Function of pectoral fins in rainbow trout: behavioral repertoire and hydrodynamic forces
Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA
* Author for correspondence (e-mail: edrucker{at}uci.edu)
Accepted 11 November 2002
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Summary |
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Key words: swimming, maneuvering, locomotion, pectoral fin, vortex wake, flow visualization, digital particle image velocimetry, rainbow trout, Oncorhynchus mykiss
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Introduction |
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One important aspect of salmoniform locomotion, however, remains poorly
understood: the role of non-axial propulsors during steady and unsteady
swimming. Although the primary source of mechanical power for locomotion
indeed is supplied by the myotomal musculature, ancillary propulsors,
including the paired fins, are commonly recruited to supplement body
undulation. During routine swimming (low-speed volitional locomotion, as
defined by Webb, 1991), trout
and salmon have been observed to use their pectoral fins, in particular, for
fine control of body position. However, aside from measurements of
pectoral-fin beat frequency (McLaughlin
and Noakes, 1998
), information on pectoral fin function in such
fishes has been strictly qualitative (e.g. the pectoral fins exhibit `swimming
movements' or `paddling movements'). There is little detailed, quantitative
information about pectoral fin use during locomotion by salmoniform fishes,
and virtually nothing is known about the hydrodynamic functions served by
active pectoral fin movement in this major taxonomic group.
The objective of the present study was to investigate the function of the
pectoral fins in a representative salmoniform fish, the rainbow trout
Oncorhynchus mykiss, during both steady and unsteady locomotion.
Specifically, we first characterized the behavioral repertoire of trout
pectoral fins by documenting patterns of use during constant-speed swimming
and during three maneuvering behaviors: hovering, turning and braking. Second,
we employed quantitative flow visualization to record pectoral-fin wake
dynamics. Empirical measurement of wake momentum flux and of resulting fluid
force enabled identification of the propulsive roles played by various
pectoral fin motions. Of the several maneuvering behaviors exhibited by trout,
we focused in particular on the mechanics of braking. Using experimental data
on the orientation of pectoral fin forces during deceleration of the body, we
evaluated a long-standing yet previously untested functional hypothesis
(Breder, 1926) regarding
braking in plesiomorphic ray-finned fishes.
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Materials and methods |
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Anatomical measurements
Trout were anesthetized using tricaine methanesulfonate (MS-222) to allow
morphological measurements of the pectoral fin. Digital photographs were taken
of fish in left lateral aspect, from which pectoral-fin base angle and surface
area were measured (ImageJ software, National Institutes of Health, USA). Fin
base angle was taken as the angle of inclination of the axis connecting the
bases of the leading- and trailing-edge fin rays, and was measured both with
the pectoral fin adducted, as when at rest, and abducted, as during
maneuvering locomotion. Surface area was measured with the fin in an adducted
and fully expanded position. After experimentation, animals were killed by
overdose of MS-222 and frozen with their bodies straight. The location of the
center of mass of the body was then estimated by suspending fish from
needle-tipped probes inserted bilaterally into the flank. Probes were moved
along the longitudinal body axis until the fish balanced; at that
anteroposterior position, the same procedure was then performed along the
dorsoventral axis. The center of mass of the body was assumed to lie at the
midpoint of the transverse axis intersecting the
anteroposteriordorsoventral balance point.
Behavioral observations and wake visualization
Trout swam individually in the center of the working area (28 cmx28
cmx80 cm) of a variable-speed freshwater flow tank under conditions
similar to those described in our previous research (Drucker and Lauder,
1999,
2000
,
2001a
,b
).
Three current speeds were used to elicit a range of steady and unsteady
swimming behaviors. Relatively low-speed swimming was selected for study,
since such behavior commonly involves use of the pectoral fins to generate
locomotor forces, and comprises the majority of the time-activity and energy
budgets of many fishes including salmonids (reviewed by
Webb, 2002
). Rectilinear axial
locomotion was induced at 0.5 BL s-1, the lowest speed at
which fish consistently oriented upstream and held station in the current, and
at 1.0 BL s-1. Low-speed maneuvering locomotion was
performed by trout in response to a visual and auditory stimulus. A
small-diameter wooden dowel was directed into the water and toward the floor
of the working area approximately 20 cm away from trout swimming steadily at
0.5 BL s-1 (cf.
Drucker and Lauder, 2001b
).
