Response latencies to postural disturbances in three species of teleostean fishes
School of Natural Resources and Environment, University of Michigan, Ann Arbor, MI 48109-1115, USA
(e-mail: pwebb{at}umich.edu)
Accepted 28 December 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: teleost fish, body/fin organization, posture, response latency, stability
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
An important factor affecting the ability to make appropriate corrections
for disturbances is response latency, the interval between the occurrence of a
perturbation and the start of a response to the resulting disturbance. Among
fishes, the ability to successfully power corrections using body and fin
motions depends on the latency being relatively small compared to the
perturbation period. Otherwise a correction may add to a disturbance, with
results graphically described as `pilot induced error'
(Anderson and Eberhardt, 2001;
Webb, 2002
). There are no
measurements of this critical aspect of stability. Therefore, I measured
response latencies to flow-induced disturbances for three species of bony
fishes.
Fishes are extremely diverse. Within this diversity are various body/fin
organization modes and these are believed to affect motor and stabilizing
capabilities (Harris, 1937a,
1953
;
Moy-Thomas and Miles, 1971
;
Rosen, 1982
;
Lauder and Liem, 1983
; Webb,
1998
,
2004
;
Eidietis et al., 2002
;
Drucker and Lauder, 2003
).
Studies on locomotion typically use species representative of modes, such as
various dogfishes typical of less derived selachians (e.g. Harris,
1937b
,
1938
; Wilga and Lauder,
1999
,
2000
,
2001
), salmonids as models for
less derived teleosts (e.g. Bainbridge,
1958
; Brett, 1964
;
Liao et al., 2003
), and
centrarchids indicative of more derived teleosts (e.g.
Gibb et al., 1994
;
Jayne et al., 1996
; Drucker
and Lauder,
2001a
,b
).
In this study, three species were chosen to represent teleost modal forms of
(1) soft-rayed fishes, (2) fusiform spiny-rayed fishes and (3) deep-bodied
spiny-rayed fishes (Rosen,
1982
). The modal body/fin organization of soft-rayed fishes is a
fusiform body with antero-ventral pectoral fins and postero-ventral pelvic
fins, for which the cyprinid, creek chub (Semotilus atromaculatus
Mitchill), was chosen. This body/fin organization facilitates swimming in
bodycaudal fin gaits (Webb,
1994
), and the main propulsors also provide median-fin control
surfaces not only posterior to but also distant from the center of mass. This
promotes unconscious control or self-correcting stability
(Aleyev, 1977
;
Weihs, 2002
;
Webb, 1998
). Then a change in
orientation of a control surface due to a disturbance generates a force that
opposes and corrects the disturbance, as with the feathers of an arrow.
Spiny-rayed fishes have radiated about a fusiform body with antero-lateral
pectoral fins and antero-ventral pelvic fins
(Rosen, 1982;
Lauder and Liem, 1983
). The
centrarchid, smallmouth bass (Micropterus dolomieu
Lacépède), was chosen as in many other studies (e.g.
Gibb et al., 1994
;
Jayne et al., 1996
; Drucker
and Lauder,
2001a
,b
).
The bass body/fin organization extends the swimming range with gaits based on
the median and paired fins (Webb,
1994
), and appears to be associated with greater fin mobility used
to actively generate control forces (Webb,
1998
). Many spiny-rayed fishes have deep bodies, providing for
larger median fins. These further expand capabilities in median and paired fin
gaits (Webb and Gerstner,
2000
; Webb, 2004
),
and also could improve powered control of stability. A common model species
for this mode of body/fin organization is the bluegill (Lepomis
macrochirus Rafinesque) (Gibb et al.,
1994
; Jayne et al.,
1996
; Drucker and Lauder,
2001a
,b
),
which was chosen here. The three species were also chosen because they are
sympatric warm-water fishes. As a result, fishes could be tested at a common
temperature within the normal range for all three species. Finally, the size
ranges of the three species overlap.
