Escape manoeuvres in the spiny dogfish (Squalus acanthias)
1 CNR-IAMC, c/o International Marine Centre, Loc. Sa Mardini, 09072
Torregrande, Oristano, Italy
2 Department of Forestry, University of British Columbia, Vancouver, British
Columbia, Canada
3 Organismic and Evolutionary Biology Program and Biology Department,
University of Massachusetts, 611 North Pleasant Street, Amherst, MA
01003-9297, USA
* Author for correspondence (e-mail: p.domenici{at}imc-it.org)
Accepted 7 April 2004
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Summary |
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Key words: dogfish, elasmobranch, escape response, locomotion, Squalus acanthias, kinematics, swimming, manoeuvrability
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Introduction |
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Escape responses in fish are usually mediated by the Mauthner neurons,
although alternative pathways may exist
(Eaton et al., 1984). Escape
responses are usually divided into two main stages based on kinematics (stage
1 and stage 2), which correspond to consecutive body contractions, beyond
which the locomotor behaviour is highly variable
(Weihs, 1973
; Webb,
1976
,
1978a
). Typically, during
stage 1, fish bend into a `C' shape (hence the term C-start) due to a
unilateral contraction of the body musculature (although bilateral muscular
activity in stage 1 was recently found in Polypterus senegalus;
Tytell and Lauder, 2002
),
while stage 2 corresponds to the return flip of the tail
(Weihs, 1973
;
Domenici and Blake, 1997
).
Jayne and Lauder (1993
) show
that the onsets of muscular activity are synchronous on one side during stage
1, whereas the contralateral muscular activity (i.e. during stage 2) are
propagated posteriorly. Recent work by Hale
(2002
) has shown that escape
responses (in the muskellunge, Esox masquinongy) may also involve
simultaneous muscle activity anteriorly on one side of the body and
posteriorly on the opposite side (S-starts). Earlier work has shown that, in
some species (e.g. angelfish, Pterophyllum eimikei, knifefish,
Xenomystus nigri), stage 2 may be a coasting phase
(Domenici and Blake, 1991
;
Kasapi et al., 1993
) and stage
2 electromyogram (EMG) activity may be absent in some cases
(Tytell and Lauder, 2002
).
Past work on schooling fish (herring, Clupea harengus) has shown that
escape responses may show short (
20 ms) and long (
100 ms) latencies
in reaction to a stimulus, associated with fast and slow head turning rates,
respectively (Domenici and Batty,
1994
). In herring, proximity to neighbours in the school may
induce long latency responses, although long latencies were also sometimes
observed in solitary individuals (Domenici and Batty,
1994
,
1997
). It is not known if
other species of fish, including dogfish, present a similar dichotomy of
responses to that observed in herring.
While previous work has investigated a variety of fish species of various
forms and sizes, little is known about the fast-start behaviour of
chondrichthyans in general (Hale et al.,
2002). Nevertheless, various species of elasmobranchs, including
embryos of spiny dogfish, possess Mauthner cells
(Bone, 1977
;
Zottoli, 1978
;
Stefanelli, 1980
). Based on
functional morphology, the spiny dogfish would be expected to show relatively
low acceleration performance, as high acceleration is dependent on a large
body depth placed posteriorly (Webb,
1984a
). On the other hand, given their relatively high flexibility
(Aleev, 1977
), spiny dogfish
can be expected to perform well in terms of manoeuvrability, i.e. to show a
tight turning radius and high turning rate when compared with other fish.
As far as we are aware, the present study is the first kinematic investigation of escape responses in chondrichthyans. The aims of this study were twofold: to investigate the pattern of variation in turning rates in dogfish and to compare the kinematics and the performance of the spiny dogfish with those of previously studied teleosts.
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Materials and methods |
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The position of the centre of mass of the fish when stretched straight (CM) was determined on one euthanized 60 cmspecimen, previously frozen in order to be stiffened and balanced. A long pin was placed transversely through the body of the fish at the position at which the fish was balanced in the horizontal plane. This position was measured and calculated to be 33% of the total length.
High-speed videography
Single fish were transferred to a 4 m-diameter experimental outdoor tank
(height 1.1 m) filled with water to a depth of 60 cm, of the same shape and
size as, and adjacent to, the holding tank. Transferral time was therefore
minimized and the dogfish did not appear to be stressed by showing high-speed
response nor an increase in ventilation after transferral but rather swam at
low speed as in the holding tank. Water temperature in the filming tank
matched that of the holding tanks (i.e. 12±1°C). Square reference
panels (5 cm squares) were laid on the bottom of the tank, approximately at
the centre of the tank. Escape responses were elicited by manually thrusting a
2 m-long pole (diameter 3 cm) towards the body of the dogfish, from outside
the tank. This proved to be the most effective means of eliciting an escape
response in the dogfish, and a similar method has been used in escape response
studies of other fish (Harper and Blake,
1990). In no instance did the pole actually touch the dogfish.
Prior to being stimulated, the dogfish were cruising undisturbed at low speed.
To avoid any wall effects (Eaton and
Emberley, 1991
), fish were only startled when they were at least
two body lengths from the nearest wall. Fish were allowed to acclimate for at
least 30 min prior to being startled. Three responses for each of the five
individuals were filmed, using a minimum interval of 30 min between trials.
