Visual cues eliciting the feeding reaction of a planktivorous fish swimming in a current
1 Department of Biology, University of Victoria, PO Box 3020 STN CSC,
Victoria, British Columbia, Canada
2 International Marine Centre, Loc. Sa Mardini, 09072 Torregrande, Oristano,
Italy
3 School of Aquatic and Fisheries Sciences, and Friday Harbor Laboratory,
University of Washington, Friday Harbor WA 98250, USA
4 CNR-IAMC, Loc. Sa Mardini, 09072 Torregrande, Oristano, Italy
* Author for correspondence (e-mail: paolo.domenici{at}iamc.cnr.it)
Accepted 23 November 2004
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Summary |
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Key words: fish, plankton, predation, vision, Cymatogaster aggregata, feeding
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Introduction |
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Planktivorous fishes that feed in currents provide an example where the
motion between a fish and its zooplankter prey are consistent and definable
(Hobson, 1972;
Hamner et al., 1988
). By
feeding zooplanktivourous fishes in flumes, Kiflawi and Genin
(1997
) demonstrated that peak
ingestion can occur at intermediate current speeds and McFarland and Levin
(2002
) showed that individuals
will cease feeding at higher speeds. Four phenomena may chronologically occur
before a fish reacts to a particle: (a) detection, (b) recognition (c)
decision (i.e. threshold of triggering mechanism at the sensory system level)
and (d) motor response. Behaviourally, only the feeding reaction can be
observed (i.e. the motor response). The timing of the feeding reaction should
be, however, largely dependent on the timing of the detection. In particular,
the distance at which a feeding reaction is triggered is limited by the
maximum detection distance.
In investigating predatorprey interactions, Dill
(1974) measured the escape
responses of prey and modelled the rate of change in apparent size of a
predator (i.e. the loom) as it approached the prey. For fish feeding on
plankters in a current, angular velocity, apparent size and loom were
described mathematically for particles that approached head-on and at various
distances offset from the position of the fish in the current
(McFarland and Levin 2002
). In
that study, the temporal-resolution of a fish's reaction to an incoming
plankter was limited by the 2D spatial resolution and by the low temporal
resolution of the system used to capture time-sequence images for analysis
(McFarland and Levin 2002
). In
this paper, using a high-speed video system, we examine the reaction of fish
under similar conditions and evaluate, in three dimensions, what attribute(s)
of a plankter appear to influence the feeding reaction of fish. We test three
alternative hypotheses: (1) The feeding reaction of planktivourous fish may be
triggered by a fixed apparent size (i.e. angular size) of the approaching
particle. (2) Fish may react to plankton once it reaches a given threshold
angular velocity as it is carried passively by the current. (3) The mechanism
triggering a fish's reaction may be the loom (i.e. the rate of change of the
angular size) of the prey while approaching the fish. The experiments were
carried out using three different current speeds and two treatments, which
provided plankton with different properties of contrast (i.e. semi-transparent
and darkened Artemia) in order to test the effect of contrast on
detection mechanisms.
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Materials and methods |
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Apparatus
Experiments were carried out in a flume tank as described in McFarland and
Levin (2002) with a working
section 50 cm long, 12 cm wide, and a water depth of 17 cm
(Fig. 1). The experimental tank
was illuminated from above with a daylight fluorescent lamp (two 20 W lights,
model F20T12 GE). Integrated irradiance was 8.2x1017 photons
cm2 s1 over 300750 nm, measured at
the water surface level of the experimental tank (OCEAN OPTICS S1000
spectroradiometer).
