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First published online August 17, 2007
Journal of Experimental Biology 210, 2979-2989 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.006437
Swimming in the upside down catfish Synodontis nigriventris: it matters which way is up
Department of Zoology, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada
* Author for correspondence (e-mail: blake{at}zoology.ubc.ca)
Accepted 27 June 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: drag, steady swimming bouts, fast-starts, body posture and orientation, depth, feeding, ventilation
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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In addition to frictional and pressure drag, fish swimming close to the
air–water interface experience wave drag. The surface wave pattern
generated is similar to that of a ship hull (Kelvin wave system)
(Lighthill, 1978
). The wave
pattern is generated by two moving pressure points, one downstream and one
upstream of the fish. These two wave systems interfere, depending on speed
relative to length. At certain speeds, transverse wave crests from the bow may
combine with those from the stern producing a large wave train and, at others,
the bow and stern wave systems cancel producing a small wave train. A second
component of the wake consists of a diverging wave system with two wake lines
forming the arms of a `V' (Crawford,
1984). A distinction can be made between the effects of wave drag
on forms that are at or near the air–water interface in shallow
versus deep water. The former case is more complex because of surface
wave and bottom interactions.
Few studies address drag at the air–water interface and its
biological significance. Swimming at or near the air–water interface in
deep water (i.e. no bottom interactions), dispersive surface waves increase
the propulsive energy required relative to deeply submerged swimming
(Hertel, 1966;
Hertel, 1969;
Prange and Schmidt-Nielson,
1970; Williams and Kooyman,
1985; Stephenson et al.,
1989; Webb et al.,
1991). The drag of a rigid body moving at constant velocity just
below the surface is about five times that when deeply submerged
(Hertel, 1966). It has been
suggested that porpoising in penguins, sea lions, seals and dolphins is a
locomotor strategy to avoid the high energy cost of moving near the
air–water interface (Au and Weihs,
1980; Blake, 1983).
A pioneering study showed that for rainbow trout Oncorhynchus mykiss
fast-starting in shallow water, distance traveled after a given time is a
positive function of water depth (Webb et
al., 1991). Near the surface, up to about 70% of the mechanical
work generated by the fish is lost. This has critical fitness significance, as
many piscivorous fish force their prey into shallow water
(Schlosser, 1987).
The genus Synodontis (Mochokidae, Siluriformes) is a monophyletic
group (Mo, 1991) containing
118 species, endemic to tropical African lakes and streams
(Teugels, 2003). Many
mochokids are benthic, nocturnal or crepuscular and feed on small
invertebrates and algae (Lowe-McConnell,
1975; Burgess,
1989). Some Synodontis species occasionally swim
inverted, e.g. S. contractus, S. multipunctatus, S. membranaceus
(Burgess, 1989); S.
nigriventris habitually does so for feeding (surface zooplankton, insect
larvae and fine detritus) and aquatic surface respiration (ASR) in hypoxic
waters (Chapman et al.,
1994).
The hydrodynamics of inverted swimming in S. nigriventris has not
been previously studied. However, the associated adaptation of reverse
countershading is well understood. The upward facing ventral surface is darker
at night and contains large numbers of melanophores at high density. Pigment
migration into the ventral melanophores is mediated by a higher concentration
of norepinephrine than that for the dorsal melanophores
(Kasukawa et al., 1986;
Nagaishi et al., 1989).
Melanosome dispersion (agented by adenosine, beta-agonists and alpha-MSH) in
the ventral skin is more effective than that in the dorsal skin
(Nagaishi and Oshima, 1989).
The mechanisms for regulating pigment migration in the melanophores maintain
the relative darkness of the ventral skin, effectively concealing the fish
when viewed from above at night (Nagaishi
and Oshima, 1989).
Several authors have suggested that inverted swimming in S.
nigriventris facilitates feeding at the surface and on the underside of
leaves (Bishai and Abu Gideiri,
1963; Lowe-McConnell,
1975; Gosse, 1986;
Burgess, 1989). ASR under
hypoxic conditions was compared in S. nigriventris and S.
afrofisheri (which does not swim inverted)
(Chapman et al., 1994). S.
afrofisheri air breathes by positioning its body nearly perpendicular to
the water surface and is highly active. In contrast, S. nigriventris
swims inverted at a shallow angle and swims slowly, implying a higher
respiratory efficiency (Chapman et al.,
1994). Functional interpretations of inverted swimming in the
context of feeding and respiration are not mutually exclusive and metabolic
energy must be expended to overcome the hydrodynamic resistance of motion in
both activities.
