Escape from viscosity: the kinematics and hydrodynamics of copepod foraging and escape swimming
Department of Marine Biology, University of Groningen, PO Box 14, 9750 AA Haren, the Netherlands
* Author for correspondence at present address: NIOO-CEME/KNAW, PO Box 140, 4400 AC Yerseke, the Netherlands
Accepted 14 October 2002
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Summary |
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High-speed film recordings at 500 frames s-1 of the motion pattern of the feeding appendages and the escape movement of the swimming legs revealed that the two swimming modes are essentially very different. While foraging, the first three mouth appendages (antennae, mandibular palps and maxillules) create a backwards motion of water with a metachronal beating pattern. During escape movements the mouth appendages stop moving and the swimming legs beat in a very fast metachronal rhythm, accelerating a jet of water backwards. The large antennules are folded backwards, resulting in a streamlined body shape.
Particle image velocimetry analysis of the flow around foraging and escaping copepods revealed that during foraging an asymmetrical vortex system is created on the ventral side of the animal. The feeding motion is steady over a long period of time. The rate of energy dissipation due to viscous friction relates directly to the energetic cost of the feeding current. During escape responses a vortex ring appears behind the animal, which dissipates over time. Several seconds after cessation of swimming leg movements, energy dissipation can still be measured. During escape responses the rate of energy dissipation due to viscous friction increases by up to two orders of magnitude compared to the rate when foraging.
Key words: copepod, Temora longicornis, swimming, hydrodynamics, kinematics, escape response, feeding current, Reynolds number regime
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Introduction |
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Temora longicornis Müller is one of the most abundant
copepods in the temperate coastal waters of the Northern hemisphere. It spends
around 99% of its time slowly cruising or hanging nearly stationary while the
feeding appendages are moving (Tiselius
and Jonsson, 1990; van Duren
and Videler, 1995
). We will refer to this type of behaviour as
`foraging'. Velocities during this swimming mode of female T.
longicornis up to 1 mm long typically range between 2 and 6 mm
s-1 (van Duren and Videler,
1995
,
1996
). T. longicornis
is also capable of high velocity escape movements generated by the swimming
legs (Singarajah, 1975
;
Buskey et al., 1987
;
van Duren and Videler, 1996
).
Velocities during this type of swimming have not been accurately measured.
This study aims to investigate the swimming velocities, motion patterns, appendage kinematics and flow characteristics associated with foraging and escaping in T. longicornis and to estimate the energetic cost of both types of swimming behaviour.
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Materials and methods |
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Swimming velocity measurements
The foraging and escape speeds of the copepods were measured in a 3-D
filming setup (van Duren and Videler,
1995). Through a set of mirrors two orthogonal views of an
aquarium (dimensions 10 cmx10 cmx12 cm) were projected into the
lens of a video camera (I2S). The camera was connected to a Sony U-matic video
recorder, running at 25 frames s-1. Illumination was provided by
two high-output infra-red light-emitting diodes. Each light-emitting diode was
placed in the focus of a lens (diameter 10 cm) behind the aquarium, creating a
parallel light beam, which is projected through the aquarium straight into the
lens of the camera. This yields silhouette images with the animals showing as
black dots against a white background.
The resulting tapes were analysed using a computer image analysis system,
which allowed processing of individual fields of video frames, resulting in a
maximum temporal resolution of 50 data points s-1. X, Y
and Z coordinates of the position of the animals in each frame were
used to calculate instantaneous swimming speeds
(van Duren and Videler,
1995).
Prior to the experiments groups of 10 adult females were selected and left in the experimental setup to acclimatise for approximately 15 min.
A 2 s light pulse of 230 µE m-2 s-1 (measured on top of the aquarium) provided by a spotlight (150 W, Philips) mounted above the setup was used to provoke escape reactions without causing any disturbances in the water. The temperature during the experiments was maintained at 15°C.
High-speed film kinematic analysis
A Locam 16 mm high-speed camera (Redlake, model 51) capable of recording up
to 500 frames s-1 was mounted on top of a dissecting microscope.
