-producing excurrent with
the minor fluid entrainment are the vortex street produced by a fish
(Sfakiotakis et al., 1999) or
a trail of vortex rings produced by a jellyfish
(Dabiri et al., 2005). The
latter is commonly observed in the form of smoke rings and described in, for
example, Batchelor (Batchelor,
2000), p. 22.
To locate a source of an odour, crayfish need to sense the direction to the
source. In a riverine environment the source is somewhere upstream. In still
water an animal can navigate by comparing the local intensity of the odour at
different locations through the plume
(Atema, 1996). However, the
animal movement may stir up the water and destroy the pattern of odour patches
formed by the source. Walking through the open environment would also increase
predation risks and may be energetically expensive. The crayfish may overcome
these difficulties in scanning the environment by varying the jet pattern,
thereby drawing odour molecules from different directions to its
chemoreceptors (Figs 6,
7). The original pattern of
odour patches is changed by the inflow in such a way that the strongest
chemical signal, i.e. the odour patch washed off from a chunk of food,
approaches the animal from the direction of the food locus. This mechanism of
odour acquisition may significantly reduce predation risks compared to odour
tracking by walking where the crayfish acts as a moving visual target. The
hydrodynamic disturbance created by jets is only detectable from a short
distance (a jet length) and is therefore less conspicuous than a walking
crayfish. When the bottom of a pond or a lake is covered by plants, scanning
the environment with the help of jets also becomes energetically profitable,
since the macrophyte stalks are less of an obstacle to the flow than they are
to a walking crayfish.
To show that production of the jets is energetically affordable, we make an
estimate based on parameters measured by Breithaupt
(Breithaupt, 2001). Consider
six appendages of the area A=10 mm2, each waving with
frequency f=6 Hz, amplitude a=5 mm, and velocity amplitude
u=2
fa20 cm s–1. Water density
=1000 kg m–3 and its kinematic viscosity 
=0.01
cm2 s–1. The Reynolds number of the flow around an
appendage can be estimated as:
 | (3) |
)
p.100], we have:
 | (4) |
 | (5) |
 | (6) |
Observations of an unrestrained crayfish show that it may use the fan organs both when walking and when hiding in a shelter. It suggests that the animal creates the inflow both to assist active search for food and to detect the food appearance in the vicinity of the shelter. To describe the exact way in which the crayfish utilizes the inflow it generates with the fan organs and to find if it uses the swimmerets to alter the flow, behavioural experiments are required involving the unrestrained animals in a large tank.
Experiments with the model (Fig. 7) suggested that the mechanism of odour attraction employed by the crayfish could well be adopted to design devices for finding chemical sources in stagnant fluids. Instead of scanning a region of interest with a probe, fluid from the region can be attracted distantly and driven through a significantly smaller sampling volume. Nozzle assemblies generating one or several jets should be more efficient in drawing distant odour patches to sensors than devices creating a point sink flow. Unlike the live animals, a man-made mechanic assembly has fewer restrictions on the parameters affecting performance of the system. By optimizing nozzle profiles the jets can be made more regular and by increasing the pump power jets can be made considerably longer than those generated by a crayfish. The intensity, the number, and the alignment of jets could be altered to obtain a desirable pattern of the inflow. Placing sensors at different locations around the nozzles would enable determination of the direction to the chemical source. Measurements of the time lag between switching the jets on and arrival of an odour plume would add data about the distance to the source.
With the inflow induced by excurrent jets, the range of odour acquisition and the directional sensitivity of the robot are defined by the length of jets rather than by physical size of the device. This would allow design of a relatively small probe with ability to access the obstructed area of interest. In some cases, induction of the inflow by jets would eliminate necessity of direct access to the area enabling, for example, chemical sensing through the mesh. Probes consisting of a sink, nozzles, and chemical sensors can be employed to search for leaks from oil or gas pipelines, to search chemical sources at the ocean bed, or for non-invasive flow monitoring. The idea is not restricted to the aquatic environment and can be used, for example, for the monitoring of plantations where access to the area of interest is restricted by stalks. A probe producing the inflow can be swept between the plant patches to measure the pesticide content or to sample the pollen.
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Acknowledgments |
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