|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online December 14, 2006
Journal of Experimental Biology 210, 107-117 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02634
Feeding, fins and braking maneuvers: locomotion during prey capture in centrarchid fishes
Department of Organismic and Evolutionary Biology, Concord Field Station, Harvard University, 100 Old Causeway Road, Bedford, MA 01730, USA
e-mail: thigham{at}fas.harvard.edu
Accepted 7 November 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: kinematics, braking, swimming, locomotion, prey capture, pectoral fin, anal fin, caudal fin, maneuvering, deceleration, suction, feeding, ram speed, accuracy
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
; Gorb and Barth,
1994; Irschick and Losos,
1998; Iwaniuk et al.,
1999; Dunbar and Badam,
2000; Budick and O'Malley,
2000; Domenici,
2001; Borla et al.,
2002; Alfaro, 2003;
Rice and Westneat, 2005;
Higham et al., 2005a;
Higham et al., 2007;
Vincent et al., 2005;
Walker et al., 2005). Because
feeding is essential for growth and reproduction, the ability of the locomotor
system to facilitate feeding contributes meaningfully to fitness. Fishes, in
particular, capture prey by suction feeding, a rapid expansion of the mouth
cavity to draw in water, but this can only be effective once the predator uses
its locomotor system to position its mouth very close to the prey
(Day et al., 2005;
Higham et al., 2005a;
Higham et al., 2006a).
Although many fishes utilize suction to capture prey, the extent to which they
rely on it depends on the ecology of the predator
(Webb, 1984a;
Webb, 1984b;
Carroll et al., 2004;
Higham et al., 2006a). A
commonly cited dichotomy separates `ram feeders' from `suction feeders', where
the former relies predominantly on swimming speed to overtake evasive prey and
the latter relies more on suction to draw non-evasive prey items towards them.
These two scenarios, although very different, require a contribution from the
locomotor system to be effective. While swimming speeds at the time of prey
capture have been measured for many fishes (e.g.
Nyberg, 1971;
Rand and Lauder, 1981;
Norton and Brainerd, 1993;
Wainwright et al., 2001;
Porter and Motta, 2004;
Higham et al., 2005a;
Higham et al., 2005b;
Higham et al., 2006a;
Higham et al., 2007), detailed
interspecific examinations of locomotor movements throughout prey capture are
rare (Rice and Westneat,
2005).
Fishes that rely predominantly on suction to capture prey tend to have
small mouths, require a high level of accuracy during feeding, and feed on
relatively non-evasive prey (Higham et
al., 2006a). By contrast, fishes that rely more on ram tend to
have a larger mouth, require less accuracy and feed on relatively evasive
prey. In both cases, braking during prey capture is likely to be important.
For fishes relying predominantly on suction, braking will enhance accuracy by
giving the predator more time to adjust the position of its mouth relative to
the prey (Lauder and Drucker,
2004; Higham et al.,
2006a) and will alleviate the negative effects of swimming speed
on suction performance (Higham et al.,
2005a). For fishes relying predominantly on ram, braking will
enable the predator to be in a good position to follow a prey item that
escapes (Webb and Gerstner,
2000; Webb, 2006).
It remains unclear whether different species employ similar mechanisms of
braking and whether the relative timing of braking is similar between species
that employ different feeding strategies. Understanding how and when fishes
decelerate is central to understanding predator-prey interactions.
Apart from feeding, deceleration is an integral component of animal
movement and is ecologically important for intermittent locomotion
(Higham et al., 2001;
Kramer and McLaughlin, 2001),
avoiding obstacles in the environment
(Webb and Gerstner, 2000) and
arriving predictably at a certain location
(Higham et al., 2005b).
Despite the pervasiveness of braking among almost all mobile animals, there is
a paucity of studies that have addressed the mechanisms underlying
deceleration (Drucker and Lauder,
2002; Drucker and Lauder,
2003; Higham et al.,
2005b; McGowan et al.,
2005). Fishes have multiple control surfaces that can contribute
to braking, including the body, paired fins (pectoral and pelvic), median fins
(dorsal and anal) and caudal fin. It is possible that certain fishes use a
particular combination of fins to brake while other fishes use a completely
different combination. This many-to-one mapping of form to function
(Wainwright et al., 2005)
could amplify the interspecific diversity of fin movements during braking.
However, with the exception of Higham et al.
(Higham et al., 2005b) and
Rice and Westneat (Rice and Westneat,
2005), little is known about the integration of fin movements
during deceleration in fishes.
During braking, fishes commonly protract their pectoral fins in order to
increase the frontal area of the body
(Breder, 1926;
Harris, 1937a;
Harris, 1937b;
Bainbridge, 1963;
Videler, 1981;
Webb, 1984a;
Geerlink, 1987;
Webb and Fairchild, 2001;
Borla et al., 2002;
Drucker and Lauder, 2002;
Drucker and Lauder, 2003;
Higham et al., 2005b;
Rice and Westneat, 2005).
Pectoral fins likely enhance stability during braking since they limit side-
to-side (yawing) movements by balancing each other if protracted together. In
addition, perciform fishes such as centrarchids have pectoral fins that are
located laterally on the body and generate a braking force such that the
reaction force goes through the center of mass of the fish
(Drucker and Lauder, 2002),
thus limiting pitching movements. While the median fins can also contribute to
braking, moving them to one side can lead to moments of yaw and roll
(Drucker and Lauder, 2001;
Standen and Lauder, 2005). By
moving to the opposite side, the caudal fin might balance the forces from the
median fins, possibly preventing a yawing maneuver. Whether species that rely
more heavily on the caudal and median fins become less steady during prey
capture is not known. If this is the case, then the accuracy of the strike
might be compromised since a yawing maneuver would likely shift the location
of the mouth relative to the prey.