Adult females were tethered to a very thinly drawn glass pipette using a
suction restraint technique (Gill,
1987; van Duren et al.,
1998
). The pipette was mounted on a micromanipulator, which in
turn was mounted on the base of the microscope. The females were placed with
their lateral side to the camera, and their body axis horizontal with respect
to the camera. Recordings were made at 300 and at 500 frames s-1 of
the swimming movements of the feeding appendages, and the escape swimming with
the pereopods. Escape responses were evoked by a gentle tap on the base of the
micromanipulator holding the pipette with the animal. The size of the
container used for filming was 6x6x4 cm.
The films were subsequently projected on a Vanguard Motion Analyser. Each frame was digitized by recording the projected image with a video camera, connected directly to an image analysis system. The coordinates of the tip position of each appendage involved in the feeding movement: antenna (A2), mandibular palp (Mdb), maxillule (mx1) maxilla (mx2) and maxillipede (mxp), and in the escape response: pereopods 1-4 (p1, p2 etc), were digitised manually.
Particle image velocimetry analysis
A detailed description of the filming set-up and the general experimental
procedure for particle image velocimetry (PIV) experiments can be found in the
accompanying paper (van Duren et al.,
2003). Tethered female copepods were positioned in the light
sheet, with their lateral side towards the camera. The light sheet was
positioned through the centre of the copepod along the rostral-caudal axis,
perpendicular to the antennules. Particle movement around the feeding and
escaping animals was recorded with a video camera (I2S) operating at 25 frames
s-1, fitted with a 35 mm macro lens and a 30 mm extension ring.
Shutter speed was set at 1/125 s. The resulting image covered a field of view
of 8.1 mmx5.9 mm. The camera was connected to a Sony U-Matic video
recorder.
The choice of the temporal resolution was based on the flow velocities. During and immediately after swimming leg movement a 0.02 s time interval was taken, but around the foraging animal and more than 0.2 s after swimming leg movement had ceased, a 0.04 s time step was taken, to ensure sufficient particle displacement between the two images.
Flow fields were calculated from the particle displacements measured in the
subsequent images (Stamhuis and Videler,
1995). These flow fields were expressed in fields of regularly
spaced velocity vectors. The resolution of the flow field (i.e. the size of
the grid cells) was chosen on the basis of the sub-image size of the sub-image
PIV analysis. For the flow fields of these experiments each grid cell
represents a surface area of 0.048 mm2.
Gradient parameters such as vorticity, shear and spatial acceleration rates
were calculated for each cell from the partial derivatives of the x
and y components of the velocity vectors (u and v)
(Stamhuis and Videler, 1995;
van Duren et al., 2003
).
Post-processing
The volume of influence around a copepod was defined as the volume of water
around the animal where the shear rate was more than 0.7 s-1
(van Duren et al., 1998).
By its nature, laser sheet PIV yields two-dimensional results. However,
carefully positioning the animal so that the main direction of flow is
parallel to the laser sheet ensures that the amount of out-of-plane motion is
minimal and the error incurred by ignoring the contribution of this component
is assumed to be very small. Flow around copepods is known to be symmetrical
when viewed dorsally, but when viewed laterally there are significant
differences between the dorsal and the ventral flows
(Fields and Yen, 1993;
van Duren et al., 2003
). Our
images show the lateral view. To estimate the volume of influence, we rotated
the velocity vectors around an imaginary axis similar to that described in van
Duren et al. (1998
).
When a vortex ring was present behind the animal, we calculated a line straight through the centre of this vortex. Although the vortex rings were not always symmetrical, the line where the sign of vorticity changed was always a straight one, parallel to the direction of the jet (Fig. 1). This line was taken to be the centre of the vortex. When no vortex ring was present (e.g. when the animal was foraging), the rotation axis was assumed to run through the feeding appendages of the animal, parallel to the body axis.
