Functional morphology of feeding in the scale-eating specialist Catoprion mento
Department of Biology, Sweet Briar College, Sweet Briar, VA 24595, USA
e-mail: jjanovetz{at}sbc.edu
Accepted 18 October 2005
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Summary |
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Key words: specialization, feeding, biomechanics, fish, lepidophagy
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Introduction |
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Catoprion mento (Cuvier), the wimple piranha, has a strange diet
and equally unusual anatomy and feeding behavior. Catoprion is a
monotypic genus of small South American characin that inhabits clear
freshwater streams and lakes with abundant submerged vegetation
(Taphorn, 1992). Its specific
name, `mento', is Greek for `chin', referring to the distinctive protuberance
created by the curve in its banana-shaped, elongate lower jaw
(Fig. 1). Its reduced,
conical-shaped teeth on the upper jaw project forward when the jaws are closed
(Gery, 1977
;
Sazima, 1983
;
Taphorn, 1992
). The dietary
breadth of Catoprion mento is one of the narrowest reported for
fishes; scales form an important proportion of the diet throughout most of
ontogeny, and adults feed almost entirely on this prey
(Vieira and Gery, 1979
;
Sazima, 1983
;
Nico and Taphorn, 1988
).
Despite our perception that scales should be an unappetizing meal, lepidophagy
is relatively widespread in fishes, having evolved independently in at least
five freshwater and seven marine families
(Sazima, 1983
). Although the
functional morphology of scale feeding has not previously been experimentally
investigated, anatomical and behavioral observations suggest that a diversity
of morphologies and attack behaviors are used by lepidophagous predators
(Roberts, 1970
;
Major, 1973
;
Liem and Stewart, 1976
;
Whitfield, 1979; Sazima, 1977
,
1983
; Peterson and Winemiller,
1997
,
1998
) and that the behavioral
origins of scale feeding may be different for different lineages
(DeMartini and Coyer, 1981
;
Sazima, 1983
;
Sazima and Machado, 1990
).
|
A number of recent studies (Drummond,
1983; Chu, 1989
;
Meyer, 1989
; Sanderson,
1988
,
1990
,
1991
;
Ralston and Wainwright, 1997
)
have investigated the correlation between trophic breadth and the degree of
functional versatility (Lauder,
1980
; Liem, 1984
)
in specialist and generalist feeders. The hypothesis of most of these studies
is that species with limited diets (trophic specialists) are expected to
exhibit a restricted range of behaviors, or show less variability in the
kinematics and muscle activity patterns of the strike, compared with
generalist species with wider diets. The feeding behavior of
Catoprion provides an opportunity to test this hypothesis in a
species specializing on a derived and specific food source. The fact that
specialized scale feeding has evolved independently multiple times may also
allow general patterns of form and function in lepidophagous fishes to be
identified.
The present study examines the attack behavior and cranial kinematics of Catoprion mento when feeding on three prey items that present different functional challenges for capture and ingestion. The specific goals of the study are threefold: (1) to determine the extent to which Catoprion is able to modulate its strike according to the specific demands of different prey; (2) to describe mechanistically the novel prey capture behavior, scale feeding and (3) to test the hypothesis that dietary specialization has resulted in restriction of an ancestral feeding repertoire of greater functional versatility.
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Materials and methods |
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Kinematics
Individual Catoprion were filmed in lateral view while feeding on
three different prey: (1) sacrificed goldfish (SL 4245 mm)
from which scales were removed by the Catoprion, (2) small, live fish
(Tanichthys albunubes) that were captured whole and (3) loose scales
that had been removed with a scalpel from goldfish, placed in the feeding tank
and were allowed to sink freely in the water column. Goldfish were tethered
with fishing line to a transparent plastic tube and oriented parallel to the
camera to ensure attacks occurred within the filming area, but the other prey
were not restrained in any way. Fishes were filmed at 250 fields
s1 with a high-speed camera (Redlake MotionScope 1000,
Indianapolis, IN, USA). A plastic 1-cm grid was placed in the tank to reduce
the depth of the filming area and to provide a metric to calibrate the video
images.