For aquatic vertebrates, centrarchid fishes have been a model group for
studies dealing with feeding (e.g. Nyberg,
1971; Lauder,
1980; Lauder et al.,
1986; Wainwright and Lauder,
1986; Norton and Brainerd,
1993; Grubich and Wainwright,
1997; Sass and Motta,
2002; Svanback et al.,
2002; Ferry-Graham et al.,
2003; Carroll,
2004; Carroll et al.,
2004; Day et al.,
2005; Higham et al.,
2005a; Higham et al.,
2006a; Higham et al.,
2006b; Carroll and Wainwright,
2006) and locomotor (e.g.
Jayne and Lauder, 1993;
Jayne and Lauder, 1994;
Jayne and Lauder, 1995;
Jayne and Lauder, 1996;
Jayne et al., 1996;
Gibb et al., 1994;
Johnson et al., 1994;
Lauder and Jayne, 1996;
Drucker and Lauder, 1999;
Drucker and Lauder, 2000;
Drucker and Lauder, 2001;
Standen and Lauder, 2005;
Higham et al., 2005b)
function. The considerable diversity in both ecology and morphology makes
centrarchids an excellent group for addressing questions regarding locomotor
function during feeding. For example, species from the genus
Micropterus, such as largemouth bass, have large mouths and are
thought to rely heavily on high swimming speeds to capture large, relatively
evasive prey (Higham et al.,
2006a). By contrast, species from the genus Lepomis, such
as bluegill, are deeper bodied, have relatively small mouths and are thought
to rely heavily on suction to capture small, relatively non-evasive prey.
To gain insights into the mechanisms and timing of deceleration during prey capture, I studied the body and fin kinematics of largemouth bass (Micropterus salmoides) and bluegill sunfish (Lepomis macrochirus) during feeding. I addressed the following three specific questions in this study. (1) How do fishes decelerate? I predicted that both species will increase their frontal area by employing their pectoral, caudal and median fins in order to decelerate. (2) How do fishes modulate the magnitude of deceleration? I predicted that both species would increase the angular excursion of their fins in order to increase frontal area and the speed of the water relative to the fins. (3) How do fishes modulate swimming speed when capturing stationary prey? Because they typically feed on evasive prey, I predicted that largemouth bass would maintain a constant, relatively high ram speed until after the prey was captured. By contrast, I predicted that bluegill would decelerate considerably prior to capturing the prey item in order to maintain strike accuracy. Although comparing two species precludes conclusive interpretations of locomotor behavior based on feeding biology, I chose two closely related centrarchid species that exhibit extremely different morphological and ecological traits related to feeding. Thus, conclusions are likely related to feeding biology rather than other factors such as phylogenetic history.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
) and feeding
(Higham et al., 2006a;
Higham et al., 2006b) studies
and are ideal for a comparative study since their ecology and morphology
differ considerably (Lauder and Jayne,
1996; Carroll et al.,
2004; Collar et al.,
2005). Furthermore, these genera (Lepomis and
Micropterus) are monophyletic and sister taxa with a most recent
common ancestor estimated about 24 million years ago
(Near et al., 2005). The fish
were collected around Davis, CA, USA and were maintained in separate 38-liter
aquaria. Data were analyzed from three individuals from each species of
similar size. The mean body mass for largemouth bass and bluegill used in
these experiments was 195.4±20.9 g and 143.0±24.7 g,
respectively. Experiments complied with all guidelines for the use and care of
animals in research at the University of California, Davis, where all
experiments were conducted.
|
Experimental protocol
Experiments were conducted in 200-liter tanks that were divided into two
sections, which facilitated obtaining start-stop episodes with a standardized
predator-prey distance. A very thin wire, angled away from the predator, was
used to suspend small goldfish (approximately 5 cm long) or ghost shrimp
(approximately 3-5 cm long). With the predator secured at one end of the tank
with a trap door, the prey item was suspended approximately 40 cm from the
door [see fig. 1 in Higham et
al. (Higham et al., 2005b)].
Once the trap door was removed, the predator was free to swim towards the prey
item and capture it. Although only sequences using tethered prey were filmed,
freely moving prey were offered to the fish after every two trials involving
tethered prey in order to maintain the fish's motivation and avoid any changes
in behavior associated with capturing tethered prey. Locomotion and feeding
were recorded from each fish using a high-speed NAC Memrecam ci digital system
(Tokyo, Japan) operating at 500 images s-1. Lateral and ventral
(via a mirror underneath the prey oriented at 45°) views of the
feeding event (Fig. 2) were
obtained.
|
Kinematic measurements
For the 120 ms prior to and the 60 ms following maximum gape, frames were
digitized at 250 Hz, since this provides a reliable estimate of acceleration
during locomotion (Walker,
1998). For each frame, the forward displacement of the fish was
calculated by digitizing the anterior margin of the eye in lateral view. Using
Igor Pro 5.01 (WaveMetrics Inc., Lake Oswego, OR, USA), the displacement data
were smoothed using a cubic spline interpolation (smoothing factor=1,
s.d.=0.001) and then the first and second derivative were calculated to obtain
velocities and accelerations, respectively. In addition to this measure of
instantaneous acceleration, the mean deceleration over the last 60 ms of prey
capture was calculated by dividing the change in velocity over this time
interval by 60 ms. From the lateral view, gape was the vertical distance
between the tip of the lower jaw and the tip of the upper jaw, and maximum
gape (MG) occurred when this distance was maximal.