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To estimate the volume of influence (Vtot), the flow
field was rotated over +90° and -90°, around the calculated axis. In
other words, we assume the part of the flow field above the rotation axis to
be representative of the flow dorsal to the animal and the part below this
axis to represent the flow ventral to the animal. The total volume of
influence (Vtot) is the sum of the volumes of two half
cylinders, one above and one below the plane through the rotation axis
(Fig. 1):
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Viscous energy dissipation
Within the volume of influence the rate of energy dissipation through
viscous friction (P) can be estimated as:
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During foraging the flow field stays stable over a long period of time. Therefore, the amount of energy the animal puts into the water is balanced by the amount of energy dissipating due to viscous friction. The rate of energy dissipation, calculated by the method described above, is therefore directly proportional to the power delivered by the feeding appendages. During an escape response, a vortex ring is formed. Such vortex rings contain kinetic energy, which eventually also dissipates into viscosity. By calculating the viscous energy dissipation rate in a time series of flow fields, from the start of an escape response until all the effects of the escape movement in the water have dissipated, we can calculate the total amount of energy delivered by the swimming legs. The power delivered by these appendages can be calculated by dividing the total energy loss by the amount of time the swimming legs have been moving.
In some of the flow fields the volume of influence may have been slightly underestimated due to the fact that the area where the shear rate exceeded the threshold level reached further than the field of view. However, the effect on the estimated rate of energy dissipation will have been minimal, since this is largely determined by the peak values in velocity gradients, which do not occur in the periphery of the volume of influence, but were always well within the field of view.
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Results |
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High-speed film measurements
Fig. 3A shows a record of
the X-position of the tips of the five feeding appendages. The
symbols in the graph correspond to the relevant appendages in the drawing of
the copepod above the graph. During feeding the two large antennules are kept
extended and they do not participate in any feeding or swimming movement. The
feeding appendages can be divided into two groups: the antennae, the
mandibular palps and the maxillules, which create the actual feeding current,
and the maxillae and the maxillipeds, which appear to have the function of
filtering and/or grasping particles from the feeding current. The three
anterior appendages beat in an adlocomotory metachronal wave with a phase
angle of 65°, with the power stroke directed backwards. The maxillule
reaches its extreme anterior position before the other two appendages. While
the mandibular palp and the antenna continue their recovery stroke, the
maxillule starts its power stroke. When the maxillule is about halfway between
its extreme positions in the power stroke, the mandibular palp starts its
power stroke, while the antenna continues to complete its recovery stroke.
When the maxillule has reached its extreme position and starts its recovery
stroke, the antenna starts its power stroke. When the mandibular palp reaches
its maximum position, its meets the forward moving maxillule and these
appendages continue their recovery stroke together. They `meet' with the
antenna, when it reaches its extreme position. The three appendages continue
their recovery stroke together for about 2 ms, until the maxillule has reached
its extreme anterior position and the cycle starts again. Meanwhile, the
maxilla and the maxillipede move synchronously, the maxillipede with a much
larger amplitude due to its greater length. The maxillipede generally does not
interfere with the movement of any of the other appendages. The tip of the
maxilla meets the tip of the maxillule when the maxillule reaches its extreme
posterior position. The setae of these two appendages overlap and a small
volume of water is enclosed between the body of the copepod and the setae of
the maxillule and maxilla. When the two appendages separate the setae probably
comb each other, although this was not properly visible on the films. The
maxilla and the maxillipede appear to be beating in opposite phase with the
mandibular palps. The setae on these two appendages are orientated in the
direction opposite to the setae on the first three appendages, and their power
stroke runs from posterior to anterior. Therefore, in terms of power and
recovery stroke they are beating in phase with the mandibular palps.
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The whole cycle of movement takes approximately 0.025 s, and the average beat frequency measured in the six analysed sequences of film was 40.7±8.0 Hz. Fig. 3B shows the tip speed velocity of the antenna. The average maximum tip speed of the largest feeding appendage was 43 mm s-1, in both directions.
At the start of an escape response, the copepods fling the laterally extended antennules backwards and hold them close to the body during the whole time that the swimming legs are moving. No movement of the feeding appendages is visible during an escape response. These extremities do not restart moving until the swimming legs have ceased all movement and have resumed their `foraging' position. Fig. 4A shows a record of the position of the tips of the swimming legs, p1 being the most anterior pereopod and p5 the reduced fifth swimming leg. The position of the tip of the relevant appendages corresponds with the copepod drawing above this graph. This last pair of legs was not clearly visible in all the analysed sequences, but due to its reduced size it probably does not contribute significantly to the total thrust produced.
