The importance of the lateral line in nocturnal predation of piscivorous catfish
1 Department of Biology, University of Konstanz, 78457 Konstanz,
Germany
2 Boston University Marine Program, MBL, Woods Hole, MA 02543,
USA
* Author for correspondence at present address: Leibniz-Institute of Freshwater Ecology and Inland Fisheries, D-16775 Stechlin, Germany (e-mail: kPohlmann{at}igb-berlin.de)
Accepted 7 June 2004
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Summary |
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Key words: catfish, lateral line, gustation, non-visual predation, prey wake
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Introduction |
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In a recent study we found that European catfish Silurus glanis
follow the wakes of piscine prey prior to attacking them in the absence of
visible light (Pohlmann et al.,
2001). In tracking wakes the predator is following past locations
of prey in more or less convoluted trails over several prey-body lengths,
which finally lead to the prey's present location. This tracking is clearly
different from the direct approach behaviour expected from the detection of
the instantaneous position of the prey through electrical, visual, or acoustic
cues emitted by the prey. Wakes contain hydrodynamic and chemical information
about the sender that persists after the sender has moved on and thus
considerably increases the `active space' in which the prey is detectable
(Westerberg, 1990
).
Directional information in wakes and other plumes can be provided both by
chemical and hydrodynamic gradients (Atema,
1996
; Webster and Weissburg,
2001
). The hydrodynamic information is estimated to be detectable
in trail lengths of several decimeters to meters and over several seconds,
depending on flow conditions and the size of the fish
(Bleckmann, 1993
). The chemical
directional information is present for at least one order of magnitude longer,
both in time and space (Westerberg,
1990
). We found catfish utilised wakes as old as 10 s and followed
2.5 cm long fish over distances of up to 40 cm for about 55 prey-body lengths,
even in our confined experimental tank with high background turbulence due to
the catfish's own movement (Pohlmann et
al., 2001
).
Wakes of moving animals are distinct flow patterns in which fine structure
depends on the size, swimming velocity and the mode of swimming of their
creator. The guppies Poecilia reticulata used in our study swim in
the push-and-coast mode, where each tail beat creates a disturbance including
a vortex ring, followed by a coast phase without fin movements dragging water
behind (Breithaupt and Ayers,
1996; McCutchen,
1977
; Müller et al.,
2000
). Wake height and the lateral distance between vortices
correspond to the size of the tail fin and thus of the fish. The specific
structure of the wake provides information about swimming style. The sense of
rotation and travelling direction of the vortices and the direction of the
dragged water give information on swimming direction of the prey. A wake shows
distinct structural changes when ageing
(Hanke et al., 2000
;
Westerberg, 1990
). Thus the
hydrodynamic structure could inform a predator if the creator of the wake is
suitable prey (size, swimming speed), in which direction it went and if the
wake is fresh enough to be worth following
(Bleckmann, 1993
).
Fish can detect hydrodynamic structures with their lateral line organs
(Kalmijn, 1988;
Dijkgraaf, 1933
). These
consist of free standing neuromasts and canal neuromasts that detect the
velocity or acceleration components and the direction of water movements. In
European catfish these neuromasts are sufficiently numerous on the body
surface, and especially in the head region
(Herrick, 1901
), to enable the
detection and spatial resolution of fine scale structures The sensitivity of
lateral line neuromasts covers the amplitude and frequency range found in
wakes of small fish (Bleckmann,
1993
; Bleckmann et al.,
1991
).
There is also chemical information in the wake. Substances are constantly
and involuntarily released by all fish and are distributed with the water
movements. Westerberg describes the evolution of a chemical trail in three
stages: the initial mixing produced by a source, a stretching and deformation
by shear and a final stage in which molecular diffusion becomes important
(Westerberg, 1990). In the
wake there is incomplete mixing before the velocity fluctuations lose their
momentum to viscosity. Molecular diffusion of chemical substances is about
1000 times slower than the viscous dampening. Thus the wake will contain small
scale `frozen' filamentous and patchy structures of odour even after the
hydrodynamic disturbance that caused them is dampened out by viscosity. At the
time when the distinct hydrodynamic signature of a wake is lost the diameter
of the chemical trail will be about 10 times larger than the source. With
increasing age of the chemical trail, molecular diffusion and shear will
remove its remaining spatial structure and dilute its concentration into a
uniform background.