Filming rate was 500 frames s-1, using a Redlake Motionscope
PCI-8000S digital high-speed camera positioned 2 m above the filming tank. All
escape responses obtained were analyzed. Video sequences were exported as AVI
files and compressed using Cinepak Codec compression software. Sequences were
calibrated from the filming reference grid and analyzed using WINanalyze
automated tracking program. The X, Y coordinates of the CM of the
fish when stretched straight (Webb,
1976
; the point on the midline, at 0.33 L from the tip of
the head) and tip of the rostrum were digitized for each escape sequence. The
CM of the shark was located on the video by measuring the length of the
midline from the tip of the rostrum to 0.33 of body length.
The characteristics of the stimulus were measured in 2-D, i.e. in the
horizontal plane, the main plane of stimulus motion. Stimulus speed was
calculated based on the distance covered by the stimulus tip during the 25 ms
preceding the escape response onset. Stimulus distance was calculated as the
shortest distance between the stimulus and the body of the fish at the onset
of the response. Stimulus angle was calculated as the angle between the tip of
the head of the fish, the tip of the stimulus and the centre of mass of the
fish (Domenici and Blake,
1993). Therefore, a frontal stimulus, in line with the head, would
correspond to 0°, while a posterior stimulus would correspond to 180°.
Stimulus position at the time of response was calculated based on the position
of the tip of the stimulus relative to the fish's body. If the point on the
body that was closest to the stimulus was half-way along the body, a 0.5
L (body length) was assigned. Stimuli near the head approached 0
L, while tail stimuli approached 1 L. In addition, the
swimming phase of the fish was defined as in Blaxter and Batty
(1987
) and Domenici and Batty
(1994
), i.e. whether the tip
of the tail was oriented away or towards the stimulus in the frame before
response onset. Tail tip orientation was scored as +1 (tail tip oriented away
from the stimulus) and -1 (tail tip oriented towards the stimulus).
Data analysis
Durations
Stage 1 (S1) duration was defined as the time between the first detectable
reaction of the fish and the change in direction of turning by the anterior
part of the body (snout to the centre of mass), following Kasapi et al.
(1993) and Domenici and Blake
(1997
). Stage 2 (S2) duration
was defined as the time between the end of stage 1 and the subsequent change
in direction of the anterior part of the body following Kasapi et al.
(1993
) and Domenici and Blake
(1997
). Total duration was
defined as the sum of stage 1 and stage 2 durations. In addition, stage 1
duration was also measured in four fish while making spontaneous turns
(`routine turns') without being startled.
Angles
Stage 1 angle was determined by the rotation of a line passing through the
centre of mass and the snout between the beginning of the response and the end
of stage 1. Stage 2 angle was determined by the rotation of a line passing
through the centre of mass and the snout between the end of stage 1 and the
end of stage 2. Since stage 2 rotation is in a direction opposite to that of
stage 1, stage 2 angle bears a negative sign. In addition, stage 1 angle was
also measured in four fish while making spontaneous turns (`routine turns')
without being startled.
Head turning rate
Head turning rate was defined as the angular velocity of the line linking
the tip of the snout and the centre of mass
(Domenici and Blake, 1997).
Head turning rate was derived from the raw angle data with a five-point
smoothing regression (Lanczos,
1956
). Mean stage 1 head turning rate (corresponding to the ratio
of stage 1 angle/stage 1 duration) and maximum stage 1 and stage 2 head
turning rates were measured.
CM turning rate
The rate of turning, during stage 1, of the centre of mass of the fish when
stretched straight (CM) was calculated by measuring the arc of the turn of the
CM divided by stage 1 duration.
Turning radius
Turning radius was measured as the radius of the path of the centre of mass
throughout stage 1, following Domenici and Blake
(1991). Turning radius was
measured in lengths (L), since previous authors have shown that
turning radius is a constant proportion of fish length
(Webb, 1976
).
Distance-time variables
Distance-time variables were measured based on the displacement of the CM.
Cumulative distance, speed and acceleration were derived from the
distance-time data by using a five-point smoothing regression
(Lanczos, 1956). Distance-time
variables were measured using two procedures: throughout the duration of the
response (dR, cumulative distance; UR,
maximum speed; AR, maximum acceleration, where subscript R
stands for response) or within a fixed time (i.e. 288 ms, the mean of the
pooled fast-start duration of both slow and fast responses;
dT, cumulative distance; UT, maximum
speed; AT, maximum acceleration, where subscript T stands
for time). This latter procedure was adopted following previous authors
(Webb, 1976
;
Domenici and Blake, 1991
) to
avoid any performance bias due to differences in fast-start duration. In
addition, the speed immediately prior to the fish's first detectable reaction
was measured for all the escape responses.
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Results |
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t-tests were used in all comparisons, except when the variances of the two samples were significantly different (F-test), in which case a Mann-Whitney test was used. N for all tests was 8 (slow responses) or 7 (fast responses), except where noted due to the absence of stage 2 in one response (see below). The mean speed prior to the response was 0.29±0.02 and 0.26±0.04 m s-1 (mean ± S.E.M.) in slow and fast responses, respectively (no statistical difference; t-test, P>0.1; N=8 and N=7, respectively). Stimulus characteristics and swim phase at the time of response onset did not differ between escape type (Table 2).
