Feeding patterns of Chelus fimbriatus (Pleurodira: Chelidae)
1 Department of Comparative Anatomy and Morphology, Institute of Zoology,
University of Vienna, Althanstraße 14, A-1090 Vienna, Austria
2 Institute for Theoretical Physics, TU-Vienna, Wiedner Hauptstraße
8-10, A-1040 Vienna, Austria
3 Department of Evolutionary Morphology, Institute of Evolutionary and
Ecological Sciences, University Leiden, Kaiserstraat 63, NL-2311GP Leiden, The
Netherlands
4 Clinic of Radiology, University of Veterinary Medicine, Vienna,
Veterinärplatz 1, A-1210 Vienna, Austria
* e-mail: p.lemell{at}vcc.at
Accepted 11 March 2002
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Summary |
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Key words: kinematics, feeding, suction, anatomy, turtle, fringed turtle, Chelus fimbriatus
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Introduction |
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Chelus fimbriatus, the matamata or fringed turtle, is often
described as a suction feeding specialist (e.g.
Ernst and Barbour, 1989;
Pritchard, 1979
;
Pritchard and Trebbau, 1984
).
A few studies have concentrated on the ethology and statistics of prey capture
in this species (Formanovic et al.,
1989
; Hartline,
1967
; Holmstrom,
1978
,
1991
;
Wise et al., 1989
). The
present study analyses the kinematics of complete feeding cycles of the
aquatic feeding specialist C. fimbriatus using high-speed video
recordings and X-ray film sequences. We describe the kinematics of the head,
hyoid, oesophagus and prey during complete feeding cycles to provide a basic
description of food uptake and transport in this species. These data are
supplemented by a morphological description. Furthermore, special features of
the matamata are characterized and the findings are compared with other
aquatic feeding turtles.
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Materials and methods |
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Anatomy
The morphology of the feeding apparatus skull, hyoid, jaw and hyoid
musculature was studied in five subadult specimens. Three were frozen
individuals (carapace length 10-15cm) from the `House of the Sea' in Vienna,
the other two (carapace length approximately 11cm) were obtained commercially.
The animals were killed by intraperitoneal injection of sodium pentobarbital
(Nembutal) and fixed in an 8% formaldehyde solution for 3 days prior to
dissection.
Computer tomographic pictures were obtained using a CT pace, third-generation from G.E. (General Electric Medical Systems) in sagittal slices (layer thickness and distance 2mm) and reconstructed in the `bone window' of Advantage Windows AW 2.0.20.
Film recordings
Three similarly sized specimens (carapace length approximately 12cm) were
selected for detailed analysis of kinematic patterns. For filming, they were
fed with dead fish 2-4cm in total length. Feeding was recorded at 500 frames
s-1 with a NAC colour HSV 1000 frames s-1 high-speed
video recorder. Recordings were made in a 40cmx16cmx25cm aquarium
with a background grid (grid squares 1cmx1cm). The aquarium was
illuminated by two Dedocool halogen spotlights (maximum 1250W) and two Kobold
lights (300W). Prior to filming, the turtles were trained for several weeks to
feed in the strong light necessary for filming. Two 45° mirrors, one in
front of and the other underneath the aquarium, were used to measure the gape
perimeter and the total oesophageal volume. Fish were suspended on a string in
the water to simulate both moving and non-moving prey.
X-ray films were taken with a Philips Optimus M200 (maximum 150 frames s-1) using a Kodak CFE film. The same sequences were recorded simultaneously with a U-matic videorecorder (Sony VO-5800PS, maximum 50 frames s-1). The contrast of the prey fish in the X-ray recordings was enhanced with the X-ray contrast medium Gastrografin (Schering). One day prior to filming, lead markers were glued to the turtles' skull (two at the level of the tympanum, one behind the nose, one on the upper jaw and one on the lower jaw) and underneath the hyoid body. The latter marker turned out to be of no use because of skin movement.