Chub were expected to be more reliant on unconscious control and least reliant on active detection and correction of disturbances. As a result, short response latencies may be less critical. Bass were expected to depend more on powered control when a shorter latency in responding to disturbances would be expected. The greatest dependence on powered control by bluegill was expected to result in the shortest latencies. Overall, fishes were expected to respond and correct for all types of flow-induced disturbances, with latencies ranking as: chub>bass>bluegill. In practice, these results were not found and differences among species reflected the nature of habitats typically occupied.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Responses to loss of a flow refuge
Experiments were performed in an enclosed recirculating flume based on the
design described by Vogel and LaBarbera
(1978). Fish swam in an
observation section, 15 cm square and 60 cm long, preceded by a 45 cm upstream
entry section. There was a 10 cm long collimator made with 1.25 cmx1.25
cmx1.25 cm grid at the upstream end of the observation section. The
downstream end of the observation section was delineated with a wire grid that
could be electrified if necessary to encourage fish to swim. The observation
section had bottom and side panels with 5 cm wide black and white stripes to
facilitate station holding.
A single 19 mm wide vertical strut extended from the top to the bottom of the observation section, 20 cm from the upstream collimator. The strut passed through the top of the observation section to a block linked to a weight. Remote removal of a brake caused the weight to rotate the strut from an orientation normal to the flow through 90° to lie parallel to the flow within 10 ms. This exposed a fish to the full speed of the flow, causing a sudden displacement downstream, a surging disturbance.
The sudden change in strut orientation occurred near the head in the visual field of the fish. As a result, a response presumed to be due to the hydrodynamic disturbance might be a response to a visual component of the stimulus triggering an escape behavior. Therefore, observations were made both in the dark (<2 lux red light) to eliminate the visual component of the stimulus and under normal laboratory illumination (45 lux white light).
A single fish was selected at random and placed in the flume. The flume temperature was the same as the acclimation temperature. The fish remained in the flume for at least 12 h at a current speed of approximately 0.5 L s1 (where L = total body length) and with the strut normal to the flow. After this acclimation period, speed was increased at 10 min intervals by increments of approximately 0.50.75 L s1. When a fish entrained on the strut, the strut was rotated parallel to the flow. The fish began to be displaced downstream by the current as soon as the strut began to rotate. Fish responded by starting to swim upstream. Once the fish returned to steady swimming, the strut was reset normal to the flow, and the procedure repeated. The tests were run until the fish was fatigued, which was defined as an inability to swim off the downstream screen.
Fish were videotaped at 250 frames s1 from above via a 45° mirror. Videotape was analyzed frame by frame to record the behavior of each fish. Response latency was defined as the time from the beginning of the rotation of the strut to a change in the use of median and/or paired fins leading to the onset of swimming. These motions were clearly distinct from those during entrainment.
At the end of each experiment, the fish was killed with an overdose of 3-aminobenzoic acid ethyl ester (MS 222). Total body length L and maximum body depth were measured to the nearest 1 mm and body mass to the nearest 0.01 g (Table 1).
|
Responses to water jets
Experiments were performed in a 50 cmx50 cm still-water tank filled
to a depth of 30 cm. The temperature was the same as the acclimation
temperature. Fish were trained to take food from a fixed location, as
described by Alexander (1969).
While taking food, a narrow water jet remotely triggered via a
solenoid valve was directed at different parts of the body from a distance of
1020 mm. The jet caused various types of disturbance: (1) a lateral jet
close to the center of mass caused a slip (lateral translation), (2) a jet
from above at the longitudinal location of the center of mass caused a heave
(a ventrally directed translation), (3) a lateral jet
25% of the body
length anterior to the center of mass primarily caused a yaw (a rotation about
the dorso-ventral axis), (4) a jet from above
25% of the body length
anterior to the center of mass primarily caused a pitch (a rotation about the
lateral axis) and (5) a lateral jet at
30% of the body depth above the
center of mass caused a roll (rotational disturbance about the long axis).
The water jet was gravity-driven from a constant head tank attached via 1.25 cm diameter tubing to a 2.5 cm long, narrow (0.35 cm diameter) aluminum tube. The water in the tubing was tinted with food coloring to be visible on videotape. The maximum force generated by the jet was measured using rigid flat disks of various diameters attached to a force transducer. Maximum force was measured for various driving heads for discs of 10, 15 and 20 mm diameter at distances of 530 mm from the orifice. The minimum height of the constant head tank for which the water jet first caused a fish response was found to be approximately 65 cm, generating a force of approximately 0.05 N. Experiments were performed with supra-threshold water heights generating forces of 0.090.1 N.