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Stage 1 duration did not differ between response types (Table 1). Stage 2 was present in all but one response (a fast response), which was therefore considered to last until the end of stage 1. In this case, this response was removed from the analysis of stage 2 variables, i.e. stage 2 duration, stage 2 angle, maximum stage 2 head turning rate (Table 1). Total duration did not differ between response types while stage 2 duration did (Table 1). The stage 1 angles (positive values) of the two response types showed no statistically significant differences while stage 2 angles (negative values) did (Table 1).
Maximum stage 2 head turning rates were statistically different (-236±52 and -99±21 deg. s-1 in fast and slow responses, respectively; Table 1). A frequency distribution plot (Fig. 4B) shows that maximum stage 2 head turning rates overlap considerably. CM turning rates were significantly different (P<0.001; Table 1). Mean turning radii were 0.074±0.007 L (body length) and 0.060±0.006 L in slow and fast responses, respectively. These values did not differ significantly (Table 1) and the mean value for the pooled responses was 0.067±0.005 L (N=15). The minimum turning radius measured was 0.041 L.
The relationship between mean S1 head turning rate and CM turning rate was not significant within either fast or slow responses (P>0.1 in both cases; Fig. 5A). CM and mean S1 head turning rates were significantly related to stage 1 duration only for slow responses (mean S1 head turning rate Y=-0.36+342X, r2=0.64, P<0.05, N=8; CM turning rate Y=1.63+1044X, r2=0.61, P<0.05, N=8; Fig. 5B). UT was not significantly related to mean S1 head turning rate and CM turning rate of slow and fast responses (P>0.01 in all cases; Fig. 5C).
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All distance-time variables were significantly higher in fast than in slow responses (Table 3), whether measured within fast-start duration (dR, UR, AR) or within a fixed time (i.e. 288 ms, the pooled fast-start duration of both slow and fast responses; dT, UT, AT). Fig. 6 shows examples of speed and head S1 turning rate profiles of a fast and a slow response. Nevertheless, despite being significantly different, distance-time variables did not form the bimodal distribution found with S1 head turning rates, and the data for fast and slow responses showed a slight overlap in the distribution (Fig. 7).
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Fast and slow responses were shown by all individuals tested. Since each fish was tested three times in succession with at least a 30 min interval between trials, the possibility that trial number had an effect on the type of fast start was tested by assigning a score to each fast-start of the series, i.e. 1 to the first escape response triggered, and 2 and 3 to the second and third escape responses, respectively. The results show that no effect of trial number on response type was present (Mann-Whitney test, P>0.5).
In order to account for individual variation, paired t-tests were carried out using one type of response (fast and slow), randomly chosen for each individual. The results are in line with those presented above. Significant differences were found for stage 1 head turning rates (mean, P<0.0001; maximum, P<0.0001), CM turning rates (P<0.05) and for all the distance-time variables within a fixed time (dT, P<0.05; UT, P<0.05; AT, P<0.005). Performance to the end of the fast start was different in terms of UR (P<0.01) and AR (P<0.05). Similarly, paired t-tests did not detect any significant differences between stimulus characteristics, swim phase or fish speed before stimulation.
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Discussion |
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Similar to our results, Domenici and Batty
(1994,
1997
) found that herring
showed slow and fast head turning rates, which were both distinct from the
head turning rates of routine turns. They also found that slow head turning
rate responses were associated with longer response latencies than fast head
turning rate responses. For any given stimulus distance, slow responses were
more frequent in schooling than in solitary fish
(Domenici and Batty, 1997
),
suggesting that schooling may raise the threshold for initiation of fast
escape responses, inducing longer latencies and slower responses that are more
appropriate in reducing the possibility of collision with neighbouring fish.
Our present work suggests that the presence of fast and slow responses may not
be limited to highly gregarious teleost fish (although dogfish can also be
found in groups; Lythgoe and Lythgoe,
1971
) but may be a more widespread phenomenon of escape types that
may be worth investigating further in other species. As suggested by Domenici
and Batty (1994
,
1997
), the two response types
may be associated with different neural commands. Nissanov et al.
(1990
) found that escape
responses triggered by electrical stimulation of single Mauthner cells
(M-cells) showed a slower head turning rate than sensory-evoked responses,
where both M-cells and parallel reticulospinal circuits were triggered. It is
therefore possible that fish may employ fast and slow responses that may be
associated with different neural commands, similar to the finding by Nissanov
et al. (1990
). In addition,
the two response types may reflect different muscle contraction speeds and
activation patterns.
Domenici and Batty (1997)
associated the occurrence of different turning rates to stimulus distance.
Here, stimulus characteristics did not differ between responses with different
turning rates (Table 2).
However, since the stimulus was not a transient one, unlike Domenici and
Batty's work, we could not test if turning rates were related to latencies.
Previous authors have also investigated the effect of swim phase of the fish
prior to stimulation on escape responses. Sillar and Roberts
(1988
) found that escape
responses were gated in tadpoles, i.e. they were inhibited when the body
flexure was towards the stimulus. Blaxter and Batty
(1987
) found that swim phase
had an effect on the direction of escape in herring, while Domenici and Batty
(1994
) found no effect of swim
phase on the escape responses of herring. In the present study, swim phase has
no significant difference between response types. In addition, response type
was not related either to the order of stimulation or to specific individuals.