Images were analyzed field by field in a customized version of NIH Image written by J. A. Walker (www.usm.maine.edu/~walker/software.htm). The field prior to the start of jaw opening was defined as time zero for each strike. Ten coordinates on the predator and one on the prey (Fig. 1) were digitized in each frame and these coordinates were entered into a custom-designed computer program (CodeWarrior, Pascal, J. Janovetz) that calculated the variables used to compare strikes. Cranial displacement variables were calculated as a change in angle over the time of the strike, subtracting the minimum value for each variable from all values for that variable. Angles were used to minimize the effects of size on kinematic variables, especially when comparing strikes from Catoprion in this study with published values from other fishes in other studies. The following 10 variables quantifying maximum displacement and time to maximum displacement of cranial movements were calculated: (1) gape angle (A,C,B) between the cranial tips of the jaws and the quadrate/articular joint; (2) cranial elevation (A,E,G), the angle formed by the non-protrusable premaxillla, the attachment of the pectoral girdle to the skull and the anterior attachment of the pectoral fin; (3) hyoid depression (H,C,G), the angle formed by the hyoid, quadrate/articular and pectoral fin; (4) opercular expansion (G,F,E), calculated as the angle between the pectoral fin, posterior point on the suture between the suboperculum and operculum, and attachment of the pectoral girdle to the skull; (5) lower jaw rotation (B,E,C), the angle formed from the tip of the dentary, attachment of the pectoral girdle to the skull, and quadrate/articular joint, and (610) time from the frame prior to jaw opening to the maximum displacement for each of the variables above. In addition to these variables quantifying cranial movements, two other variables describing strikes were calculated: (11) prey distance (A,K) in cm, calculated as the linear distance from the premaxilla to the point on the prey that first breaks the plane of the gape, and (12) total gape cycle time (ms), the elapsed time from the frame prior to jaw opening until cranial elements have returned to their resting positions. Individual feeding sequences varied widely (range 128476 ms) in the total elapsed time of the strike.
To visualize the overall pattern of cranial movement for each prey type, strikes were standardized by aligning each by the time of maximum gape angle. Five strikes from each of the same five individuals were analyzed for each of the three prey types, for a total of 75 strikes. Only successful strikes where the prey was captured or scales were removed were analyzed.
Statistical analyses
A multivariate analysis of covariance (MANCOVA) was performed using prey
type and individual standard length as covariates to determine whether prey
type and predator size have an effect on strike kinematics. A series of
two-way analyses of variance (ANOVAs) were then performed to determine whether
mean values for each of the 12 kinematic variables differed among prey types
and individuals. If a significant effect was found, individual
t-tests were performed to determine which pairs of comparisons were
significantly different. To control for multiple comparisons, levels of
statistical significance were adjusted using the sequential Bonferroni
technique (Rice, 1989),
resulting in significance values ranging from 0.004 to 0.05
(0.05/120.05/1). To describe the major axes of variance in feeding
behavior on different prey, a principal components analysis was performed on
the 12 kinematic variables. Of the 12 factors extracted from the correlation
matrix, only two have an eigenvalue greater than 1
(Norman and Streiner, 1994
)
and were used to describe feeding behaviors. A scatter plot of these two axes
(PC 1 and PC 2) was constructed to illustrate the position of each feeding
sequence in multivariate space. All statistical analyses were performed using
JMP 3.1 (SAS Institute, 1995
)
or StatView 5.0.