Constant speed (steady) and fast-start (unsteady) swimming near the
air–water interface has relevance to many fish in the context of
feeding, e.g. exploiting allochthonous sources
(Moyle and Cech, 1988), ASR
(Chapman et al., 1994) and
predator–prey interactions (Webb et
al., 1991). S. nigriventris is vulnerable to piscivorous
and aerial predators and acceleration (fast-starts) allows for escape from
both. It was hypothesized that: (1) based on known values for technical
streamlined bodies (Hertel,
1966; Hertel,
1969), the drag at the air–water interface would be x5
higher than that when deeply submerged due to energy losses from wave
generation; (2) Drag would be posture dependent (dorsal side up
versus inverted) because the fish approximate 3-D technical bodies of
triangular section where drag is posture dependent [drag coefficients of 0.7
and 1.1 for apex and base directed into the flow, respectively
(McCormick, 1979)]; (3)
increased drag in surface proximity relative to that when deeply submerged for
both postures would require increased thrust and be reflected in increased
tailbeat frequency at any given velocity; (4) fast-start swimming performance
at the air–water interface would be inferior to that when deeply
submerged (lower velocity and acceleration and higher propulsive energy cost
due to energy losses from wave generation) and also posture dependent.
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Materials and methods |
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Live fish were terminated with MS 222 shortly before being weighed in air
and water (to ±0.001 g; Mettler PK300 scale, Columbus, OH, USA, with
manufacturer's suspension apparatus) and fish density (
f) was
calculated from:
f=(Wa–Wo)–1
Waw, where Wa,
Wo and w were weight in air, weight in
water and water density, respectively. The centre of mass of each fish was
determined by suspending the fish from the mouth and marking the vertical line
of gravity, then repeating this procedure with suspension from the cloaca. The
centre of mass was the point where the two lines crossed.
Swimming behaviour
Five live fish were obtained from a commercial dealer and held in a 0.60
mx0.30 mx0.40 m aquarium with gravel bottom, natural plants and
ironwood branches, containing fresh, aerated, dechlorinated water and 0.3%
salt at 25±1°C. The natural routine swimming behaviour of the fish
during the day (illumination by fluorescent lights for 12 h from above) and
night (12 h illumination by infrared lamp, PAR38, Jieneng Special Lighting and
Equipment Ltd., Xiaogan, Hubei, China) was recorded on video tape (Sony
DCR-TRV280, IR enabled; Hi8 120 min tapes) for 2 h in daylight and under
infrared light for a period of 5 days. It was unlikely that the fish could
detect the infrared light (Lythgoe,
1988).
Drag
Measurements were made in a PerspexTM re-circulating flow tank (1.84
mx0.52 mx0.22 m). A 0.5 h.p. electric motor (1 h.p.=745.7 W)
rotated a propeller (0.16 m diameter) to produce flow. Water velocities were
measured using a current meter (12.400±0.005 m s–1; A.
OTT Kempton TYP., Bayern, Germany) placed 1.25 m down from a flow-rectifying
grid (0.21 mx0.20 m) made of straws (0.5 cm diameter) located just in
front of the propeller. Wall interference effects were assumed to be small as
the ratio of the width of the flow tank and fish was of the order of 10.
Drag (D) was measured with a force transducer (an aluminum spar of length 10 cm, width 0.7 cm and thickness 0.1 cm, respectively) attached to a strain gauge bridge, connected to a digital electronics board, calibrated with weights (1.5 g; Sto-A-Weigh, Pinebrook, NJ, USA) and mounted on a vertical adjustable stand, allowing the spar to be placed accurately at different depths below the water surface.
Force transducer accuracy and precision were determined by comparing the
measured drag coefficient
[CD=2D(wApV2)–1]
of a three-dimensional PerspexTM plate (0.6 cmx2.5 cmx2.5 cm)
oriented normal to the flow with established technical values (1.17)
(Hoerner, 1965) at Reynolds
numbers 103–104
(Re=LVv–1, where V and
were water velocity and kinematic viscosity of water, respectively). The
drag on the spar was subtracted from that of the plate and spar together to
give the drag of the plate. The measured average normal drag coefficient based
on ten repeated measurements was 1.22±0.04 (mean ± 2 s.e.m.) for
Re
1.8x103, which was close to that
expected.