From ventral view coordinates, instantaneous two-dimensional fin angles were calculated every 20 ms starting from 120 ms before MG and ending 60 ms after MG. The pectoral fin and anal fin angles were calculated between lines from the anterior margin of the base of the fin to the distal tip of the fin and a point on the body posterior to the fin. The caudal fin angle was calculated between lines from a point on the body posterior to the base of the fin to the base of the fin and the tip of the fin.
Pectoral fin drag
The methods of Geerlink (Geerlink,
1987) were used to calculate a theoretical value of maximal drag
created by the pectoral fins (Dpec) of bluegill and
largemouth bass. The following equation was used:
Dpec=
SpecU2CD,
where is the density of the surrounding water (1026 kg m-3),
Spec is the summed frontal area of the two pectoral fins
if they are fully extended in a vertical position, U is the velocity
of the fish at the time of MG, and CD is the drag
coefficient [1.17 as in Geerlink
(Geerlink, 1987)].
Statistical analyses
To determine whether the species differ morphologically, an analysis of
variance (ANOVA) was performed using species (fixed) as the independent
variable. The dependent variables, which were analyzed separately, were
pectoral fin aspect ratio (AR), and the log10-transformed
residuals from a least-squares regression of body mass and the area of each
fin (pectoral, anal and caudal). For pectoral fin area and AR, the
average of the left and right fin was used for each individual in the ANOVA.
In order to correct for multiple statistical tests, 
(0.05) was
adjusted using a sequential Bonferroni test
(Rice, 1989).
In order to determine how deceleration was modulated, multiple regressions were performed on each species separately, with the mean deceleration over the last 60 ms of prey capture as the dependent variable. The independent variables were ram speed at the time of MG, maximum pectoral fin angle, maximum anal fin angle and maximum caudal fin angle. Additional least-squares regressions were performed in order to determine the correlation between continuous variables. All variables in these analyses were log10 transformed to normalize variances, and in each case this allowed the variables to meet the assumptions of the parametric procedures.
Nine variables were included in a principal components analysis (PCA) to
reduce dimensionality and search for axes of correlated kinematic variation:
magnitude and timing of maximum caudal, anal and pectoral fin angles, maximum
average deceleration, angular excursion of the body along the z-axis,
and swimming speed at MG. The resulting principal components (1 and 2) became
the axes of a multidimensional locomotor kinematic space, and were visualized
in graphical form. To determine if the two species occupied different regions
of kinematic space, an ANOVA was performed with species (fixed) and individual
(nested within species; random) as the independent variables and the PC scores
from a particular axis as the dependent variable. In order to properly account
for the replication of observations within individuals, the denominator in the
F-test for the main effect of species was individual (nested within
species) (Zar, 1996). SYSTAT
version 9 (SPSS Inc., Chicago, IL, USA) was used for all statistical
analyses.
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
Throughout the approach to the prey, largemouth bass swam at a much higher speed than bluegill sunfish (Fig. 3; Table 2). Between 120 ms and 40 ms prior to MG, largemouth bass decelerated. During the 40 ms prior to MG, largemouth bass accelerated. Following MG, largemouth bass decelerated continually and substantially. Bluegill exhibited a similar sequence of events, although the acceleration before MG occurred during the 20 ms, rather than 40 ms, prior to MG (Fig. 3).
|
|
Ram speed, at the time of MG, was positively correlated with MG for largemouth bass (Fig. 4; r2=0.58; P<0.001). Although both species decelerated maximally following prey capture, the timing of maximum deceleration was much later for largemouth bass (30.3 ms after MG) than bluegill (6.7 ms after MG). Because the magnitude of deceleration was much higher for largemouth bass than bluegill, both species had similar ram speeds 60 ms after MG (Fig. 3A).
|
|
For both bluegill (r2=0.43; P<0.0001) and
largemouth bass (r2=0.31; P<0.01), increased
ram speeds 120 ms prior to MG resulted in increased magnitudes of deceleration
following prey capture (Fig.
6A). In addition, increased ram speeds 120 ms prior to MG resulted
in greater angular excursions (in the z-axis) of the body over the
final 80 ms of the feeding event for largemouth bass
(r2=0.52; P<0.001) but not bluegill
(r2=0.005; P>0.5)
(Fig. 6B). The model consisting
of maximum fin angles and ram speed at the time of MG explained 84%
(P<0.001) and 77% (P<0.001) of the variation in mean
deceleration in largemouth bass and bluegill, respectively. However, maximum
fin angles alone explain 37% (P>0.05) and 15% (P>0.05)
of the variation in mean deceleration in largemouth bass and bluegill,
respectively. Thus, ram speed accounts for a substantial amount of variation
in mean deceleration. For largemouth bass, the maximum angle of the pectoral
fin was also increased in order to increase the magnitude of deceleration.
Using the equation from Geerlink
(Geerlink, 1987) (see above),
largemouth bass and bluegill had theoretical values of maximum drag
(Dpec) equal to 0.62 and 0.04, respectively.
|
From the PCA, swimming (ram) speed at the time of MG, mean deceleration during the final 60 ms, and angular excursion of the body in ventral view were the most highly correlated variables with principal component 1 (PC 1; Fig. 7; Table 3). I will refer to this axis as the `ram speed' axis. Variables describing the angles of the fins loaded strongly on PC 2, and I will refer to this axis as the `fin' axis (Fig. 7; Table 3). Largemouth bass had significantly higher scores on PC 1 than bluegill (P=0.002), but there was no difference between species on PC 2 (P>0.05).
|
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Fin function during deceleration
Protraction of the pectoral fins during prey capture is a mechanism of
deceleration employed by largemouth bass and bluegill
(Fig. 5A). However, largemouth
bass protract their fins faster and to a greater extent
(Fig. 5A), suggesting that they
generate more reverse thrust with their fins
(Higham et al., 2005b).