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The swimming legs are co-ordinated differently from the feeding appendages. The appendages move metachronally only during the power stroke, when the appendages beat in an adlocomotor sequence. The recovery stroke is synchronised. Of the four normal sized swimming legs, p4 is the first to start the power stroke, when it has completed its power stroke and has reached its extreme posterior position, p3 starts and completes its power stroke, then p2 and finally p1. When p1 has reached its extreme position, all four swimming legs start the combined recovery stroke, which is much slower than the individual power strokes. Fig. 4B shows a record of the tip velocity in horizontal direction of p1 (note that negative velocities represent the power stroke, i.e. a backwards movement relative to the copepod). During escape responses we measured beat frequencies of the swimming legs between 44 and 117 Hz.
PIV measurements
Fig. 5A shows a flow field
around a foraging adult female T. longicornis. Highest velocities are
found around the feeding appendages, and in this area the largest velocity
gradients are also found. To the ventral side of the animal is an area of
relatively high vorticity (Fig.
5B); the centre of this vortex system is located just ventral from
the position of the maxillipeds. The flow field does not change over time,
while the animal is foraging.
|
During an escape response, the flow field around the animal changes markedly over time. Figs 6A-D show a sequence of flow fields of a single escape response. Fig. 6A shows the velocity distribution immediately after the start of swimming leg movement (t=0). Fig. 6B shows a similar plot at t=0.08, Fig. 6C at t=0.28 just after cessation of swimming leg movement and Fig. 6D at 0.5 s after the start of swimming leg movement.
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A jet of water starts to develop as soon as the swimming legs start moving. This jet is in the centre of a vortex ring, which is however not clearly shown by the velocity plot. Fig. 7A-D shows the vorticity distribution at the same points in time as the velocity fields. After cessation of leg movement, the vortex ring moves backwards, becomes wide and dissipates altogether within 0.5-1 s.
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In multiple escape responses, the next jump starts before the effects of the previous one are fully dissipated. Fig. 8A,B shows the velocity magnitude and the vorticity distribution 0.04 s after the start of the third jump, 0.08 s after cessation of swimming leg movement of the previous jump.
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The volume of influence, where the animal has a significant influence on the water movement, remains constant at approximately 10 mm3 in foraging animals. During escape responses this changes dramatically over time. Fig. 9A-C shows the change of volume of influence over time in the three escape responses analysed here. The open symbols indicate the points in time where the swimming appendages were moving. In each graph t=0 indicates the time of the first start of swimming leg movement. The maximum volumes reached during escape responses range between 100 and 300 mm3. A copepod of this species, with a metasome length of 0.8 mm, has a volume of approximately 0.06 mm3, so this range corresponds to a volume of 1700-5000 times its body volume.
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The total amount of energy dissipating due to viscous friction in the feeding current of an adult female T. longicornis is approximately 2x10-11 W. This value increases by 2 to 3 orders of magnitude during an escape response. Fig. 10A-C shows the viscous energy dissipation over time for all three animals. Table 1 shows for each animal the total amount of time the swimming legs have been moving, the total amount of energy dissipated into the water over the amount of time the effects of the escape response were visible and the power delivered by the swimming legs. Since in foraging females the power dissipation remains constant over time, the rate of energy dissipation in the water is balanced by the power input of the moving limbs.
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Discussion |
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Limb beat patterns
In both swimming modes propulsion is generated by the metachronal beating
of a group of appendages. Among invertebrates various metachronal rhythms are
widely used (Sleigh and Barlow,
1980). According to these authors, metachronal patterns have two
major functions. Firstly, they ensure that each individual limb can execute
its motion pattern without conflict with neighbouring limbs, and secondly, one
single limb, working as a member of a metachronal system, can move water more
efficiently than an isolated limb. This is supported by the work of Jiang et
al. (1999
); in a model they
varied the distribution of the same amount of total force that a copepod
exerts on the water, and found that by distributing the force over a larger
volume of water, more water was entrained over the feeding appendages at lower
energetic cost.