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Results |
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Feeding behavior on fish and loose scales
In contrast to scale feeding, the kinematic patterns of Catoprion
capturing whole fish (Fig. 4)
and loose scales (Fig. 5) were
similar to patterns reported for other fishes while suction feeding. Maximum
mean attack velocities were lower than during scale feeding, averaging 0.38 m
s1 for strikes on fish and 0.17 m s1 for
strikes on loose scales. Prey capture followed the general
anterior-to-posterior sequence of cranial movement (Figs
6,
7) well documented for
suction-feeding fishes (Lauder,
1985; Lauder and Shaffer,
1993
). Strikes began with an increase in gape due to lower jaw
rotation, followed by nearly synchronous raising of the head and depression of
the hyoid, expanding the volume of the buccal cavity and creating a vacuum
that draws in water and prey (Lauder,
1985
; Liem, 1993
).
Finally, the opercular apparatus expanded laterally, allowing the volume of
water that entered the buccal cavity during prey capture to drain.
Displacement of cranial elements were greater during feeding on fish but the
time to reach these excursions was shorter than when feeding on scales (Figs
6,
7), a pattern that has been
consistently reported for other fish species when feeding on evasive
vs non-evasive prey (Lauder,
1981
; Sanderson,
1988
,
1990
,
1991
;
Chu, 1989
).
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When feeding on fish, Catoprion again stalked to within a short
distance of the prey before accelerating rapidly during the attack
(Fig. 4). Predator velocity
remained high throughout the strike, indicating that a combination of ram and
suction feeding modes was used (Norton and
Brainerd, 1993). Jaw opening did not begin until
Catoprion were an average of 1.11 cm from the fish. Jaw opening
proceeded rapidly, averaging a maximum value of 83° (linear gape distance
1.08±0.17 cm), which is well below the functional gape limit for the
species, after 73 ms. Maximum gape was achieved after the prey had entered the
mouth. Mean values for cranial elevation and hyoid depression during capture
of evasive prey were also high, and the mean value for maximum opercular
expansion at 38° was the only variable higher during fish feeding than
scale removal. Maximum values for all cranial displacement variables were
lower when feeding on loose scales (mean linear gape, 0.81±0.097 cm)
than on fish despite taking a longer time to reach that maximum value. Only
distance from the prey at the start of jaw opening was not statistically
different between the two behaviors (Table
1). There was no evidence of a preparatory phase of constriction
of cranial elements to reduce buccal volume prior to the onset of jaw opening,
as has been reported in some derived groups of fishes
(Gibb, 1995
).
Comparisons among prey capture behaviors
MANCOVA results revealed a highly significant effect of prey type
(P<0.0001, F=28.37, d.f.=24,120) and a non-significant
effect of predator standard length (P>0.16, F=1.48,
d.f.=12,60) on strike kinematics in these Catoprion individuals
specifically chosen for their similarity in size. The overall patterns of
suction feeding on scales and fish are similar, with differences between the
two behaviors due largely to the lower rates of movement of cranial elements
in feeding on loose scales. Rates of displacement of cranial elements appear
similar between feeding on loose scales and scale removal for gape angle,
hyoid depression and lower jaw rotation during most of the strike. Rates of
displacement for these three variables increase as prey contact is made during
scale feeding, appearing more similar to the slopes of the gape profiles for
fish feeding. The plateau phases of prolonged maintenance of cranial elevation
and opercular expansion at angles near maximum during scale feeding are
apparent from these graphs, with this stage lasting approximately one-third of
the entire gape cycle time. Cranial and opercular elements begin to return to
their resting positions only after the jaws are almost completely closed by
retraction of the lower jaw.
Histograms comparing mean values for the six displacement (Fig. 8) and six timing (Fig. 9) variables used to compare prey capture behavior clearly show that Catoprion mento is able to modulate characteristics of the strike to match the demands of different prey. All 12 variables were highly significantly different between prey types (Table 2) while only two variables, maximum opercular expansion and time to maximum hyoid depression, differed significantly among individuals. Of the 36 pair-wise comparisons among the three prey types (Table 1), only two are not significantly different: cranial elevation during scale feeding and fish feeding, and distance from the prey at the start of the strike during captures of fish and loose scales. The uniformly longer times to maximum displacements during scale feeding are not surprising given the greater distances the cranial elements are moving during this prey capture behavior. The consistently lower magnitudes but longer times to maximum for cranial movements when suction feeding on loose scales compared with capturing fish are consistent with compensations in behavior shown by other fishes when capturing prey capable of performing escape behaviors.