Therefore, the factors affecting turning rates are still unclear, and they may
be related to both the internal state (motivation) of the animal and some yet
to be measured stimulus characteristics.
Other response types observed by previous authors include single and double
bend responses (Domenici and Blake,
1991) and C- or L- (i.e. unilateral bend) and S-start responses
(Webb, 1976
;
Hale, 2002
). Domenici and
Blake (1991
) and Kasapi et al.
(1993
) classified single and
double bend responses on the basis of the absence/presence of stage 2. In the
present study, all responses but one (a fast response) showed the presence of
stage 2. However, various responses (five in total, both fast and slow) showed
small stage 2 angles (<2°) associated with short stage 2 durations
(<50 ms). Therefore, in dogfish, the intensity of stage 2 appears to
correspond to a gradient, from low intensity (and absence of reversal of head
direction, in one case) to higher intensities (i.e. maximum stage 2 angle near
30°), and neither stage 2 angle nor stage 2 duration show clear bimodal
patterns of distribution (not shown). Similarly, no bimodal pattern in maximum
stage 2 head turning rate between response types was found
(Table 1; Fig. 4). Foreman and Eaton
(1993
) also found that the
intensity of stage 2 (measured as the EMG integral) showed a gradient, from a
minor EMG (or even complete absence of a signal) to a high-intensity EMG
signal. Given the overlap in stage 2 variables, we suggest that the
hypothesized distinction between fast and slow responses would not correspond
to the distinction between double bend and single bend responses. Similarly,
Domenici and Blake (1991
)
found no differences in the relationship between stage 1 angle and S1 duration
(equivalent to head turning rate) of single and double bend responses.
Webb (1976) divided
fast-starts in trout into L- (later called C- by most authors; see
Domenici and Blake, 1997
) and
S-starts, based on the fish's body form at the end of stage 1. More recently,
Hale has found that different EMG patterns and kinematics were present during
the C and S escape responses of pike
(Hale, 2002
). In the present
study, no S-start was observed in dogfish, although this may be due to the
relatively low sample size used. It is possible that the presence of S- and
C-starts in fish escape responses may be species-specific, where sit-and-wait
predators such as pike, which use fast-start in line as a predator attack, may
also use in-line (S-starts) fast-starts as escape responses.
Performance differences between slow and fast responses
The two response types showed non-overlapping values of stage 1 head
turning rates (both maxima and means). Stage 1 head turning rate was almost
twice as high in fast compared with slow responses. Such differences were not
associated with different stage 1 angles. While a tighter turning radius might
be expected in fast responses, differences were not significant. CM turning
rates were also higher in fast response. Maximum stage 2 head turning rates
differed between fast and slow responses, similar to stage 2 duration and
angle. This suggests that the intensity of stage 2 is stronger in fast
responses, although values of stage 2 maximum head turning rates overlapped
with those of slow responses.
All distance-derived variables were higher in fast than in slow responses.
While this is to be expected because locomotor performance is related to
muscle contraction speed (Wardle,
1975), this is the first demonstration that higher turning rate
can lead to higher locomotor performance. The distribution pattern of
distance-derived performance is, however, not bimodal, unlike for head turning
rates (Fig. 7). Therefore, it
is possible that overlapping turning rates during stage 2
(Fig. 4B) may account for some
degree of overlap in the performance between the two escape types
considered.
If the possibility that dogfish possess two types of escape responses is
confirmed, this would mean that they can employ a two-gear system with which
they respond to startling stimuli. Such a system would allow them to react
using different response intensities and, therefore, energetic costs, perhaps
depending on the degree of the perceived threat. As suggested above, this
system does not appear to be graded, possibly as a result of neuromuscular
design features. Domenici and Batty
(1994,
1997
) found that herring, a
teleost with Mauthner neurons (Meredith,
1985
), show such response types (i.e. high and low head turning
rate responses), both differing from routine turns. Therefore, it is possible
that a two-gear system may be a common feature of the escape responses of many
fish, including teleosts and chondrichthyans, regardless of the presence of
the Mauthner system.
The relationship between mean S1 head turning rate and CM turning rate was
investigated. The turning rate of the head and that of the CM should be
related (Domenici, 2001),
particularly if the anterior part of the animals is relatively rigid and if
the CM and the head start off in line and end up in line with the swimming
trajectory of the fish. While previous authors working on aquatic vertebrates
have investigated either the head turning rates
(Eaton et al., 1981
; Domenici
and Batty, 1994
,
1997
;
Spierts and van Leeuwen, 1999
;
Budick and O'Malley, 2000
;
Walker, 2000
) or CM turning
rates (Gerstner, 1999
;
Fish et al., 2003
), the
relationship between these two variables has never been tested. Our results
show that head and CM turning rates are not related within each escape type.
However, fast responses show higher head and CM turning rates than slow
responses. The order of magnitude is similar for maximum S1 head turning rate
and CM turning rate (Table 1). This implies that the overall expectation of similar magnitude is confirmed.