Fish responses were recorded on videotape (250 frame s1), and subsequently analyzed frame by frame to observe behavior patterns and response latencies. Response latency was defined as the time from the beginning of a displacement to the first deployment of median and/or paired fins. These clearly differed from normal fin motions of fishes at the feeding station. Each fish was used once for each of the disturbances, and sample sizes are included in Table 1.
At the end of an experiment each fish was killed with an overdose of 3-aminobenzoic acid ethyl ester. Total body length and maximum body depth were measured to the nearest 1 mm and body mass was measured to the nearest 0.01 g (Table 1).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Fishes were immediately displaced downstream when the strut was rotated parallel to the flow. Most fish began swimming to return upstream. Occasionally, a fish showed a startle response, turning downstream and then heading back upstream usually before contacting the grid.
Response latencies for fishes in normal white light and low intensity red light did not differ for the three species studied (two-tailed t-tests, P>0.4). Therefore, these data were combined for each species. Response latencies were independent of the water speed for chub, averaging 129±29 ms (mean ± 2 S.E.M.; N=59). However, latency declined with speed for bass and bluegill (Fig. 1) from approximately 700 ms at entrainment speeds of 10 to 20 cm s1 to approximately 200 ms at speeds between 35 and 50 cm s1. Because of the experimental design, it could not be determined if the decrease in latency with speed involves an adaptive response to the increasing rate of disturbance at higher speeds and/or learning. The mean response latency for chub was significantly smaller than the minimum values for bluegill (N=25) and bass (N=26) [repeated-measures analysis of variance (ANOVA) followed by Tukey's multiple comparison tests, P<0.01], but values for bass and bluegill were similar (P>0.9). The average speed at which a response was initiated for chub and the minimum values for bluegill and bass were independent of species (ANOVA, P>0.06) averaging 5.7±1.8 cm s1.
|
Responses to water jets
The force generated by the water jet increased with the driving
gravitational head (Fig. 2).
The jet was coherent enough that force was essentially unaffected by either
the disc diameter or the distance from the orifice to the body for the range
of distances used in the experiments (ANOVA, P>0.9).
|
All fish were displaced by the water jet. At the beginning of a response to a translational disturbance, the average displacement speed was similar for slips and heaves, and independent of species (ANOVA, P>0.14), averaging 7.6±3.0 cm s1. Rotation rates at the start of a response were also independent of species (P>0.11), averaging 21±9 deg. s1 for yaw and pitch, consistently higher, but not significantly so (P>0.1) than that of 16±7 deg s1 for rolls.
Response patterns to disturbances were similar for all three species. Fish first responded to both translational and rotational disturbances by extending the median and caudal fins and usually the paired fins. Fishes usually made no further substantial motor responses to translational disturbances. Thus after the initial fin extension, fishes essentially ignored translational disturbances. Similarly, fish sometimes ignored yawing and pitching disturbances. Usually they swam away from the feeding site, correcting posture as they did so with various median (including caudal), and paired fin motions. Rolling disturbances were never ignored. Fish from all three species actively corrected rolls. Some fish corrected the roll while swimming away from the stimulus area, but most used asymmetrical beats of median and paired fins to return the body to an upright posture.
There were no differences in response latencies for translational, pitching and yawing disturbances (ANOVA, P>0.05) for each species (Fig. 3). Therefore, these data were combined. The resultant response latencies varied, 123±19 ms for chub being significantly smaller than those of 201±24 ms for bass and 208±52 ms for bluegill (ANOVA followed by Tukey's multiple comparison tests, P<0.05). Values for the two centrarchids were not significantly different (P>0.08).
|
The response latency for rolling disturbances for each of the three species studied was significantly smaller than that for other disturbances (P<0.05), but there were no significant differences among species (P<0.04). The overall average response latency was 70±15 ms.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The initial response to all the jet-induced disturbances was extension of the median (including the caudal) fins and the paired fins. Such fin extension would increase resistance to translational and rotational motions, and hence damp further growth of a disturbance. In contrast, fin extension in the flume would increase drag, increasing the rate at which a fish was accelerated to the current speed, and hence increasing the rate of displacement downstream. Therefore, fin extension in the flume would amplify the downstream surging disturbance. Fin extension, however, did not occur following strut rotation in the flume. Thus fishes responded in appropriate ways to minimize amplification of the disturbance in the two dynamically different treatments of current in the flume and in still water.