Although largemouth bass have significantly smaller pectoral fins than
bluegill (Table 1), the drag
force exerted by a fin is proportional to its velocity squared. Thus, a
smaller fin, if protracted at a faster rate, has the potential for generating
comparable or greater forces than a larger fin. Using the methods of Geerlink
(Geerlink, 1987), the maximum
drag forces exerted by the pectoral fins are much greater in largemouth bass
than bluegill. Thus, despite having smaller pectoral fins, the swimming speed
of largemouth bass appears to result in much higher drag forces from pectoral
fins. When the area of the pectoral fins of bluegill sunfish is reduced, the
fish compensate by protracting their fins at a higher speed in order to
maintain a similar level of deceleration
(Higham et al., 2005b). This
behavioral modulation, combined with the results in the current study,
suggests that fin morphology might not be the only factor that defines braking
ability. For example, for a given pectoral fin (shape and size), the ability
of the fish to hold that fin against the flow of water would depend largely
upon the ability of the abductor muscles to generate and sustain the necessary
forces. A fish might then reach a threshold swimming speed where the fin
muscles would no longer generate forces great enough to match the force
exerted by the water on the fin. Thus, the ability of the pectoral fin
abductor muscles to protract the pectoral fins to a position where drag is
maximal could potentially limit the forces generated by fins, and ultimately
braking performance.
Few studies have quantified pectoral fin angles during prey capture in
fishes (Higham et al., 2005b;
Rice and Westneat, 2005). Rice
and Westneat examined the pectoral fin angles of two herbivorous species of
parrotfish, Sparisoma radians and Scarus quoyi, during
feeding (Rice and Westneat,
2005). As in largemouth bass and bluegill, both parrotfish species
sweep their pectoral fins forward to initiate a braking maneuver as they
approach the prey item. However, the braking maneuvers by the parrotfishes
resulted in a large drop in swimming speed prior to contact with the prey
item. This is quite different from the results of the present study in which
largemouth bass and bluegill both showed a large increase in swimming speed
prior to prey capture. One explanation is that the parrotfishes studied by
Rice and Westneat commonly feed from substrate, and braking after prey
capture, as in bluegill and largemouth bass, would result in a collision with
the substrate and potential injury. Future studies that examine the locomotor
kinematics of largemouth bass and bluegill feeding from substrate would
provide further insight into the differences between these groups of
fishes.
When a fish generates suction, the flow enters the mouth and exits the
posterior opercular slits. This allows the fish to ingest water at the same
time that water is expelled, resulting in a volume of ingested water far
exceeding the volume of the buccal cavity
(Day et al., 2005;
Higham et al., 2006a). The
water that exits the opercular cavities during the feeding event is in close
proximity to the anterior surfaces of the abducted pectoral fins
(Fig. 2F). Thus, the speed of
water passing the pectoral fins might be increased by this added flow out of
the opercular cavities, resulting in a further increase in drag generated by
the pectoral fins. This might enable fishes that have laterally placed
pectoral fins to take advantage of suction feeding for deceleration.
Largemouth bass and bluegill might take advantage of this, but bass have a
much higher volumetric flow rate during feeding, so their benefit would likely
be greater. Future studies that measure the flow exiting the opercular
cavities around pectoral fins during feeding would provide insight regarding
this potential method of enhancing deceleration.
The caudal and anal fins of both bluegill and largemouth bass were
abducted, increasing the frontal area of the body and enhancing deceleration
(Fig. 2). The use of caudal and
median fins during braking has been observed in many species of fishes (e.g.
Videler, 1981;
Higham et al., 2005b). The
median fins are capable of generating yawing and rolling movements of the body
(Jayne et al., 1996;
Drucker and Lauder, 2001;
Webb, 2004;
Standen and Lauder, 2005).
During braking, however, both median fins are abducted to a common side
(Higham et al., 2005b), thus
reducing the possible rolling movement from one of the median fins. In almost
all cases, the caudal fin moved to the opposite side of the median fins, which
likely limits the yawing movements that might be caused if they were abducted
to the same side. However, largemouth bass did exhibit an overall yawing
movement during feeding (Table
2), and it was positively correlated with ram speed
(Fig. 6B). The caudal fin of
largemouth bass is approximately three times the size of the anal fin and is
larger than the summed area of the pectoral fins
(Table 1). Thus, the yawing
movement of largemouth bass likely stems from the disproportionately large
caudal fin. The caudal fin of bluegill is less than twice the size of the anal
fin and is smaller than the summed area of the pectoral fins
(Table 1). This suggests that
the pectoral fins are generating more force than the caudal fin, which would
help prevent yawing movements. Future studies that quantify the forces, using
digital particle image velocimetry (DPIV), generated by the caudal and median
fins during braking would provide further insight into their relative
contributions to the overall braking force.
Mechanisms for modulating deceleration
The ability of a predator to modulate deceleration is imperative for
arriving at a prey item at a predictable speed. I predicted that the angular
excursions of the fins would increase in order to increase the magnitude of
deceleration. The increased excursions would increase the speed of the
surrounding water relative to the fin and thus result in higher drag forces.
In addition, I thought that largemouth bass, because they exhibit greater
deceleration, would exhibit greater fin excursions compared with bluegill.
Given that the magnitude of deceleration of largemouth bass is approximately
four times that of bluegill (Table
2), it is surprising that largemouth bass only exhibit greater
pectoral, and not other, fin excursions than bluegill during braking. What are
largemouth bass doing to achieve this level of deceleration? Within each
species, the only variable positively correlated with magnitude of
deceleration was ram speed. Since the speed of largemouth bass prior to, and
at the time, of prey capture is much greater than that of bluegill
(Fig. 3), the drag force
(proportional to velocity squared) from the body is much greater in largemouth
bass. Given the nature of the aquatic environment, this mechanism for
modulating deceleration might be very common among aquatic animals.