Fish were attached to the spar in a natural position oriented with their
long axis parallel to the flow with median fins (two dorsal and two pelvic)
and caudal fin deployed and kept rigid by a thin steel wire to minimize body
and/or fin flutter (Webb,
1975). Total drag was determined by subtracting the drag of the
fish and spar together from that of the spar. Drag measurements (dorsal side
up and inverted) were made at four water velocities (0.38 m
s–1, 0.47 m s–1, 0.55 m
s–1, 0.63 m s–1) and at fifteen different
depths dw [depth from the bottom of the flume to the point
of maximum body depth at 0.31±0.01 l (mean ± 2 s.e.m.);
0.032–0.102 m]. The drag coefficients
[CD=2D(wApV2)-1]
for all fish and water velocities (N=20) were calculated using the
drag force measurements and morphological data
(Table 1). Drag at body
orientation angles (angle of the long axis of the body to the horizontal) of
20°, 45° and 90° was calculated for both postures at and near the
surface (0.032 m, 0.037 m and 0.042 m).
Steady swimming bouts
Fish were filmed using a high-speed camera (125 Hz; Troubleshooter, Model
TS500MS, Fastec Imaging, San Diego, CA, USA; Berkey Coloran Halide 650 W bulb)
in a tank (2.45 mx1.22 mx0.47 m; depth0.3 m;
25±1°C) as if from above with a mirror angled at 45°. A
removable rigid plastic grid (1.65 cm2 cells) was fitted tightly to
the interior walls of the tank. For each of five fish, 5 measurements were
made for each posture at water depths
[depth set by removable
plastic grid (1.65 cm2 cells) fitted tightly to the interior walls
of the aquarium to the point of maximum body depth at 0.30±0.01
TL; 0.025 m, 0.04 m and 0.09 m] corresponding to submersion depth
indices (h/d, where h was the distance from the water
surface to the centre line of the fish and d was maximum body depth)
of 0.6, 1.2 and 3.4, respectively (Table
2). Feeding ceased the day before experiments to ensure a
post-absorptive digestive state (Beamish,
1964). Fish outlines from video segments (7–10 tailbeats
with no wall interference) were analyzed by ImageJ (National Institutes of
Health;
http://rsb.info.nih.gov/ij).
Tailbeat frequency (number of tailbeat cycles, tail movement from one side of
the body to the other and back again, divided by duration), amplitude
(distance between the lateral most positions of the tip of the tail during one
complete tailbeat cycle), stride length (speed divided by tailbeat frequency),
propulsive wave velocity (time between peaks in lateral displacement between
the tip of the snout and tail divided by body length) and propulsive
wavelength were determined.
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Wavelength was determined following published methods
(Dewar and Graham, 1994;
Donley and Dickson, 2000). The
time between peaks in lateral displacement at the tip of the snout and tail
was measured (lateral displacement over time for the wave of undulation to
pass). This was repeated 10 times for each steady swimming bout to obtain a
mean progression time. Propulsive wave velocity was obtained by dividing the
body length by the mean progression time, and was divided by tailbeat
frequency to give propulsive wavelength.
Fast-starts
An aquarium (0.35 mx0.21 mx0.24 m) covered with black paper was
filmed from above (250 Hz). Fish were acclimatized for 1 week to experimental
lighting conditions (Halide 650 W bulb). Feeding ceased the day before
experimentation. Fast-starts were induced by striking the side of the aquarium
with a plastic bulb attached to a 1 m pole and filmed at three water depths
[depth set by the removable
plastic grid (1.65 cm2 cells) fitted tightly to the interior walls
of the aquarium to the point of maximum body depth at 0.30±0.01
TL; 0.025 m, 0.04 m and 0.09 m]. One measurement (distance/time) for
each posture was made per fish (N=5) per day (total of 30
measurements) to allow for recovery. Video sequences of the escape responses
(against the rigid plastic grid) were analyzed using ImageJ
(http://rsb.info.nih.gov/ij/).