In a chemical trail a predator could use the degree to which small-scale
concentration fluctuations have been smoothed out within the trail to
determine the distance and direction to the source, independent of flow
conditions (Atema, 1996;
Westerberg, 1990
).
Fish are known to have extraordinarily sensitive chemical senses enabling
them to distinguish between different species and even individuals
(Brown and Smith, 1994;
Kleerekoper, 1969
;
Mann et al., 2003
). Olfaction
in fish is located exclusively in the nose, while gustation is perceived
inside the mouth and, in some fish, also on parts of the body surface. In
catfish there are high numbers of taste receptors on the whole body surface,
with highest densities on the barbels and in the head region
(Atema, 1971
). In catfish
gustation is the major chemical sense involved in foraging and feeding
(Atema, 1971
;
Todd, 1971
;
Wunder, 1927
). Bullheads
(Ictalurus natalis and I. nebulosus) are able to locate
stationary food by their chemical sense alone using true gradient search
(Bardach et al., 1967
;
Johnsen and Teeter, 1980
);
when locating dead meat the external taste sense is used exclusively
(Atema, 1971
).
In the present study we compared the foraging behaviour of catfish with ablated lateral lines or ablated external gustation to that of intact catfish, in order to study the involvement of these senses in wake following. We used a video-based infrared (IR) illuminated system allowing 3-D evaluation of the animal behaviour with the exclusion of visible light.
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Materials and methods |
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Guppies Poecilia reticulata (Peters 1859) were chosen for their
slow swimming behaviour and for their low tendency to thigmotactic (wall
hugging) behaviour, minimising wall effects. They mostly use push-and-coast
swimming, the hydrodynamics of which are well described
(Müller et al., 2000;
Videler et al., 1999
). Guppies
(total length 2.0-5.1 cm) were obtained from a local aquarium fish supplier.
Four different catfish Silurus glanis (Linnaeus 1758) were used as
predators, total lengths 20-31 cm. They were obtained from an aquaculture
facility (Ahrenhorster Edelfisch, Badbergen, Germany) 7 weeks prior to the
first trials and had been fed with live fish ever since to ensure their
familiarity with living piscine prey. All fish were kept in holding tanks in
the experimental room so they were subjected to the same temperature
(18°C) and light regime (12 h:12 h light:dark cycle with dawn and dusk
periods simulated by 30 min of lower light intensity). Catfish were kept
individually in holding tanks and returned to these tanks after each trial.
Between trials each individual catfish spent at least one day unfed in its
holding tank. Guppies were kept in one large holding tank as a group of about
100 fish.
The experimental tank was cleaned and filled with aged, non-chlorinated
tapwater at ambient temperature before each trial, because catfish are known
to deploy aggressive territorial behaviour to the chemical stimulus of another
catfish (Todd et al., 1967).
After the catfish was acclimated in the experimental tank for at least 1 h in
darkness each trial started with the introduction of a single guppy. For this,
the investigator entered the experimental room through a double curtain to
ensure total darkness and added one individual guppy with a small amount of
water (<50 ml) into the middle of the experimental tank. 5 min after the
prey had been consumed (viewed on monitors next door) the next guppy was
added. To avoid satiation a trial ended when 10 guppies had been eaten. A
trial was aborted when the added prey fish was not consumed within 20 min.
Thus, in each trial 0-10 guppies could be consumed.
We ran 16 trials for each of three treatments: intact catfish (control), catfish with ablated lateral lines, and catfish with ablated external taste. Each trial consisted of the subsequent addition of 1-10 guppies, depending on the number of captures.
We compared the behavioural performance after the two ablations with the
behaviour of the same fish before ablations. The control data were part of the
data reported previously (Pohlmann et al.,
2001).
Ablations
Ablation of the lateral line using CoCl2 is reversible. We used
the same four catfish as in the control trials. A single catfish was put into
an incubation tank containing calcium-free artificial freshwater with 0.5 mmol
l-1 CoCl2 (Karlsen
and Sand, 1987). Calcium counteracts the effect of
CoCl2 by competitively displacing it. Added to Ca2+-free
water, cobalt ions fully suppress the lateral line function without affecting
the inner ear (Karlsen and Sand,
1987
). Co2+ is thought to block the hair cell
sensitivity by competitively inhibiting Ca2+ flux through membrane
channels, thus inhibiting the receptor current in lateral line hair cells or
by modifying the permeability of the transducer membranes to other ions.