The metachronal beat pattern of the A2, mdp and mx1 results in a slow
smooth gliding motion, associated with a steady, predictable flow field. Most
crustaceans that have a smooth locomotion pattern achieve this by an
adlocomotory limb beat pattern, with a phase shift between the (pairs of) legs
proportional to the beat cycle divided by the number of limbs
(Barlow and Sleigh, 1980;
Stamhuis and Videler, 1998). An increase in beat frequency often coincides
with a decrease in phase angle (Sleigh and
Barlow, 1980
). T. longicornis has five pairs of feeding
appendages. Based on this total number of limbs a phase shift of 60°.
could be expected, which is close to our measurements of 65°. However,
this phase shift only applied to the three anterior appendages, the ones that
are responsible for the actual propulsive motion. On the basis of three
locomotive appendages, we would expect to find a phase angle of 120°,
which is considerably larger than what we found. It is likely that the
swimming motion of T. longicornis appears to be smooth, despite the
small phase angle between the propulsive limbs, due to the high beat frequency
of these limbs. However, it is possible that the `recovery strokes' of the
maxilla and the maxillipede also contribute to the smoothing of the swimming
motion.
In contrast, the beat pattern of the swimming legs is only metachronal
during the power stroke of the limbs. The successive power strokes are
followed by a synchronous recovery stroke. This system maximises thrust, while
the synchronous recovery stroke reduces the drag of the five pairs of
appendages to little more than the amount of drag that a single pair of legs
would experience during a metachronal recovery stroke
(Morris et al., 1985). The
resulting swimming motion and the associated flow fields are less steady than
the motion produced by the fully metachronal pattern of the feeding
appendages. Some copepods can maintain very high, steady escape speeds for a
certain length of time due to the very high frequency of the swimming legs
(Yen and Strickler, 1996
).
Those copepods, such as Cyclops scutifer, which use the swimming legs
for routine swimming show a characteristic `hop and sink' motion
(Strickler, 1975
).
The difference in locomotory pattern between the two groups of appendages
indicates a difference in nervous locomotor control
(Sleigh and Barlow, 1980)
between the sets of appendages.
The metachronal movement of the swimming legs of T. longicornis is
very similar to that of other copepods
(Strickler, 1975;
Alcaraz and Strickler, 1988
;
Morris et al., 1990
). Morris
et al. (1990
) analysed and
modelled the swimming movements of Acanthocyclops minutus, a copepod
only slightly smaller than T. longicornis, which swims with jumps,
created using its swimming legs, similar to the escape movement of T.
longicornis. They tested the effect of different parameters on their
model predictions. Increasing the viscosity of the fluid medium decreases the
jump distance, while increasing the density of the medium had the opposite
effect; i.e. the higher the Reynolds regime, the more effective this
propulsion system.
Flow characteristics
The conclusion that the two systems are designed to operate under different
flow regimes is matched by the observed flow phenomena in the water. The flow
field around a foraging T. longicornis is purely laminar. The flow
field is also stable over a period of time and the rates of laminar shear in
the feeding current are generally higher than the shear rate due to turbulence
in its environment (Saiz and
Kiørboe, 1995; van
Duren et al., 2003
). The stability and predictability of its
hydrodynamical surroundings allow the copepod to use chemo- and
mechanoreception to gain information about the nature, size, quality and
distance of objects and organisms in its vicinity
(Andrews, 1983
;
Légier-Visser et al.,
1986
; Granata and Dickey,
1991
; Yen and Strickler,
1996
).
The wake of an escaping copepod reaches much further. Our experiments
indicate that the volume of influence increases 100- to 300-fold and a
distinct vortex ring appears behind the swimming legs, similar in shape but
larger in magnitude and intensity than the vortex ring reported by van Duren
et al. (1998) behind a hopping
copepod. The feeding current also contains an area of higher vorticity close
to the feeding appendages, but no vortex rings occur. Vortex rings are
strictly associated with higher Reynolds number regimes
(Vogel, 1981
).
