Morphology predicts suction feeding performance in centrarchid fishes
1 Section of Evolution and Ecology, University of California, One Shields
Avenue, Davis, CA 95616, USA
2 Department of Biology, Western Kentucky University, Bowling Green, KY
42101, USA
3 Department of Biological Sciences, Florida Institute of Technology,
Melbourne, FL 32901, USA
* Author for correspondence (e-mail: mcqcarroll{at}ucdavis.edu)
Accepted 4 August 2004
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Summary |
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Key words: Centrarchidae, suction feeding, functional morphology, performance, modeling, buccal pressure, trade-offs
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Introduction |
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Suction feeding on elusive prey involves explosive cranial kinematics that
incur hydrodynamic loading, measurable as subambient pressures inside the
mouth (buccal) cavity (Alexander,
1969; Van Leeuwen and Muller,
1983
). The magnitude of subambient buccal pressure indicates the
strength of suction generated by the fish and is expected to increase with the
velocity of water flow into the mouth
(Muller et al., 1982
). The
magnitude of buccal pressure is known to increase with increasing speed of
kinematic movement (Sanford and
Wainwright, 2002
; Svanback et
al., 2002
) or in situations where increased kinematic speed would
be expected, such as increased predator motivation
(Lauder, 1980
) or increased
prey elusivity (Nemeth, 1997
).
Therefore, buccal pressure magnitude is considered a metric of suction feeding
performance (Grubich and Wainwright,
1997
; Lauder,
1983b
; Lauder et al.,
1986
).
The only previous analysis to estimate pressure-generating capacity
directly from musculoskeletal morphology was performed by Alexander
(1969). In that study, which
was also the first to measure buccal pressure during feeding, measured
pressure was compared with estimates of pressure generation capacity to
understand which muscles actuate suction feeding kinematics. It has since been
observed that pressure magnitudes differ among species with divergent
morphologies (Lauder, 1983b
;
Norton and Brainerd, 1993
). We
devised a mechanical model of force transmission, parameterized it with
morphological measurements from individual fish and compared those
measurements to pressures measured during suction feeding on elusive prey. We
applied this model to a morphologically diverse group of centrarchid fishes
(Fig. 1). It was predicted that
the biomechanical model could explain variation in pressure magnitudes among
individuals, that fish would not exceed the maximum possible pressure
magnitude predicted by the model and that the model would yield realistic
estimates of muscle force production.
|
The model
Buccal pressure gradients are generated by dorsal rotation of the head,
lateral expansion of the suspensoria and ventral rotation of the hyoid and
lower jaw (Lauder, 1980).
These kinematic events are actuated by ventral musculature (sternohyoideus and
hypaxials) and dorsal musculature (epaxials)
(Muller, 1989
;
Osse, 1969
). The primary
assumption of our model is that buccal pressure magnitude is limited by the
ability of muscles to produce force and the ability of skeletal elements to
transmit that force (cf. Alexander,
1969
).
Rotation of the neurocranium involves rotation relative to the pectoral
girdle and vertebral column (Thys,
1997). Manipulation of anesthetized fish revealed that pectoral
rotation occurred at the joint between the supracleithrum and post-temporal
bone (S-PT joint) (Gregory,
1933
) and that this joint shared a common axis with intervertebral
rotation. Therefore, this landmark was used as the fulcrum to estimate the
torques involved in pressure production.
The buccal cavity may be modeled as an expanding cylinder with subambient
buccal pressure distributed across its internal surface
(Muller et al., 1982). These
pressures can be resolved into a force vector oriented normal to the buccal
surface of the neurocranium. The magnitude of this force is equal to the
magnitude of buccal pressure multiplied by the surface area of the cylinder's
projected area. The resolved force of subambient buccal pressure exerts a
torque on the neurocranium. The torque generated by the epaxial muscles must
be greater than the torque generated by subambient buccal pressure
(Fig. 2A).
|
Thus, the minimum pressure a fish can generate depends on the force
generated by the muscle, the moment arm of the epaxial musculature
(Lin), the projected area of the buccal surface over which
force is distributed (Abuccal) and the moment of area of
the buccal surface (Lout)
(Fig. 2A).
Lin is the distance from the centroid of the epaxial cross
section to the S-PT joint, while Lout is the distance from
this joint to the area moment of the projected buccal area
(Fig. 2A). Muscle force is the
product of muscular physiological cross-sectional area (PCSA) and
normalized stress generated by the muscle (Pm)
(Lindstedt et al., 1998).