The artificial freshwater was made by adding stock solution (1.78 mmol
l-1 KCl, 3.57 mmol l-1 KNO3, 3.57 mmol
l-1 NaH2PO4, 7.14 mmol l-1
MgSO4 and 14.28 mmol l-1 NaCl) to deionized water until
the conductivity had reached 350 µS cm-1, matching the
conductivity in the catfish holding tanks; NaOH was added to match the pH at
7.6 (modified after Karlsen and Sand,
1987). Catfish were kept in the CoCl2 solution for 6 h
prior to transfer into the test tank filled with artificial calcium-free
freshwater. The catfish was left to acclimate there for 1 h prior to the start
of a trial. The maximum time a catfish spent in the test tank was 3 h, which
is well within the time (over 24 h) that the total ablation of the lateral
line persists in calcium-free water
(Karlsen and Sand, 1987
). To
evaluate if lacking motivation was the reason that catfish did not attack prey
in some trials, we offered those catfish a fresh guppy directly in front of
their mouth after each trial without captures. For data analysis only, trials
were included in which the catfish subsequently readily took this fish. To
test for possible effects of the calcium-free artificial freshwater we ran one
trial similar to the lateral line ablation trials but without CoCl2
in the incubation tank. The feeding behaviour was similar to that of the
control trials (data not shown).
The ablation of the external taste is invasive and irreversible. It was
done 2 months after the end of the lateral line ablations. We only
taste-ablated animals that had been used in the control and (reversible)
lateral line ablation experiments to have comparable data for individual
animals motivated to track. We removed the dorsal (chemosensory) area of the
bilateral facial lobes in the dorsal medulla oblongata using the method
developed earlier (Atema,
1971). This brain lesion was developed for a related species,
Ictalurus nebulosus, where this external taste system is necessary to
localise dead meat (non-moving, odorous food) and to trigger food pick up. It
remains the only procedure to eliminate exclusively this one chemosensory
system that guides the catfish's localisation behaviour for dead meat. The
taste system of fish consists of two distinct parts. The one that we ablated
is innervated by the facial nerve (VII), subserving all taste buds on the body
skin, lips, and anterior part of the mouth and ends in the facial lobe in the
dorsal medulla oblongata. We did not ablate the other taste system that
contains the taste buds on the posterior part of the mouth and on the gill
arches, and is innervated through nerves IX and X ending in bilateral vagal
lobes in the dorsal medulla oblongata, because vagal lobe ablation blocks
swallowing, not locating behaviour (Atema,
1971
).
We evaluated the success of the ablation after surgery and after every other trial by offering the catfish a piece of liver in the experimental tank. Liver was our catfish's favourite food and intact fish show strong searching behaviour immediately after introduction of liver to the tank finding and consuming it within seconds. Catfish with ablated external taste, both Ictalurus nebulosus and Silurus glanis, took a long time to locate the food despite repeated chance contacts and close passes.
According to these criteria the taste ablation was successful in 2 of the 4 animals used earlier. By running 16 trials between both animals we ensured sufficient sample size.
Again, after each trial without attacks we put a fresh guppy onto the catfish's lips to evaluate hunger/motivation. In all these tests the guppy was immediately consumed.
Parameters and evaluation
We determined all attacks by reviewing the video recordings of top and side
view. Attacks consisted of successful captures and of snaps not leading to
capture but directed at the guppy from a distance of less than 2 cm. Both
unsuccessful attacks and captures show that the prey had been accurately
localised by the predator. For each trial we recorded the time between
introduction of prey and first attack and the time from introduction to
capture (further referred to as `time-to-first-attack' and `time-to-capture').
From the video recordings we further determined if the guppy was moving prior
to the attack. All attacks were categorised based on the video recordings as
one of three types: (1) wake-following: the predator swam along the same path
as the moving prey, eventually attacking it; (2) head-on encounters: the
predator encountered moving prey without prior path similarity; (3) attacks on
stationary guppies. In a previous study we showed that our categorisation was
justified by quantitatively analysing a sub-sample of the swim paths,
calculating similarity indices between swim paths of predator and prey, and
cross-validating our classification on the basis of these similarity indices
(Pohlmann et al., 2001).