Swimming speed and prey capture
Largemouth bass approach their prey at much higher speeds than bluegill
(Fig. 3). This result supports
the notion that largemouth bass rely more heavily on ram, and bluegill rely
more on suction to capture prey (Carroll et
al., 2004; Higham et al.,
2006a). While both largemouth bass and bluegill decrease their ram
speed as they approach the prey item, they both accelerate immediately prior
to MG (Fig. 3). This might
allow the predator to adjust its location relative to the prey item and then
lunge forward at the last moment. Because largemouth bass commonly feed on
relatively evasive prey such as fish, it is not surprising that they
accelerate more than bluegill immediately preceding MG. This might enhance
their chances of capturing a prey that has the potential for initiating an
escape response. Alternatively, this acceleration might be a passive result of
ingesting water during suction feeding. This is supported by the fact that
largemouth bass have a much larger MG and ingest a much larger volume of water
than bluegill (Higham et al.,
2006a). Given that suction feeding naturally draws the predator
forward (Muller et al., 1982),
the higher volume flow rate exhibited by largemouth bass might result in
higher accelerations of the body than for bluegill. In addition, MG was
positively correlated with ram speed at the time of MG
(Fig. 4). Given that MG is
positively correlated with volume and volumetric flow rate in largemouth bass
(Higham et al., 2006a), the
correlation between ram speed and MG might simply be a result of increased
forces pulling the fish forward. This passive increase in swimming speed due
to suction generation might obscure interspecific comparisons of ram speed if
the species differ in the size of the ingested volume of water. Future studies
that measure ram speed should thus be cautious when interpreting ram speeds as
solely reflecting the motivation of the predator.
Largemouth bass typically feed on evasive prey such as fishes, and these
prey items likely require higher ram speeds in order to be caught. Largemouth
bass decelerate maximally much later than bluegill, supporting the idea that
bass maintain speed until the prey item is in the mouth. However, largemouth
bass do decelerate following prey capture, suggesting that overshooting the
prey item too much might be disadvantageous. Webb and Gerstner suggest that
predators feeding on evasive prey benefit from not overshooting the prey in
case the prey manages to escape (Webb and
Gerstner, 2000). Not overshooting would put the predator in a good
position to continue the chase and perhaps capture the prey item. Bluegill
also decelerate during prey capture, but the reasons are likely to be
different than for largemouth bass. Bluegill are more likely to feed in
cluttered habitats or from substrate, and decelerating would prevent a
collision in the environment. In addition, bluegill have much smaller mouths
and likely depend more on accurately positioning their mouth relative to the
prey item (see below for discussion), which might be compromised by swimming
fast (Higham et al.,
2006a).
An alternative explanation for why largemouth bass swim faster than
bluegill during prey capture is that they are simply better swimmers than
bluegill. This would suggest that bluegill are relegated to suction feeding as
a result of their relatively poor ability to swim. However, several studies
have shown that bluegill are morphologically specialized for suction feeding
(Carroll et al., 2004; Collar
and Wainwright, in press) and are better at generating a suction-induced flow
of water than largemouth bass (Higham et
al., 2006a; Higham et al.,
2006b). In addition, bluegill can reach swimming velocities that
are comparable to those of largemouth bass
(Domenici and Blake, 1997).
These lines of evidence strongly suggest that the locomotor behavior of
bluegill and largemouth bass during prey capture is strongly related to their
feeding ecology rather than their swimming capabilities.
The prey item in this study was tethered rather than freely moving. While
tethering prey could potentially confound the experimental results, it also
reflects an ecologically relevant prey capture situation for largemouth bass
and bluegill. Both of these species feed on prey that is commonly located on
or close to substrate, such as crustaceans
(Collar et al., 2005). In
addition, capturing prey prior to the initiation of an escape response (i.e.
prior to prey movement) has been advocated as an advantage of ram feeding (see
Nemeth, 1997) and is common in
studies of fish feeding. Future studies that examine locomotor behavior of
fish attacking a moving prey item would provide insight into the flexibility
of locomotor behavior and whether differences between species persist
regardless of prey presentation.
Braking and strike accuracy
Strike accuracy is imperative for successful prey capture and is an often
overlooked aspect of suction feeding performance
(Higham et al., 2006a). The
constraints imposed by accuracy likely diminish with an increased MG because
the ingested volume of water increases considerably with an increase in MG
(Higham et al., 2006a; Higham
et al., 2006c). Because increases in swimming speed decrease strike accuracy
(Webb and Skadsen, 1980;
Higham et al., 2006a; Higham
et al., 2006c), it is possible that only those species with larger mouths are
able to maintain high swimming speeds and still successfully capture prey.
Indeed, largemouth bass swim faster and have a much larger MG than bluegill.
This idea is corroborated by a study of 18 species of cichlid fishes in which
MG was significantly and positively correlated with ram speed (Higham et al.,
2006c). Future studies that directly measure accuracy through ontogeny, and
over a large range of ram speeds, could provide insight into the relationships
between ram speed, MG and strike accuracy. Largemouth bass became increasingly
unsteady (increased yawing movements during prey capture) with an increase in
ram speed (Fig. 6B). This is
probably an additional mechanism for decreased strike accuracy with an
increase in ram speed. It is possible that, if bluegill swam faster, they
would suffer a reduction in strike accuracy, which might significantly reduce
the rate of successful prey capture.