However, CM and head turning rates must be relatively decoupled from each
other since they are not significantly related within each fast-start type
considered.
Turning rates decrease with stage 1 duration only in slow responses, while they are not related to stage 1 duration in fast responses. This result may imply differences in the temporal patterns of turning rate in slow and fast responses, possibly related to differences in the neural commands. Speed (UT) is not affected by turning rates in either fast or slow responses, although fast responses show higher speed and turning rates than slow responses. Therefore, while CM and head turning rates may be rough predictors of locomotor performance when applied to all responses, detailed analysis of the kinematics of the whole body may be necessary in order to unravel the relationship between kinematics and performance of each response type.
Comparison with other species
Based on morphological features, we expected dogfish to exhibit relatively
tight turns, because of their relatively high flexibility
(Aleev, 1977), and relatively
low locomotor performance during fast-start, due to their relatively low body
depth posteriorly (Webb,
1978a
,
1984a
). As shown by Brainerd
and Patek (1993
), high
flexibility during fast-starts may be associated with number of vertebrae.
Spiny dogfish have more vertebrae (72 precaudal vertebrae;
Springer and Garrick, 1964
)
than many of the teleosts whose turning radius has been investigated (reviewed
by Domenici and Blake, 1997
;
e.g. Salmo gairdneri, 60-66 vertebrae; Esox lucius, 57-65
vertebrae; Coryphaena hyppurus, 31 vertebrae; Thunnus
albacares, 39 vertebrae;
www.fishbase.org).
However, recent work by Kajiura et al.
(2003
) shows that vertebral
count did not have significant effects on flexibility during unsteady
manoeuvres in three cartilaginous fishes, while cross-sectional shape did.
Therefore, high flexibility in dogfish may be related to body shape and other
factors such as the stiffness of the inter-vertebral tissue. Our results
confirmed the expectations based on functional morphology arguments.
Fig. 8 shows the turning radius
of dogfish in comparison with those of teleost fish and other vertebrates,
based on data reviewed by Domenici
(2001
). This figure is based
on mean values. The value for dogfish (0.067 L) is in the low part of
the range when compared with other aquatic vertebrates and it is similar to
that of a manoeuvre specialist such as angelfish (0.065 L;
Domenici and Blake, 1991
). The
minimum turning radius achieved during a single event can also be considered a
relevant measure of maximum performance during a single event. The minimum
turning radius measured in a single event is 0.041 L in dogfish.
Other vertebrate species show relatively small minimum turning radius during a
single event, i.e. sealion (0.09 L;
Fish et al., 2003
), four
species of coral reef fishes (0-0.09 L;
Gerstner, 1999
), boxfish
(0.0005 L; Walker,
2000
). Although these studies were not based on escape responses,
they show that minimum turning radius in certain manoeuvre specialists such as
coral reef fishes can be even tighter than that shown by dogfish. The ability
to turn along tight paths can be of fundamental importance during
predator-prey relationships (Howland,
1974
; Webb, 1976
),
particularly for species living in structurally complex environments
(Domenici, 2003
). Dogfish are
benthic fish that may live in groups on various types of bottoms (sand and
mud, rocky bottoms; Wetherbee et al.,
1990
; Masuda and Allen,
1993
). Predators of dogfish may include larger elasmobranches
(Harvey, 1989
;
Stillwell and Kohler, 1993
).
Dogfish are mainly piscivorous (Tanasichuk
et al., 1991
; Beamish et al.,
1992
). High manoeuvrability in dogfish may, therefore, be
advantageous during predator-prey encounters, both as predators and prey. The
tight turning radius of dogfish may be due to their high flexibility when
compared with teleost species (Aleev,
1977
). This is in contrast with pelagic fish such as tuna, with
very rigid bodies, whose turning radii are an order of magnitude higher than
that of dogfish (i.e. 0.47 L;
Blake et al., 1995
). In
addition, dogfish appear to move their pectoral fins asymmetrically during
turning (P. Domenici, personal observation) and this behaviour may aid in
producing a tight turning radius, although whether such a movement is active
or passive remains to be ascertained. Eaton and Hackett
(1984
) suggested that escape
responses in most fish are associated with abducting their pectoral fins
against the body, with a few exceptions such as in the hatchet fish. However,
other species appear to fold out their pectoral fins
(Kasapi et al., 1993
;
Domenici and Blake, 1997
).
Therefore, the role of specific pectoral fin movements during the escape
response of different fish species is an area that needs further
attention.
|
Turning rate is another relevant measurement of manoeuvrability in fish, as
it can be used to evaluate agility defined as the ability of a fish to quickly
reorient its body (Webb, 1994). Turning rate decreases with fish length
(reviewed in Domenici, 2001).
Domenici (2001
) includes
values only for fish up to about 30 cm, although values for other vertebrates
(cetaceans) in excess of 1 m are included. Therefore, the value predicted for
a 58 cm dogfish based on fig. 7
of Domenici (2001
) needs to be
considered with caution as it comprises both teleosts and cetaceans, as well
as head and CM turning rates. Nevertheless, a 58 cm dogfish is predicted to
show a mean turning rate of
800 deg. s-1, which is within the
same order of magnitude as our results for CM and S1 head turning rates of
fast responses (Table 1), while
values for slow responses are somewhat lower. Therefore, dogfish appear to be
capable of escaping using similar rates of bending as would be predicted for
other vertebrates of a similar size, although comparable data (in terms of
size) for fish are lacking. Therefore, considering both turning radius and
turning rates as measures of manoeuvrability, dogfish appear to perform
relatively well, although not exceptionally, when compared with other aquatic
vertebrates.