Corrections to the jet-induced disturbances after the initial fin extension varied with the nature of the disturbance. Translational disturbances were usually not corrected. Rotational yaw and pitch disturbances were occasionally corrected. Rolls were always corrected. Rolls were also distinct in that response latencies were smaller, averaging 70 ms, compared to latencies of the order of 130200 ms for other disturbances.
These response patterns suggest that the various types of disturbances
differ in their importance. The long latency and absence of a motor correction
to slip and heave disturbances suggests these do not pose functional problems
for fishes. Yawing and pitching disturbances, while having the same latency as
translational disturbances, were sometimes corrected, and hence presumably
present some challenge. Surges and rolls were always corrected and hence
presumably present important challenges to a fish. In the flume, failure to
correct a surge would result in a fish becoming impinged on the downstream
grid. A similar correction should be expected in natural habitats because
failure to correct a current-induced surge would result in a fish being
displaced from preferred habitats, typically those with favorable flow and/or
food supply (Fausch, 1984;
Allan, 1995
).
The importance of rolling stability probably relates to functions
associated with the normal upright posture
(Eidietis et al., 2002;
Webb, 2002
). Fishes are
hydrostatically unstable in roll (or a best neutrally stable) because the
center of mass is typically above the center of buoyancy
(Aleyev, 1977
;
Webb and Weihs, 1994
;
Webb, 2002
). Therefore fishes
must work continuously to control posture
(Alexander, 1990
;
Eidietis et al., 2002
;
Webb, 2002
) and control
systems to detect and correct rolling disturbances are essential. In contrast,
fish are essentially hydrostatically stable in all planes and pitch and
yaw.
Control of posture is also important for camouflage
(Cott, 1940;
Muntz, 1990
). Fish are
typically light when viewed from below and dark from above, so that rolling
would make fish more visible. Translations and yawing rotations would not
affect the orientation of cryptic coloration. Fishes naturally pitch (tilt)
when swimming at low speeds (He and
Wardle, 1986
; Webb,
1993
; Wilga and Lauder,
1999
,
2000
,
2001
), which has the potential
to affect camouflage. Pitch angles may be as large as 1015°, but
these are presumably insufficient to substantially affect camouflage.
Eidietis et al. (2002) also
suggested that rolling could have negative impacts on sensory systems. Vision,
in particular, may be affected. The underwater light environment is complex,
with light intensity and wavelength differing along all lines of sight (Muntz,
1973
,
1990
;
Lanchester and Mark, 1975
;
Lythgoe, 1979
;
Land, 1999
). The distribution
of rods and cones sensitive to different wavelengths often varies over the
retina. This is associated with differences in light characteristics falling
on different retinal areas when the body is upright. Translational and yawing
disturbances would not affect general patterns of incident light. Pitching
could cause light from various environmental origins to fall on different
parts of the retina, but given the occurrence of tilting in normal behavior,
this is presumably small at normal pitch angles. In contrast, rolling would
quickly alter light patterns within the eye. Degradation of sensory signals as
a result of rolling might also be anticipated for other distance senses, such
as the lateralis system.
Response latencies also proved variable among disturbance types and among
species. In general, response latencies were large compared with those of
about 12 ms for the initiation of fast starts following artificial stimulation
(Eaton and Hackett, 1984;
Casagrand et al., 1999
;
Eaton et al., 2001
;
Webb and Zhang, 1994
). This
behavior, however, is initiated as a reflex response to potentially
life-threatening situations (Eaton et al.,
2001
). Other behaviors require more complex assessment of both
stimuli and an appropriate response. For example, response latencies of
predators responding to prey maneuvers are about 100 ms
(Webb, 1984
). Postural
response latencies are of the same order as these, although rolling response
latencies were substantially shorter and others were longer
(Fig. 3).
The small response latencies for rolling disturbances, the convergence of these latencies among the three species tested, and the immediate correction of rolling disturbances all support the idea that rolling disturbances present special challenges for fishes, necessitating prompt correction.