Balancing the torques about the neurocranium yields the following equation for
predicted pressure:
![]() | (1) |
If Pm were correctly estimated, the magnitude of
predicted pressure derived from morphological variables should correlate with
measured pressure with a slope of one. However, any estimate of
Pm would be unreliable given the lack of data on muscle
force production during suction feeding. Rather than use a suspect estimate of
Pm, the morphological parameters of the model were
combined into a unitless morphological potential:
![]() | (2) |
One assumption of the model is that Pm is constant
among the sizes and species of fish used in this study. Muscle force per
cross-sectional area remains relatively constant across body sizes
(James et al., 1998) and
species differences as long as the percentage of contractile cytostructure per
fiber is conserved (Lindstedt et al.,
1998
).
Using the model to estimate Pm was judged to be more parsimonious than using an a priori estimate. Furthermore, this approach does not alter the correlation between measured morphology and performance: the regression between morphological potential and measured pressure would not be affected by multiplying morphological potential by a constant, and an estimate of Pm could be chosen, post hoc, to produce a slope of one.
One of the advantages of this model is that it pertains only to the force balance at the time of peak pressure. The model assumes that normalized muscle force at this point (Pm) is similar across species but does not make any further assumptions about the complex relationships between muscle dynamics, skeletal kinematics and buccal pressure.
Although the ventral and dorsal musculoskeletal systems work together to
generate suction feeding kinematics, they must resist buccal pressure
independently. The muscles of the ventral expansion system cannot contribute
force to dorsal expansion and could therefore be ignored in this study.
Ventral expansion operates through a much more complex musculoskeletal system
than dorsal expansion, making modeling of force transmission more difficult
(Aerts, 1991;
De Visser and Barel, 1998
).
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Materials and methods |
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In vivo pressure performance
Fish were housed in 100 liter tanks at 22°C in accordance with animal
use and care protocols (#10168, University of California, Davis and #9901,
Florida Institute of Technology). Fish were maintained on a diet of cut squid
(Loligo sp.), goldfish (Carassius auratus) and freshwater
shrimp (Palaemonetes sp.). Feeding was discontinued 34 days
prior to experimentation.
Fish were anaesthetized by exposure to 0.3 g l1 of buffered MS-222 and placed in a surgical tray containing freshwater. A large-bore needle was forced through the neurocranium caudal to the ascending process of the pre-maxilla but rostral to the braincase. The needle emerged inside the anterior buccal cavity, lateral to the vomer but medial to the pterygoids. A plastic cannula was fashioned from PE-90 tubing and threaded into the needle. The needle was then removed leaving the cannula implanted in the skull. The flared proximal end of the cannula was held flush against the roof of the buccal cavity by a small sleeve of Tygon tubing (Cole-Parmer, Vernon Hills, IL, USA) that was pushed down the protruding cannula and pressed against the fish's skin.
A Millar SPR-407 microcatheter-tipped pressure transducer (Millar Instruments, Inc., Houston, TX, USA) was threaded into the cannula and held in place by a sleeve of Tygon tubing. The pressure transducer was positioned such that it extended 1 mm into the buccal cavity of the fish, exposing the sensing element to buccal pressure. Transducer implantation took no more than 20 min, and all fish recovered from the procedure shortly after return to their tank. Recordings commenced with all fish within 36 h after surgery.
The goal of the feeding trials was to elicit maximal pressure generation.
Prey types were therefore selected for elusiveness and large size
(Nemeth, 1997). Freshwater
shrimp are highly elusive and were found to elicit largest pressure magnitudes
in the Lepomis species but not in M. salmoides and P.
nigromaculatus. These two species were fed large goldfish (36 cm)
depending on individual size. To prevent satiation, fish were fed only a few
prey items every 46 h over a period of 12 days.
In Florida, pressure traces were digitized at 1000 Hz on a DAQpad 6070E data acquisition system (National Instruments, Austin, TX, USA) and recorded on a PC running a custom LabView virtual instrument (National Instruments). In California, pressure traces were digitized at 1000 Hz with a Sonometrics II data acquisition system (Sonometrics Corp., London, Ontario) and recorded on a PC running Sonoview software. Buccal pressure was measured directly from each trace.
