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First published online December 14, 2006
Journal of Experimental Biology 210, 27-36 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02619
No trade-off between biting and suction feeding performance in clariid catfishes
1 Department of Biology, Universiteit Antwerpen, Universiteitsplein 1,
B-2610 Antwerpen, Belgium
2 Evolutionary Morphology of Vertebrates, Ghent University, K.L.
Ledeganckstraat 35, B-9000 Gent, Belgium
3 Department of Movement and Sports Sciences, Ghent University,
Watersportlaan 2, B-9000 Gent, Belgium
* Author for correspondence (e-mail: Sam.VanWassenbergh{at}ua.ac.be)
Accepted 26 October 2006
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Key words: prey capture, X-ray video, kinematics, catfish, buccal volume
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Such evolutionary trade-offs are often observed in case
certain components of the musculo-skeletal system have to participate in
different functions: a certain change in one aspect of the system increases
the performance of a given function, but at the same time may reduce the
organism's efficiency in performing an other, morphologically coupled function
(e.g. Vanhooydonck and Van Damme,
2001; Van Damme et al.,
2002; Pasi and Carrier,
2003; Schondube and Del Rio,
2003). Identifying such conflicts in the performance of
ecologically relevant functions is basic to our understanding of the
evolutionary processes associated with species radiations. Furthermore,
analyses of the constraints on the compatibility of functions may provide
insight into the ecological potential (potential niche width) of animals
(Barel, 1983).
One of the most striking examples of a complex and integrated system that
has to fulfil a large number of crucial biological functions is probably the
cranial musculo-skeletal system of fishes
(Liem, 1980). It has to cope
with capturing, processing and transporting prey, breathing water or air,
participating in sensory perceptions, providing protection for the major sense
organs and brains, and serving as a streamlined bow in locomotion. Logically,
each of these functions calls for specific, structural and dynamical
requirements to the animal's cranial system. As a result, the morphological
diversity in a certain trait exhibited in taxa will be evolutionary
constrained due to the disparate functional demands on this trait. This was
demonstrated recently in the oral jaw system of Labrid fishes
(Alfaro et al., 2005).
Different functional aspects can also be distinguished within the process
of prey capture: prey can either be caught by suction feeding (generating a
flow of water that drags the prey towards and into the mouth) and/or by biting
(e.g. scraping algae or picking molluscs off the substrate with the oral
jaws). It is hypothesised that biting a prey or sucking it directly into the
mouth are two functionally conflicting ways of getting food into the buccal
cavity (Barel, 1983;
Bouton et al., 1999;
Sibbing and Nagelkerke, 2001).
It is therefore assumed that suction feeding and biting can be combined only
to a certain extent, and at certain costs. This hypothesis appears to be
supported by the observation that specialized biters usually possess other
anatomical, functional, dietary and behavioural features that distinguish them
from species that rely primarily upon suction feeding to capture prey
(Alfaro et al., 2001).
However, many fish species still seem to combine biting and suction
seemingly efficiently (Turingan and
Wainwright, 1993; Bouton et
al., 1998; Van Wassenbergh et
al., 2004; Janovetz,
2005), and to our knowledge, no experimental study has yet
directly demonstrated the proposed inverse relationship between biting and
suction performance (see Bouton et al.,
1998). Consequently, the underlying biomechanical basis
responsible for the proposed conflicting demands on the oral jaw apparatus
(for biting) and the buccal expansion apparatus (for suction feeding) remains
to be demonstrated.
In this paper, suction performance is quantified and compared between
species of air-breathing catfish (Clariidae) that differ in bite performance.
In this group of fishes, hypertrophy of the jaw adductors
(Fig. 1) is a derived feature
that has evolved at least four times independently
(Jansen et al., 2006) and is
associated with a drastic increase in maximal bite force
(Herrel et al., 2002) and a
larger proportion of hard prey (mainly coleopterans) in the diet
(Huysentruyt et al., 2004).