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A principal components analysis of all 75 strikes supports the ANOVA results that the dietary specialist Catoprion mento is able to modify the kinematics of prey capture according to the demands made by different prey. The two major axes of variation, which together account for nearly 85% of the variation in strike kinematics (Table 3), almost completely separate strikes by prey type (Fig. 10). Variables loading highly on PC1 (63.8% of variance) largely separate scale feeding from strikes on fish and loose scales. That 10 of 12 variables, all but angles of maximum cranial elevation and opercular expansion, load similarly and relatively highly on this factor supports the uniqueness of this behavior from other types of prey capture. PC2, which accounts for 21.1% of total variance among prey capture behaviors, effectively distinguishes strikes on live fish from strikes on loose scales. The displacement variables maximum opercular expansion and cranial elevation load particularly highly on this factor, although all displacement variables except linear distance from prey at the start of jaw opening load positively and have relatively high coefficients for PC2. Loadings for all timing variables are similar in magnitude and negative in sign for this factor. PC2 is interpreted as differentiating strikes that rapidly reach large cranial displacements from strikes that proceed to lower angular excursions at a slower rate.
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Discussion |
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Modulation of suction feeding
The ability to create negative intra-oral pressure has been found in all
ancestrally aquatic osteichthyans (fishes) studied to date, and the retention
of this ability may be required for transport of captured food even if the
prey is actually captured by a behavior other than suction feeding (e.g.
biting). Many secondarily aquatic tetrapods also capture prey underwater by
suction feeding and show a pattern of cranial movement similar in sequence and
magnitude to that seen in fishes (Shaffer
and Lauder, 1985; Lauder and
Shaffer, 1993
; Lauder and
Prendergast, 1992
). As expected, Catoprion retains this
ability to generate negative pressure by increasing the volume of the buccal
cavity. Video images clearly show that prey are sucked into the mouth along
with a volume of water and are not simply overtaken by the predator. Suction
feeding, and modulation of the kinematic movements that generate negative
pressure, have been retained in this dietary specialist from a biting
lineage.
The amount of negative pressure generated during suction feeding depends on
both the magnitude and speed of volume change in the buccal cavity, with
greater pressures produced by larger, more rapid displacement of cranial
structures (Lauder et al.,
1986; Grubich and Wainwright,
1997
). Most fishes possess the ability to modify feeding behavior
and kinematics of the strike according to the evasiveness of the prey (Liem,
1978
,
1979
;
Vinyard, 1982
;
Sanderson, 1990
;
Norton, 1991
;
Nemeth, 1997b
), as well as
size of the prey (Lauder,
1981
; Ferry-Graham,
1997
) and position of the prey in the water column
(Lauder, 1981
). Among those
fishes able to modulate feeding behavior, without exception, more evasive prey
elicit faster strikes with greater displacement of the cranial elements
responsible for buccal expansion, as would be predicted by hydrodynamic theory
(Vogel, 1989
;
Denny, 1993
). The fewer
studies that directly measure changes in buccal pressure during feeding
confirm that strikes on evasive prey are characterized by decreases in
intra-oral pressure of greater magnitude than strikes on non-evasive prey
(Nemeth, 1997a
;
Grubich and Wainwright,
1997
).
Comparison of strikes in Catoprion feeding on non-evasive loose
scales with strikes on evasive fish supports this pattern. All displacement
and timing variables are significantly different between the two prey types
and differ in the direction predicted by the functional demands of creating a
powerful vacuum underwater; during strikes on fish, the buccal cavity is
expanded to a greater magnitude, and at a faster rate, than strikes on scales.