General patterns of feeding behaviour
Twenty video sequences from a total of 46 (three specimens with five, seven
and eight recordings, respectively) were suitable for the description of the
general patterns of feeding kinematics (the selection criterion used was that
the turtle's head moved parallel to the background grid). One entire feeding
cycle was recorded on X-ray film, and eight further sequences were taken from
X-ray video (U-matic). The latter sequences were used for analysing intraoral
transport and swallowing. To calculate kinematic variables, only data derived
from the NAC video sequences were used.
Kinematic analyses
The film sequences were digitized and analysed using AviDigitiser (©
P. Snelderwaard). The frame immediately before mouth opening was defined as
time zero.
A series of distance and timing variables was measured from each gape cycle to describe the movements of the jaws, hyoid apparatus, oesophagus and prey and to allow comparisons with other selected turtle species. The following distance variables were measured from the digitized points (Fig. 1): prey parameter, the distance between the prey and a fixed point on the background grid; snout parameter, the distance between the tip of the snout and a fixed point on the background grid; gape distance, the distance between the most ventral point of the anterior surface of the premaxilla and the most dorsal point of the anterior surface of the mandibular symphysis; hyoid depression, the perpendicular distance between a line along the dorsal border of the cranium and the most ventral point visible externally on the hyoid apparatus; and neck dimensions, dorsoventral and transverse distances at the level of the second branchial horn and just in front of the shell (to locate the position of each point correctly, we used landmarks on the turtle's neck).
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From these data, timing variables (Table 1) and oesophageal volume (the volume of water inhaled) during prey capture were calculated. The oesophageal volume was calculated from the measured areas of the gape and four neck segments (see Fig. 1).
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The ram-suction index (RSI), introduced by Norton and Brainerd
(1993) to describe the feeding
mechanisms of fishes, was determined:
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Results |
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The posterior half of the lower jaw is used for the muscle insertions of the adductor complex and the depressor; the anterior part is composed of thin dentaries (arrow in Fig. 2B). Depression of the mandible during prey capture enables a maximum mouth opening of approximately 80°, which is unique for turtles.
The hyoid apparatus is one of the largest in aquatic feeding turtles. From the breadth of its anterior part [hyoid body and branchial horn I (cbI); see Fig. 2B], it is obvious that depression and expansion of the buccal chamber will incorporate a larger volume than in other aquatic feeding turtles.
The main muscle systems of the jaws and hyoid apparatus are shown in Fig. 3. In contrast to other aquatic feeding turtles, the jaw adductors except the adductor mandibulae externus are poorly developed. The external adductor is covered anteriorly by a half-folded skin overlayed by mucus, which acts as a lubricant. This may be necessary, since a cartilago transiliens is missing. This cartilage, which is present in all cryptodires and pleurodires, is usually embedded within the external tendon and facilitates gliding of the external adductor over the trochlear process of the quadrate (cryptodires) or the pterygoid bone (pleurodires). The skin unfolds during mouth opening, functioning as a cheek, which is obviously advantageous for suction feeding. For optimal functioning of jaw adduction, the muscles of the external, internal and posterior complex must work together (Fig. 3A). The horizontal traction of the external complex is transformed into a vertical force by the external tendon, enabling the lower jaw to be lifted by retraction. The muscles of the internal and posterior complex and the medial part of the external adductor form a muscular crescent in the lower temporal fossa. The pterygoid muscle forms the topographic equivalent to the externus complex (protraction). The fibres of the posterior adductor run vertically, producing a mainly medial traction. The medial part of the external adductor produces slight retraction close to the jaw articulation. Protraction and retraction combine to lift the lower jaw. These components act synergistically in closure, reducing horizontal stresses at the articulation. Since the posterior muscles and the medial part of the external complex closely adjoin the articulation, they are responsible for fixation of this joint. Medial traction is a result of all the jaw muscles working together.