To determine the time spent close (within 4 cm) to prey while tracking we
analysed all tracking events leading to attacks in both ablation treatments as
well as 22 sequences of tracking in the control trials. Those latter were the
same sequences used earlier to quantitatively confirm the categorisation of
capture behaviour (see Pohlmann et al.,
2001).
Two wake-tracking sequences, one control sequence and one sequence of taste-ablated catfish, were digitized (at 25 Hz; Adobe Premiere 5.1, Adobe Systems, Mountain View, CA, USA) and the positions of the tips of the heads of both predator and prey were manually tracked using motion analysis software (Winanalyze 1.1, Weinberger, Karlsruhe, Germany). The resulting three-dimensional swim paths of predator and prey were plotted after smoothing with a running average of 5 points to eliminate tracking inaccuracies (see Fig. 1).
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We used logistic regression analyses with post-hoc contrast analyses for pairwise comparison (JMP 4.02) to determine differences across treatments in `time-to-first-attack', `time-to-capture', `time spent close to prey while tracking' and in `time spent hovering'. Hovering was a behaviour observed particularly in catfish with ablated lateral lines, in which their elongated confluent fins were undulating while the fish stayed in place.
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Results |
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In trials with lateral-line ablated fish, 18 guppies elicited 18 attacks of which only three were successful (see Table 1).Almost all attacks (88%) in the lateral line ablation trials were categorised as head-on encounters; one attack (6%) was directed toward a stationary guppy and one attack was categorised as wake following. The latter, however, occurred close to a wall and the path similarity was short so that it may have been incidental. In comparison to the control trials, lateral line-ablated animals showed a somewhat altered swimming behaviour: they spent significantly more time hovering in one place than control or taste-ablated animals (Fig. 2D). They also pushed their heads more strongly into the aquarium corners without the forward probing with their maxillary barbels, typical of intact catfish.
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When the external taste was ablated, 56 guppies elicited 67 attacks of which 40 were successful. We categorised 27% of all attacks as wake-following, 58% as head-on encounters and 15% as attacks on stationary guppies (Table 1). The capture success rates (captures/all attacks) were similar in the control and the taste ablation trials (0.66 and 0.6, respectively), but much lower in the lateral line ablation trials (0.17).
The percentage of wake-following was highest in the control, intermediate in the taste ablation and lowest in the lateral line ablation trials (see Table 1). When following wakes, taste-ablated catfish spent significantly more time close to the guppies (within 5 cm of the prey) before attacking than intact animals (Fig. 2C; P=0.0119, d.f.=1, F=6.988; Fig. 1: compare shorter distances indicating close following between C3 and G3 in A with C3 and G3 in B). In the taste ablation trials there were an additional 12 sequences of obvious wake-following which did not lead to an attack. This was observed only twice in the control trials and never in the lateral line ablation trials. Finally, in the control and lateral line ablation trials but not in the taste ablation trials the catfish showed an interest (spending time and repeated returning) in places where the guppy had hung out recently, indicating the possible detection of chemical traces from the prey.
With all three treatments, stationary guppies were attacked less frequently than expected from the (high) percentage of time they spent resting compared to the time they spent swimming.
The time-to-first-attack was significantly longer in the lateral line ablation trials than in the control trials, while there were no significant differences between the taste ablation and the control trials (Fig. 2A). The time-to-capture was significantly longer in the lateral line ablation trials than in both the control and the taste ablation trials, but there was no significant difference between control and taste ablations (Fig. 2B). Note that in the lateral line ablation trials the number of observations was very low because without a functional lateral line only three guppies were captured successfully.
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Discussion |
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The lateral line may also play a role in feedback about the catfish's own
locomotion. The ability of trout to hold station behind a solid object in fast
flowing water requires an intact lateral line organ
(Montgomery et al., 2003). In
our study, lateral line-ablated catfish altered their swimming behaviour in
the absence of visual information, with extended instances of hovering in one
place. However, the altered swimming behaviour of the catfish predator cannot
be the reason for the observed predation differences, because even in trials
with little or no hovering (7 or 4 out of 16 trials, respectively) the numbers
of attacks and captures were considerably diminished compared to the controls
and no wake-tracking occurred.