Distance-time performance in dogfish appears to be lower than that of most
teleost species (Domenici,
2001). Temperature can have an effect on fast-start performance
(Webb, 1978b
). The temperature
used in our study is within the range used in other studies
(Domenici and Blake, 1997
),
although slightly higher than the average of previous fast-start studies
(approximately 16°C from Domenici and
Blake, 1997
) and therefore it is possible that low temperature may
account in part for low performance. The speed of both fast and slow responses
appears to be considerably lower than those reported in other studies, which
include teleosts of sizes similar to the dogfish. According to
fig. 1 of Domenici
(2001
), a 58 cm-long fish
should have a maximum speed of
3 m s-1, which is considerably
higher than the speeds reported here (1.19 and 0.79 m s-1 for fast
and slow responses, respectively). In addition, it is important to consider
that, in most other performance studies, fish performed escape responses from
a standing start (e.g. trout, pike, angelfish), while dogfish start from a
swimming speed of
0.27 m s-1. Dogfish can swim at speeds
faster (e.g. 1.9 m s-1 for a 47 cm dogfish reported by
Aleev, 1977
) than those
reported here, although it may take them a few tail beats in order to get to
such speeds. As was found for speed, acceleration in our study appears to be
at the lower end of the range when compared with other studies
(Domenici and Blake, 1997
;
Domenici, 2001
), being 31 and
19 m s-2 for fast and slow response, respectively, while it ranges
from
20 to >150 m s-2 in other studies on teleosts reviewed
by Domenici (2001
). Size is
unlikely to be the reason for such a low performance, there being no evidence
of an effect of size on acceleration across fish species
(Domenici, 2001
), and, indeed,
acceleration may increase with size within a single species in relation to
changes in morphology resulting from ontogeny
(Wakeling et al., 1999
;
Hale, 1999
). Low locomotor
performance in dogfish escape responses is most likely related to their
relatively small body depth posteriorly, compared with accelerator specialists
such as pike and angelfish, whose large posterior depth allows for high thrust
generation during fast-start manoeuvres
(Harper and Blake, 1990
;
Domenici and Blake, 1991
).
The present results suggest that two escape types may occur in the dogfish.
From these results and other recent studies
(Tytell and Lauder, 2002;
Hale, 2002
;
Hale et al., 2002
) it is
becoming apparent that escape responses can be highly variable both within and
across species. Some of this variability may be due to flexibility in the
neural and muscular systems, although in some cases, as in the fast and slow
escape responses observed in the dogfish, discrete behaviours and therefore
differential neuromuscular control may be the basis for kinematic differences.
Future studies, integrating kinematics and neuromuscular data, should be aimed
at studying the variability of escape responses (e.g. by using a variety of
species and different stimulus characteristics) in order to further our
understanding of the functional basis of both graded and discrete categories
of escape behaviours.
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Acknowledgments |
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References |
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---|
Aleev, Y. G. (1977). Nekton. The Hague: W. Junk.
Beamish, R. J., Thomson, B. L. and McFarlane, G. A. (1992). Spiny dogfish predation on chinook and coho salmon and the potential effects on hatchery-produced salmon. Trans. Am. Fish. Soc. 121,444 -455.
Blake, R. W., Chatters, L. M. and Domenici, P. (1995). The turning radius of yellowfin tuna (Thunnus albacares) in unsteady swimming manoeuvres. J. Fish Biol. 46,536 -538.
Blaxter, J. H. S. and Batty R. S. (1987). Comparisons of herring behaviour in the light and dark: changes in activity and responses to sound. J. Mar. Biol. Assoc. UK 67,849 -860.
Blaxter, J. H. S., Gray, J. A. B and Denton, E. J. (1981). Sound and startle responses in herring shoals. J. Mar. Biol. Assoc. UK 61,851 -869.
Bone, Q. (1977). Mauthner neurons in elasmobranches. J. Mar. Biol. Assoc. UK 57,253 -259.
Brainerd, E. L. and Patek, S. N. (1993). Vertebral column morphology, C-start curvature, and the evolution of mechanical defenses in Tetraodontiform fishes. Copeia 1998,971 -984.
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.
Dill, L. M. (1974). The escape response of the zebra danio (Brachydanio rerio). I. The stimulus for escape. Anim. Behav. 22,710 -721.
Domenici, P. (2001). Scaling the locomotor performance in predator-prey interactions: from fish to killer whales. Comp. Biochem. Physiol. A 131,169 -182.
Domenici, P. (2002). The visually-mediated escape response in fish: predicting prey responsiveness and the locomotor behaviour of predators and prey. Mar. Fresh. Behav. Physiol. 35,87 -110.[CrossRef]
Domenici. P. (2003). Habitat type, design and the swimming performance of fish. In Vertebrate Biomechanics and Evolution (ed. V. Bels, J. P. Gasc and A. Casinos), pp.137 -160. Oxford: Bios Scientific Publishers.