Measurement of maximal performance is a general problem in comparative
physiology (Garland and Losos,
1994). This is especially true in feeding studies where
motivational effects may heavily influence performance. Our strategy for data
collection was to make every possible attempt to elicit maximal performance
from individual fish including starving prior to experimentation, limiting
stress during experiments and feeding large and elusive prey. Buccal pressures
are known to decrease precipitously with decreasing predator motivation
(Lauder, 1980
), so an average
minimum pressure will be heavily biased by the number of strikes recorded
after a fish is no longer performing maximally. Therefore, the single lowest
buccal pressure from each fish was used in the final analysis rather than the
mean.
Morphological parameters
Apart from the buccal cast measurement (see below), morphological
parameters were measured on the individual fish used in the study. After
pressure recordings, fish were killed by overdose of MS-222. Standard length
and mass were measured on the freshly killed fish. Fish were then fixed in 10%
formaldehyde for two weeks before being transferred to a 75% ethanol solution
for storage. Fish were dissected, and the distance from S-PT joint to the
rostral and caudal extents of the buccal cavity was measured. The buccal
moment arm was taken as the average of these distances, because the area
moment of the buccal projected area should be halfway between the rostral and
caudal extents of the buccal cavity, assuming a cylindrical cavity.
Estimates of epaxial PCSA were made from cross sections of the muscle, cut perpendicular to the orientation of muscle fibers at the minimum perpendicular distance to the S-PT joint (along the line of the moment arm; Fig. 2A). The ventral margin of each section was the axis of the S-PT joint itself, as only fibers dorsal to the joint would be capable of rotating the neurocranium. The fibers in the cut section appeared to be consistently oriented rostro-caudally, with apparent uniform orientation throughout each slice (Fig. 2B). However, the possibility that some fibers deviated from normality means the estimate represented the maximum possible PCSA for each section. Each section was digitally photographed against a ruler. IMAGEJ (NIH, Washington, DC, USA) was used to measure the area and centroid of each section. Because each section was cut perpendicular to muscle fibers, this area was an estimate of the total PCSA of the epaxial muscles. The moment arm was measured as the distance between the centroid and the ventral margin of each section, which, as noted above, was cut level to the S-PT joint.
Buccal cast measurements
Measurements of buccal surface area could not be made on fixed specimens,
so the buccal surface area of individuals used in this study could not be
measured directly, as was done with other morphological parameters. Instead,
buccal casts were made from an additional size series of each species, and the
regression of buccal surface area with standard length was used to generate an
estimate of individual buccal projected area
(Table 1).
|
Buccal casts were made by injecting commercial silicon sealant into the
mouths of freshly killed fish (cf. Norton,
1995). The dimensions of the buccal cavity were measured from
landmarks impressed in the silicon cast.
Buccal area was measured at full buccal expansion, but maximum pressure
generation is known to occur before full buccal expansion
(Sanford and Wainwright,
2002). Based on data collected by Sanford and Wainwright
(2002
), it was determined that
peak subambient pressure occurred at 67% of the maximum buccal width in the
largemouth bass (Micropterus salmoides), the only species for which
such data are available. Therefore, the surface area term used in the model
was calculated as the length of the buccal cavity multiplied by 67% of its
width.
Statistical tests
Morphological variables were log-transformed and compared among species
with multiple pairwise analyses of covariance (ANCOVAs; 10 comparisons).
Significant differences among scaling parameters were determined by sequential
Bonferroni correction with an initial -level of 0.05. Linear regression
was used to test the hypothesis that morphological potential is significantly
correlated with minimum individual buccal pressure and to estimate
Pm. An analysis of variance (ANOVA) was used to test
species effects on the residuals. Maximum predicted pressure generation
capacity was calculated by multiplying a Pm of 200 kPa by
the measured morphological potential for each fish. These values were compared
with measured pressures using a single t-test. Statistics were
performed in SYSTAT 9 (SPSS Inc., Chicago, IL, USA) and JMP 4 (SAS Institute,
Cary, NC, USA).
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Results |
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Interspecific morphological variation
Projected buccal surface area increased with standard length in all species
(Table 1;
Fig. 4). Significant
differences in scaling intercepts were found between most species, with the
exception of L. macrochirus and M. salmoides
(P=0.09), and L. punctatus and M. salmoides
(P=0.84). The remaining morphological variables were found to
increase with standard length in all species. The relative size of epaxial
PCSA and epaxial moment appeared to differ more among species than did buccal
area and buccal moment (Fig.