Our CoCl2 concentrations (0.5 mmol l-1) and exposure
time (9 h) were well below the toxic level reported by Karlsen and Sand
(1987) for roach (1 mmol
l-1, 1-2 weeks exposure) and by Janssen
(2000
) for Mexican blind
cavefish (2 mmol l-1, 10-17 h). In addition, toxicity is always a
function of body mass and our catfish were much larger than those utilised in
the above-mentioned studies. Janssen
(2000
) found an increased
swimming activity, change of spatial use and strong mucus excretion prior to
the death of the cobalt-exposed fish. Our catfish, in contrast, decreased
their movement and did not alter their spatial use of the test tank; neither
in the incubation tank nor in the test tank did they show any enhanced mucus
production. None of our catfish died during the entire study and their
behaviour after recovery in tapwater was unchanged. The fact that lateral
line-ablated catfish readily consumed dead fish confirm findings by Enger et
al. that cobalt treatment does not noticeably reduce feeding motivation
(Enger et al., 1989
). Cobalt
does not impair olfaction in the sublethal concentrations applied in this
study (Brown et al., 1982
).
Altogether, this gives us confidence that the altered swimming and
prey-following behaviour was not caused by cobalt toxicity.
We do not exclude the possibility that internal gustation or olfaction were
involved in the decision to follow a detected wake or to trigger an attack.
But those senses alone did not suffice to follow wakes or readily attack prey,
as shown by the lateral line ablation trials. Despite the obvious importance
of the lateral line for finding the prey, we recorded 18 attacks of lateral
line-ablated animals on guppies. These attacks were in general (88% of all
attacks; Table 1) head-on
encounters that could have occurred by chance or been elicited by chemical,
electro- or auditory receptors. All these alternative receptors, however,
could not compensate for the lack of wake-tracking performance caused by
lateral line ablation (see also Pohlmann
et al., 2001).
External taste on the other hand, while critical for locating dead meat,
does not seem to be mandatory for recognising and following wakes, since
catfish with their external taste ablated still showed a considerable
percentage of wake-following prior to attacks and no delay in
time-to-first-attack or time-to-capture. That the percentage of wake-following
here was lower than in the control is the result of our decision to exclude
instances of apparent wake-following that did not lead to attacks
(Table 1). These were excluded
because we could not be certain if any overlap of trajectories not leading to
attacks, particularly short segments, were accidental or the result of the
predator's recognising the wake of the prey. Including the 12 obvious
instances would bring the percentage of wake-following to 50%, comparable to
that of the control experiments. This and the observation that prey fish were
attacked after a longer period of closely following the prey suggests that
external gustation may normally help trigger the actual attack, as described
for the pick-up response of non-moving food items in bullhead catfish
(Atema, 1971). Perhaps
olfaction, or internal taste stimulated by odour entering the mouth cavity
with the respiratory flow, partially supplemented the missing external taste
before the - delayed - final strike. This trigger delay in taste-ablated
animals is seen both in the significantly extended time spent close to prey
when tracking (Fig. 2C) and in
the instances when wake-following catfish did not strike at all. Apart from
the longer hesitation before the actual attack and the resulting extended
tracking distance, the wake-tracking behaviour of taste-ablated animals did
not differ in terms of swim path resemblance or swimming behaviour from that
of intact catfish we described earlier
(Pohlmann et al., 2001
). No
casting movements of the catfish across the guppy's swim path were observed in
any of the treatments (see Fig.
1B), but one has to keep in mind that the catfish head including
barbles is wide enough to cover an even somewhat aged trail of a small
guppy.