Domenici, P. and Batty, R. S. (1994). Escape manoeuvres of schooling Clupea harengus. J. Fish Biol. 45 (suppl. A),97 -110.[CrossRef]
Domenici, P. and Batty, R. S. (1997). The escape behaviour of solitary herring and comparisons with schooling individuals. Mar. Biol. 128, 29-38.[CrossRef]
Domenici, P. and Blake, R. W. (1991). The kinematics and performance of the escape response in the angelfish (Pterophyllum eimekei). J. Exp. Biol. 156,187 -205.
Domenici, P. and Blake, R. W. (1993). Escape
trajectories in angelfish (Pterophyllum eimekei). J. Exp.
Biol. 177,253
-272.
Domenici, P. and Blake, R. W. (1997). Fish
fast-start kinematics and performance. J. Exp. Biol.
200,1165
-1178.
Eaton, R. C. and Emberley, D. S. (1991). How stimulus direction determines the trajectory of the Mauthner-initiated escape response in a teleost fish. J. Exp. Biol. 161,469 -487.[Abstract]
Eaton, R. C. and Hackett J. T. (1984). The role of Mauthner cells in fast-starts involving escape in teleost fish. In Neural Mechanisms of Startle Behavior (ed. R. C. Eaton), pp. 213-266. New York: Plenum Press.
Eaton, R. C., Lavender, W. A. and Wieland, C. M. (1981). Identification of Mauthner initiated response patterns in goldfish: evidence from simultaneous cinematography and electrophysiology. J. Comp. Physiol. A 155,813 -820.
Eaton, R. C., Nissanov, J. and Wieland, C. M. (1984). Differential activation of Mauthner and non-Mauthner startle circuits in zebrafish: implication for functional substitution. J. Comp. Physiol. A 155,813 -820.
Fish, F. E. (1997). Biological design for enhanced manoeuvrability: analysis of marine mammal performance. In Tenth International Symposium on Unmanned Untethered Submersible Technology, pp. 109-117. Durham, NH: Autonomous Undersea Systems Institute.
Fish, F. E., Hurley, J. and Costa, D. P.
(2003). Maneuverability by the sea lion Zalophus
californianus: turning performance of an unstable body design.
J. Exp. Biol. 206,667
-674.
Foreman, M. B. and Eaton, R. C. (1993). The direction change concept for reticulospinal control of goldfish escape. J. Neurosci. 13,4101 -4133.[Abstract]
Gerstner, C. L. (1999). Maneuverability of four species of coral-reef fish that differ in body and pectoral-fin morphology. Can. J. Zool. 77,1102 -1110.[CrossRef]
Hale, M. E. (1999). Locomotor mechanics during
early life history: effects of size and ontogeny on fast-start performance of
salmonid fishes. J. Exp. Biol
202,1465
-1479.
Hale, M. E. (2002). S- and C-start escape responses of the muskellunge (Esox masquinongy) require alternative neuromotor mechanisms. J. Exp. Biol. 205,2005 -2016.[Medline]
Hale, M. E., Long, J. H., McHenry, M. J. and Westneat, M. W. (2002). Evolution of behaviour and neural control of the fast start escape response. Evolution 56,933 -1007.
Harper, D. G. and Blake, R. W. (1990). Fast-start performance of rainbow trout Salmo gairdneri and northern pike Esox lucius. J. Exp. Biol. 150,321 -342.
Harper, D. G. and Blake, R. W. (1991). Prey capture and the fast-start performance of northern pike Esox lucius.J. Exp. Biol. 155,175 -192.
Harvey, J. T. (1989). Food habits, seasonal abundance, size, and sex of the blue shark, Prionace gluaca, in Monterey Bay, California. Calif. Fish Game 75, 33-44.
Howland, H. C. (1974). Optimal strategies for predator avoidance: the relative importance of speed and manoeuvrability. J. Theor. Biol. 134,56 -76.
Kajiura, S. M., Forni, J. B. and Summers, A. P. (2003). Maneuvering in carcharhinid and sphyrnid sharks: the role of the hammerhead shark cephalofoil. Zoology 106, 19-28.
Kasapi, M. A., Domenici, P., Blake, R. W. and Harper, D. G. (1993). The kinematics and performance of the escape response in the knifefish Xenomystus nigri. Can. J. Zool. 71,189 -195.
Jayne, B. C. and Lauder, G. V. (1993). Red and white muscle activity and kinematics of the escape response of bluegill sunfish during swimming. J. Comp. Physiol. A 173,495 -508.
Lanczos, C. (1956). Applied Analysis. Eaglewood Cliffs, NJ: Prentice Hall.
Lythgoe, J. N. and Lythgoe, G. (1971). Fishes of the Sea. The Coastal Waters of the British Isles, Northern Europe and the Mediterranean. London: Blandfor Press.
Masuda, H. and Allen, G. R. (1993). Meeresfische der Welt - Groß-Indopazifische Region. Herrenteich, Melle: Tetra Verlag.
Meredith, G. E. (1985). The distinctive central utricular projections in the herring. Neurosci. Lett. 55,191 -196.[CrossRef][Medline]
Nemeth, D. (1997). Modulation of attack
behavior and its effect on feeding performance in a trophic generalist fish.
