Kinematics of aquatic and terrestrial escape responses in mudskippers
Department of Biological Sciences, Northern Arizona University, PO Box 5640, Flagstaff, AZ 86011, USA
* Author for correspondence (e-mail: bos{at}dana.ucc.nau.edu)
Accepted 10 August 2004
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Summary |
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Key words: escape response, mudskipper, Periophthalmus argentilineatus, terrestrial environment, aquatic environment, intervertebral bending
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Introduction |
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Amphibious fishes provide an unusual opportunity to examine environmental
effects on escape behavior. Voluntary amphibious behavior is widespread among
bony fishes and has been documented in 11 families, 26 genera and at least 100
species (Graham, 1997).
Amphibious fishes are exposed to a wide range of novel predators during
terrestrial excursions, including birds, reptiles and mammals, and must
perform some type of escape behavior to avoid capture by these predators
(Clayton, 1993
). Amphibious
fishes continue to spend a significant portion of their time in an aquatic
environment, where they are exposed to aquatic predators. Thus, these species
must retain the ability to perform effective escape responses in the water
even after they have evolved a terrestrial escape response
(Harris, 1960
). This raises
two questions. First, how does an amphibious fish perform an escape response
in a terrestrial environment? Second, how similar is a terrestrial escape
response to an aquatic escape response?
Mudskippers (family Gobiidae, subfamily Oxudercinea) are an ideal group in
which to study terrestrial escape responses. Most species are intertidal
specialists, and many spend more than half of their time on land and can
survive for several days without access to water
(Clayton, 1993;
Gordon et al., 1978
). Field
studies indicate that mudskippers have both aquatic and terrestrial predators
and are a major source of food for both fish and birds in their natural
habitats (Clayton, 1993
;
Clayton and Vaughan, 1988
;
Mukherjee,
1971a
,b
).
Mudskippers also show a variety of novel behaviors that allow them to exploit
terrestrial habitats, including a `crutching' behavior that is used for steady
locomotion and a `skipping' behavior that is analogous to jumping in
tetrapods. This skipping behavior is employed to avoid predation
(Harris, 1960
). Thus, skipping
appears to be the ecological equivalent of an aquatic escape response but is
performed in a terrestrial environment.
During a terrestrial escape response, mudskippers first bend the axial
skeleton to move the head and tail together. This can be considered a
preparatory phase (analogous to stage 1 of aquatic escapes) because the fish
has started the escape behavior but the center of mass is not moving away from
the threat (Weihs, 1973).
During the propulsive phase (analogous to stage 2 of aquatic escapes),
mudskippers use the stiffened ventral rays of the caudal fin to push off the
ground as they rapidly straighten their bodies and accelerate away from a
threat (Harris, 1960
).
Clearly, aquatic and terrestrial environments pose different challenges for
a fish attempting to move rapidly away from a predator. Although fish on land
do not contend with the high density and viscosity of water, they must instead
accommodate the constraints of weight and gravity. Biewener and Gillis
(1999) suggested that organisms
can produce movements across disparate environments via three
non-exclusive methods. First, there may be no alteration in musculoskeletal
function across environments. Second, the same locomotor muscles may be
activated differently by the central nervous system. Third, different
locomotor muscles may be recruited across environments.
Mudskipper terrestrial escape responses clearly employ the same locomotor structures (the axial skeleton, caudal fin and associated musculature) as aquatic escape responses and superficially appear to employ the same movement patterns. This suggests that mudskippers either do not alter musculoskeletal function across the two environments or that they modulate muscle activity patterns to create a different behavior in each habitat. However, even if there is no alteration in musculoskeletal function across environments, divergent physical conditions will have consequences for animal movement patterns.
Therefore, despite their superficial similarity, we predict that specific aspects of mudskipper terrestrial escapes are quantitatively different from aquatic escapes. For example, even if the muscluloskeletal movements that produce the escape response are the same on land as in the water, we predict that escape performance will be slower (durations of stage one and stage two, maximum acceleration and velocity) in the aquatic environment because water provides a much greater resistance to movement than does air. Therefore, mudskippers on land should achieve a greater maximum velocity during the escape response and take less time to achieve maximum velocity due to reduced drag in the terrestrial environment.
By contrast, we predict that axial bending patterns used in the response
will be similar across environments. Although hydrodynamic drag will have
ramifications for bending movements produced during the preparatory phase of
the escape response, previous research suggests that bending kinematics for
fish fast-starts are constrained by vertebral morphology
(Brainerd and Patek, 1998).
Therefore, although hydrodynamic resistance to bending is reduced in the
terrestrial environment, we predict that intervertebral bending is ultimately
limited by the mechanical design of the vertebral column and that this
constraint will generate similar bending patterns across the two
environments.
In the present study, we examine the escape behavior of mudskippers in the water and on land with two primary objectives. First, we describe and quantify the terrestrial escape response of the mudskipper. Second, we measure performance (e.g. maximum velocity, acceleration and timing) and kinematic (e.g. axial bending) variables for aquatic and terrestrial escape responses and use these variables to test the general hypothesis that mudskipper terrestrial escapes are quantitatively different from aquatic escapes.