However, unlike the response of other fishes to evasive prey (Norton,
1991,
1995
; Cook, 1995),
Catoprion does not initiate the strike from a greater distance from
the prey, although attack velocities during the strike are higher.
Suction-feeding strikes on fish or loose scales are statistically different in
most variables and easily separable along an informative axis of principal
component space, confirming that Catoprion is able to assess the
escape potential of prey and directionally modify feeding behavior to increase
capture success.
Functional morphology of scale-feeding behavior in Catoprion
A diet of scales and the ability to remove them from other fishes are
derived features in Catoprion. Phylogenetic hypotheses for the
Serrasalminae (Machado-Allison,
1982; Orti et al.,
1996
) suggest that a largely herbivorous diet of seeds, leaves and
aquatic vegetation is primitive for the subfamily. Ancestral serrasalmines
have the ability to both generate effective suction that is used for prey
capture and intra-oral transport of food to the esophagus and to produce a
forceful bite (Janovetz,
2001
). Many aspects of the scale-feeding strike in
Catoprion differ from capture of the other two prey items used in
this study as well as previously reported feeding behaviors in other fishes.
Scale feeding in Catoprion is, to date, the most extreme example of
what has been described in the literature as `ram feeding' (Liem, 1980a;
Norton and Brainerd, 1993
).
Ram and suction feeding are considered as two ends of a continuum in one axis
of prey capture that is defined by the relative movements of the predator and
the prey (Norton and Brainerd,
1993
). In pure ram feeding, only predator movement is used to
capture stationary prey, while in pure suction feeding the stationary predator
draws the prey towards it and into the mouth using only negative pressure. The
tethered prey used in this study are unable to move, but as Catoprion
often attacks fish 23 times its own length
(Sazima, 1983
; J.J., personal
observation), prey movement is likely to range from extremely small to
non-existent. The term `ram feeding' is particularly appropriate for
Catoprion as, unlike in other ram-feeding fishes where predator
velocity is used to merely overtake and engulf prey whole, Catoprion
actually uses the force of its strike during collision with the prey to knock
scales free (Janovetz, 2003; Janovetz and Westneat, manuscript submitted for
publication).
Many of the unusual kinematic features of scale feeding can be understood in light of the different functional demands of this feeding mode compared with suction feeding. A very gradual increase in gape by lower jaw rotation begins while Catoprion is still nearly 2 cm from the prey. This slow rate of gape increase lasts for approximately 150 ms (Fig. 3) before prey contact is made, which is almost longer than the average time for the entire gape cycle when feeding on fish. Low rates of cranial expansion allow water to `leak' into the buccal cavity and prevent the explosive volume change necessary to generate suction. Typically, a gape angle of over 80° is achieved, almost solely due to lower jaw rotation, before the Catoprion begins a rapid acceleration towards the goldfish. After this, lower jaw rotation does not appreciably increase until contact is made with the prey. After rapid acceleration to strike velocity but just before collision with the goldfish, cranial elevation begins and is followed soon after by lateral expansion of the opercular series. That lower jaw rotation stabilizes briefly near the maximum angle for fish strikes, increasing again only after prey contact, may suggest that a lower jaw angle of near 80° is the functional limit for active, muscular control of jaw rotation but that the jaw is anatomically capable of being passively rotated a further 30°. Measurement of muscle activity in the jaw abductors with electromyography or sonomicrometry or estimates of the potential shortening capabilities of fibers from the levator operculi and geniohyoideus muscles from anatomical dissection would help answer this question.
The upper jaw (premaxilla and maxilla) of all serrasalmines is
non-protrudable due to the derived condition of a ligamentous attachment of
these ancestrally mobile elements to the neurocranium
(Machado-Allison, 1982).
Cranial elevation serves to orient the everted, tusk-like premaxillary teeth
of Catoprion into a forward-facing position to effectively rasp
scales from the flanks of fish. While lower jaw adduction begins and is nearly
completed during prey contact, very little upper jaw depression occurs during
contact, resulting in a plateau stage of stability. Beneski et al.