In examining the flow phenomena around swimming copepods with the
techniques described above, we have to take into account that the animals were
tethered in order to keep them and their wake in view and in focus. When an
animal is tethered, instead of moving its body through water, it moves water
past its body. Although tethering does not affect the behaviour or the
appendage movement of a copepod (Hwang et
al., 1993), it can increase the volume of influence of an animal
(Emlet, 1990
). For foraging
copepods in this study, as well as for the hopping copepod described in van
Duren et al. (1998
), the
effects were probably fairly minimal. Copepods create a feeding current to
draw a large volume of water over their feeding appendages, and in fact use
their body drag and negative buoyancy as a `natural tether'
(Strickler, 1982
). Similarly,
the hops described by van Duren et al.
(1998
) are probably created to
give a hydromechanical signal. This movement is designed to shift a bulk of
water, without displacing the animal very much. Escape responses, on the
contrary, are designed to move an animal as fast and as far as possible away
from danger, and in this case we cannot ignore the effects of the tether on
the flow morphology and on the volume of influence. Yen and Strickler
(1996
) filmed the wake of free
swimming Euchaeta rimana using a Schlieren optical path. They found
that both an adult female and a smaller copepodid shed vortices in their wake
with the same frequency as that of the swimming leg oscillations. This is
almost certainly also what happens in the wake of an escaping T.
longicornis. Because the copepod is tethered in our study, the body of
the animal does not move away from the vortex and the next oscillation of the
swimming legs effectively `feeds' the already existing vortex ring behind the
animal. Only when the animal executes a few consecutive jumps, with a resting
period of several tenths of a second inbetween, can we discern multiple
vortices.
Energetics
T. longicornis moves its feeding appendages nearly 100% of the
time. During feeding, the copepods in this study lost
1.1-3.0x10-11 W due to viscous dissipation. Berner
(1962) measured an average
oxygen uptake of 0.0323 µl O2 copepod-1
h-1 at 15°C. Taking an oxycaloric value of 1 ml
O2=20.1 J (Videler,
1993
), this would amount to a total energy use of
1.8x10-7 W, indicating that the cost of the feeding current
would be 0.0061-0.017% of the total energy budget. However, it would be
unrealistic to assume that copepods can transfer metabolic energy into water
movement without any losses along the way. Losses will occur because the
mechanical efficiency of the motion of the moving limbs (
p)
and the efficiency with which muscles transfer chemical energy into kinetic
energy (
m) will both be less than 1. Total swimming efficiency
(
tot) can be calculated as:
![]() | (6) |
Our study finds that the power delivered by the swimming legs during an
escape response is 60-400 times higher than the mouth parts deliver while
creating the feeding current. This is close to the figure mentioned by
Strickler (1975,
1977
), who argued that the
energetic costs of high speed evasive movements would be 400-fold higher than
the normal hop-and-sink swimming method of Cyclops scutifer. The
behavioural experiments of van Duren and Videler
(1996
) indicated that, under
their standard experimental conditions (presence of food, absence of
kairomones or pheromones, no water movement), female T. longicornis
escaped with a frequency of 0.3 jumps min-1 or 18 escape responses
an hour. Assuming a mean leg movement duration of 0.2 s per escape response,
this would result in a total mean swimming leg movement of 3.6 s per hour, or
0.1% of the animal's total time budget. Again, assuming the same values for
p and
m, this would translate into a total
energy expenditure of between 2.3x10-11 and
1.1x10-10 W or 0.01-0.06% of the total energy budget. In the
experiments of van Duren and Videler
(1996
) male T.
longicornis, tested under the same circumstances, showed a fivefold
higher escape frequency than the females. If females increased their escape
frequency to this level, the increase of their energy consumption would be
0.07-0.3%. It appears therefore that only a very extreme increase in escape
frequency may start to have a significant effect upon the energy budget of
this species. This does not altogether mean that energy expenditure will never
be an issue in copepod escape behaviour. Copepods often seem to fatigue after
a number of escapes, e.g. after a number of successive attacks by a fish. The
much higher energy demand of escape swimming could possibly lead to a
short-term power transformation limitation even if the energy demand does not
have an impact on the total budget.