Following Webb (Webb, 1976),
we digitized the centre of mass of the stretched straight fish as a reference
point (located by measuring the length of the midline from the tip of the
rostrum to 0.37±0.01 TL) and the tip of the rostrum. Duration,
distance, average velocity and acceleration, maximum velocity and acceleration
were measured for the centre of mass. The velocity and acceleration data were
derived from the raw distance-time data by using a five-point smoothing
regression (Lanczos,
1956).
Energy loss from wave generation near the surface was estimated following
Webb et al. (Webb et al.,
1991), by comparing the average work performed by a `control fish'
(Wc; i.e. a fish swimming deeply submerged, in this case
0.09 m): Wc=2m(1+
)s
2ct–2, where was the
longitudinal added mass coefficient (representing the mass of water entrained
by the accelerating fish), sc was distance traveled by the
control fish and t was time. It was assumed that the fish perform the
same amount of work regardless of water depth. This assumption is reasonable
for a fast-start response where it can be presumed that performance is
maximized (Webb et al., 1991).
The longitudinal added mass coefficient is small (order of 0.2)
(Webb, 1982) and was assumed
to be unaffected near the surface. The proportion of energy lost
(Wd) relative to the control fish was
Wd=1–(s 2ts
–2c), where st was distance
traveled by fish in shallow water (i.e. water depths of 0.025 m and 0.04
m).
Statistics
The effect of body posture on drag, steady swimming bouts and fast-start
performance was compared by employing independent two-sample t-tests.
The effects of body orientation angles on drag and the effects of water depth
on fast-start performance (duration, distance, average velocity, maximum
velocity, average acceleration, maximum acceleration) were determined by ANOVA
(SPSS 13.0 for Windows). The locations of any significant differences were
obtained from the Student–Newman–Keuls test. Drag coefficients and
densities for S. nigriventris and other catfishes were compared using
one-sample t-tests (Zar,
1999). The null hypothesis was rejected at P=0.05 in all
cases.
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Drag was proportional to velocity squared in all cases
(D=aV2+bV+c, where a, b and c were
depth-dependent constants; r2>0.95) and decreased with
water depth for both body postures (Fig.
1). Inverted drag was about 15% less than that for dorsal side up
in surface proximity (N=120; P<0.05) with no postural
effects when deeply submerged (N=120; P>0.05). The drag
augmentation factor (
, defined as the ratio of drag in surface
proximity to that deeply submerged) was a function of the submersion depth
index (h/d; Fig. 2)
and maximal (2.0) for both postures near the water surface
(h/d0.5), vanishing (i.e. =1.0) when h/d2.7
(depth9 cm).
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All fast-starts were rectilinear (Fig. 4B) and away from the stimulus. Average and maximum velocity and acceleration decreased in surface proximity (N=15; P<0.05; Table 3). Performance levels in all categories were higher for the inverted posture (N=10; P<0.05). The proportion of energy lost in wave generation increased with decreasing h/d for both postures (Fig. 6). At submersion depth indices of 0.6 and 1.2, the losses inverted were about half of that for dorsal side up.
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2.0 for h/d=0.5
and h/d2.7 for =1 (Fig.
2). The drag of streamlined technical bodies in surface proximity
(Hoerner, 1965;
Hertel, 1966;
Hertel, 1969) has been
employed to assess the swimming energetics of marine mammals
(Au and Weihs, 1980;
Blake, 1983;
Blake, 2000) and penguins
(Blake and Smith, 1988). At
Reynolds numbers >106, drag augmentation due to gravitational
waves on a streamlined body close to the surface (h/d0.5) may be
x5 that when deeply submerged and vanishes for h/d>3 (i.e.
=1) (Hertel, 1966;
Hertel, 1969). Whilst the
general trend of depth dependence of on h/d of S.
nigriventris is similar to that for streamlined technical bodies, the
magnitude of drag augmentation is about a half
(Fig. 2).
This reflects differences in Reynolds number (i.e. size and speed), Froude
number
[Fl=V2(gTL)–1,
where g is gravitational acceleration] and body form (a
streamlined circular axisymmetric section versus a broadly triangular
one). From a practical standpoint (e.g. scale model ship testing), it is
impossible to simultaneously scale both the Reynolds number and the Froude
number because their ratio
(g1/2TL3/2v–1)
must remain constant [see Newman, chapter 1, for details
(Newman, 1977)]. If length is
decreased, either the gravitational acceleration must be increased or the
kinematic viscosity decreased. However, a rough approximation allows for the
relative magnitude of the sum of frictional and pressure drag relative to that
of wave drag to be assessed (Newman,
1977; Lighthill,
1978):
D(0.5wApV2)–1=CD(Re,Fl)
and
CD(Re,Fl)
CF,P(Re)+CW(Fl),
where CF,P is the sum of the frictional and pressure drag
coefficient and CW is the wave drag coefficient.