Nevertheless, our observations have shown that even the species with the most
extreme jaw adductor hypertrophy still apply considerable buccal expansion
before impacting the jaws onto the prey, and manage to drag relatively large
prey into the mouth by suction. Furthermore, as Clariidae appear to generate
suction predominantly by expanding their buccal cavity in the ventral
direction (Van Wassenbergh et al.,
2004), the fact that the jaw adductors are bulging dorso-laterally
from the head (see Fig. 1) may
indicate the avoidance of spatial interference with the buccal expansion
system in course of the evolution. In this way, it is possible that the
trade-off between biting and suction feeding performance, as suggested for
other groups of fishes (Barel,
1983; De Visser and Barel,
1996), does not apply to Clariidae.
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), species
with eel-like bodies, hypertrophied jaw adductors and a narrow skull roof have
arisen at least four times independently within the Clariidae. Each time, a
sister group relation with a non-specialized Clarias-like ancestor is
observed. In this study, we focus on two lineages from which three clariid
species were selected (Fig. 2):
Clarias gariepinus (Burchell 1822), Gymnallabes typus
(Günther 1867) and Channallabes apus (Günther 1873).
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). Its
overall cranial morphology resembles that of Heteropneustes fossilis,
which can be considered as a sister species of Clariidae
(Agnese and Teugels, 2005;
Diogo, 2005;
Jansen et al., 2006).
Biomechanical modelling has shown that the maximal bite forces that can be
exerted by C. gariepinus are considerably less than species with jaw
adductor hypertrophy (Herrel et al.,
2002) (Fig. 2).
Yet, C. gariepinus has a broad diet, which not only includes
relatively soft prey such as insect nymphs, fish and shrimps, but also harder
prey such as crabs, beetles and snails
(Bruton, 1979). Although this
species shows different kinds of foraging behaviours, including bottom
feeding, surface feeding or group hunting, prey are generally captured by a
combination of suction feeding and biting
(Bruton, 1979;
Van Wassenbergh et al., 2004).
The individuals used in the experiments (see further) were either
aquarium-raised specimens obtained from the Laboratory for Ecology and
Aquaculture (Catholic University of Leuven, Belgium) or specimens obtained
from aquacultural facilities (Fleuren and Nooijen BV, Someren, The
Netherlands).
In contrast to C. gariepinus, G. typus and C. apus have
bulging, hypertrophied, jaw adductors and a narrow skull roof
(Fig. 1)
(Cabuy et al., 1999;
Devaere et al., 2001;
Devaere et al., 2005). This
increase in jaw muscle size, the reduction of the bony skull roof, and the
development of the more anguilliform body is the result of independent,
convergent evolution in these two species
(Agnese and Teugels, 2005;
Jansen et al., 2006)
(Fig. 2). Additionally, bite
performance in G. typus and C. apus is much better than in
C. gariepinus (Fig.
2). This appears to be reflected in the diet, with the species
with jaw adductor hypertrophy exhibiting a special preference for coleopterans
(Huysentruyt et al., 2004).
G. typus individuals were commercially imported from the west of
Tropical Africa (exact location unknown), and C. apus were
wild-caught in Northern Gabon.
Quantifying suction performance
The velocity and travel distance of a standardised prey that is sucked into
the buccal cavity was measured using high-speed X-ray videos
(Fig. 3). In order to minimise
the chance of prey escaping during a suction feeding attempt, the prey has to
be displaced into the buccal cavity as fast as possible (importance of prey
velocity). It is also advantageous for a predator to transport the prey over a
large distance, starting to draw the prey toward its mouth from as far as
possible away (minimising approaching distance) to as far as possible inside
the mouth cavity (reducing the chance of prey escape before the mouth is
closed). Therefore, prey velocity as well as travel distance of the prey are
crucial aspects of suction performance.
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These prey were spherical, 6 mm diameter pieces of meat from boiled North Sea shrimp. In order to visualise the position of the centre of the prey, a small, steel marker was inserted into the middle of each prey. These prey were attached loosely on the tip of a blunt-tipped needle so that very little force was needed to release the prey from the needle. The prey-loaded needles were placed horizontally at the end of a narrow, projecting corridor (25 cm long, 8 cm wide, 15 cm high) in the 20 l test aquaria in which the catfish were trained to capture food. The thin Plexiglas walls (2 mm) of the corridor minimised the amount of X-ray absorption. X-ray videos (250 frames s-1) were recorded using a Philips Optimus M200 X-ray generator (Philips, Eindhoven, The Netherlands) coupled to a 14-inch image intensifier and a Redlake MotionPro camera (Redlake, Tucson, AZ, USA).