Alcaraz and Strickler (1988)
calculated that the routine hop and sink swimming of C. scutifer,
performed with the swimming legs, accounted for 0.069% of its total energy
budget. This is remarkably close to our estimates of the impact of the cost of
the feeding current of T. longicornis, despite large differences in
the way the two movements are created. Perhaps this relatively low cost of
swimming can provide an explanation for the large variability of routine
swimming and feeding movements among copepods. Optimising food intake is more
important than minimising energy expenditure. Any extra cost involved in a
change of swimming motion to facilitate food capture is not going to have a
great impact on the total energy budget. Escape swimming, on the other hand,
should by its very nature optimise the transfer of metabolic energy into
forward motion. This may explain the fact that we find very little variation
in escape kinematics among different copepod species.
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Acknowledgments |
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References |
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Alcaraz, M., Paffenhöfer, G. A. and Strickler, J. R. (1980). Catching the algae: A first account of visual observations on filter feeding calanoids. In Evolution and Ecology of Zooplankton Communities. Special symposium American Society of Limnology and Oceanography, 57 edn. (ed. W. C. Kerfoot), pp.241 -248. Hanover: University Press of New England.
Alcaraz, M. and Strickler, J. R. (1988). Locomotion in copepods: pattern of movements and energetics of Cyclops.Hydrobiologia 167/168,409 -414.
Andrews, J. C. (1983). Capture enhancement by deformation of the active space in the low reynolds number feeding current of calanoid copepods. Can. J. Fish. Aq. Sci. 40,1293 -1302.
Barlow, D. I. and Sleigh, M. A. (1980). The propulsion and use of water currents for swimming and feeding in larval and adult Artemia. In The Brine Shrimp Artemia, 12545 edn. (ed. G. Persoone, P. Sorgeloos, O. Roels and E. Jaspers), pp.61 -73. Wetteren: Universal Press.
Berner, A. (1962). Feeding and respiration in the copepod Temora longicornis (Müller). J. Mar. Biol. Assn. UK 42,625 -640.
Buskey, E. J., Mann, C. G. and Swift, E. (1987). Photophobic responses of calanoid copepods: possible adaptive value, J. Plankton Res. 9, 857-870.
Emlet, R. B. (1990). Flow fields around ciliated larvae: effects of natural and artificial tethers. Mar. Ecol. Prog. Ser. 63,211 -225.
Fields, D. and Yen, J. (1993). Outer limits and inner structure: The 3-dimensional flow field of Pleuromamma xiphias (Calanoida: Metrinidae). Bull. Mar. Sci. 53, 84-95.
Gill, C. W. (1987). Recording the beat pattern of the second antennae of calanoid copepods. Hydrobiologia 148,73 -78.
Goldspink, G. (1997). Muscle energetics and animal locomotion. In Mechanics and Energetics of Animal Locomotion (ed. R. M. Alexander and G. Goldspink), pp.57 -81. Chapman and Hall.
Granata, T. C. and Dickey, T. D. (1991). The fluid mechanics of copepods feeding in a turbulent flow: A theoretical approach. Prog. Oceanog. 26,243 -261.
Hwang, J. S., Turner, J. T., Costello, J. H., Coughlin, D. J. and Strickler, J. R. (1993). A cinematographic comparison of behavior by the calanoid copepod Centropages hamatus Lilljeborg: Tethered versus free-swimming animals. J. exp. mar. Biol. Ecol. 167,277 -288.
Hwang, J. S., Costello, J. H. and Strickler, J. R. (1994). Copepod grazing in turbulent flow: elevated foraging and habituation of escape responses. J. Plankton Res. 16,421 -431.
Jiang, H., Meneveau, C. and Osborn, T. R. (1999). Numerical study of the feeding current around a copepod. J. Plankton Res. 21,1391 -1421.[Abstract]
Jonsson, P. R. and Tiselius, P. (1990). Feeding behaviour, prey detection and capture efficiency of the copepod Acartia tonsa feeding on planktonic ciliates. Mar. Ecol. Prog. Ser. 60,35 -44.
Klein Breteler, W. C. M. and Gonzales, S. R. (1986). Culture and development of Temora longicornis (Copepoda, Calanoida) at different conditions of temperature and food. Syllogeus 58,71 -84.