Implications for turning maneuvers
Turning maneuvers are commonly executed using pectoral fins
(Breder, 1926;
Drucker and Lauder, 2001;
Lauder and Drucker, 2004;
Walker, 2004;
Drucker et al., 2006). One
mechanism of turning is to extend the pectoral fin on one side of the body
while keeping the other fin against the body. The drag generated by the
extended fin on the inside of the turn acts as a pivot and contributes to the
rotational torque on the center of mass, resulting in yawing rotation
(Breder, 1926;
Drucker and Lauder, 2001;
Walker, 2004;
Drucker et al., 2006). Even
with a smaller pectoral fin, an increased rate of fin protraction will result
in an exponential increase in the drag force, and ultimately the yawing
rotation. Given the relationship between fluid speed and drag, the swimming
speed of a fish will likely also have profound effects on turning performance.
In addition, the morphology of pectoral fins is likely linked to the swimming
behavior of a fish. For example, fishes that typically swim fast, such as
largemouth bass, might benefit from having smaller pectoral fins because less
muscle power would be required to extend one of them during a turning
maneuver.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Alfaro, M. E. (2003). Sweeping and striking: a
kinematic study of the trunk during prey capture in three thamnophiine snakes.
J. Exp. Biol. 206,2381
-2392.
Bainbridge, R. (1963). Caudal fin and body movement in the propulsion of some fish. J. Exp. Biol. 40, 23-56.[Abstract]
Borla, M. A., Palecek, B., Budick, S. and O'Malley, D. M. (2002). Prey capture by larval zebrafish: evidence for fine axial motor control. Brain Behav. Evol. 60,207 -229.[CrossRef][Medline]
Breder, C. M. (1926). The locomotion of fishes. Zoologica N. Y. 6,159 -297.
Budick, S. A. and O'Malley, D. M. (2000). Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. J. Exp. Biol. 203,2565 -2579.[Abstract]
Carroll, A. M. (2004). Muscle activation and
strain during suction feeding in the largemouth bass Micropterus
salmoides. J. Exp. Biol.
207,983
-991.
Carroll, A. M. and Wainwright, P. C. (2006). Muscle function and power output during suction feeding in largemouth bass, Micropterus salmoides. Comp. Biochem. Phsyiol. 143A,389 -399.[CrossRef]
Carroll, A. M., Wainwright, P. C., Huskey, S. H., Collar, D. C.
and Turingan, R. G. (2004). Morphology predicts suction
feeding performance in centrarchid fishes. J. Exp.
Biol. 207,3873
-3881.
Collar, D. C. and Wainwright, P. C. (in press). Discordance between morphological and mechanical diversity in the feeding mechanism of centrarchid fishes. Evolution.
Collar, D. C., Near, T. J. and Wainwright, P. C. (2005). Comparative analysis of morphological diversity: does disparity accumulate at the same rate in two lineages of centrarchid fishes? Evolution 59,1783 -1794.[CrossRef][Medline]
Day, S. W., Higham, T. E., Cheer, A. Y. and Wainwright, P.
C. (2005). Spatial and temporal patterns of water flow
generated by suction feeding bluegill sunfish Lepomis macrochirus
resolved by Particle Image Velocimetry. J. Exp. Biol.
208,2661
-2671.
Domenici, P. (2001). The scaling of locomotor performance in predator-prey encounters: from fish to killer whales. Comp. Biochem. Physiol. 131A,169 -182.[CrossRef]
Domenici, P. and Blake, R. W. (1997). The kinematics and performance of fish fast-start swimming. J. Exp. Biol. 200,1165 -1178.[Abstract]
Drucker, E. G. and Lauder, G. V. (1999). Locomotor forces on a swimming fish: three-dimensional vortex wake dynamics quantified using digital particle image velocimetry. J. Exp. Biol. 202,2393 -2412.[Abstract]
Drucker, E. G. and Lauder, G. V. (2000). A hydrodynamic analysis of fish swimming speed: wake structure and locomotor force in slow and fast labriform swimmers. J. Exp. Biol. 203,2379 -2393.[Abstract]
Drucker, E. G. and Lauder, G. V. (2001). Wake dynamics and fluid forces of turning maneuvers in sunfish. J. Exp. Biol. 204,431 -442.[Abstract]
Drucker, E. G. and Lauder, G. V. (2002). Wake
dynamics and locomotor function in fishes: interpreting evolutionary patterns
in pectoral fin design. Integr. Comp. Biol.
42,997
-1008.
Drucker, E. G. and Lauder, G. V. (2003).
Function of pectoral fins in rainbow trout: behavioral repertoire and
hydrodynamic forces. J. Exp. Biol.
206,813
-826.
Drucker, E. G., Walker, J. A. and Westneat, M. W. (2006). Mechanics of pectoral fin swimming in fishes. In Fish Biomechanics (ed. R. E. Shadwick and G. V. Lauder), pp. 369-423. San Diego: Academic Press.
Dunbar, D. C. and Badam, G. L. (2000). Locomotion and posture during terminal branch feeding. Int. J. Primatol. 21,649 -669.
Ferry-Graham, L. A., Wainwright, P. C. and Lauder, G. V. (2003). Quantification of flow during suction feeding in bluegill sunfish. Zoology 106,159 -168.
Geerlink, P. J. (1987). The role of the pectoral fins in braking of mackerel, cod and saithe. Neth. J. Zool. 37,81 -104.
Gibb, A. C., Jayne, B. C. and Lauder, G. V.
(1994). Kinematics of pectoral fin locomotion in the bluegill
sunfish Lepomis macrochirus. J. Exp. Biol.
189,133
-161.