(1995
) describe a period of
relative stability in gape angle in some ambystomatid salamanders of the
subgenus Linguaelapsus, during which time the tongue pad is
protracted, reshaped to fit the prey and retracted. They conclude that this
period of stability is necessary for the accurate aiming of the tongue pad. In
Catoprion, stability of the upper jaw during prey contact probably
provides a firm `battering ram' for force transfer.
Momentum from the initial approach, as well as added force from tail and
body undulations during prey contact, is probably transmitted to the prey
largely through the upper jaw. A non-protrudable premaxilla, which may have
evolved initially to withstand the high bite forces generated while feeding on
seeds, is a putative preadaptation for the ramming strike of
Catoprion during scale feeding. In this sense, the ligaments
responsible for binding the upper jaws are analogous to the `collagen tract
within the lower lip' of Liem and Stewart
(1976), who hypothesized that
the tract stabilized the jaws of scale-eating cichlids from Lake Tanganyika
during bites. This anatomical shift in biological design, while advantageous
for withstanding the force of a scale-feeding attack, prevents upper jaw
protrusion, a character that has been widely hypothesized to increase
suction-feeding performance in teleost fishes
(Motta, 1984
).
In most Halecostome fishes (Amia + teleosts), the mobile maxilla
and descending arm of the premaxilla swing forward during prey capture to
laterally occlude the gape and restrict the flow of water that is sucked into
the mouth largely to a volume in front of the predator (Lauder,
1980,
1985
;
Liem, 1993
). The inability of
Catoprion (and all piranhas) to occlude the gape means that water
lateral to the mouth, and therefore not useful for prey capture, will enter
the buccal cavity and reduce the effective suction force for prey capture. The
enormous gape of Catoprion compounds this problem, creating an
equally large lateral area on each side to admit water. Despite early debate
(Muller et al., 1982
; Lauder,
1983b), it is now generally agreed that the gill bars isolate buccal and
opercular cavities during suction feeding
(Muller et al., 1985
;
Lauder, 1986
). The gill bars
remain closed early in the strike, preventing reverse flow into the buccal
cavity from the operculum, and open after peak gape, providing an exit through
the operculum for excess water engulfed during the strike
(Lauder, 1985
). Throughout
most of the acceleration and prey-contact phases of scale feeding, the
opercular series remains laterally expanded in Catoprion, exhibiting
a plateau phase similar to cranial elevation. Although direct measurement of
gill bar spacing was not done, this probably indicates that buccal and
opercular cavities are hydrodynamically linked during scale feeding, allowing
the efficient exit of the large volume of water engulfed during attacks
covering such a large distance. Catoprion appears able anatomically
to segregate buccal and opercular cavities and behaviorally appears to do this
while feeding on fish and loose scales. That this sequence of kinematic
events, crucial for effective suction feeding, is not performed during scale
feeding is further support that scale feeding in Catoprion mento is a
novel and distinct form of prey capture.
Is specialization limiting for Catoprion mento?
Recently, there has been great interest in functional morphology in
relating the functional versatility (the range of kinematic, muscle activity
or other behavioral responses) of organisms to a measure of their resource
utilization in the wild (e.g. Sanderson,
1988,
1990
,
1991
;
Ralston and Wainwright, 1997
;
Ferry-Graham et al., 2002
).
The expectation of most of these studies is that specialists will have less
functional versatility than generalists. Specifically in feeding studies, the
hypotheses are that species with narrow dietary breadth will have a more
stereotypical or restricted range of feeding responses to prey and that this
limited repertoire results in reduced performance when feeding on prey other
than those typically found in the diet.
Catoprion mento, according to both an ecological and morphological
definition, is a trophic specialist. Its natural diet throughout most of
ontogeny contains scales and, as adults, Catoprion feeds almost
exclusively on this derived food source
(Sazima, 1983;
Taphorn, 1992
;
Vieira and Gery, 1979
).