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Water flow was generated by a two-bladed propeller and current speed controlled by varying the voltage via a variac to the AC/DC motor (Dayton AC/DC model 2MO338 motor; Lincolnshire, IL, USA). A catch screen was placed 10 cmdownstream from the working section to isolate fish in the flume. To assure repeatability of current speed for different trials, the voltage output of the variac was prescribed through the use of a digital voltmeter. Three layers of collimators (5 cm wide) were positioned upstream to produce a homogeneous flow through the working section. Viewed through the collimators, the upstream aperture of the collimator tubes provided a dark background to the fish. The background radiance from the collimator, as measured with an OCEAN OPTICS S1000 spectroradiometer between 300 and 750 nm, was only 3.1% when compared with the radiance from a white Teflon reflective surface and was similar to the radiance from a black surface (4.3%). Flow speed was calibrated from dye injected in the water upstream from the collimators and filmed at 125 images s1 using a high-speed video camera (Red Lake, model 1000 S series motionscope; San Diego, CA, USA). The current flow as seen by discrete dye travel in the horizontal dimension was laminar over the working section, with minor turbulence only observed just upstream from the catch screen. To avoid wall effects, only trials in which a fish initiated a reaction towards the prey more than 2 cm from the walls, bottom and water surface, were analysed.
Fish movements were recorded at 125 images s1 with the video camera placed perpendicular to the flume. We capture 3D-movements of each fish by positioning a 30 cmx60 cm mirror at 45° above the experimental tank (Fig. 1). Therefore, lateral and top images of the fish were produced at one time, the bottom half of the camera filming the fish laterally to determine height in the water column and position along the length of the flow tank, while the upper half of the camera filmed through the mirror and viewed the fish from above against the floor of the tank, allowing positions across the width of the flow tank to be determined. Frame-by-frame analysis of the horizontal and vertical positions of each fish at the time of first departure from a steady swimming mode and at the moment of engulfment of a plankter (Artemia nauplii) was accomplished though use of the software Scion Image (NIH image analysis). The 3D-coordinate position (x, y, z) of each fish in the flume was established against two ruled grids, one placed on the backwall of the flume and another on the bottom of the flume. For horizontal positions of the fish (x, y), the midpoint between the eyes of each fish was used as reference, and for the vertical position (z) the centre of the fish's observable (right) eye.
Experimental procedure
Artemia nauplii were used as in Kiflafi and Genin (1997), since
they have a shape and size similar to the prey of shiner pearch, calanoid
copepods, and because they lack escape behaviour
(Coughlin and Strickler, 1990;
Trager et al., 1994
).
Individual fish did not require conditioning to swim in the flume and, even
though naïve, fed on Artemia when introduced [also reported for
natural zooplankton by McFarland and Levin
(2002
)]. As suggested by Webb
(1982
) for visual reaction in
fish, the size of an Artemia (i.e. particle diameter) was considered
as the mean between its length and width (mean size 0.053±0.002 cm;
N of subsample =10).
Two sets of experiments differing in prey type were carried out. Perch collected in August of 2000 were used in the first set of trials, where naturally semi-transparent Artemia nauplii were released into the flume-tank (Fig. 2). In a second set of experiments, shiner perch collected in April 2002 were presented with darkened Artemia (Fig. 2). A stone for grinding a Sumi ink stick with water was used to make liquid black ink. Darkening was obtained by adding a suspension of black ink (0.037 g in 1 l of water) into the Artemia's tank overnight. The Sumi ink produced a darkening of the Artemia gut.
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In both experiments, fish were acclimated in the flume tank at zero current
speed for 40 min before each experiment. Current speed was then increased
slowly over a 2 min period to the chosen trial speed. The order of trial
speeds was chosen at random among the six possible combinations of orders
using slow (0.52 body length s1 for semi-transparent
Artemia and 0.66 body length s1 for darkened
Artemia), intermediate (1.88 body length s1 for
semi-transparent Artemia and 1.60 body length s1
for darkened Artemia), and fast flow speeds (3.12 body length
s1 for semi-transparent Artemia and 3.01 body
length s1 for darkened Artemia). These speeds are
within the range in which C. aggregata swims using pectoral fin
locomotion, i.e. they are lower than the gait transition speeds (from pectoral
fin to caudal fin locomotion), observed in this species and size
(Mussi et al., 2002). Ten
minutes after a trial speed was reached, live darkened or natural
(semi-transparent) Artemia nauplii were introduced from behind the
collimator baffles and in the approximate centre of the section (i.e. midway
between the walls and in midwater). We assumed that, after recirculating in
the flow tank (i.e. Artemia took a full trip around the flow tank
before being preyed upon), the nauplii were distributed randomly over the tank
cross section. The numbers of trials for the natural (semi-transparent)
Artemia experiment were 15, 15 and 19 for slow, intermediate and fast
current speeds, respectively, and 10 trials at each current speed were
performed using darkened Artemia. Each trial involved one single
fish. For each individual in both darkened and natural conditions, up to four
prey captures were analysed at each current speed.