In addition to the expectation that fishes would respond to all
disturbances, it was anticipated that latencies would vary among species. The
body/fin organization of less derived soft-rayed fishes and behavior is wakes
suggest these fish are more reliant on self-correction
(Breder, 1926; Harris,
1937a
,
1953
;
Aleyev, 1977
;
Webb, 2004
;
Liao et al., 2003
). As a
result, response latency might be diminished in importance. In contrast, the
median and paired fins play a larger role in swimming of more derived fishes,
which also seem to make greater use of powered control, actively generating
forces to correct a disturbance (Webb,
1998
). In practice, fishes are usually in dynamic equilibrium,
with corrective forces balanced among many control surfaces in orthogonal
planes distributed around the center of mass
(Lauder and Drucker, 2003
;
Webb, 2003
,
2004
). As such, short
latencies would promote stability for all three species. However, similar
response latencies were found only for rolling disturbances, which, it is
argued above, present the greatest challenges to overall functionality for all
species.
Latencies for other disturbances tended to be shorter for chub, rather than
longer as anticipated. Given that fishes appear to be in dynamic equilibrium,
if seems more likely that habitat features underlie response differences among
species (Webb, 2004). Thus
creek chub, as the name indicates, are stream fishes and, like other
soft-rayed species, are common in more turbulent riffles and races
(Schlosser, 1982
; P. W. Webb
and A. G. Fairchild, manuscript submitted for publication). Salmonids, also
are soft-rayed species, well known for occupying turbulent streams. In lakes,
cyprinids are abundant in shallow littoral zones, even during storm conditions
(P. W. Webb, unpublished observations). Bluegill and ecomorphologically
similar species are more common in lakes and ponds
(Scott and Crossman, 1973
)
where flow is greatly reduced. In these habitats, percomorphs tend to move
offshore and avoid storm-induced turbulent situations
(Helfman, 1986
). Bass are
found in both lotic and lentic habitats, but in slow moving water in streams
(Probst et al., 1984
).
Thus fishes appear to respond to disturbances in two general ways. First,
they may correct the disturbances, and when fishes are in dynamic equilibrium,
active modulation of trimming forces and creation of powered forces will be
essential. Nevertheless, the large response latencies suggest that such
control may be limited to low frequency perturbations. Recent studies of fish
interacting with Kármán wakes downstream of a D-shaped strut
have shown that fish not only respond to but also exploit low frequency
disturbances (4 Hz; Liao et al.,
2003
). In contrast, long response latencies may require reliance
on self-correction for many naturally occurring disturbances. Body shape can
provide self-correction (Bartol,
2002
,
2003
). Fin deployment,
especially of fins posterior to the center of mass, also provide some measure
of self-correction (Breder,
1926
; Alexander,
1967
; Gosline,
1971
; Aleyev, 1977
;
Weihs, 1989
,
1993
;
Webb, 2004
). Self-correction
may be most important at high speeds when control surface anterior to the
center of mass may be furled (Webb,
2004
).
Second, fish may avoid unsteady flows. Turbulence generators exploit this
in fish barriers (Fletcher,
1990,
1992
;
Cada, 2001
). In streams, low
current speeds are expected to be associated with lower turbulence intensities
and low currents are often selected by fishes
(Fausch, 1984
; P. W. Webb and
A. G. Fairchild, manuscript submitted for publication). During migration,
salmonids seek low speeds where flow is likely to be more steady
(Hinch and Rand, 1998
;
Hinch et al., 2002
). Many reef
fishes shelter or vacate the immediate reef vicinity on flood tides, and tend
to be active towards ebb tides (Potts,
1970
; Hobson,
1974
). Finally, fishes with lower stabilizing abilities chose
hydrodynamically quieter habitats.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Alexander, R. McN. (1990). Size, speed and buoyancy adaptations in aquatic animals. Amer. Zool. 30,189 -196.
Alexander, R. McN. (1967). Functional Design in Fishes. London: Hutchinson.
Alexander, R. McN. (1969). Mechanics of the feeling action of a cyprinid fish. J. Zool. Lond. 159, 1-13.
Aleyev, Y. G. (1977). Nekton. The Hague: Junk.
Allan, D. A. (1995). Stream Ecology. London: Chapman and Hall.
Anderson, D. F. and Eberhardt, S. (2001). Understanding Flight. New York: McGraw-Hill.
Bainbridge, R. (1958). The speed of swimming of fish as related to size and to the frequency and the amplitude of the tail beat. J. Exp. Biol. 35,109 -133.