Introducing the dowel upstream of or lateral to the head elicited braking or
low-speed (non-fast-start) turning, respectively. The fish's immediate
response to the stimulus precluded any interaction between the pectoral fin
wake and the wake shed by the dowel. In still water (i.e. with the flume
current turned off), trout used slow fin motions to maintain a stable
orientation and to hold body position in the water column; this behavior we
termed hovering. To characterize patterns of movement of the pectoral fins and
body during both steady swimming and maneuvering, fish were imaged
simultaneously in lateral and ventral aspect using synchronized digital
high-speed video cameras (Redlake MotionScope PCI 500) operating at 250 frames
s-1 (1/500 s shutter speed). Review of these light video recordings
(39 sequences from three fish) allowed each swimming behavior to be defined
kinematically.
In separate swimming trials the wake of the pectoral fin was visualized
using digital particle image velocimetry (DPIV). This technique provides
empirical data on patterns of water flow in two-dimensional sections of a
swimming fish's wake (as described in detail by
Willert and Gharib, 1991;
Drucker and Lauder, 1999
;
Lauder, 2000
). For our DPIV
experiments with rainbow trout, an 8 W continuous-wave argon-ion laser
(Coherent Inc., Santa Clara, CA, USA) was focused into a thin light sheet (1-2
mm thick) which illuminated reflective microparticles suspended in the water.
Particle motion induced by pectoral fin activity was recorded by imaging the
laser sheet with one of the Redlake video cameras (250 frames s-1,
1/1000 s shutter speed); the second camera synchonously recorded a
perpendicular reference view showing the position of the fin relative to the
visualized transection of the wake. In separate experiments, the laser was
oriented to reveal two perpendicular flow planes: frontal (horizontal) and
parasagittal (vertical) (cf. fig. 2 in
Drucker and Lauder, 1999
). In
this study we focused our analysis on laser planes that maximized the image of
within-plane flow for each swimming behavior. During steady swimming, hovering
and yawing turns, wake flow was studied within the horizontal plane; for
braking, the vertical flow plane was examined.
Kinematic and hydrodynamic analysis
Unsteady maneuvers induced by the experimental stimulus involved
three-dimensional body movements. To define these swimming behaviors
quantitatively, continuous variation in body velocity in the X, Y and
Z directions (see reference axes in
Fig. 1) was partitioned into
discrete ranges. The distance traveled by an anatomical reference point
visible in both lateral and ventral views (the proximal end of the pectoral
fin's leading edge) was measured over the course of the fin stroke duration
(i.e. abduction + adduction time) using ImageJ software. These excursion and
timing data allowed calculation of mean body velocities X, Y and
Z (cm s-1). Such body velocities are expected to differ
slightly from those obtained by tracking motion of the fish's center of mass,
a landmark whose position could not be consistently imaged in our relatively
high-magnification video field. For the purpose of distinguishing turning from
braking, the following kinematic criteria were applied: a turning event was
defined as a maneuver involving translation of the body away from the given
stimulus (Z>0) without backward displacement of the body
(X0); braking was defined as maneuvers with X<0. In
addition to linear velocity, the average angular velocity of the body was
calculated by measuring the degree of rotation of the longitudinal body axis
over the pectoral-fin stroke period. From ventral and lateral video views,
respectively, yawing rotation during turning and pitching rotation during
braking were measured (N=22 events per behavior).
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In total, 83 DPIV video sequences of steady and unsteady locomotion from
five fish were reviewed to establish general wake flow patterns. Of these,
detailed quantitative analysis was restricted to scenes in which the fish swam
at a constant speed, either during prolonged rectilinear locomotion or
immediately before maneuvers, and the pectoral fin intersected the light sheet
at approximately mid-span (N=15 each for turning and braking;
N=12 for hovering; N=5 for steady straight-ahead swimming).