Fish first reacted to an approaching particle by a noticeable change in
position at the time TR
(Fig. 3). Because a latent
period must occur between when the reaction is triggered by the particle and
the actual visible reaction of the fish
(Dill, 1974;
Domenici, 2002
), we have
defined the theoretical time at which the particle triggers fishes' `inner
reaction' as TL (the reaction at the sensory system
level). The time of the fish's first `visible reaction' was defined as
TR (the reaction at the motor level), and the time at
which the fish captured the particle was defined as TC.
The hypothesized delay between TL and
TR would be due to the conductive times of the
neurosensory and neuromuscular systems. While we were not able to determine
TL experimentally, its definition is needed in order to
facilitate further theoretical considerations.
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Neither darkened nor semi-transparent Artemia nauplii were visible on the video images. However, the jaw protrusion of the fish that corresponded to the engulfing of an Artemia was visible. Previous video recordings from close up at all speeds indicated that the position of the tip of the mouth at maximum mouth protrusion was a good estimator of the position of an Artemia at the time of capture along the tank axis. The vertical position of the particle was therefore estimated as the midpoint between the two edges of the mouth tip at maximum protrusion, while the position of the particle across the width of the tank was estimated by using the top image of the tip of the mouth at the time of maximum protrusion, in accordance with previous observations. Therefore, the time TR and the position of the mouth at TC when a fish captured a particle (easily detectable by jaw protrusion), were used to estimate the position of the nauplius at TR. This assumes that nauplii moved passively within the current (TR to TC in Fig. 3). The vertical distance between a fish and a food particle at TR (Zvertical) was estimated from video side views. The video top view provided estimates of Yforward (the distance between the fish and the prey approaching along the current axis), and X'lateral (the lateral distance between the fish and the prey along the axis perpendicular to the current, in the horizontal plane).
The geometry in Fig. 3 was
reconstructed for each capture event, and all analyses were done using the
plane Dtotal
XlateralYforward, where
Dtotal is the estimated total distance between the fish's
eyes and the food at TR, and Xlateral
is the overall lateral distance between the fish's eyes and the axis of motion
of the prey along the current. Dtotal is at an angle alpha
() from the fish's axis. Left and right responses were pooled as if
they were all responses to particles approaching on the right side of the
fish.
The angular size threshold (ßR, i.e. ß at
TR) of the prey was calculated as the angle subtended by
the plankton onto the fish's eye at the time of reaction
(Fig. 3). The apparent loom
threshold (R, i.e. loom at TR) was
calculated as in Dill's (1974
)
equation, modified for the case of approaching objects not necessarily in line
with the fish's body axis, following McFarland and Levin
(2002
).
McFarland and Levin's equation (equation 26 in
McFarland and Levin, 2002),
for the general case of a particle coming towards the fish in any direction,
corresponds to:
![]() | (1) |
![]() | (2) |
Using particle diameter P=2R and considering current
speed Uc=Uy (i.e. considering
current towards the fish having a positive speed) for particles approaching,
we obtain:
![]() | (3) |
The apparent angular velocity threshold (i.e. R, the
angular velocity of the particle at TR) was calculated
following McFarland and Levin
(2002
). Their equation
(equation 6 in McFarland and Levin,
2002
) for the general case of a particle coming in any direction
corresponds to:
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Since in our case Ux is equal to zero (see above), the
equation becomes:
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The minus sign is due to the fact that McFarland and Levin
(2002) consider speed as
negative when approaching the fish. We switched the sign to positive, as in
our case Uc=Uy. In addition,
Xlateral is equal to Dtotal sin
(equation 3 in McFarland and
Levin, 2002
). Therefore, the equation becomes:
![]() | (6) |
The effect of current speed and plankton type (natural vs
darkened) was tested using two-way ANOVAs (analysis of variance) for each
feeding reaction variable (i.e. Dtotal,
Xlateral, Yforward,
Zvertical, , angular size, angular velocity, loom).