Bartol, I. K., Gharib, M., Weihs, D., Webb, P. W., Hove, J. R.
and Gordon, M. S. (2003). Hydrodynamic stability of
swimming in ostraciid fishes: role of the carapace in the smooth trunkfish
Lactophrys triqueter (Teleostei: Ostraciidae). J. Exp.
Biol. 206,725
-744.
Bartol, I. K., Gordon, M. S., Gharib, M., Hove, J. R., Webb, P. W. and Weihs, D. (2002). Flow patterns around the carapaces of rigid-bodied, multi-propulsor boxfishes (Teleostei: Ostraciidae). Integ. Comp. Biol. 42,971 980
Bellwood, D. R. and Wainwright, P. C. (2001). Locomotion in labrid fishes: implications for habitat use and cross-shelf biogeography on the Great Barrier Reef. Coral Reefs 20,139 -150.[CrossRef]
Breder, C. M. (1926). The locomotion of fishes. Zool. 4,159 -297.
Brett, J. R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. J. Fish. Res. Bd. Can. 21,1183 -1226.
Cada, G. F. (2001). The design of advanced hydroelectric turbines to improve fish passage survival. Fisheries 26,14 -23.
Casagrand, J. L., Guzik, A. L. and Eaton, R. C.
(1999). Mauthner cell and reticulospinal neuron responses to
onset of acoustic pressure and acceleration stimuli. J.
Neurophysiol. 82,1422
-1437.
Cott, H. B. (1940). Adaptive Coloration in Animals. London: Methuen.
Denny, M. (1988). Biology and the Mechanics of the Wave-Swept Environment. Princeton, NJ: Princeton University Press.
Drucker, E. G. and Lauder, G. V. (2001a).
Locomotor function of the dorsal fin in teleost fishes: experimental analysis
of wake forces in sunfish. J. Exp. Biol.
204,2943
-2958.
Drucker, E. G. and Lauder, G. V. (2001b). Wake
dynamics and fluid forces of turning maneuvers in sunfish. J. Exp.
Biol. 204,431
-442.
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.
Eaton, R. C. and Hackett, J. T. (1984). The role of the Mauthner cell in fast-starts involving escape in teleost fishes. In Neural Mechanisms of Startle Behavior (ed. R. C. Eaton), pp. 213-266. New York: Plenum Press.
Eaton, R. C., Lee, R. K. K. and Foreman, M. B. (2001). The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog. Neurobiol. 63,467 -485.[CrossRef][Medline]
Eidietis, L., Forrester, T. L. and Webb, P. W. (2002). Relative abilities to correct rolling disturbances of three morphologically different fish. Can. J. Zool. 80,2156 -2163.[CrossRef]
Fausch, K. D. (1984). Profitable stream positions for salmonids: Relating specific growth rate to net energy gain. Can. J. Zool. 62,441 -451.
Fletcher, R. I. (1990). Flow dynamics and fish recovery experiments: Water intake systems. Trans. Amer. Fish. Soc. 119,393 -415.
Fletcher, R. I. (1992). The failure and rehabilitation of a fish-conserving device. Trans. Amer. Fish. Soc. 121,678 -679.
Fulton, C. J. and Bellwood, D. R. (2002). Ontogenetic habitat use in labrid fishes: an ecomorphological perspective. Mar. Biol. Prog. Ser. 236,255 -262.
Fulton, C. J., Bellwood, D. R. and Wainwright, P. C. (2001). The relationship between swimming ability and habitat use in wrasses (Labridae). Mar. Biology 139, 25-33.[CrossRef]
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.
Gosline, W. A. (1971). Functional Morphology and Classification of Teleostean Fishes. Honolulu, HI: University Press of Hawaii.
Harris, J. E. (1937a). The role of fin movements in the equilibrium of fish. Annu. Rep. Tortugas Lab., Carnegie Inst. 1936-37,91 -93.
Harris, J. E. (1937b). The mechanical significance of the position and movements of the paired fins in the teleostei. Papers Tortugas Lab., Carnegie Inst. 31,173 -189.
Harris, J. E. (1938). The role of the fins in the equilibrium of swimming fish II. The role of the pelvic fins. J. Exp. Biol. 15,32 -47.
Harris, J. E. (1953). Fin patterns and mode of life in fishes. In Essays in Marine Biology (ed. S. M. Marshall and P. Orr), pp. 17-28. Edinburgh: Oliver and Boyd.