Water velocity fields in the wake of the pectoral fin were calculated from
consecutive digital video images (480 pixelsx420 pixels, 8-bit
grayscale) by means of spatial cross-correlation
(Willert and Gharib, 1991). To
study the relatively weak vortices shed by trout pectoral fins, we employed a
new image processing algorithm that greatly improved the accuracy and spatial
resolution of DPIV flow analysis. With InsightUltra software (TSI Inc., St
Paul, MN, USA), which utilizes recursive local-correlation
(Hart, 2000
), we measured
velocity fields 8-9 cm on each side that contained nearly 2300 vectors (i.e.
52 horizontalx44 vertical or 30 vectors cm-2). For all
swimming behaviors except hovering in still water, the average free-stream
flow velocity of the flume was subtracted from each vector matrix to reveal
vortical structures in the wake and to allow measurement of flow structure and
strength (for details, see Drucker and
Lauder, 1999
). Vortex circulation was calculated using a
custom-designed computer program. Jet flow induced by pectoral fin motion was
quantified as follows: (i) jet velocity was measured as the mean magnitude of
velocity vectors comprising the region of accelerated flow; (ii) jet angle was
taken as the average orientation of these vectors, measured relative to the
longitudinal axis of the fish at the onset of the pectoral fin stroke. Both
jet measurements were made at the end of pectoral fin adduction, at which time
vortices and associated jet flow were fully developed.
Estimating the fluid force exerted by the pectoral fin involved measuring
the rate of change in wake momentum over the stroke duration. On the basis of
observed planar flow patterns (see Results), the three-dimensional shape of
the wake generated by each fin stroke was taken as a vortex ring (cf. Drucker
and Lauder, 1999,
2000
,
2001b
). Ring momentum was
calculated as the product of water density, vortex circulation and ring area
(the latter two measurements made at the end of the fin stroke). Ring area was
taken as
R2, where R is half the distance
between paired vortex centers. Following earlier work
(Milne-Thomson, 1966
),
time-averaged wake force was then computed as the total momentum divided by
the period of propulsive fin motion. Total force exerted by the pectoral fin
was resolved geometrically into perpendicular components within the frontal
plane (thrust and lateral force) and parasagittal plane (thrust and lift)
according to the mean jet angle. Further details of the calculation of wake
force by this method can be found in earlier studies
(Spedding et al., 1984
;
Dickinson, 1996
;
Dickinson and Götz, 1996
;
Drucker and Lauder, 1999
). The
accuracy of wake force estimates provided by the DPIV technique has previously
been demonstrated by the measurement of a hydrodynamic force balance on
steadily swimming fishes (Drucker and
Lauder, 1999
; Nauen and
Lauder, 2002a
).
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Results |
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Low-speed turning maneuvers elicited from trout were submaximal escape responses involving excursions of both pectoral fins. At the onset of a turn, as the experimental stimulus was issued (Fig. 3A,B), the pectoral fin on the same side of the body as the source of the stimulus (the `strong-side' fin) rapidly abducted and the body rotated toward the contralateral or `weak' side (Fig. 3C,D). As the fish translated away from the stimulus, the strong-side fin returned toward the body while the weak-side fin, delayed in its movements, reached a position of maximal abduction. This turning maneuver in trout involved both yawing rotation (mean 13° s-1) and bending of the anterior trunk (Fig. 3E,F; Table 1). Rapid deceleration of the body, unlike turning, was characterized by temporally and spatially symmetrical excursions of the left and right pectoral fins. When trout were stimulated to brake, the fins were synchronously abducted and flexed along their long axes so that the trailing edges were elevated and protracted (Fig. 4A-D). These fin motions caused the fish to move posteriorly and to pitch nose-downward (mean 11 ° s-1) (Fig. 4E,F; Table 1).