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The function of the major visceral muscles is indicated in Fig. 3B. The hyoid apparatus is retracted by the well-developed coracohyoideus. At the same time, three muscles are responsible for hyoid depression. These are the branchiomandibular and the two geniohyoid muscles. The main work is done by the branchiomandibular, which encloses the more rigid cbI in a sheathlike manner. Compression of this muscle alone would depress the hyoid and pull it forwards, but in association with retraction caused by the coracohyoideus, the hyoid apparatus moves posteroventrally. Both geniohyoid muscles are mainly responsible for the lateral distension of the branchial horns, but also for their depression in combination with the retraction.
The tongue of C. fimbriatus is very small. Thus, it neither occupies space within the oral cavity that could otherwise be utilized for volumetric expansion and suction nor acts as an impediment to high-velocity fluid flow, which would increase the force and energy requirements of suction feeding.
Description of the strike kinematics
Prey capture
Before the strike, a very slow stalking motion of approximately
0.4cms-1 (see Table
1) towards the prey occurs until the tip of the snout is
approximately 2 cm away from the fish. During this approach phase, the head
and cranial half of the cervical vertebrae show very little vertical or
horizontal motion with respect to the shell. The first two cervical vertebrae
(C1, C2) are typically aligned with the skull
(Fig. 4). C3-C7 are arranged in
a half-elipsoid curve: angles -
(the angles between more-or-less
straight vertebral segments of C3/C4, C5, C6/C7 and C8; see
Fig. 4) lie within a very small
range (115-120°). The curved neck allows forward expansion of one-third of
the total neck length during the strike.
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Figs 5A and 6A show the turtle just before the capture sequence begins. After this time, the direction of the forward thrust of the head is fixed, and the head traces a straight line from the starting position towards the prey. During the strike, no vertical adjustments of the head direction take place. The fast forward thrust of the skull and neck towards the prey item does not start until approximately one-third of the maximum gape has been reached. Approximately 20 ms later, the gape is at its maximum (Figs 5B, 6B). At this point, hyoid depression has just begun and the neck is nearly fully stretched. The fish has not yet moved, but 4 ms later (Fig. 5C) it disappears within the mouth. The neck reaches maximum extension with all cervical vertebrae aligned with the skull, and the geniohyoid musculature begins to pull apart the hyoid horns. In Fig. 5D, the forward motion of the head has stopped and the head then moves slightly upwards (Fig. 5E) before being retracted. The neck is still completely extended, the hyoid has reached its maximum depression and the horns are maximally distended laterally. The oesophagus is filled with the large amount of water sucked in during the gape cycle until the mouth is closed (Fig. 5F).
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Prey movement through the mouth cavity can be clearly followed in the X-ray film sequences: the prey is sucked inwards (Fig. 6B) and then floats just above the hyoid up to the level of the second branchial horn (cbII) (Fig. 6C). It drifts upwards in a half-circle and then forwards to the level of cbI (Fig. 6D,E). After the mouth has been closed (Fig. 6F), the prey sinks down to floor of mouth (the hyoid apparatus). The neck is retracted slightly, bringing cervical vertebrae C8-C5 into their prestrike positions; C4-C1 remain aligned with the skull. Shortly thereafter, the mouth is again opened slightly to expel the excess water by returning the hyoid apparatus to its starting position (Fig. 6G-J). The fish is retained by the jaws.
Intraoral transport and swallowing
Before the transport phase, 2-3 very slight hyoid movements (depression of
approximately 3 mm) take place. This results in a small amount of water being
sucked in and blown out again. Two different kinematic patterns can then be
used to bring the prey into position for swallowing. The first, used in 75% of
the filmed events, is slow suction. The hyoid is depressed slightly
(depression of approximately 5 mm); then, after the mouth has been opened
enough to release the prey from the jaws, the fish floats further inwards up
to the end of the cbII, where it is held by the horizontal part of the rods
(compare with Fig. 2). The gape
cycle during this transport phase takes between 250 and 600 ms.
In the second transport pattern (Fig. 7), the prey is also sucked in very slowly, but hyoid depression is of the same extent as during prey capture. The anterior part of the oesophagus increases in volume slowly (1-1.5 s; Fig. 7A-D) so that the fish can be held between the second branchial horns (Fig. 7E). By expelling the water very slowly (Fig. 7E-G), the turtle keeps the prey at the posterior end of the hyoid apparatus (Fig. 7H).