To account for multiple simultaneous two-way ANOVAs, the level of significance
was adjusted within columns using the sequential Bonferroni technique
(Rice, 1989
).
Theoretical considerations on how angular size, angular velocity and loom should vary as the particle approaches
If the time at which a particle first triggers a fish's reaction (i.e. the
threshold at the sensory system level at TL), is caused by
a given angular size (ßL), angular velocity
(L) or loom (
L) of an approaching
particle, independent of its speed, then the `apparent' angular size
ßR, angular velocity
R or loom
R (i.e. at TR), should vary with
current speed as the approaching object covers a longer distance between
TL and TR (assuming a constant
latency) when travelling at higher speeds. The potential effect of current
speed on the threshold for the fish's response can be visualised by plotting
how angular size, loom, and angular velocity vary as a function of
Yforward (Fig.
4). Since current speed for each trial is constant, decreasing
values of Yforward also correspond to time. The angular
size increases continuously as the particle travels along
Yforward (Fig.
4A) and its rate of increase is higher the smaller the lateral
distance Xlateral is. Therefore, assuming the theoretical
angular size ßL to be constant at different flow speeds, the
experimental angular size ßR should increase with current
speed.
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Loom increases as the particle travels along the current up to a certain
(relatively small) value of Yforward, and then decreases
again (except if Xlateral=0 cm). For example, for an
Xlateral value of 2, loom increases up to
Yforward values around 1.5 cm
(Fig. 4B). Therefore, if we
assume L to be constant at different current speeds, then
R should increase with current speed up to
Yforward values of about 1.5 cm, as the distance covered
by the particle along Yforward would increase with current
speed. Loom decreases only when very close to the fish. The angular velocity
, conversely, increases continuously as the particle travels along
Yforward, although this increase has different rates depending on
Xlateral (Fig.
4C). In particular, if we assume
L to be
constant at different speeds, then
R should increase with
current speeds (as Yforward gets shorter). Therefore, we
expect that the angular variable(s) implicated in the mechanisms triggering
the feeding reaction should increase with speed.
For those angular variables that are found to increase with speed, we estimated latency as follows. To find a theoretical constant value of latency for all current speeds, an index of homogeneity (IH) between each average `angular variable' (i.e. angular size, angular velocity or loom) calculated at TL (i.e. assuming a given latency) at different current speeds was calculated using (maximum `angular variable' minimum `angular variable') / minimum `angular variable'. Each angular variable at TL was calculated as the theoretical value that the fish would experience if, for each sequence, the particle had triggered a reaction at a position with Xlateral at TL being the same as at TR (since a straight course was assumed), while Yforward was considered longer at TL than at TR by a distance that was calculated as the current speed multiplied by the theoretical latency.
The alternative hypotheses for the three mechanisms triggering feeding reaction were further tested as follows:
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Results |
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Current speed and darkening had no effect on angular size, and no interaction effect between darkening and current speed was found (Table 2 and Fig. 6). Conversely, both angular velocity and loom were affected by current speed (P<0.001 in both cases), as well as darkening (P=0.0106 and P<0.001, respectively), and the interaction of these two factors was significant for loom (P<0.005) (Table 2 and Fig. 6).
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Angular variables involved in triggering the feeding reaction to plankton
are expected to increase with current speeds, except for loom at very small
distances (see above and Fig.
4). While loom may theoretically decrease at small distance from
the fish, loom increases with decreasing Yforward when the
Yforward and Xlateral ranges of all
observed speeds are considered (only intermediate speed is shown as an
example, in Fig. 4). The
results show that with semi-transparent Artemia, ßR
does not vary significantly with speed
(Table 2 and
Fig. 6), R
increased with current speed, while
R was lowest at the
intermediate speeds, and higher at the low and the high current speeds.