Therefore:
CW(Re,Fl)=CD(Re,Fl)–CF,P(Re)
and the contribution of frictional and pressure drag and wave drag are about
equal (i.e. CF,P+CW=0.41,
CF,P=0.21; Table
4). Larger, faster bodies also generate drag components [e.g.
ventilation drag (arising from pressure differences between the anterior and
posterior of the form) and spray] not produced by S.
nigriventris.
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By convention, a plot of the square root of the Froude number
against
resistance is employed to assess the magnitude of wave drag generated by
bodies at or close to the water surface. Small wave drag peaks occur at
Fl0.2 and 0.3 and a large broad peak at the critical
Froude number (Fcrit) of 0.45 (e.g.
Lighthill, 1978). For
m (mean body length of the `drag tested' fish) over
a velocity range of 0.38–0.63 m s–1,
0.32<Fl>0.54. At Fcrit=0.45,
V=0.53 m s–1 (about 4 TL
s–1) in still water or holding position against a current of
the same speed. For the live fish (
m),
Fcrit=0.45 corresponds to V=0.35 m
s–1 (5.8 TL s–1). Specific swimming
speeds of this order are prolonged swimming (20 s to 200 min)
(Beamish, 1978), which ends in
fatigue. Limits to prolonged swimming duration near the surface may be set by
Fcrit. To exceed these speeds, the fish must swim out of
surface proximity. Night video recordings in a large aquarium showed that
rapid swimming to/from refuge is common (65% of time/activity frequency
distribution) and occurs deeply submerged. Upper values of velocity for
inverted, rapid constant speed swimming in the water column are 0.32 m
s–1 (Table 2:
h/d=3.4, velocity based on mean ± 2 s.e.m.), close to the
velocity corresponding to Fcrit (0.35 m
s–1). For S. nigriventris deeply submerged
(h/d>2.5),
CD(Re,Fl)=CF,P(Re)=0.21,
where 40 000<Re>91 000
(Table 4). In surface proximity
(h/d=0.5),
CD(Re,Fl)=CF,P(Re)+CW(Fl)=0.41
over the same Re range.
Drag inverted is about 15% less than that dorsal side up in surface proximity (N=120; P<0.05; Fig. 1). The power (P) required to overcome total drag is: P=DV, and this implies that swimming inverted at the air–water interface is energy efficient relative to swimming dorsal side up and that there is no relative hydrodynamic disadvantage to swimming inverted at depth.
Drag coefficients for S. nigriventris when deeply submerged are
less than those of rheotactic catfish (N=30–45;
P<0.05; Table 4).
S. nigriventris is neutrally buoyant [specific gravity1.01,
cf. S. afrofisheri (Chapman et
al., 1994)] similar to many nektonic fishes (e.g.
Aleyev, 1977)
(Table 2). Rheotactic catfishes
are characterized by high drag, density, morphological frictional adaptations
(e.g. frictional pads, odontodes) and armour (e.g. large opercular spines)
(Blake, 2006). S.
nigriventris is smooth skinned with small opercular spines and few
frictional adaptations.
Body orientation angle, drag and aquatic surface respiration (ASR)
Hypothesis 2 is supported; drag increases with body orientation angle
(N=60; P<0.05) and is lower for the inverted posture
(N=360; P<0.05; Fig.
3). When inverted at a low body orientation angle (
20°),
S. nigriventris presents a low drag streamlined profile to the flow.
With increasing body orientation angle, the form becomes less streamlined
until at 90° when the fish approximates a triangular form with apex
directed into the flow. If the zoological ventral side faced forward
(corresponding to the dorsal side up posture), the base of the triangular
section would face the flow. The drag coefficients of 3-D technical triangular
sections are higher when the base is directed into the flow
(CD=0.7 and 1.1 for apex and base directed into the flow,
respectively, Re>103)
(McCormick, 1979). The ratio
of the drag coefficients for the two directions of facing is 0.65, close to
that measured for Synodontis (0.68;
Fig. 3).