4). In general, L. macrochirus and L. punctatus
had the largest epaxial PCSA and moments while M. salmoides had the
smallest. However, the limited sample sizes of these measurements preclude
useful statistical comparisons.
|
Morphology and performance
Morphological potential calculated from the model successfully accounted
for variation among individuals in minimum suction pressure
(Fig. 5; P<0.0001,
r2=0.71). The slope of this relationship estimates a
muscle force per cross-sectional area of 68.5±6.7 kPa with an intercept
at 11.8±1.9 kPa. No significant species effect was found among
residuals around the regression line (ANOVA, P=0.06), although L.
macrochirus tended to out-perform its estimated performance and L.
punctatus tended to under-perform its estimated performance
(Fig. 5). Finally, measured
values were significantly lower than those predicted with a
Pm of 200 kPa (paired t-test,
P<0.0001), with an intercept set at 11.8 kPa as derived from the
regression. However, two individuals of M. salmoides out-performed
their predicted maximum pressure generation ability (represented by the bold,
broken line in Fig. 5).
|
A detectable within-species regression was found in L. macrochirus (r2=0.38, P=0.034) but not in any of the other species. The slope of this regression was not significantly different to that of the among-species regression either including (P=0.51) or without (P=0.80) L. macrochirus.
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Discussion |
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Species such as L. macrochirus and L. punctatus, with
smaller buccal projected areas, shorter buccal moment arms, larger epaxial
muscles and longer epaxial moments, tended to produce the largest pressure
magnitudes (Figs 4,
5). Species, such as M.
salmoides and P. nigromaculatus, with larger buccal projected
areas, longer buccal moments, smaller epaxial muscle areas and shorter epaxial
moments, tended to produce smaller pressure magnitudes (Figs
4,
5). This trend has been
observed in previous studies of these and other species
(Lauder, 1983b;
Norton and Brainerd, 1993
) but
was never explained in terms of musculoskeletal mechanics.
The results of the present study present two prominent difficulties. First,
there is considerable residual variation around the regression line. Second,
with the exception of L. macrochirus, the model does not account for
within-species variation in pressure (Fig.
5). Residual variation may result from variation in individual
performance. Some fish may not have fully activated their epaxial muscles,
thus reducing buccal pressure (Lauder et
al., 1986; Grubich and
Wainwright, 1997
). Furthermore, because morphological potential
resulted from three measurements on individual fish and one regression based
on standard length, there was a strong potential for error in estimated
morphological potential.
This potential for error on both axes may explain the failure to detect within-species variation in morphological potential and to account for within-species variation in pressure generation. Therefore, while the model ought to apply within and among species, measurement error may have precluded meaningful within-species comparisons in most of the species used in this study. The detectable interspecific regression in L. macrochirus may result from the large range of sizes used in the study and the allometric growth observed in this species with respect to morphological potential (Fig. 6). The slope of this regression is not significantly different from that of the among-species slope, suggesting that the model applies equally within L. macrochirus as among all included species.
|
Phylogenetic effects (Felsenstein,
1985) did not appear to influence the relationship between
morphology and performance in the species studied. L. microlophus is
believed to be the sister species of L. punctatus plus L.
miniatus (Near et al.,
2004
), yet the range of pressure generation within L.
punctatus and L. microlophus species spans much of the range
measured in the study (Fig. 5). To a lesser extent, within-species variation in L. macrochirus also
spans this range. Finally, M. salmoides is more closely related to
the Lepomis species than to P. nigromaculatus
(Near et al., 2004
). However,
M. salmoides and P. nigromaculatus are more similar to one
another in morphological potential and pressure generation than M.
salmoides is to the Lepomis species. These results suggest that
shared evolutionary history is not driving the overall trends observed in this
study.
Scale effects
One of the most interesting results of the study was that one species
(L. macrochirus) spanned much of the range of pressure generation and
morphological potential, with smaller individuals tending to have larger
morphological potential and lower buccal pressures
(Fig. 6). By contrast, M.
salmoides showed no size dependence in pressure or morphological
potential despite the large range of body size used during the experiments
(Fig. 6). This species is known
to maintain isometry in many variables throughout ontogeny
(Richard and Wainwright,
1995). These findings suggest that there are no general scaling
effects on pressure, independent of relevant morphological parameters.