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Pectoral-fin stroke timing and linear velocity of the body during maneuvering also varied significantly with behavior. During turning and braking, the fin stroke generating the strongest wake flow, and hence greatest fluid force, was abduction. The duration of pectoral fin abduction (TAB) was 127±8 and 207±13 ms (mean ± S.E.M.), respectively, for these two maneuvers (unpaired t-test, d.f.=28; P<0.01). By definition, turning and braking differed in the direction of body motion along the X-axis. For the former, the body moved anteriorly over the course of the pectoral-fin stroke cycle (X=+0.9 cm s-1 on average); for the latter, body motion was posteriorly directed (mean X=-3.5 cm s-1) (Fig. 5). In addition, turns involved significantly faster body translation toward the weak side (mean difference=1.6 cm s-1; t-test, d.f.=28; P<0.001). Both maneuvering behaviors were characterized by sinking in the water column (Y<0), with braking exhibiting a greater downward body velocity than turning by 1.6 cm s-1 on average (Fig. 5).
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Wake dynamics and locomotor force
Pectoral fin motions exhibited during maneuvering generate distinctive wake
flow patterns. While maintaining a stationary body position in still water,
trout use asymmetrical left- and right-side fin strokes to produce alternating
anterior- and posterior-directed jet flow. During this hovering maneuver, fin
protraction results in the entrainment of water behind the propulsor; flow
around the lateral and medial margins of the fin takes the form of paired
attached vortices with opposite-sign circulation
(Fig. 6, left side). These
vortices remain bound to the fin at the end of the protraction half-stroke,
and are not shed anteriorly as free vorticity. At the end of the retraction
half-stroke, the pectoral fin is feathered and sheds attached flow posteriorly
into the wake (Fig. 6, right
side). Because contralateral fin strokes are out of phase with each other,
wake flow is generated in opposite directions on opposite sides of the body at
once (velocity range=1.1-7.5 cm s-1;
Table 1). During turning, by
contrast, the dominant wake flow is generated unilaterally. Abduction of the
strong-side fin results in the appearance of a single free vortex within the
horizontal plane of analysis. This flow structure contains a region of
relatively high-velocity jet flow oriented anteriorly and laterally
(Fig. 7B). Braking maneuvers
are characterized by the production of paired counterrotating vortices by each
pectoral fin. Each half-stroke generates a single vortex, with abduction
typically creating stronger rotational flows than adduction (cf. clockwise and
counterclockwise vortices in Fig.
7D). For braking and turning, the velocity of the central region
of accelerated flow ranged from 2.5 to 11.3 cm s-1 (mean 6 cm
s-1; Table 1).
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The paired-vortex flow pattern observed for trout during deceleration of
the body is similar to that noted previously for other fishes swimming by
pectoral fin propulsion (Drucker and Lauder,
1999,
2000
,
2001b
), and we assume that
centers of opposite-sign rotation within planar flow fields represent
transections of a roughly symmetrical, three-dimensional vortex ring (see also
Spedding et al., 1984
;
Spedding, 1986
;
Nauen and Lauder, 2002a
).
Vortex circulation generated by fin abduction (
AB) exceeded
that produced by fin adduction (
AD) by nearly twofold on
average (mean ± S.E.M.=19.9±1.4 and 11.4±0.9
cm2 s-1, respectively). This pattern contrasts with
results of earlier DPIV studies of fishes swimming by pectoral fin propulsion,
in which
AB and
AD were comparable (e.g.
Drucker and Lauder, 1999
). In
perfect cross sections of a symmetrical vortex ring, opposite-sign paired
vortices have circulations of equal magnitude, according to Helmholtz's
theorem (Fung, 1990
). In our
studies with trout, to avoid underestimating total vortex ring circulation due
to possible out-of-plane flow on adduction, or by non-transverse sectioning of
the vortex ring, we calculated stroke-averaged wake momentum during braking
using
AB only, rather than the mean of
AB
and
AD. Pectoral fin force then was taken as this momentum
value divided by TAB. For turning, during which only one
vortex appears on abduction, momentum and force were calculated similarly by
modeling the wake as a vortex ring whose medial portion remains attached to
the fin at the end of abduction (cf. fig. 8 in
Drucker and Lauder, 1999
). In
this case, vortex ring diameter was approximated by measuring the distance
between the centroid of the pectoral fin and the center of the shed vortex at
the end of abduction.