The physiological and morphological properties of the lateral line sensory
system and its neuronal processing have been studied in detail (Bleckmann,
1993,
1994
). Sensitivity, frequency
resolution and directionality have been investigated with artificial stimuli
(mostly vibrating spheres). The biological significance of lateral line
systems, however, can only be recognised by studying the behaviour in its
natural context (Bleckmann,
1993
). The lateral line system has been shown to be involved in
many different behaviours such as detection and localisation of stationary
objects (Abdel-Latif et al.,
1990
), obstacle entrainment and rheotaxis in fast-flowing streams
(Baker and Montgomery, 1999
;
Montgomery et al., 1997
,
2003
;
Sutterlin and Waddy, 1975
) and
intraspecific communication such as schooling
(Partridge and Pitcher, 1980
;
Pitcher et al., 1976
) and
mating (Satou et al., 1993
,
1994
). Lateral line
involvement was also shown in different feeding behaviours of fish. Surface
feeding by topminnows, Aplocheilus lineatus, on struggling prey is
mediated by the head lateral line
(Bleckmann, 1980
;
Bleckmann and Schwartz, 1982
).
Here distance determination by lateral line analysis of water surface waves
requires only one intact canal organ, while determination of source direction
depends on the spatial interaction of several organs
(Bleckmann and Schwartz,
1982
). The lateral line is further involved in detection and
localisation of live zooplankton and crustaceans
(Hoekstra and Janssen, 1985
;
Montgomery et al., 1995
;
Montgomery, 1989
;
Montgomery and Hamilton,
1997
). Blinded sculpins Cottus bairdi consume live prey
and react to other moving objects but ignore dead prey. Inactivation of the
lateral line eliminates the feeding response to live prey
(Hoekstra and Janssen, 1985
).
The spatial integrity of lateral line organs also seems to be necessary for
correct directional response in the sculpin.
There are only two studies in which the involvement of the lateral line was
tested in piscivorous fish, both using diurnal visual predators. Blinded pike
Esox lucius, which are visual ambush predators, attack live fish from
distances of up to 10 cm only if their lateral line is intact
(Wunder, 1927). Intact
bluegills Lepomis macrochirus attack live fish in the absence of
visible light when it is moving or after touch
(Enger et al., 1989
). When
their lateral line is ablated they attack prey only after touch. We made
similar observations with rather non-visual catfish.
Montgomery et al. hypothesise that deteriorating visual conditions may
increase the importance of lateral line cues
(Montgomery et al., 1995).
They report an observation on estuarine star-gazers Leptoscopus
macropygus, which initiated a strike in complete darkness when the front
of the prey had just barely passed over the mouth without touch. This rapid
strike mechanism is activated by lateral line input. They argue that the short
range of the lateral line system is often seen as a disadvantage, but in terms
of initiating a strike it does have the benefit of indicating the close
proximity of the prey without the need for sophisticated central processing to
determine target range. This is clearly different in the wake-following we
observed: here, catfish follow a series of past locations constituting the
trail that leads to the prey, thus deriving directional information. Even in
our spatially limited tank we found wake-tracking over distances as long as
120 cm. Our study shows for the first time that fish evolutionarily adapted to
conditions of limited visibility are utilising the lateral line to detect and
follow the trails left by their prey. Using the hydrodynamic trail will
considerably enhance the encounter probability under natural circumstances.
Trail following was also reported for copepods following the trails of their
mating partners (Doall et al.,
1998
). However, copepods were found to use chemical and not
hydrodynamic cues in the wakes (Weissburg
et al., 1998
).
Our finding that nocturnal piscivores follow hydrodynamic cues in the wake
of potential prey fish extends the classical definition of predation tactics
in fish. Wake-tracking can be categorised as stalking behaviour, which is
normally considered to have a major visual component
(Keenleyside, 1979).
Fish behaviour and predation strategies are plastic and catfish can deploy a variety of strategies, depending on the environmental conditions and the nature of their prey. Wake-following is not the only predatory strategy, as shown in our ablation experiments, but certainly important under natural conditions, because being able to utilise wakes dramatically extends the space in which the presence and location of prey is detectable. Catfish are slow predators that have little chance to capture prey in light conditions when prey are aware of their approach (J.A. and K.P., personal observation). Both Silurus glanis and Ictalurus nebulosus do not even respond to the visual presence of small goldfish in well-lit tanks but attack the prey after chemically or hydrodynamically detecting their presence (J.A. and K.P., personal observation). Thus capture success of a slow predator should improve by searching for and tracking prey in the dark when the prey is visually less defended, and approaching from behind where all sensory systems of the prey (e.g. lateral line, olfaction) are less likely to detect the predator's approach.
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Acknowledgments |
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Footnotes |
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