Gorb, S. N. and Barth, F. G. (1994). Locomotor behavior during prey-capture of a fishing spider, Dolomedes plantarius (Araneae, Araneidae) - galloping and stopping. J. Arachnol. 22,89 -93.
Grubich, J. R. and Wainwright, P. C. (1997). Motor basis of suction feeding performance in largemouth bass, Micropterus salmoides. J. Exp. Zool. 277, 1-13.[CrossRef]
Harris, J. E. (1937a). The mechanical significance of the position and movements of the paired fins in the Teleostei. Pap. Tortugas Lab. 31,173 -189.
Harris, J. E. (1937b). The role of the fins in the equilibrium of the swimming fish. II. The role of the pelvic fins. J. Exp. Biol. 14,32 -47.
Higham, T. E., Davenport, M. S. and Jayne, B. C.
(2001). Maneuvering in an arboreal habitat: the effects of
turning angle on the locomotion of three sympatric ecomorphs of
Anolis lizards. J. Exp. Biol.
204,4141
-4155.
Higham, T. E., Day, S. W. and Wainwright, P. C.
(2005a). Sucking while swimming: evaluating the effects of ram
speed on suction generation in bluegill sunfish Lepomis macrochirus
using digital particle image velocimetry. J. Exp.
Biol. 208,2653
-2660.
Higham, T. E., Malas, B., Jayne, B. C. and Lauder, G. V.
(2005b). Constraints on starting and stopping: behavior
compensates for reduced pectoral fin area during braking of the bluegill
sunfish Lepomis macrochirus. J. Exp. Biol.
208,4735
-4746.
Higham, T. E., Day, S. W. and Wainwright, P. C.
(2006a). Multidimensional analysis of suction feeding performance
in fishes: fluid speed, acceleration, strike accuracy and the ingested volume
of water. J. Exp. Biol.
209,2713
-2725.
Higham, T. E., Day, S. W. and Wainwright, P. C.
(2006b). The pressures of suction feeding: the relation between
buccal pressure and induced fluid speed in centrarchid fishes. J.
Exp. Biol. 209,3281
-3287.
Higham, T. E., Hulsey, C. D., Rican, O. and Carroll, A. M. (2007). Feeding with speed: prey capture evolution in cichlids. J. Evol. Biol. doi:10.1111/j.1420-9101.2006.01227.x .
Hoff, K. S., Lannoo, M. J. and Wassersug, R. J. (1985). Kinematics of midwater prey capture by ambystoma (Caudata: Ambystomatidae) larvae. Copeia 1985,247 -251.
Irschick, D. J. and Losos, J. B. (1998). A comparative analysis of the ecological significance of maximal locomotor performance in Caribbean Anolis lizards. Evolution 52,219 -226.[CrossRef]
Iwaniuk, A. N., Pellis, S. M. and Winshaw, I. Q. (1999). The relationship between forelimb morphology and behaviour in North American carnivores (Carnivora). Can. J. Zool. 77,1064 -1074.[CrossRef]
Jayne, B. C. and Lauder, G. V. (1993). Red and white muscle-activity and kinematics of the escape response of the bluegill sunfish during swimming. J. Comp. Physiol. A 173,495 -508.
Jayne, B. C. and Lauder, G. V. (1994). How swimming fish use slow and fast muscle fibers: implications for models of vertebrate muscle recruitment. J. Comp. Physiol. A 175,123 -131.[Medline]
Jayne, B. C. and Lauder, G. V. (1995). Are muscle fibers within fish myotomes activated synchronously? Patterns of recruitment within deep myomeric musculature during swimming in largemouth bass. J. Exp. Biol. 198,805 -815.
Jayne, B. C. and Lauder, G. V. (1996). New data on axial locomotion in fishes: how speed affects diversity of kinematics and motor patterns. Am. Zool. 36,642 -655.
Jayne, B. C., Lozada, A. F. and Lauder, G. V. (1996). Function of the dorsal fin in bluegill sunfish: motor patterns during four distinct locomotor behaviors. J. Morphol. 228,307 -326.[CrossRef]
Johnson, T. P., Syme, D. A., Jayne, B. C., Lauder, G. V. and Bennett, A. F. (1994). Modeling red muscle power output during steady and unsteady swimming in largemouth bass. Am. J. Physiol. 267,R481 -R488.
Kramer, D. L. and McLaughlin, R. L. (2001). The behavioral ecology of intermittent locomotion. Am. Zool. 41,137 -153.[CrossRef]
Lauder, G. V. (1980). The suction feeding
mechanism in sunfishes (Lepomis): an experimental analysis.
J. Exp. Biol. 88,49
-72.
Lauder, G. V. and Drucker, E. G. (2004). Morphology and experimental hydrodynamics of fish fin control surfaces. IEEE J. Oceanic Eng. 29,556 -571.[CrossRef]
Lauder, G. V. and Jayne, B. C. (1996). Pectoral fin locomotion in fishes: testing drag-based models using three-dimensional kinematics. Am. Zool. 36,567 -581.
Lauder, G. V., Wainwright, P. C. and Findeis, E. (1986). Physiological mechanisms of aquatic prey capture in sunfishes: functional determinants of buccal pressure changes. Comp. Biochem. Physiol. 84A,729 -734.[CrossRef]
McGowan, C. P., Baudinette, R. V. and Biewener, A. A.
(2005). Joint work and power associated with acceleration and
deceleration in tammar wallabies (Macropus eugenii). J.
Exp. Biol. 208,41
-53.