Turning maneuvers were characterized by the production of anterolaterally directed wake force, with the lateral component exceeding the anterior component by a factor of 2.5 on average (Table 1). Braking involved the exertion of significantly greater anterior force than turning (unpaired t-test, d.f.=28; P<0.05), and a substantial dorsally oriented component of force. When corrected for interindividual variation in pectoral fin area (mean ± S.D.=3.18±0.34 cm2, N=4 fish) swimming forces ranged from approximately 0.5 to 1.5 mN cm-2 (Table 1). Since the three-dimensional morphology of the wake was not well defined for hovering, locomotor forces were not estimated for this behavior.
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Discussion |
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The impressive kinematic versatility of the trout pectoral fin during
maneuvering may be facilitated by the mobility of the fin base. In previous
studies of paired fin function in fishes, the angle of inclination of the
fin's insertion on the body () has been viewed as influencing the
propulsor's kinematic range of motion
(Geerlink, 1989
;
Lauder and Jayne, 1996
;
Drucker and Jensen, 1997
;
Wainwright et al., 2002
;
Walker and Westneat, 2002
).
More vertically oriented fin bases restrict fin oscillation to primarily
anteroposterior (fore-and-aft) motions within a horizontal plane, whereas more
horizontally oriented bases dictate a primarily dorsoventral (up-and-down)
motion within a vertical plane (see
Drucker and Lauder, in press
).
In rainbow trout, the insertion of the pectoral fin on the body is a flexible
hinge joint, which defines a primary dorsoventral kinematic axis but also
allows additional degrees of freedom of motion. When the pectoral fin is
adducted (e.g. at rest during steady swimming), the base of the fin lies at a
moderate angle to the horizontal (mean ± S.D.=42±5°,
N=4 fish) (Fig. 8A).
However, when the fin is abducted (i.e. in a position relevant for
propulsion), the anterior fin base is depressed, which markedly reduces
(Fig. 8B-D; mean
± S.D.=10±3°). Similar mobility of the pectoral fin base is
visible in trout and salmon performing agonistic displays (see fig. 7 in
Kalleberg, 1958
). In
salmoniform fishes, contraction of the arrector ventralis (`Marginalmuskel' of
Jessen, 1972
), which inserts
on the proximal end of the first fin ray, may play an important role in
causing this fin rotation.
With a nearly horizontal pectoral fin base during maneuvering, coupled with
spanwise fin rotation, trout can achieve fore-and-aft fin movements that are
critical for the generation of anteroposterior wake flows (Figs
6,
7). In general, fin base angle
cannot be considered a fixed meristic for a given species, but rather a
variable whose value depends on propulsor motion. Fin base angle as measured
externally may be influenced by changes in position of the bases of pectoral
fin rays relative to internal skeletal elements such as the radials, scapula
and coracoid supporting the fin. Each of these elements is mobile, although
magnitudes of pectoral girdle excursion during locomotion are not known. For
relating fin design to locomotor kinematics and function (e.g. Drucker and
Lauder, 2001a,
in press
), the most
appropriate measure may be the `functional fin base angle' the degree
of inclination of the fin in a position used for swimming.
The absence of pectoral fin motion during steady swimming by the fish
examined in this study conflicts with the results of an earlier report of the
swimming behaviors of trout in their natal streams
(McLaughlin and Noakes, 1998).
For young-of-the-year brook trout Salvelinus fontinalis, the
relationship between pectoral-fin beat frequency and swimming speed was highly
variable, but the frequency of oscillation decreased significantly as speed
increased. However, a majority of the fish observed during steady locomotion
(approximately 65%) beat their pectoral fins at all swimming speeds (fig. 1C
in McLaughlin and Noakes,
1998
). This fin activity observed in the field may not be directly
comparable to that documented under more controlled laboratory conditions.
When swimming against a current with large-scale turbulence, as in natural
streams, trout are likely required to use their paired fins for correcting
heading and attitude in response to local flow disturbance. Such stabilizing
behavior is not expected when fish swim against a microturbulent current, as
in the present flow tank study. Our results indicate for trout that corrective
pectoral fin motions may not be necessary during steady swimming if the flow
environment is sufficiently homogeneous. Further investigation of propulsor
motions used in the field, in particular involving quantitative kinematic
analysis, will improve our understanding of the diverse behavioral repertoire
of the salmoniform pectoral fin.