Therefore, an index of homogeneity IH was calculated only
for angular velocity. IH was highest when a theoretical
latency of 385 ms was considered. That is, if we assume a latency of 385 ms,
the values for the angular velocity when the fish's `inner reaction' occurs
(
L) are relatively constant (i.e. 0.26 rad
s1, 0.28 rad s1 and 0.26 rad
s1 for slow, intermediate and fast speeds,
respectively).
When darkened Artemia were used, the angular size
ßR is relatively constant at different current speeds, while
both R and
R increased with current speed
in darkened Artemia (Fig.
6). Therefore, IH was calculated for both loom
and angular velocity. However, a maximum IH was found only
for loom, and it resulted in a latency of 230 ms. Using this theoretical
latency,
L is relatively constant (i.e. 0.013 rad
s1, 0.015 rad s1 and 0.013 rad
s1 for slow, intermediate and fast speeds, respectively).
Conversely, IH increased indefinitely when increasing
values of latency were applied to
L.
The frequency distributions of Xlateral of the semi-transparent vs darkened treatments were compared using a Chi square test. Four bins (01, 12, 23, >3 cm) were used for the comparison (Fig. 7). The distributions of the two treatments are significantly different (Chi2 22.69; 3 d.f.; P<0.0001). The highest peak in the distribution for the darkened treatment was in the bin Xlateral=01 cm, i.e. for particles almost in line with the fish.
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The comparison between the Yforward and
Xlateral positions of the particles at
TR and the theoretical values of these positions based on
the average experimental angular size, angular velocity and loom at each
current speed is shown in Fig.
8. For the semi-transparent Artemia experiments, the
theoretical values of Yforward and
Xlateral at TR based on the average
angular velocity are closer to the experimental values than those based on the
average loom or angular size for the fast current speed (ANOVA;
P<0.01; Tukey post test, P<0.01 and P<0.05
for the comparisons between loom and R, and
ßR and
R, respectively), although
differences were not significant for the intermediate and slow speeds
(Fig. 8). The theoretical
values of Yforward and Xlateral based
on the average loom for intermediate and fast speeds are closer to the
experimental values than those based on angular velocity (intermediate and
fast; ANOVA; P<0.05; Tukey Post-test, P<0.05 in both
cases), although there were no significant differences when values based on
averages ßR and
R were compared. Differences
were not significant in any case for the slow speed
(Fig. 8).
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Discussion |
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The geometry of the particle position and, in particular, its lateral distance, at which the feeding reaction occurs can give us some insights on the main visual mechanism involved. A relatively distant food particle travelling towards the fish at a given lateral distance (Xlateral) from the nasalcaudal axis has a relatively low angular velocity, which is increasing very slowly. As the particle approaches, a sharp increase in angular velocity takes place, and it reaches a peak (Fig. 4) whenYforward=0 and subsequently decreases as the particle travels along its rectilinear path. By contrast, a straight-on particle (Xlateral=0) has zero angular velocity throughout its approach towards the fish. Conversely, loom and angular size are maximised when lateral distance is minimal. This scenario suggests that preference for particles coming at a lateral distance Xlateral=0 implies angular size or loom as the mechanisms triggering the feeding reaction. Conversely, if particles coming at small lateral distance are not attacked, then angular velocity may be the mechanism involved in the feeding reaction.
It is reasonable to suppose that fish would capture most particles at low
Xlateral values for minimizing energy expenditure, if
detection mechanisms were not limiting factors. However, in spite of possible
energetic advantages of capturing prey in line with fish's nasalcaudal
axis, very few particles were taken in when semi-transparent Artemia
travelled at small Xlateral values (i.e. <1 cm;
Fig. 7). In fact, most
particles produced a reaction when they approached off-axis with peak
frequency values of Xlateral at 23 cm, and with
values of Xlateral as high as 6 cm
(Fig. 7). These results
suggested that a threshold angular velocity R might alert a
fish to approaching semi-transparent Artemia, and promote the feeding
reaction to food at greater reaction distances
(Fig. 5).