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When the prey has been positioned at the end of the second branchial horn, it is swallowed by contractions of the constrictor musculature supported once again by a slow water flow.
Special features during feeding
The first important feature of the feeding of Chelus fimbriatus is
the almost pressure-wave-free prey capture. Any moving mass in a liquid
produces wave-like disturbances in the surrounding medium that must be
compensated for by a predator.
The matamata is able independently to lift its skull or depress its lower jaw. The strategy it chooses depends on the position of the prey (Table 2). A fish on the ground is taken up by a straight forward thrust of the head, the lower jaw is maximally depressed to bring it into position under the prey. When the prey is immediately in front of the head, the skull is slightly lifted before gape begins (20-25°; see Fig. 5A). During the forward thrust, a small increase in the skull angle is observed. A fish lying above a fictitious horizontal line from the turtle (a line from the skull to the carapace) is stalked with a head angle of approximately 45°. This angle decreases during the subsequent capture phase, reaching approximately 0 ° at the end of the thrust phase. The lower jaw is opened to one-third of its maximum gape (approximately 0.5 cm) and is then thrust forward in a straight line. These patterns suggest that the turtle tries to avoid the production of pressure waves that would affect the prey.
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The second notable feature is the enormous increase in oesophageal volume. Although the true oesophageal volume cannot be calculated from the film sequences, the proportional volume increase may be estimated by measuring the changes in overall neck dimensions. During the first 10 ms, the volume remains more-or-less constant. During the forward thrust phase, the volume increases up to twofold as a result of stretching of the neck and oesophagus. During the closing phase, the volume of the oesophagus is further increased by the inflow of water. By mouth closure, the oesophagus has expanded to approximately four times its starting volume.
Ram-suction index
For the feeding sequences recorded here using fish prey, the calculated RSI
during prey capture was always positive (0.071-0.664). No correlation between
RSI and prey item length was found. Over the whole cycle, the ram component
was predominant, in contrast with previous findings.
Fig. 8A shows changes in Dpred and Dprey over time. RSI calculated using these values is given in Fig. 8B. This approach provides quantitative information on the change from ram to suction feeding. Following a pure ram phase (RSI=+1), suction starts in the last third of the feeding cycle and becomes predominant only during the final stages of the capture process. Suction and movement of the prey start when the turtle's head reaches its highest velocity (0.3 cm in 2 ms at t=0.02 s; Fig. 8A). After suction has started, the speed of the forward thrust decreases, and the animal stops moving forwards after a few milliseconds. The rapid increase in suction shortly before the prey disappears (thereby determining the end point of the calculation of RSI) means that values up to -0.8 are reached.
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Discussion |
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The extremely flattened skull is comparable with that of certain representatives of Tryonichidae (e.g. Chitra spp., Cyclanorbis spp.). Its streamlined shape leads to an almost pressure-wave-free capture strike useful for an ambush predator. The shape of the lower jaw is also unique for turtles. From the high speed of mouth opening, two different opening mechanisms can be postulated: muscular power alone or muscles aided by the forward thrust of the head. In the first case, the power necessary to open the mouth would have to be maintained over the whole period of mouth opening, while in the second case only a small gape and therefore a short period of muscle activity to initiate the opening, together with the water resistance due to the forward thrust of the head would extend the gape to its maximum value. An analysis of the present recordings indicates that the motion of the lower jaw is linked directly to the head's forward motion. Mouth closure occurs at one-third of the opening velocity and starts after maximum neck extension has been reached. Since, at that time, a considerable inward flow is occurring, the movement of the jaw is presumably aided by forces resulting from Bernoulli's law. The power requirements of the jaw musculature during prey capture are therefore probably minimised.
The hyoid apparatus is one of the largest known in turtles. It covers the whole floor of the mouth up to the start of the oesophagus. This development, together with its rigidity, allows a large suction force, comparable only with the feeding performance of Chitra indica (R. Gemel, personal communication), to be generated.