S. nigriventris and S. afrofisheri (dorsal side up
swimmer) are similar in form and respire at the surface when
PO2<15 mmHg, orienting their body at about
20° and nearly perpendicular to the surface, respectively
(Chapman et al., 1994). The
drag at 90° is 2.1–3.0 times that at 20° for a velocity range of
0.38–0.63 m s–1 for S. nigriventris
(Fig. 3). This suggests that
the resistance of S. afrofisheri is more than double that of S.
nigriventris during ASR. The inverted posture facilitates efficient
skimming of the well-oxygenated microlayer at the surface of hypoxic waters.
The mormyrid Petrocephalus catostoma swims inverted during ASR at a
body orientation angle of about 45° to the air–water interface
(Chapman and Chapman, 1998).
It is likely that drag will be independent of posture in P. catostoma
because of its symmetrical laterally compressed body form.
Steady swimming bouts and fast-starts
Speed increases with water depth for both postures (N=75;
P<0.05; Table 2),
supporting hypothesis 3. Increased drag at any given swimming speed at the
surface must be compensated for by an increase in thrust production. This is
reflected kinematically; at any given speed, tailbeat frequency and stride
length are higher and lower, respectively, in surface proximity for both
postures than that at depth (N=75; P<0.05;
Fig. 5). In addition, tailbeat
frequency is higher near the surface for dorsal side up relative to that
inverted (N=50; P<0.05). There is no significant
difference for slopes between the two postures deeply submerged
(N=50; P>0.05) where drag is posture independent.
Hypothesis 4 is supported; fast-start performance decreases in surface
proximity and is higher in the inverted posture
(Table 3). The decrement in
performance near the air–water interface can be attributed to energy
lost in wave generation. In surface proximity (h/d=0.6;
Fig. 6), about 40% of the
mechanical work was lost in wave generation in the dorsal side up posture and
20% when inverted. Maximum `inverted' accelerations (20–30 m
s–2; Table 3)
are comparable to those of trout (Domenici
and Blake, 1997) (see Table
1) and other locomotor generalists (sensu
Webb, 1984;
Blake, 2004). Energy losses due
to wave generation at a similar submersion depth index are less than for
rainbow trout (70%) in shallow water (Webb
et al., 1991). The reason for this is attributable to the
hydrodynamics of fast-start resistance in surface proximity for shallow
versus deep water.
Dispersive wave systems in shallow water are slowed down, changing the
relationship between wavelength and speed relative to deep water. Waves have
to become longer to maintain a given speed. There is a critical wave speed
(Vcrit) that cannot be exceeded:
[fig. 7 in Wellicome (Wellicome,
1967)]. For boats, when the non-dimensional parameter
is
<0.5, the resistance in shallow water relative to that in deep water is
about the same. However, resistance in shallow water rises sharply between
to three times that in deep water and falls rapidly for values of
.
For
,
the resistance in deep water is greater than that in shallow water [Fig. 7 in
Wellicome (Wellicome, 1967)].
The initial rise in resistance occurs because the transverse waves become
longer and steeper and require more energy to maintain at any given speed. The
resistance due to diverging waves remains as they travel much more slowly than
the transverse waves and are unaffected. Beyond Vcrit, the
transverse waves cannot keep up and cease to exist, hence resistance falls.
This analysis is based on steady motions. For unsteady motions, wave pattern
changes are time dependent and we assume that such effects are small given the
accelerations involved and a reasonable first approximation, justifying a
quasi-steady approach.
Webb et al. give a mean velocity of 0.5 m s–1 for the mean
distance traveled by the centre of mass over 100 ms with
dw=0.05 m corresponding to
[fig. 1 in Webb et al.
(Webb et al., 1991)]. For this
value, wave drag enhancement for shallow water relative to deep water is about
25% (Wellicome, 1967) (Fig.
7). Referencing velocity to the maximum distance traveled by the centre of
mass over the same period (mean ±2 s.e.m. of V=0.58 m
s–1) gives
,
corresponding to a 100% increase in resistance relative to deep water
(Wellicome, 1967) (Fig. 7).
Given this and the large amplitude C-start motions of trout relative to the
low amplitude fast-start pattern of S. nigriventris
(Fig. 4B), it is not surprising
that values of energy loss for trout fast-starting in shallow water
(Webb et al., 1991) are higher
than those for S. nigriventris in deep water.