By contrast, with darkened Artemia, the peak response frequency
occurred when prey approached closest to a fish's nasalcaudal axis. The
larger reaction to darkened prey at low Xlateral
(Fig. 7), suggested that loom
or angular size rather than angular velocity might have triggered a fish's
reaction to darkened prey (Fig.
8). However, further explanations, are needed to account for the
decline in frequency at Xlateral values >3 cm in
semi-transparent Artemia (Fig.
7). This decline may be related to the energetic cost of feeding
at larger Xlateral and to the fact that peak values of
R decline as Xlateral increases
(Fig. 4C).
The effect of current speed on each angular variable suggests that angular velocity is the mechanism triggering the response to semi-transparent Artemia, while loom is the mechanism triggering the reaction to feed on darkened plankton. This is because angular velocity for the semi-transparent Artemia and loom for the darkened Artemia were the only variables that both (1) increased with current speed as expected if a relatively constant latency and a constant angular threshold are assumed (2) allowed calculation of a reasonable latency. These results are in line with our comparison between the experimental Yforward and Xlateral and the expected Yforward and Xlateral based on averages angular size, angular velocity or loom. Such a comparison suggests that angular velocity may be the variable that triggers the feeding reaction to semi-transparent Artemia, although differences are significant only for high current speed. Conversely, the fitting of the experimental data with the model for the darkened Artemia treatment is not significantly different between angular size and loom. This is because the shapes of the curve for angular size and loom are very similar (Fig. 8). However, as discussed above (Materials and methods section), if angular size was the mechanism triggering the feeding reaction, one would expect the position of the particle at the apparent reaction time (TR) to be different for different current speeds. Let us consider a realistic example in which the sensory threshold occurs at a given angular size corresponding to a distance of 10 cm at TL. Let us consider a given latency of 200 ms. In this case, at TR, high-speed particles should be closer to the fish, at approximately 5 cm distance from the fish vs 9 cm distance for slow speed particles. This assumes the same time interval (200 ms) between when the sensory threshold is reached (i.e. TL) and the motor response (i.e. TR) in the fish at all current speeds. Conversely, if a loom mechanism is considered, higher current speed would cause both (1) higher rate of change of the looming angle and (2) a longer distance travelled between TL and TR. Higher loom in high speed would cause reaching the sensory threshold from a larger distance. As a realistic example, let us consider that sensory threshold (i.e. at TL) of loom may be reached at 10 cm for high speed particles vs 6 cm for slow speed particles. However, this difference may be in large part cancelled out, at least in our experimental conditions, by the longer distance travelled by the high speed particles. Following our example, during a given latency period of 200 ms, higher speed would allow particles to travel approximately 5 cm vs 1 cm travelled at slow speed. This would cause slow and fast particles to be at a similar distance (i.e. 5 cm according to our example) from the fish at the time of the fish's response. Therefore, loom, but not angular size, can explain particles travelling at different speeds to be in similar positions (Fig. 8DF) relative to the fish at the time of reaction (TR). We conclude that loom is the most likely variable involved in triggering the feeding reaction of fish preying on darkened Artemia.
Latency and speed
The reaction models based on average angular velocity R
or loom
R fit better at high, rather than at low, current
speed for darkened and semi-transparent Artemia, respectively
(Fig. 8). An explanation could
be that variability in the time for reaction may decrease with current speed
(i.e. when a fish needs to minimize latency to successfully capture the
particle). Previous work on escape response in zebra danio (Brachidanio
rerio) showed that predator speed had no effect on the apparent loom
threshold, while it had an effect on the reaction distance and, therefore,
latencies were considered negligible (Dill,
1974
). However, latencies of escape responses are likely to be
shorter than those of feeding reactions, as escape responses are triggered by
the Mauthner cells, a pair of giant neurons in the hindbrain of most fish
species (Eaton and Hackett, 1984). Batty
(1989
) reported escape response
latency to visual stimuli to be about 40 ms. The reaction to an approaching
prey (e.g. plankton), may have a longer latency of the order of 100300
ms, because more time is needed to process a prey's movement and trajectory,
and then to direct an attack. This range corresponds approximately at the
values found for maximizing IH (i.e. assuming that fish
respond to a given value of angular velocity or loom at all current
speeds).