Koehl, M. A. R. and Strickler, J. R. (1981). Copepods feeding current: Food capture at low Reynolds number. Limnol. Oceanogr. 26,1062 -1073.
Légier-Visser, M. F., Mitchell, J. G., Okubo, A. and Fuhrman, J. A. (1986). Mechanoreception in calanoid copepods. A mechanism for prey detection. Mar. Biol. 90,529 -535.
Morris, M. J., Kohlhage, K. and Gust, G. (1990). Mechanics and energetics of swimming in the small copepod Acanthocyclops robustus (Cyclopoida). Mar. Biol. 107,83 -91.
Morris, M. J., Gust, G. and Torres, J. J. (1985). Propulsion efficiency and cost of transport for copepods: a hydromechanical model crustacean swimming. Mar. Biol. 86,283 -295.
Pavlova, E. V. (1981). Rate of movements of copepods in plankton from the Indian ocean. Ekologiya Morya 5,61 -65 [in Russian].
Saiz, E. and Kiørboe, T. (1995). Predatory and suspension feeding of the copepods Acartia tonsa in turbulent environments. Mar. Ecol. Prog. Ser. 122,147 -158.
Singarajah, K. V. (1975). Escape reactions of zooplankton: effects of light and turbulence. J. Mar. Biol. Assn. UK 55,627 -639.
Sleigh, M. A. and Barlow, D. I. (1980). Metachronism and control of locomotion in animals with many propulsive structures. In Aspects of Animal Movement (ed. H. Y. Elder and E. R. Trueman), pp. 49-67. Cambridge: Cambridge University Press.
Stamhuis, E. J. and Videler, J. J. (1995).
Quantitative flow analysis around aquatic animals using laser sheet particle
image velocimetry. J. Exp. Biol.
198,283
-294.
Strickler, J. R. (1982). Calanoid copepods, feeding currents and the role of gravity. Science 218,158 -160.
Strickler, J. R. (1977). Observation of swimming performances of planktonic copepods. Limnol. Oceanogr. 22,165 -170.
Strickler, J. R. (1975). Swimming of planktonic Cyclops species (Copepoda, Crustacea): pattern, movements and their control. In Swimming and Flying in Nature, 12801 edn. (ed. T. Y. T. Wu, C. J. Brokaw and C. Brennen), pp. 599-614. New York: Plenum Press.
Tiselius, P. and Jonsson, P. R. (1990). Foraging behaviour of six calanoid copepods: observations and hydrodynamic analysis. Mar. Ecol. Prog. Ser. 66, 23-33.
Trager, G., Achituv, Y. and Genin, A. (1994). Effect of prey escape ability, flow speed, and predator feeding mode on zooplankton capture by barnacles. Mar. Biol. 120,251 -259.
van Duren, L. A., Stamhuis, E. J. and Videler, J. J. (1998). Reading the copepod personal ads: increasing encounter probability with hydromechanical signals. Phil. Trans. R. Soc. Lond. B 353,691 -700.[CrossRef]
van Duren, L. A., Stamhuis, E. J. and Videler, J. J.
(2003). Copepod feeding currents: flow patterns, filtration rates
and energetics. J. Exp. Biol.
206,255
-267.
van Duren, L. A. and Videler, J. J. (1995). Swimming behaviour of developmental stages of the calanoid copepod Temora longicornis at different food concentrations. Mar. Ecol. Prog. Ser. 126,153 -161.
van Duren, L. A. and Videler, J. J. (1996). The trade-off between feeding, mate seeking and predator avoidance in copepods: behavioural responses to chemical cues. J. Plankton Res. 18,805 -818.[Abstract]
Videler, J. J. (1993). Fish Swimming. London: Chapman and Hall.
Vogel, S. (1981). Life in Moving Fluids. Boston: Willard Grant Press.
Yen, J. and Strickler, J. R. (1996). Advertisement and concealment in the plankton: what makes a copepod hydrodynamically conspicuous? Invert. Biol. 115,191 -205.
Yen, J., Sanderson, B., Strickler, J. R. and Okubo, A. (1991). Feeding currents and energy dissipation by Eucheta rimana, a subtropical pelagic copepod. Limnol. Oceanogr. 36,362 -369.