Kinematic speed is known to decrease with increasing body length in M.
salmoides, L. macrochirus and L. punctatus
(Wainwright and Shaw, 1999)
and probably does so as well in the other species measured in this study.
Muscle shortening velocity is also known to decrease with increasing body size
(James et al., 1998
;
Rome et al., 1990
). Despite
the dynamic nature of pressure generation
(Fig. 3), there appear to be no
size effects on pressure generation independent of changes in morphology.
Instead, pressure appears to depend only on muscle force production, which is
not thought to scale with size (Bennett et
al., 1989
; James et al.,
1998
; Lindstedt et al.,
1998
).
Morphological trade-offs
Suction feeding fish are often grouped into `ram' and `suction' feeders
(see Norton, 1995;
Wainwright et al., 2001
).
`Suction' feeding morphologies, represented by L. macrochirus, are
characterized by smaller mouths, deeper bodies, increased pressure magnitudes
and decreased use of body translation during prey capture
(Norton and Brainerd, 1993
).
`Ram' feeders, represented by M. salmoides, have larger mouths,
shallower bodies, decreased pressure magnitudes and increased use of body
translation during prey capture (Webb,
1984
). These feeding strategies have been discussed as though they
represent divergent suites of potentially independent morphological,
performance and behavioral traits (e.g.
Norton and Brainerd, 1993
).
Our results suggest a functional explanation for these patterns, based on the
fact that the ratio of mouth size to body depth (which correlates with epaxial
PCSA and moment length) appears to determine a fish's capacity for suction
pressure generation.
Suction feeding requires that a predator generates a large enough buccal
volume to contain its prey and draw the prey into that volume faster than the
prey can escape (Muller et al.,
1982). To meet these demands, fish must overcome hydrodynamic
resistance, which is dominated by subambient pressure inside the buccal cavity
(Alexander, 1969
). A larger
mouth increases the size of prey that can be taken by an individual fish
(Keast, 1985
;
Werner, 1974
) but appears to
decrease the ability to generate pressure (Figs
4,
5).
In light of this result, the increased use of body translation by fish with
larger mouths relative to body depth may result from a need to compensate for
decreased suction performance, a direct consequence of larger mouth size. How
this decreased suction performance is mediated is not clear because increased
suction pressure magnitude does not appear to increase the maximum distance
from which prey can be drawn into the buccal cavity
(Svanback et al., 2002;
Wainwright et al., 2001
).
Fish with smaller mouths may compensate for their inability to take larger
prey by increased effectiveness of feeding on smaller prey. In particular, the
rapid drop in pressure generated by fish such as L. macrochirus may
create acceleration forces capable of dislodging attached or clinging
macroinvertebrates. Benthic macroinvertebrates are known to contribute to the
diets of L. macrochirus and other fish with similar morphologies
(Etnier and Starnes, 1993;
Werner, 1977
).
Trade-offs associated with molluscivory
Another interesting potential morphological trade-off is revealed within
the Lepomis species. L. microlophus specializes on mollusk
prey, using its hypertrophied pharyngeal jaws and muscles to crush snails
(Lauder, 1983a). Its low
morphological potential results from a reduced epaxial muscle PCSA and moment
arm combined with increased buccal moment arm. These differences appeared to
result from dorsal and caudal displacement of the pectoral girdle, possibly
due to the greater space occupied by hypertrophied pharyngeal muscles and
jaws. The pharyngeal jaws are often thought of as functionally independent of
the oral jaws (Liem, 1974
).
Yet, in the case of L. microlophus, it appears possible that
increased pharyngeal crushing ability may have compromised suction feeding
performance.
Conclusions
This study successfully explains interspecific variation in suction feeding
performance in terms of musculoskeletal morphology. The model may be generally
used to investigate the ecological and evolutionary ramifications of
morphological variation among teleost fish. Specifically, the model addresses
the functional implications of variation in body depth and mouth size, both of
which are known to be common axes of diversification among fishes
(Keast and Webb, 1966;
Winemiller, 1991
;
Yonekura et al., 2002
).
However, the relationship between suction pressure generation and prey capture
ability is poorly understood at present, as is the relationship between
suction pressure and other metrics of suction feeding performance, such as
volume change per unit time (Muller,
1989
). Therefore, we advocate caution using the model to explain
patterns of trophic diversity without actual measurements of prey capture
performance (e.g. Norton,
1995
).
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Acknowledgments |
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