The musculature of matamatas exhibits some peculiarities. The lack of a
cartilago transiliens at least in the subadult individuals studied
here (adult specimens were not available for investigation) and the
line of action of the external adductor, which is closely connected to the
cheek, are unusual for turtles. The typical line of action of the external
adductor in pleurodires is from the mandible over the trochlear process to the
supraoccipital bone (Lemell et al.,
2000). In C. fimbriatus, as in other turtles,
this muscle is divided. The pars profunda is particularly well-developed,
changing its direction three times. This is a unique situation in turtles, but
is presumably necessary because of the enormous water pressure exerted on the
lower jaw during feeding. Since the mouth is closed while the turtle is still
moving forwards, the more usual lever system with one vertical and one
horizontal arm would have to be very large to produce sufficient force. This,
however, would be difficult to accommodate in a flattened skull shape.
Therefore, in C. fimbriatus, a type of pulley block with three
changes of direction has been developed to facilitate adduction of the lower
jaw. In such a lever system, the musculature can be kept small while
generating the same or even higher muscle forces than in other aquatic feeding
turtles with well-developed adductor musculature.
This species has a reduced tongue to allow more space for volumetric expansion of the oral cavity. The development of a `cheek' is also very useful for a suction feeding species. During mouth opening, this cheek bounds the lateral side of the mouth from just behind the eyes. This allows a suction force similar to that of fish and aquatic amphibians to be developed.
The anterior half of the oesophagus has a large lumen that can be distended
to four times its original volume. Such a distensible oesophagus a
feature of most Chelidae is a prerequisite for a suction feeding
specialist that uses a bidirectional flow system (Lauder and Shaffer,
1986,
1993
). The bidirectional
system becomes functionally unidirectional by greatly delaying the reverse
flow of water out of the mouth until the jaws seize the prey. The larger the
inner volume of the oesophagus, the larger the period of suction that can be
applied.
Strike kinematics
The traditional characterization of feeding in lower vertebrates involves a
terminology used to define the different phases of prey capture in ray-finned
fishes: preparation or slow opening (SO), expansion or fast opening (FO),
compression or fast closing (FC) and recovery or slow closing/power stroke
(SC/PS) (for reviews, see Lauder,
1985; Bramble and Wake,
1985
). The SO phase in fishes and salamanders is used mainly to
decrease the buccal cavity volume prior to mouth opening by medial compression
of the suspensorium, protraction of the hyoid apparatus and adduction of the
lower jaw. This phase can also be found in some aquatic feeding turtles such
as Pelusios castaneus (Lemell and
Weisgram, 1997
) and Terrapene carolina
(Bels et al., 1997
;
Summers et al., 1998
) in which
the mouth is opened slowly to generate low pressure within the mouth cavity by
protraction of the hyoid. The kinematic patterns during the FO phase used by
turtles and by fishes and salamanders are quite similar. Rapid mouth opening
is immediately followed by a postero-ventral movement of the hyoid apparatus,
and peak hyoid depression follows peak gape. During the FC phase, the hyoid
apparatus remains depressed until the mouth is closed. It is usually brought
back into its starting position during the SC phase. Our observations suggest
that C. fimbriatus also uses these typical aquatic feeding
patterns.
Certain features, however, are notable. In contrast to fishes, aquatic
salamanders and some turtles, no slow opening phase was observed in our video
sequences. The morphology of C. fimbriatus makes this phase
unnecessary: at rest, the hyoid apparatus lies just underneath the palate,
establishing a permanent `waterless' space. Compared with Chelydra
serpentina (Lauder and Prendergast,
1992), a ram feeding specialist, and with Chelodina
longicollis (Van Damme and Aerts,
1997
), a suction feeder, the FO phase (time to maximum gape) of
C. fimbriatus is faster (see Table
3). This phase is faster in aquatic salamanders and fishes (for
reviews, see Lauder and Shaffer,
1986
,
1993
) and substantially slower
in less-specialized aquatic feeding turtles.