The escape fast-starts of S. nigriventris are rectilinear,
directly away from the stimulus direction
(Fig. 4B), in contrast to the
common pattern of `C' or `S' starts (defined by body shape at the end of the
first contraction of the lateral musculature) employed by escaping prey and
attacking predators, respectively. However, some fish execute one type of fast
start for both behaviours [e.g. S-starts and C-starts for both prey capture
and escape responses in pike (Schriefer
and Hale, 2004) and archer fish
(Wohl and Schuster, 2007)
respectively]. In addition, whilst many piscivorous predator–prey
interactions occur on an essentially x,y-plane, some fish execute
escape responses that involve the acceleration of the centre of mass in three
dimensions [e.g. marbled hachet fish Carnegiella strigata
(Eaton et al., 1977),
knifefish Xenomystus nigri
(Kasapi et al., 1993) and
limnetic sticklebacks Gasterosteus spp.
(Law and Blake, 1996)].
Variability in fast-start behaviour for fish with different modes of life and
predator–prey relationships is to be expected. O'Steen et al.
(O'Steen et al., 2002) have
shown that fast-start behaviour is closely linked to survival and evolves
quickly with changes in predation pressure.
S. nigriventris in surface proximity is vulnerable to attack from
below and above. If the attack paths of both piscivorous and aerial predators
occur on planes at a high angle relative to the surface, the evasive
rectilinear response of S. nigriventris would quickly maximize the
distance away from an attack. Unfortunately, nothing is known about the
dynamics of natural predator–prey interactions in S.
nigriventris. Arguably, the classic, evasive C-start (two-dimensional
response) could also place the fish off a predator's attack path. However,
good C-start and turning performance are associated with lateral compression
and flexibility (Domenici and Blake,
1997; Blake, 2004)
and S. nigriventris is not characterized by these features.
Evolution of the inverted habit
Based on the Baldwin effect (selection of general learning ability with
selected offspring tending to have an increased capacity for learning new
skills), Dawkins suggests that inverted swimming in S. nigriventris
evolved by natural selection favoring individuals that learned to exploit food
from the water surface and underside of floating leaves [p. 401 in Dawkins
(Dawkins, 2005)]. Selection
has favoured this propensity to learn to the point where the behaviour has
become instinctive. Nocturnality (low competition for resources and low
predation pressure relative to the diurnal situation), reverse countershading
and ASR likely co-evolved with the inverted habit.
Koblmüller et al. analyzed the mitochondrial control region of the
NADH dehydrogenase subunit 6 gene to establish a phylogeny in West and Central
and East African synodontids
(Koblmüller et al.,
2006). A composite consensus phylogenetic tree suggests that a
Central and/or West African common ancestor gave rise to Chiloglanis
sp., Microsynodontis batesii and the genus Synodontis. Major
cladogenetic events for Synodontis [estimated employing the r8s
computer model for inferring absolute rates of molecular evolution and
divergence times in the absence of a molecular clock
(Sanderson, 2003)] give the
age of the genus at about 35 million years. The oldest fossil records of
Synodontis are earlier than 20 million years old
(Stewart, 2001). At about 20
million years ago, six major lineages of Synodontis diverged from a
Central and/or West African ancestor in East Africa
(Koblmüller et al.,
2006).
There are examples of Central and West African [e.g. S. nigriventris,
S. nigrita (Sanyanga,
1998)] and East African [e.g. S. zambezensis
(Sanyanga, 1998), S.
njassae (Thompson et al.,
1996), S. multipunctatus
(Burgess, 1989)] synodontids
that sometimes swim inverted. It would be interesting to map the phylogeny of
S. nigreventris and other synodontids capable of inverted swimming
onto the extent of the habit. However, whilst S. nigriventris is
substantially older than the East African species, the internal branches of
the phylogenetic tree interrelating the major Central and West African
lineages are short and unresolved
(Koblmüller et al.,
2006). The route and rate of evolution of inverted swimming in
S. nigriventris from its oldest living ancestor [Chiloglanis
sp., which feeds on benthic invertebrates and employs an oral suction disc to
maintain position in fast-flowing water
(Ntakimazi, 2005;
Kleynhans, 1997)] awaits
further phylogenetic studies.
List of symbols and abbreviations
f
w
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Acknowledgments |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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