Pectoral fin function during maneuvering locomotion
The use of quantitative flow visualization to study the wake of freely
swimming fish provides insight into the functional roles played by the fins
during locomotion. Previous studies have collected empirical data on wake flow
generated by rainbow trout, but this work has focused on the mechanics of the
axial propeller during straight-ahead constant-speed swimming
(Blickhan et al., 1992;
Lauder et al., in press
;
Nauen and Lauder, 2002b
). The
present application of DPIV to investigate wake dynamics in trout has revealed
that the paired fins also serve important locomotor functions, in particular
during unsteady maneuvering.
For negatively buoyant fishes (e.g. Synchropus picturatus;
Blake, 1979) as well as for
flying animals (insects and birds;
Weis-Fogh, 1973
;
Rayner, 1979
;
Ellington, 1984
), hovering
involves the generation of relatively large lift forces with the paired
appendages to balance body weight. For rainbow trout, which are only slightly
negatively buoyant (Webb,
1993
), `hovering' motions of the paired fins undoubtedly generate
some lift, but serve primarily to maintain a stationary and stable body
position in still water. Unlike many other fishes that undulate large,
broad-based pectoral fins along their anteroposterior axes (e.g.
Blake, 1978
), trout possess
relatively small pectoral fins, which oscillate about narrow bases in a fore
and aft motion during hovering. The broadside orientation of the fin during
the protraction half-stroke results in an induced jet flow behind the
propulsor directed anteriorly (left side of
Fig. 6;
Table 1); this momentum flow
toward the surface of the fin reflects the production of drag. During the
retraction half-stroke of hovering, the pectoral fin is feathered slightly,
allowing attached fluid to be shed away from the fin and into the wake
posteriorly (right side of Fig.
6; Table 1), a
thrust-producing flow pattern (cf. Drucker
and Lauder, 2002
). When hovering, therefore, each pectoral fin
serves the alternating functions of braking and propulsion. Playing these
roles simultaneously on opposite sides of the body, the fins exert a
rotational moment around the center of mass of the body during each
half-stroke. Over the course of two consecutive half-strokes opposite-sign
moments are balanced, as evidenced by the lack of discernible yawing of the
body during this maneuver.
Unlike fast-start turning, which is characterized by extreme and rapid
axial bending (e.g. Domenici and Blake,
1997), the turning behavior examined in this study was a low-speed
startle reaction powered primarily by the pectoral fins. In response to the
experimental stimulus, trout used strong-side pectoral fin abduction to yaw
the body (angular velocity range=4-41 ° s-1;
Table 1) and to translate it
toward the weak side (linear velocity range=1.0-2.8 cm s-1;
Fig. 5). These body velocities
are comparable to those measured in bluegill sunfish Lepomis
macrochirus performing the same maneuver
(Drucker and Lauder, 2001b
).
In trout, pectoral fin abduction during turning generates anterolaterally
directed wake flow (Fig. 7B).
The fluid force acting to move the fish away from the turning stimulus arises
in reaction to the dominant laterally oriented component of momentum added to
the wake. Despite the production also of an anterior component of pectoral fin
force (mean 1.1 mN, Table 1),
whose reaction resists forward motion of the body, trout were consistently
observed to travel anteriorly during turning (X>0,
Fig. 5). One explanation for
this phenomenon is that turning forces are not generated solely by the
pectoral fins. In addition to strong-side pectoral fin motion, turning trout
exhibited low-amplitude axial bending and abduction of the pelvic fin
posterior to the center of mass (Fig.
3), as well as abduction of the dorsal fin toward the strong-side
of the body (not figured; fin obscured by body in ventral view,
Fig. 3). These propulsive fin
motions may contribute to the forward translation of the body observed during
the maneuver. The simultaneous use of multiple fins by fishes is well
documented (e.g. Arreola and Westneat,
1996
; Gordon et al.,
2000
). However, the partitioning of swimming force among these
propulsors as yet has received very little experimental study (see Drucker and
Lauder, 2001a
,
2002
).
The pattern emerging from analysis of wake dynamics in trout is that the
pectoral fins do not function primarily as thrust-generating surfaces.