Muller, M., Osse, J. W. M. and Verhagen, J. H. G. (1982). A quantitative hydrodynamical model of suction feeding in fish. J. Theor. Biol. 95, 49-79.[CrossRef]
Near, T. J., Bolnick, D. I. and Wainwright, P. C. (2005). Fossil calibrations and molecular divergence time estimates in centrarchid fishes (Teleostei: Centrarchidae). Evolution 59,1768 -1782.[CrossRef][Medline]
Nemeth, D. H. (1997). Modulation of attack behavior and its effect on feeding performance in a trophic generalist fish, Hexagrammos decagrammus. J. Exp. Biol. 200,2155 -2164.[Abstract]
Norton, S. F. and Brainerd, E. L. (1993). Convergence in the feeding mechanics of ecomorphologically similar species in the Centrarchidae and Cichlidae. J. Exp. Biol. 176, 11-29.[Abstract]
Nyberg, D. W. (1971). Prey capture in the largemouth bass. Am. Midl. Nat. 86,128 -144.[CrossRef]
Porter, H. T. and Motta, P. J. (2004). A comparison of strike and prey capture kinematics of three species of piscivorous fishes: Florida gar (Lepisosteus platyrhincus), redfin needlefish (Strongylura notata), and great barracuda (Sphyraena barracuda). Mar. Biol. 145,989 -1000.[CrossRef]
Rand, D. M. and Lauder, G. V. (1981). Prey capture in the chain pickerel, Esox niger: correlations between feeding and locomotor behavior. Can. J. Zool. 59,1072 -1078.
Rice, A. N. and Westneat, M. W. (2005).
Coordination of feeding, locomotor and visual systems in parrotfishes
(Teleostei: Labridae). J. Exp. Biol.
208,3503
-3518.
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43,223 -225.[CrossRef]
Sass, G. G. and Motta, P. J. (2002). The effects of satiation on strike mode and prey capture kinematics in the largemouth bass, Micropterus salmoides. Environ. Biol. Fishes 65,441 -454.[CrossRef]
Standen, E. M. and Lauder, G. V. (2005). Dorsal
and anal fin function in bluegill sunfish Lepomis macrochirus:
three-dimensional kinematics during propulsion and maneuvering. J.
Exp. Biol. 208,2753
-2763.
Svanback, R., Wainwright, P. C. and Ferry-Graham, L. A. (2002). Linking cranial kinematics, buccal pressure, and suction feeding performance in largemouth bass. Physiol. Biochem. Zool. 75,532 -543.[CrossRef][Medline]
Videler, J. J. (1981). Swimming movements, body structure and propulsion in cod Gadus morhua. Symp. Zool. Soc. Lond. 48,1 -27.
Vincent, S. E., Herrel, A. and Irschick, D. J. (2005). Comparisons of aquatic versus terrestrial predatory strikes in the pitviper, Agkistrodon piscivorus. J. Exp. Zoolog. Part A Comp. Exp. Biol. 303,476 -488.
Wainwright, P. C. and Lauder, G. V. (1986). Feeding biology of sunfishes: patterns of variation in the feeding mechanism. Zool. J. Linn. Soc. 88,217 -228.[CrossRef]
Wainwright, P. C., Ferry-Graham, L. A., Waltzek, T. B., Carrol,
A. M., Hulsey, C. D. and Grubich, J. R. (2001). Evaluating
the use of ram and suction during prey capture by cichlid fishes.
J. Exp. Biol. 204,3039
-3051.
Wainwright, P. C., Alfaro, M. E., Bolnick, D. I. and Hulsey, C.
D. (2005). Many-to-one mapping of form to function: a general
principle in organismal design? Integr. Comp. Biol.
45,256
-262.
Walker, J. A. (1998). Estimating velocities and accelerations of animal locomotion: a simulation experiment comparing numerical differentiation algorithms. J. Exp. Biol. 201,981 -995.[Abstract]
Walker, J. A. (2004). Kinematics and performance of maneuvering control surfaces in Teleost fishes. IEEE J. Oceanic Eng. 29,572 -584.[CrossRef]
Walker, J. A., Ghalambor, C. K., Griset, O. L., McKenney, D. and Reznick, D. N. (2005). Do faster starts increase the probability of evading predators? Funct. Ecol. 19,808 -815.[CrossRef]
Webb, P. W. (1984a). Body and fin form and strike tactics of four teleost predators attacking fathead minnow (Pimephales promelas) prey. Can. J. Fish. Aquat. Sci. 41,157 -165.
Webb, P. W. (1984b). Body form, locomotion and foraging in aquatic vertebrates. Am. Zool. 24,107 -120.
Webb, P. W. (2004). Maneuverability - general issues. IEEE J. Oceanic Eng. 29,547 -555.[CrossRef]
Webb, P. W. (2006). Stability and maneuverability. In Fish Biomechanics (ed. R. E. Shadwick and G. V. Lauder), pp. 281-332. San Diego: Academic Press.
Webb, P. W. and Fairchild, A. G. (2001). Performance and maneuverability of three species of teleostean fishes. Can. J. Zool. 79,1866 -1877.[CrossRef]
Webb, P. W. and Gerstner, C. L. (2000). Fish swimming behaviour: predictions from physical principles. In Biomechanics in Animal Behaviour (ed. P. Domenici and R. W. Blake), pp. 59-77. Oxford: BIOS Scientific.
Webb, P. W. and Skadsen, J. M. (1980). Strike tactics of Esox. Can. J. Zool. 58,1462 -1469.[Medline]
Zar, J. H. (1996). Biostatistical Analysis. Upper Saddle river, NJ: Prentice Hall.
This article has been cited by other articles:
|
|
 |
|
  P. C. Wainwright, R. S. Mehta, and T. E. Higham Stereotypy, flexibility and coordination: key concepts in behavioral functional morphology J. Exp. Biol., November 15, 2008; 211(22): 3523 - 3528. |