J. Exp. Biol. 200,2155
-2164.
Nissanov, J. and Eaton, R. C. (1989). Reticulospinal control of rapid escape turning manoeuvres in fishes. Am. Zool. 29,103 -121.
Nissanov, J., Eaton, R. C. and DiDomenico, R. (1990). The motor output of the Mauthner cell, a reticulospinal command neuron. Brain Res. 517, 88-98.[CrossRef][Medline]
Rand, D. M. and Lauder, G. V. (1981). Prey capture in the chain pickerel, Esox niger: correlations between feeding and locomotor behaviour. Can. J. Zool. 59,1072 -1078.
Sillar, K. T. and Roberts, A. (1988). A neuronal mechanism for sensory gating during locomotion in a vertebrate. Nature 331,262 -265.[CrossRef][Medline]
Spierts, I. L. and Leeuwen, J. L. (1999).
Kinematics and muscle dynamics of C- and S-starts of carp (Cyprinus
carpio L.). J. Exp. Biol.
202,393
-406.
Springer, V. G. and Garrick, J. A. F. (1964). A survey of vertebral numbers in sharks. Proc. US Nat. Museum 116,73 -96.
Stefanelli, A. (1980). I neuroni di Mauthner degli Ittiopsidi. Valutazioni comparative morfologiche e funzionali. Lincei Mem. Sci. Fis. Natur. XVI, 1-45.
Stillwell, C. E. and Kohler, N. E. (1993). Food habits of the sandbar shark Carcharhinus plumbeus off the U.S. northeast coast, with estimates of daily ration. Fish. Bull. 91,138 -150.
Tanasichuk, R. W., Ware, D. M., Shaw, W. and McFarlane, G. A. (1991). Variations in diet, daily ration, and feeding periodicity of Pacific hake (Merluccius productus) and spiny dogfish (Squalus acanthias) off the lower west coast of Vancouver Island. Can. J. Fish. Aquat. Sci. 48,2118 -2128.
Tytell, E. D. and Lauder, G. V. (2002). The
C-start escape response of Polypterus senegalus: bilateral muscle
activity and variation during stage 1 and 2. J. Exp.
Biol. 205,2591
-2603.
Wakeling, J. M., Kemp, K. M. and Johnston, I. A.
(1999). The biomechanics of fast-starts during ontogeny in the
common carp Cyprinus carpio. J. Exp. Biol.
202,3057
-3067.
Walker, J. A. (2000). Does a rigid body limit
maneuverability? J. Exp. Biol.
203,3391
-3396.
Wardle, C. S. (1975). Limits of fish swimming speed. Nature 255,725 -727.s[Medline]
Webb, P. W. (1976). The effect of size on the fast-start performance of rainbow trout Salmo gairdneri and a consideration of piscivorous predator-prey interaction. J. Exp. Biol. 65,157 -177.[Abstract]
Webb, P. W. (1978a). Fast-start performance and body form in seven species of teleost fish. J. Exp. Biol. 74,211 -226.
Webb, P. W. (1978b). Temperature effects on acceleration of rainbow trout Salmo gairdneri. J. Fish. Res. Bd Can. 35,1417 -1422.
Webb P. W. (1984a). Body form, locomotion and foraging in aquatic vertebrates. Am. Zool. 24,107 -120.
Webb, P. W. (1984b). Body and fin form and strike tactics of four teleost predators attacking fathead minnow (Pimephales promelas) prey. Can. Fish. Aquat. Sci. 41,157 -165.
Webb, P. W. (1986a). Locomotion and predator-prey relationships. In Predator-Prey Relationships (ed. G. V. Lauder and M. E. Feder), pp.24 -41. Chicago: University of Chicago Press.
Webb, P. W. (1986b). Effect of body form and response threshold on the vulnerability of four species of teleost prey attacked by largemouth bass (Micropterus salmoides). Can. J. Fish. Aquat. Sci. 43,763 -771.
Webb, P. W. (1994a). 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: Cambridge University Press.
Webb, P. W. and Skadsen, J. M. (1980). Strike tactics of Esox. Can. J. Zool. 58,1462 -1469.[Medline]
Webb, P. W. and Zheng, 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. (1973). The mechanism of rapid starting of slender fish. Biorheology 10,343 -350.[Medline]
Weihs, D. and Webb, P. W. (1984). Optimal avoidance and evasion tactics in predator-prey interactions. J. Theor. Biol. 106,189 -206.
Wetherbee, B. M., Gruber, S. H. and Cortes, E. (1990). Diet, feeding habits, digestion, and consumption in sharks, with special reference to the lemon shark, Negaprion brevirostris. In Elasmobranchs as living resources: advances in the biology, ecology, systematics, and the status of the fisheries. NOAA Tech. Rep. NMFS 90 (ed. H. L. Pratt, Jr, S. H. Gruber and T. Taniuchi), pp. 29-47.
Zottoli, S. J. (1978). Comparative morphology of the Mauthner cell in fish and amphibians. In Neurobiology of the Mauthner Cells (ed. D. S. Faber and H. Korn), pp13 -41. New York: Raven Press.