Although the standardised prey were relatively small, results from a
previous study on prey capture kinematics using X-ray videos
(Van Wassenbergh et al., 2005)
indicated that C. gariepinus does not reduce its suction effort while
capturing this type of prey compared to, for example, firmly attached shrimps
(Fig. 4). Note that our catfish
often had to perform several attempts to detach a single piece of shrimp by
suction. Also for G. typus and C. apus, no modulation of
prey capture kinematics as a function of size, shape or attachment strength
could be discerned (Van Wassenbergh et
al., 2006a). Consequently, although a certain amount of
strike-to-strike variability will inevitably occur
(Van Wassenbergh et al.,
2006a), there is no reason to assume that our experimental prey
may have elicited submaximal suction performance. In addition, we are
convinced that the X-ray video recording process (in particular the vibration
that is suddenly produced by switching on the X-ray generator) provides
further motivation to the anxious catfish to capture the prey as fast and
efficient as possible, in order to return quickly to their preferred hiding
places in the aquarium.
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Prey velocities were determined in the fish-bound frame of reference,
primarily because of simplicity: this enabled us, for example, to display prey
trajectories and plots of prey velocity versus prey position with
respect to the fish (see further). Note, however, that differences in the
swimming velocity of the fish towards the prey during suction feeding can
complicate the interpretation of the fish-bound frame velocity data: forward
translation of the head with open mouth and closed branchiostegal and
opercular valves causes a positive pressure component inside the mouth cavity
(Muller et al., 1982), which
reduces the effort needed to expand the head. In other words, a certain amount
of compensatory suction (needed to keep the water and prey motionless in the
earth-bound frame) is indirectly powered by the fish's swimming musculature,
which facilitates buccal expansion. For the present study on clariid
catfishes, however, the animals' velocity in the direction of the prey is
always relatively low compared to the measured velocity of the prey in the
earth-bound frame (average 7.9% for the three sequences with the fastest prey
movement for each individual). Consequently, although minor interspecific
differences in approaching speed are observed (mean ± standard
deviation of 0.085±0.011 m s-1 for C. gariepinus,
0.052±0.015 m s-1 for G. typus and
0.040±0.011 m s-1 for C. apus), these differences
will probably have little effect on the results of our study. On the other
hand, if this small difference in velocity is due to the fish sucking
themselves forward (due to momentum conservation), comparing fish-bound frame
velocities of the prey is the most appropriate approach. Given that the
head-to-body mass ratio follows the same trend as the approaching speed
(highest in C. gariepinus and lowest in C. apus), the latter
situation is a distinct possibility.
The small difference between the density of the prey (average density of 1029 kg m-3) and the density of the water (1000 kg m-3) implies that the force due to gravitation after the prey is released from the needle is relatively low and may be neglected, given that the velocity of the prey sinking in motionless water after 0.1 s (the approximate maximum duration of prey transport in our catfish) is only 0.024±0.002 m s-1 (mean ± s.d.; N=20). Consequently, the velocity of the prey is almost entirely induced by suction and the prey's velocity profile will adequately reflect the amount of suction generated by the catfish. Furthermore, this gravitational factor is equal for all species and will thus not influence the results of our comparative study.
The species included in the analysis differ in absolute head size: the
anguilliform species G. typus and C. apus have smaller heads
than the more fusiform C. gariepinus. If suction performance is
subject to scaling effects, then this may influence the results. Scaling data
on suction flow velocities in C. gariepinus
(Van Wassenbergh et al.,
2006b) allows us to evaluate the importance of differences in head
size on the output of the suction performance experiments described above.