At higher current speeds (e.g. 40 cm s1) than those used
here, C. aggregata swam in a flume but did not attempt to capture
plankton (McFarland and Levin,
2002). This may have been due to sensorymotor constraints,
which influenced the fish's reaction time preventing successful capture when
plankton approached at high speeds. Furthermore, feeding may become
energetically costly at very high current speeds, even if fish may be capable
of capturing the prey.
Plankton visibility
Transparency in the aquatic environment represents a significant adaptive
cryptic mechanism (Johnsen
2001a,b
,
2002
). However, visual
adaptations, such as UV and polarization vision, have evolved among
planktivores to increase apparent visual contrast
(Lythgoe and Hemmings, 1967
;
Lythgoe, 1979
;
Loew et al., 1993
;
McFarland and Loew, 1994
;
Cronin et al., 1994
;
Shashar et al., 1998
).
Foraging success in planktivores is also strongly dependent on the light,
turbidity, background space light, and visibility of pigmented parts, such as
the eyes or the gut of the prey (Vinyard,
1980
; McFall-Ngai,
1990
; Thetmeyer and Kils,
1995
; Johnsen and Widder,
1998
; Tsuda et al.,
1998
; Utne-Palm,
1999
; Utne-Palm and Stiansen,
2002
). Under the same background light conditions, fish predation
was shown to be higher when transparent prey with larger eyes were used
vs prey with small eyes (Zaret
1972
), and reaction distances for transparent prey were
significantly lower than those for pigmented prey
(Thetmeyer and Kils, 1995
;
Tsuda et al., 1998
;
Utne-Palm 1999
). However, it
was shown by video imaging in the near field that transparent zooplankton
irradiated from above when viewed horizontally against a darker background
appeared as bright targets due to light scattering off their bodies
(Loew and McFarland, 2000
).
Some planktivorous fish search for prey outside Snell's window (i.e. a cone
angle of about 97.2° through which the terrestrial hemisphere can be
seen), because prey are seen against a dark background
(Lythgoe, 1979
).
In our study, feeding reaction to zooplankton appeared to occur at longer
distances for semi-transparent Artemia than for a darkened one. This
result would be in line with Loew and McFarland's
(2000) observations, and is in
agreement with the general observation that changes in prey contrast may cause
differences in reaction distances, although most observations are on pigmented
prey against a light background (e.g.
Utne-Palm, 1999
). In our
study, the dark background of the collimator tubes would enhance the
visibility of semi-transparent plankton; therefore, semi-transparent
Artemia should be visible at a greater distance due to their higher
light scattering (diffuse reflectance) against the dark background. Because
light was weakly reflected from a dark Artemia's body there would be
less contrast between the target and the background in darkened
Artemia (Fig. 2 and E.
R. Loew and W.N.McF., unpublished).
The higher visibility of the natural (semi-transparent) plankton at longer distances, however, does not explain why shiner perch did not react to semi-transparent particles coming straight on. At small Xlateral, fish could theoretically react to a threshold angular velocity, although such a threshold would be reached at very small values of Yforward (Fig. 4) (i.e. when it may be too late for the fish to react in time to catch the prey). Alternatively, fish could have used loom as a mechanism triggering their feeding reaction. A threshold loom would be reached at relatively high values of Yforward for the case of small Xlateral (Fig. 4). If we assume that the apparent size of semi-transparent and darkened particles was the same, then a Yforward of about 6 cm should trigger a reaction when Xlateral=0, as in the semi-transparent Artemia at intermediate speed. Because relatively few fish reacted to natural plankton at small Xlateral values, it is possible that the apparent size of the darkened plankton was greater than that of the natural plankton, although there we have no evidence that darkening can cause a change in apparent size. If semi-transparent Artemia had a relatively small apparent size, for any value of Xlateral and Yforward, loom for a darkened Artemia would be greater than for a semi-transparent Artemia. In this case, it would be possible that when using semi-transparent Artemia, a threshold loom may have occurred when the prey was too close to the fish to react in time for prey capture. Alternatively, it may be possible that shiner perch do not have enough behavioural flexibility in order to shift from a reaction based on angular velocity mechanism to one based on loom within a single feeding session, and it may be `locked' in using the most favourable mechanism of detection for any given contrast conditions. However, we are not aware of any supporting evidence from other sources, and therefore this suggestion remains highly speculative.