Although the fins can indeed generate posteriorly oriented fluid flow, this
function is limited to the retraction stroke of hovering during which jet
velocities are relatively low. For the other maneuvers examined here, the
largest component of locomotor force was oriented either laterally (turning)
or anteriorly and dorsally (braking) (Table
1). The regulation of body posture and position by the paired fins
of trout provides a clear example of active stability maintenance in fish to
control both external (i.e. turbulence-induced) and self-generated (i.e.
locomotor) perturbations (cf. Weihs,
1993; Webb, 1993
,
2002
).
Hydrodynamics of braking: testing Breder's hypothesis
In an effort to decelerate their bodies, ray-finned fishes (Actinopterygii)
commonly extend the pectoral fins bilaterally to produce a retarding drag
force (Breder, 1926;
Harris, 1938
;
Bainbridge, 1963
;
Videler, 1981
;
Geerlink, 1987
;
Jayne et al., 1996
;
Webb and Fairchild, 2001
). One
influential model proposed in the early part of the twentieth century attempts
to explain the physical mechanism by which such braking is achieved. Breder
(1926
) proposed for elongate
fishes with the pectoral fins low on the body that braking forces are oriented
horizontally without a vertically oriented lift component
(Fig. 9A). Since the center of
pressure of the pectoral fin (taken as the centroid of the fin surface) lies
below the center of mass of the body (CM), the reaction to this braking force
exerts a substantial pitching or `somersaulting' moment which must be opposed
by action of the posterior fins to avoid an uncontrolled maneuver. Although
much-cited since its introduction, the model of Breder has persisted untested
in the literature.
|
We used rainbow trout as a representative plesiomorphic actinopterygian
taxon possessing anteriorly and ventrally positioned pectoral fins to evaluate
the following hypothesis: during paired-fin braking, the line of action of the
braking force lies below the center of mass of the body
(Breder, 1926)
(Fig. 9A). The experimental
measurements required to test this hypothesis are illustrated in
Fig. 9B: using
parasagittal-plane DPIV we compared the angular inclination of the
stroke-averaged reaction force vector to that of the CM. Breder's model was
considered supported if the former is significantly less than the latter.
Although rainbow trout have a more limited ability to extend the pectoral
fins from the body than do many derived fishes (e.g.
Gibb et al., 1994;
Westneat, 1996
;
Drucker and Jensen, 1997
;
Walker and Westneat, 1997
;
Drucker and Lauder, in press
),
this species can nevertheless generate an anteriorly directed component of
force for decelerating the body. During braking, trout rapidly bend the
pectoral fin along its longitudinal axis so that the trailing edge is elevated
and protracted (Fig. 4). A
similar pectoral fin motion has been observed in juvenile salmonid fish during
benthic station-holding (e.g. Kalleberg,
1958
; Keenleyside and
Yamamoto, 1962
; Arnold et al.,
1991
). The function of this fin motion is to direct a central wake
jet (i.e. relatively high-velocity fluid flow between counterrotating
vortices) in an anterodorsal direction (Figs
7D,
10A;
Table 1). The average
orientation of the braking-force line of action, defined by the mean momentum
jet angle, is summarized in Fig.
10B. In trout, the braking reaction force is inclined on average
at an angle of 64° below the horizontal. This angle
is
significantly less than the angle of inclination of the center of mass of the
body (one-sample comparison of
to hypothesized mean ß of
22.3°: d.f.=14; P<0.001), a result supporting the hypothesis
of Breder (1926
).
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The fact that the braking-force line of action in trout lies far below the
horizontal orientation postulated by Breder
(1926)
(Fig. 9A) indicates that
ventrally positioned pectoral fins may have larger than expected moment arms
for exerting torque around the CM. During braking we observed trout to recruit
fins posterior to the CM, presumably to counter the `somersaulting' moment
induced by pectoral fin extension. Specifically, the soft-rayed dorsal fin is
erected and abducted to one side, and the trailing edges of the pelvic fins
are protracted and elevated in a manner similar to that of the pectoral fins
anteriorly (Fig. 4C). In spite
of these simultaneous fin motions to control the braking maneuver, however,
trout exhibit pronounced pitching of the body during deceleration
(Fig. 4A,C,E; ventral rotation
of the longitudinal body axis anterior to the CM, range: 1-13°; pitching
rate: 2-44° s-1).