Although the results of this study generally did not show significant
differences in maximal flow velocities in relation to head size, the average
(and thus most likely) scaling relationship shortly posterior to the mouth
aperture is a decrease in peak flow velocity with increasing size proportional
to (cranial length)-0.24. To account for this, we additionally
compared the prey velocity data as a function of cranial length with respect
to the scaling relationship of flow velocity for C. gariepinus
(Van Wassenbergh et al.,
2006b).
|
). The expanding buccal volume is approximated by a
series of elliptical cylinders, in which the major and minor axis of each
ellipse corresponds to the width and height of the buccal cavity at a certain
position along the head's mediosagittal axis. The following data is needed for
this: (1) the dimensions of the buccal cavity (i.e. the width and height at
specific points along the midsagittal axis), for example from the head in
compressed state; and (2) measurements of the changes of these ellipse axes in
time during suction feeding. The first type of data is obtained from lateral and ventral view radiographs of an unexpanded head of each of the species in which the bucco-pharyngeal cavity is filled with a radio-opaque (Barium) fluid (Fig. 5A). The line connecting the upper jaw tip to a point equidistant between the base of the right and left pectoral fin served as the mediosagittal axis. Height and width of the buccal cavity were measured at 21 points equally distributed along this axis. For C. apus, which lacks pectoral fins, a fixed point at the approximate position of the pectoral girdle joint was used instead. It was assumed that this situation (i.e. the buccal volume distribution for the preserved specimen at rest) reflects the moment prior to start of the suction event (Fig. 5B).
To obtain the second type of data, high-speed videos were recorded for C. gariepinus (two individuals; cranial lengths of 28.4 and 29.5 mm), G. typus (one individual; 22.0 mm cranial length) and C. apus (two individuals; cranial lengths of 24.5 and 26.0 mm) capturing pieces of cod (Gadus morhua) that were pinned onto a plastic coated steel wire (Fig. 4, third type of prey). The recordings were made using a Redlake Imaging Motionscope digital high-speed video camera at 250 frames per second simultaneously in lateral and ventral view on the feeding catfish, using a mirror placed at 45° (Fig. 5C). Two floodlights (600 W) provided the necessary illumination. Three feeding sequences that were approximately perpendicular to the camera lens were selected for each individual. Next, the upper and lower contours of the catfish's head were digitised frame by frame (50 points each) in the lateral and ventral view. At the same time, the coordinates of the mediosagittal axis, described above, were also digitised. The contour coordinates were recalculated in a new frame of reference moving with the fish, with the upper jaw tip as origin and mediosagittal axis as the x-axis. Next, the distance between the corresponding coordinates of the upper and lower contours, and between the left and right contours were extracted at 21 equally spaced intervals along the mediosagittal axis. Digitisation noise was reduced after applying a fourth order, zero phase-shift Butterworth low-pass filter (cut-off frequency of 30 Hz) to the profiles of length and width versus time. Finally, buccal volume models were calculated for each video frame by assuming that the thickness of the tissue layer between the internal (buccal cavity) and external (head contours) boundaries of the head remains constant (Fig. 5B,D). To allow comparison between individuals of different size, all models were isometrically scaled to a length of 25 mm.
Statistics
In order to test whether the species differ in the maximal suction velocity
of the standardised prey, the total distance travelled by the prey, and a
variable combining these two aspects of suction performance (peak prey
velocity x total distance of travel), two-way analyses of variance
(ANOVAs) were performed. Unless stated otherwise, the independent variables in
these analyses are species (fixed) and individual (nested within species:
random).
However, as G. typus is represented only by a single data point (i.e. maximum for one individual), a comparison of the maximum prey velocities between the three species studied was not possible. Therefore, two alternative statistical approaches were used. First, only the two species with the most extreme difference in bite performance, C. gariepinus and C. apus, were compared by ANOVA. In that case, differences between these two species could be analysed if variation between individuals (random effect) is accounted for without the nested design. We also performed a second approach by pooling the individuals from the species with jaw adductor hypertrophy (Figs 1, 2). In this way, maximal suction performance of the powerfully biting catfish (G. typus and C. apus) was compared to the species with the weakest bite (C. gariepinus) using the mixed-model, nested ANOVA-design described above. The significance level of P=0.05 is used. All statistical analyses were performed with SPSS 13.0 (SPSS Inc., Chicago, USA).