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Another difference from other aquatic feeding vertebrates is the duration
of the closing phase. In C. fimbriatus, this phase is approximately
four times longer than the opening phase, while in C. serpentina and
C. longicollis, the closing phase is approximately twice as long as
the opening phase (Table 3).
From our qualitative observations, matamatas seem to use a relatively constant
closing velocity with no clear separation into FC and SC phases. In addition,
no crushing of the prey and, therefore, no power stroke during the SC phase
take place, although there is a recovery phase between single gape cycles. In
Table 3, the kinematics of
three feeding specialists including C. fimbriatus are compared with
that of feeding generalists such as P. castaneus
(Lemell and Weisgram, 1997), a
purely aquatic feeding turtle, and T. carolina
(Bels et al., 1997
;
Summers et al., 1998
), an
emydid turtle that is able to feed both on land and in water. The very long
opening phase of T. carolina can be attributed to its extended SO
phase: T. carolina uses a terrestrial feeding style in water. In
general, the velocities of all the cephalic elements of the feeding
generalists are slower than those of specialists.
The term `compensatory suction' was introduced by Van Damme and Aerts
(1997) to describe the active
compensation by the predator for the production of a pressure wave at the
position of the prey due to the fast forward thrust of the head during a
strike. This term should also ensure that the term `ram feeding' is reserved
for feeding events with continuous through-flow. In C. serpentina and
C. longicollis, the production of a pressure wave is mainly
compensated by depression of the hyoid apparatus during the forward thrust of
the head. In C. fimbriatus, compensatory suction is not needed: no
noticeable pressure wave was detected at the position of the prey. To
illustrate the mechanism better, the skull and lower jaw can be compared with
two ships sailing apart at a small angle. The bow waves of these ships make an
acute angle and meet somewhere behind their bows. The effects on the position
of the prey are neglible at this point and they will be compensated by the
onset of suction (see Fig. 8).
Although the large volume of water entering the mouth during the fast forward
thrust of the head is accommodated by enormous enlargement of the oesophagus
to up to twice its initial volume, it is important to note that, in contrast
to active compensation as defined above, no substantial hyoid depression and
therefore no suction was recognizable.
Ram-suction index
The RSI allows the ratio of ram to suction to be assessed in individual
strikes of aquatic predators. However, its applicability to the feeding
performance of C. fimbriatus is questionable: matamatas have often
been described as a clear example of suction feeding (e.g.
Ernst and Barbour, 1989;
Pritchard, 1979
;
Pritchard and Trebbau, 1984
).
The mean RSI calculated here was +0.36±0.23 (mean ± S.D.,
N=20), which indicates a dominant contribution from head motion. The
equation used for RSI will tend to overestimate the ram component because,
particularly for fish feeding (for which this index was initially introduced),
even pure suction will lead to forward thrust due to momentum conservation,
and an RSI of -1 will therefore never be obtained.
For turtles such as the matamata, a feeding mechanism based mainly on the
conservation of momentum has been proposed by Van Damme and Aerts
(1997). They suggested that
the large volume of water sucked in during feeding causes the head to be
thrown forward. This mechanism would reduce the use of the turtle's neck
musculature solely to aiming the head towards the prey. To test this
hypothesis, we calculated head velocity and water flow rate through the
turtle's mouth. Using the model of Van Damme and Aerts
(1997
) with input data taken
from our recordings (volume changes of the turtle's oesophagus and the area of
the gape), the mass of the head at any time during the strike can be
calculated assuming conservation of momentum. Instead of remaining constant
during the strike, the mass varied by up to two orders of magnitude,
indicating the existence of additional forces acting on the turtle's head.
Although our model includes crude simplifications because of lack of
information about the complex interplay between head, neck and other parts of
the turtle's body, it suggests that, although suction will certainly increase
the final velocity of the head, an important contribution to the forward
thrust comes from the neck musculature.
It is clear from our X-ray film that the intake of the prey occurs largely by suction. A strong suction force will extend the effective capture range and increase the potential size of prey.
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Acknowledgments |
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References |
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