The potential importance of multiple fin surfaces in controlling braking is
revealed through a comparison of forces derived from wake velocity fields and
from the dynamics of body motion. From analysis of DPIV data, we estimate the
anteriorly directed braking force generated by the left and right pectoral
fins together as 5 mN (i.e. 2 fins x 2.5 mN,
Table 1). Following Newton's
second law, we can calculate the total force required to decelerate the body
using mean kinematic measurements from Oncorhynchus mykiss. During
braking, trout decrease their forward velocity by 3.5 cm s-1, on
average (Fig. 5), over the
duration of the pectoral-fin stroke cycle (the period of abduction +
adduction, mean 430 ms), and therefore experience a mean body deceleration of
8 cm s-2. For trout of the length studied (body mass approximately
160 g; Webb, 1991), such a
deceleration requires a total braking force of 13 mN. We conclude that the
two- to threefold discrepancy between pectoral fin force and total braking
force reflects a significant contribution of the median fins (tail, dorsal and
anal fins) and pelvic fins to body deceleration.
It is noteworthy that Breder
(1926) selected Esox
sp. as a representative long-bodied fish for modeling pectoral fin braking. In
such fishes, the paired fins are protracted beneath the body to generate
anteriorly directed force (fig. 57 A in
Breder, 1926
). Although
Oncorhynchus mykiss is fully capable of such excursions (e.g. during
hovering, Fig. 2A,C), our
experimental population never used them in this way in response to the braking
stimulus offered. Empirical flow visualization work with additional taxa is
required to define better the range of fin kinematics involved in different
hydrodynamic functions.
Evolutionary patterns in pectoral fin mechanics
The paired fins of fishes are characterized by both structural and
functional evolutionary transformations. Within ray-finned fishes, the
pectoral fins exhibit distinct trends of change in their position and
orientation on the body (Breder,
1926; Greenwood et al.,
1966
; Rosen, 1982
;
Parenti and Song, 1996
;
Drucker and Lauder, in press
).
The inclination of the pectoral fin base, for example, is typically horizontal
in plesiomorphic taxa; in its apomorphic condition the fin base is more
vertically oriented. An expected consequence of differences in pectoral-fin
base angle is taxonomic variation in both the range of motion and functional
repertoire of the fin (Drucker and Lauder,
in press
). Recent work on pectoral fin function in a basal
actinopterygian (white sturgeon; Wilga and
Lauder, 1999
) and chondrichthyan outgroups (leopard and bamboo
sharks; Wilga and Lauder,
2000
,
2001
) confirms that a
horizontally oriented fin base restricts fin excursions to a primary
dorsoventral kinematic axis. Despite their phylogenetic distance from
salmoniform fishes, sturgeon and sharks are capable of `cupping' the trailing
edge of the pectoral fin in a manner generally similar to that observed in
trout (Fig. 4) to generate
forces for maneuvering.
Unlike these basal taxa with comparatively rigid paired fins, however,
rainbow trout can rotate the pectoral fin base more than 30° during
locomotion (Fig. 8).
Correspondingly, trout exhibit a greater range of motion of the fin despite
having a relatively shallow fin base inclination. Although not as mobile as
the vertically oriented pectoral fins of many perciform fishes, the
salmoniform pectoral fin does exhibit a diverse range of locomotor activities.
Use of the pectoral fins for hovering, turning and braking constitutes a
behavioral repertoire comparable to that of higher teleostean fishes (cf.
Aleev, 1969;
Geerlink, 1987
;
Drucker and Lauder, 2001b
).
The functional data presented in this study for salmoniform fish,
representative of the plesiomorphic teleost condition, illuminates a trend of
increasing kinematic and functional versatility of the pectoral fins within
Actinopterygii. Future study of additional clades using quantitative flow
visualization techniques will further our understanding of the relationship
between propulsor design and locomotor function in swimming fishes.
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