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No significant differences were found between the species in the maximum relative distance (expressed in numbers of cranial lengths) travelled by the prey from the moment of its release from the needle until the end of prey displacement (ANOVA, P always >0.13). Also relative travel distance multiplied by peak prey velocity did not differ significantly between the species (Table 1). This variable can be considered as a combination of the prey velocity magnitude and the distance (relative to head length) over which a certain prey velocity level is maintained.
Buccal expansion
Increases in the volume of the buccal cavity were calculated for a number
of suction feeding sequences by modelling
(Fig. 8). The largest buccal
volume increases were observed for C. gariepinus (0.76±0.10
cm3; mean ± standard error), the smallest for G.
typus (0.53±0.07 cm3), and C. apus was
intermediate (0.68±0.10 cm3). However, if expansion in the
lateral direction is removed (by keeping the horizontal radii constant in
time), the interspecific differences are considerably reduced
(0.50±0.04, 0.43±0.08 and 0.50±0.07 cm3,
respectively). Consequently, a substantial difference is noted in the average
amount of volume increase due to lateral expansion (0.26±0.07,
0.10±0.08 and 0.18±0.05 cm3, respectively).
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). The short and
robust oral jaws of specialized biters (e.g.
Turingan and Wainwright, 1993;
Friel and Wainwright, 1999;
Albertson et al., 2003) as
opposed to long, highly protrusible jaws of some specialized suction feeders
(e.g. Motta, 1984;
Westneat, 1989;
Ferry-Graham et al., 2002) are
a well-studied example of this. Given the diversity in food characteristics,
it is therefore not surprising that the mode of feeding (suction or biting) is
usually reflected in the fishes' diet, which in turn can often be predicted
fairly well from morphology (Sibbing and
Nagelkerke, 2001).
However, developing a certain morphological or behavioural modification to increase bite performance (e.g. enabling the fish to crush hard prey) does not necessarily imply a reduced performance in capturing other, maybe less available or less preferred prey types by suction. This will only be the case if every possible option to increase this bite performance (e.g. increasing jaw adductor cross-sectional area, increasing the moment arms of the lower jaw closing leverage or increasing the strength of the oral jawbones) reduces suction feeding performance. Consequently, although it is obvious that the optimal design for a biter and a suction feeder are different (illustrated by the extreme morphologies of specialists), it may still be possible that some adaptations for biting do not compromise suction performance. Unfortunately, very little is known about potential interferences between the system causing buccal expansion and the system producing bite forces. Therefore, an important goal is to identify evolutionary pathways of specialisation towards biting or suction feeding and their respective functional consequences. We may learn from this to what extent biting and suction feeding can be combined efficiently.
The result of the present study on clariid catfishes exemplifies the
possibility of increasing bite performance considerably
(Fig. 2) without substantially
compromising suction performance (Figs
6,
7;
Table 1). The anguilliform
species with hypertrophied jaw adductors, G. typus and C.
apus, are able to produce bite forces that are, respectively, more than
five and 11 times larger than C. gariepinus
(Fig. 2)
(Herrel et al., 2002).
However, these species still manage to accelerate a standardised prey to
similar velocities during suction feeding. A logical question following these
observations is: `why doesn't biting performance trade-off with suction
performance in these Clariidae?'
A functionally important characteristic of Clariidae is their
dorsoventrally flattened heads (Figs
1,
5). Alexander
(Alexander, 1970) recognised
that fishes with this type of head shape predominantly rely on ventral
expansion (i.e. depression) of the buccal cavity for suction feeding, and less
on lateral expansion (i.e. suspensorium abduction). Our modelling of the
volume increase of the buccal cavity during expansion in Clariidae supports
this: if only ventral expansion occurred (on average) 74% of the total
observed volume increase would still had been reached, whereas lateral
expansion only would result in 20% of the total expansion (the remaining 6% is
due to the interaction between both directions of expansion). Clariidae differ
in this aspect from the more laterally flattened cichlid fishes, the group for
which the trade-off between biting and suction has been studied most
intensively (Barel, 1983;
De Visser and Barel, 1996;
De Visser and Barel, 1998;
Bouton et al., 1998;
Bouton et al., 1999). It has
been proposed for cichlid fishes that in order to accommodate thicker jaw
adductor muscles (increasing bite force) the cichlid's head has to widen,
which implies a lateral displacement of the touching point between the hyoid
and the suspensorium. This displacement increases the angle between the hyoid
bars, which in turn would reduce the optimality of the starting position of
the hyoid (De Visser and Barel,
1996). However, the morphological modification causing this
trade-off for cichlid fishes, i.e. widening of the head as a result of jaw
adductor hypertrophy, does not occur in Clariidae [for illustrations see
Herrel et al. (Herrel et al.,
2002)]. In these catfishes, the neurocranial roof has been reduced
to a small, medial ridge of bones, which makes room available for the jaw
adductor muscles to `bulge' dorsolaterally from the head without the need for
adjusting the spatial configuration of the hyoid-suspensorium apparatus. In
addition, the suprapreopercle and the fourth infraorbital bones, positioned
respectively at the posterior and anterior margins of the jaw adductors, have
reduced considerably (Cabuy et al.,
1999; Devaere et al.,
2001).