He, P. and Wardle, C. S. (1986). Tilting behavior of the Atlantic mackerel, Scomer scombrus, at low swimming speeds. J. Fish. Biol. 29 Suppl. A, 223-232.
Helfman, G. S. (1986). Fish behavior by day, night, and twilight. In The Behavior of Teleost Fishes (ed. T. J. Pitcher), pp. 479-512. London, Chapman and Hall.
Hinch, S. G. and Rand, P. S. (1998). Swim speeds and energy use of upriver-migrating sockeye salmon (Oncorhynchus nerka): role of local environment and fish characteristics. Can. J. Fish. Aquat. Sci. 55,1821 -1831.
Hinch, S. G., Standen, E. M., Healey, M. C. and Farrell, A. P. (2002). Swimming patterns and behaviour of upriver migrating adult pink salmon (Oncorhynchus gorbuscha) and sockeye (O. nerka) salmon as assessed by EMG telemetry in the Fraser River, British Columbia. Hydrobiologia 483,147 -160.
Hobson, E. S. (1974). Feeding relationships of teleostean fishes on coral reefs in Kona, Hawaii. Fish. Bull. US 72,915 -1031.
Jayne, B. C., Lozada, A. and Lauder, G. V. (1996). Function of the dorsal fin in bluegill sunfish: motor patterns during four locomotor behaviors. J. Morphol. 228,307 -326.
Lanchester, B. S. and Mark, R. F. (1975). Pursuit and prediction in the tracking of moving food by a teleost fish (Acanthaluteres spilomelanurus). J. Exp. Biol. 63,627 -645.
Land, M. F. (1999). Motion and vision: why animals move their eyes. J. Comp. Physiol. A 185,341 -352.
Lauder, G. V. and Drucker, E. G. (2003). Morphology and experimental hydrodynamics of piscine control surfaces. In Biology-inspired Maneuvering Hydrodynamics for AUV Application (ed. F. E. Fish), pp.C1 -C26. Proc. 13th Int. Symp. Unmanned Untethered Submersible Technology. Durham, New Hampshire: Autonomous Undersea Systems Institute.
Lauder, G. V. and Liem, K. F. (1983). The evolution and interrelationships of the actinopterygian fishes. Bull. Mus. Comp. Zool. Harvard Univ. 150,95 -197.
Liao, J., Beal, D. N., Lauder, G. V. and Trianyafyllou, M. S. (2003). The Kármán gait: novel body kinematics of rainbow trout swimming in a vortex street. J. Exp. Biol. 206,1059 -1073.
Lythgoe, J. N. (1979). The Ecology of Vision. Oxford, UK: Clarendon Press.
Moy-Thomas, J. A. and Miles, R. S. (1971). Palaeozoic Fishes. Philadelphia, PA: Saunders Company.
Muntz, W. R. A. (1973). Yellow filters and the absorption of light by the visual pigments of some Amazonian fishes. Vision Res. 13,2235 -2254.
Muntz, W. R. A. (1990). Stimulus, environment and vision in fishes. In The Visual System of Fish (ed. R. H. Douglas and M. B. A. Djamgoz), pp.491 -511. London: Chapman and Hall.
Pavlov, D. S. and Tyurukov, S. N. (1988). The role of hydrodynamic stimuli in the behavior and orientation of fishes near obstacles. Voprosy Ikhtiologii 28,303 -314.
Pavlov, D. S., Lupandin, A. I. and Skorobogatov, M. A. (2000). The effects of flow turbulence on the behavior and distribution of fish. J. Ichthyol. 40,S232 -S261.
Pavlov, D. S., Skorobagatov, M. A. and Shtaf, L. G. (1982). The critical current velocity of fish and the degree of flow turbulence. Rep. USSR Acad. Sci. 267,1019 -1021.
Pavlov, D. S., Skorobagatov, M. A. and Shtaf, L. G. (1983). Threshold speeds for rheoreaction of roach in flows with different degrees of turbulence. Rep. USSR Acad. Sci. 268,510 -512.
Potts, J. A. (1970). The schooling ethology of Lutianus monostigma (Pisces) in the shallow reef environment of Aldabra. J. Zool. Lond. 161,223 -235.