Under the conditions of our experiments, we may be dealing with both
positive and negative contrast situations. For the natural prey irradiated
from above viewed against the darker background there may be positive contrast
due to internal scatter. However, for the darkened prey the contrast may be
negative. Since on- and off-channels use separate pathways that may differ in
properties, it is possible that some of the observed differences in feeding
reaction mechanisms may be due to the way the visual system handles positive
and negative contrast (Wheeler,
1982).
Limitations of our study
We have examined a fish's response to food in a flume tank where turbulence
in the water flow was minimized, and where the detection of plankton was
constrained by the dimensions of the flume. Therefore, this study was
simplified compared with foraging in natural water currents. In nature,
turbulence (Aksnes and Giske,
1993; Kiorboe and Saiz,
1995
; McFarland and Levin,
2002
), as well as schooling can affect foraging behaviour in
planktivores (Ryer and Olla,
1991
; O'Driscoll,
1998
; Lachlan et al.,
1998
; Foster et al.,
2001
). Nevertheless, individual responses in a flume to
approaching zooplankton allowed us to standardize feeding reaction parameters
and to define a fish's reaction to plankton.
In our study, fish reaction to approaching zooplankton was assumed to be
independent of the particle shape or its intrinsic motion. In order to
standardize prey size and behaviour, we used only Artemia nauplii.
Artemia is a non-evasive prey since no significant escape motion has
been recorded (Coughlin and Strickler,
1990) and, generally, planktivores preferentially select
non-evasive prey items, even when the evasive prey are larger
(Drenner et al., 1978
; Vinyard
1980
,
1982
). Although
Artemia is not a natural prey of shiner perch, perch showed similar
behavioural patterns when feeding on natural plankton
(McFarland and Levin, 2002
).
In addition, by staining Artemia with black ink, we provide an artificial
set-up that may have affected the behaviour of Artemia or its
physiology (e.g. any chemical cues it may provide). However, as suggested by
its lack of significant evasive behaviour
(Coughlin and Strickler, 1990
),
Artemia was most likely just passively carried by the current and
therefore its behaviour should not have affected our results.
The dark background we used does not correspond to the most common environment where plankton is found. However, certain environmental conditions, i.e. twilight, as well as in certain conditions of turbidity, cloudiness and depth, may also provide a relatively dark background. Nevertheless, conditions of visibility created in laboratory set-ups such as ours are quite different from natural conditions, and it would be interesting to investigate the feeding reactions of planktivorous fishes to a variety of plankton types in natural conditions.
Conclusions
Our results showed that at high current speeds, angular velocity was the
likely cue for triggering the feeding reaction when semi-transparent
Artemia were used. Loom appeared to be the main mechanism when prey
were darkened. It is possible that both mechanisms act in concert during some
of the feeding phases (detection, pursuit, capture), although one mechanism
might eventually prevail in detecting certain prey characteristics (e.g.
motion type, prey contrast).
As our major conclusion, we suggest that prey contrast dramatically affects detection and the subsequent feeding reaction. When prey contrast was high due to scattering (semi-transparent prey), feeding reactions occurred at greater distances and at increasing Xlateral values where angular velocity tends to be higher. When prey contrast was low (darkened treatment), reaction distances diminished and feeding reactions occurred for prey approaching at smaller lateral distance (Xlateral). This study showed that visual behaviour of planktivores is highly flexible because fish appear to be able to utilize different visual properties of the approaching object for their reaction to prey. Although angular velocity was the main cue for triggering feeding reactions to semi-transparent plankton at high current speeds, it is still possible that during the tracking of a plankter after a prey's detection, loom may have a role in determining the time of engulfment. This and other issues will be explored in a further paper dealing with the pursuit and capture of plankton.
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