Anatomically, Catoprion has a longer jaw with a distinctive curve,
reduced and everted pedicel-like teeth and an even less protrudable maxilla
than its vegetarian serrasalmine ancestors. Has the functional versatility of
Catoprion been restricted in conjunction with this specialization of
diet and anatomy? Despite extreme modification of the feeding system and a
natural diet of very narrow breadth, Catoprion actually appears to
have an increased range of feeding behaviors in its repertoire.
Catoprion has retained the ancestral ability to generate suction to
capture prey, to modulate the specific kinematics of a ram/suction attack, but
has also evolved a novel feeding behavior, with distinct kinematic parameters,
when removing scales from fish. In the case of Catoprion,
specialization appears to have added to the range of feeding modes
behaviorally available.
If behaviorally able to feed on a variety of prey, why does the natural
diet of Catoprion contain such a reduced subset of the available
resources and why does Catoprion specialize on nutritionally less
profitable prey (Futuyma and Moreno,
1988; Robinson and Wilson,
1998
)? For Catoprion, the costs of specialization may be
largely anatomical. Many derived features of the trophic anatomy, both
autapomorphic for Catoprion and synapomorphic for the Serrasalminae,
alter the biological design of the feeding apparatus in a direction predicted
by biomechanics to compromise effective suction feeding or forceful biting.
The enormous gape of Catoprion, coupled with the inability of the
non-protrudable upper jaw to laterally occlude the gape, should result in
reduced water flow from directly in front of the mouth and therefore in
reduced suction-feeding performance. The reduced teeth, small adductor muscles
and velocity-emphasizing (Barel,
1983
; Westneat,
1995
) lever design of the long lower jaw will limit effective bite
force. Although prey capture performance was not quantified and
Catoprion is able to feed effectively under the restricted conditions
necessary for filming, in more natural settings these functional consequences
of its derived trophic anatomy may reduce the ability of wimple piranha to
capture evasive prey using suction or to remove more than scales during
biting.
When can the Jack-of-one-trade have his cake and eat it too?
While most studies comparing trophic specialists and generalists have found
an equal ability to modulate feeding behavior (Sanderson,
1988,
1990
;
Ralston and Wainwright, 1997
),
some have not (Lauder, 1981
;
Chu, 1991; Sanderson, 1991
,
but see Sanderson, 1988
for
comparison of the same three species). Liem
(1984
,
1990
) proposed the intriguing
hypothesis that suction feeding is an extremely flexible feeding mode that is
so useful and effective in a wide variety of feeding situations that the
assumed advantage of specialization, increased efficiency, is rarely a
selective pressure. All fishes appear to use suction for hydraulic transport
of captured food to the esophagus (Bemis and Lauder, 1983), and this behavior,
although using the same mechanism as feeding, is usually considered distinct
from feeding (Gillis and Lauder, 1993). This dual biological role for suction
generation suggests that loss of this ability would affect not just prey
capture but also prey transport and implies an almost inherent modulation
capability.
Recent functional studies of fishes from a range of phylogenetic positions confirm that the ability to modulate feeding behavior according to the functional demands of the prey is ancestral for teleosts. The presence of modulation, even in specialists, should therefore be the null hypothesis in fish feeding studies, and expectation of its loss should be explained in the context of providing a selective advantage. The rarely stated but presumed advantage of a specialized feeding mode is that this single behavioral response is optimal for feeding on the few items in the diet and that maintaining behavioral flexibility somehow compromises this behavior, perhaps by slowing the behavior to allow for sensory feedback. This neural cost of behavior has never been demonstrated for a vertebrate, however. Morphological trade-offs in biological design are well documented, and it is perhaps more likely that anatomy limits the range of behavioral responses that allows a species to forage efficiently. Additional studies of fish feeding behavior, which mechanistically explain the complex function of the vertebrate skull, are a valuable contribution to our understanding of the evolutionary and ecological processes that create and maintain organismal diversity.
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Acknowledgments |
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References |
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