As no factors of potential interference between the systems for hyoid
depression (i.e. caudoventral rotation of the hyoid bars and the pectoral
girdle, coupled by the sternohyoideus muscle) and the adaptations for
increasing bite force can be identified in Clariidae, it is not surprising
that no interspecific differences in the volume increase due to ventral
expansion are observed in these catfishes
(Fig. 8). However, especially
in G. typus, but also in C. apus, the contribution to the
total volume increase by lateral expansion (i.e. suspensorium abduction) does
seem to be restricted with respect to the species without the hypertrophied
jaw muscles, C. gariepinus (Fig.
8). Consequently, the increase in bite performance may interfere
with the capacity of abduction (lateral swing) of the suspensoria. This was
also concluded previously from a study comparing the prey capture kinematics
of C. gariepinus with a species with a moderate degree of jaw
adductor hypertrophy, Clariallabes longicauda
(Van Wassenbergh et al.,
2004). Two reasons have been suggested to explain this reduced
lateral expansion. Firstly, a considerable increase of the visco-elastic jaw
adductor mass inserting both on the suspensorium and the neurocranium may
passively constrain the lateral swing of the suspensorium. Secondly, a
stronger and increasingly interdigitated connection of the suspensorium with
the neurocranium may be needed in order to resist the large reaction forces
and moments caused by the large bite forces exerted onto prey. This more
firmly `locking' of the suspensorium associated with adductor mandibulae
hypertrophy has been observed in all Clariidae
(Cabuy et al., 1999;
Devaere et al., 2001;
Herrel et al., 2002) and could
therefore restrict the suspensorium in rotating laterally. However, despite
this reduction in lateral expansion capacity
(Fig. 8), the overall effect of
this on maximal suction feeding performance is apparently negligible (Figs
6,
7,
Table 1).
In conclusion, the results of our study comparing species from two
evolutionary lineages of Clariidae demonstrates that convergent morphological
evolution toward increasing bite performance does not necessarily lead to a
reduced suction feeding performance. This is in contrast to what has been
proposed for other groups of fishes (Barel,
1983). Clariid catfishes have dorsoventrally flattened heads and
predominantly rely on ventral expansion of the buccal cavity to produce
suction. We hypothesise that potential spatial constraints by increasing the
jaw adductor size on the buccal expansion system is avoided by the narrowing
of the roof of the neurocranium, enabling the jaw adductors to develop freely
in the dorsolateral region of the head without interfering with the depression
of the hyoid. Although a reduced capacity of lateral expansion (suspensorium
abduction) is observed in the powerfully biting species (presumably due to
passive resistance of the jaw adductor mass spanning the suspensorium and/or
the strengthened articulation of the suspensorium with the neurocranium) the
contribution of this lateral expansion to the total buccal expansion is
relatively limited and, probably for this reason, does not result in a reduced
suction capacity.
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Cabuy, E., Adriaens, D., Verraes, W. and Teugels, G. G. (1999). Comparative study on the cranial morphology of Gymnallabes typus (Siluriformes: Clariidae) and their less anguilliform relatives, Clariallebes melas and Clarias gariepinus. J. Morphol. 240,169 -194.[CrossRef]
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