Probst, W. E., Rabeni, C. F. Covington, W. G. and Marteney, R. E. (1984). Resource use by stream-dwelling rock bass and smallmouth bass. Trans. Amer. Fish. Soc. 113,283 -294.
Rosen, D. E. (1982). Teleostean interrelationships, morphological function and evolutionary inference. Amer. Zool. 22,261 -273.
Schlosser, I. J. (1982). Fish community structure and function along two habitat gradients in a headwater stream. Ecol. Monogr. 52,395 -414.
Scott, W. B. and Crossman, E. J. (1973). Freshwater fishes of Canada. Bull. Fish. Res. Bd. Canada 184,1 -966.
Shtaf, L. G., Pavlov, D. S. Skorobogativ, M. A. and Baryekian, A. S. (1983). Fish behavior as affected by the degree of flow turbulence. Voprosy Ikhtiologii 3, 307-317.
Vogel, S. (1994). Life in Moving Fluids. Princeton, NJ: Princeton University Press.
Vogel, S. and LaBarbera, M. (1978). Simple flow tanks for research and teaching. BioSci. 26,638 -643.
Webb, P. W. (1984). Chase response latencies of some teleostean piscivores. Comp. Biochem. Physiol. 79A, 45-48.
Webb, P. W. (1993). Is tilting at low swimming speeds unique to negatively buoyant fish? Observations on steelhead trout, Oncorhynchus mykiss, and bluegill, Lepomis macrochirus. J. Fish. Biol. 43,687 -694.
Webb, P. W. (1994). The biology of fish swimming. In Mechanics and Physiology of Animal Swimming (ed. L. Maddock, Q. Bone and J. M. V. Rayner), pp.45 -62. Cambridge, UK: Cambridge University Press.
Webb, P. W. (1998). Entrainment by river chub, Nocomis micropogon, and smallmouth bass, Micropterus dolomieu, on cylinders. J. Exp. Biol. 201,2403 -2412.
Webb, P. W. (2002). Control of posture, depth, and swimming trajectories of fishes. Integ. Comp. Biol. 42,94 -101.
Webb, P. W. (2003). Maneuverability definitions and general issues. In Biology-inspired Maneuvering Hydrodynamics for AUV Application (ed. F. E. Fish), pp.B1 -B9. Proc. 13th Int. Symp. Unmanned Untethered Submersible Technology. Durham, New Hampshire: Autonomous Undersea Systems Institute.
Webb, P. W. (2004). Stability and maneuverability. In Fish Physiology (ed. R. E. Shadwick and G. V. Lauder). San Diego, Elsevier Science. In press.
Webb, P. W. and Gerstner, C. L. (2000). Swimming behaviour: predictions from biomechanical principles. In Biomechanics in Animal Behaviour (ed. P. Domenici and R. W. Blake), pp. 59-77. Oxford, UK: Bios Scientific Publishers Ltd.
Webb, P. W. and Weihs, D. (1994). Hydrostatic stability of fish with swimbladders: Not all fish are unstable. Can. J. Zool. 72,1149 -1154.
Webb, P. W. and Zhang, H. (1994). The relationship between responsiveness and elusiveness of heat-shocked goldfish (Carassius auratus) to attacks by rainbow trout (Oncorhynchus mykiss). Can. J. Zool. 72,423 -426.
Weihs, D. (1989). Design features and mechanics of axial locomotion in fish. Amer. Zool. 29,151 -160.
Weihs, D. (1993). Stability of aquatic animal locomotion. Contemp. Math. 141,443 -461.
Weihs, D. (2002). Stability versus maneuverability in aquatic animals. Integ. Comp. Biol. 42,127 -134.
Wilga, C. D. and Lauder, G. V. (1999). Locomotion in the sturgeon: Function of the pectoral fins. J. Exp. Biol. 202,2413 -2432.
Wilga, C. D. and Lauder, G. V. (2000). Three-dimensional kinematics and wake structure of the pectoral fins during locomotion in Leopard sharks, Triakis semifasciata. J. Exp. Biol. 203,2261 -2278.
Wilga, C. D. and Lauder, G. V. (2001). Functional morphology of the pectoral fins in bamboo sharks, Chiloscyllium plagiosum: benthic vs. pelagic station-holding. J. Exp. Biol. 249,195 -209.