In addition to the two main goals of the study, we used the mudskipper
terrestrial escape response to estimate fish axial muscle power. Because
escape behaviors are under intense selection, muscle power production during
an escape is thought to approach maximal muscle power output
(Frith and Blake, 1995).
However, it is difficult to estimate muscle power production in an aquatic
environment. When a fish accelerates in water, it not only moves its own mass
but also the mass of the water around it (i.e. it has `added mass'). Thus,
this added mass must be included in calculations of muscle power, and the
assumptions inherent in the resulting hydrodynamic calculations are difficult
to test (Frith and Blake,
1995
). One way to circumvent these complications is to examine a
fish out of water (Korff et al.,
1996
). As outlined by Alexander
(1968
), estimates of power are
relatively simple in terrestrial jumping species because aerodynamic drag is
minimal (in comparison to hydrodynamic drag) and kinetic energy can be
determined using high-speed imaging (Aerts,
1998
; Korff et al.,
1996
; Wilson et al.,
2000
). Thus, a third goal of this study was to use the terrestrial
escape response of the mudskipper (which is analogous to jumping) to estimate
power output for this species and to compare our results with published values
for aquatic behaviors in other fishes and jumping in tetrapods.
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Materials and methods |
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Morphometrics
Center of mass and axial muscle masses were determined using three
preserved specimens. The center of mass was identified by suspending preserved
specimens (three individuals) from needle probes using methods outlined by
Drucker and Lauder (2003).
Subsequently, both sides of the axial musculature were removed, skinned and
weighed for each individual. The average of the two sides of the axial
musculature for each individual was used to estimate the muscle mass for
propulsion of the jump. These three individuals were also cleared and stained
(Taylor, 1967
). Intervertebral
joints were measured on the cleared and stained specimens by taking a digital
image with a Nikon coolpix 950 digital camera and measuring joint lengths with
NIH Image analysis software (v. 1.62). We detected little variation in joint
number among individuals. Fish used for morphometrics were similar in size and
shape to those used for kinematic analyses (two of the three fish were also
used for kinematics).
High-speed digital imaging
Kinematic and performance data were collected for seven individuals of
Periophthalmus argentilineatus. Single individuals were removed from
the tank, weighed and placed in an acrylic filming chamber. A Motionscope
high-speed CCD camera (Redlake, San Diego, CA, USA) was mounted over the
mudskipper, perpendicular to the substrate, to obtain a dorsal view for
kinematic measurements. For terrestrial performance measures, the camera was
placed in a lateral view to record jumping behavior. Behaviors were recorded
at 250 or 500 frames s-1 at a shutter speed of 1/500 of a second. A
blunt probe was used to elicit an escape response from the fish. Proximity to
the probe was usually enough to elicit an escape response (i.e. the fish
typically jumped before they were touched by the probe). Fish performed
34 escape responses per session, although some sessions were terminated
early when the fish showed signs of fatigue.
Analysis
Digital video (AVI) files from the Motionscope camera were converted to
JPEG image sequences for motion analysis. To quantify movements produced
during the preparatory phase, we used two complementary metrics of axial
bending. Overall axial bending was quantified using the curvature coefficient
calculation proposed by Webb
(1978,
1983
) and subsequently
modified by Brainerd and Patek
(1998
). The coefficient is
calculated by dividing the bent vertebral chord length by the straight length;
a smaller coefficient denotes more bending. Bending kinematics were analyzed
using the Jayne and Lauder
(1993
) intervertebral bending
program, following techniques detailed in that study. Briefly, maximally bent
fish were outlined in a series of points using an image measurement program.
Next, the program interpolated a midline through the outline and calculated
intervertebral angles based on the number and length of the intervertebral
segments (determined from cleared and stained specimens).
For movement calculations during the propulsive phase, the location of the center of mass was identified on the digital images as a spot just posterior to the pectoral fins. This location was converted to X and Y coordinates in consecutive frames throughout the escape response using Didge software (A. J. Cullum, 1999; Ph.D. http://biology.creighton.edu/faculty/cullum/index.html). Because calculations of velocities and accelerations from position data are subject to measurement error, data from the consecutive frames were uploaded into QuickSAND software (J. A. Walker, 1997; Ph.D. software http://www.usm.maine.edu/~walker/software.html). With this software, we used a cubic-spline algorithm and an estimated error variance to mathematically reduce the effects of digitizing error, effectively smoothing the data and removing noise. The program was used to calculate velocity and acceleration over each 4 ms frame throughout the behavior by taking the first and second derivatives of the smoothed displacement. The acceleration calculated from the program is derived from the absolute position of the fish and serves as an estimate of whole-animal performance.
To determine the acceleration produced by the axial myomeres and to
estimate power production, the horizontal and vertical acceleration vectors
were calculated separately. For the vertical acceleration vector, the
acceleration due to gravity was added, which resulted in a larger value that
reflects the effort required by the muscles to move the animal against
gravity. Thus, the total acceleration produced by the axial muscles during the
escape response was calculated by adding the horizontal and vertical
acceleration vectors using the methods of Marsh and John-Alder
(1994). For each mudskipper,
total acceleration was multiplied by body mass and the velocity of the animal
over the same time interval. This provided an estimate of whole-animal
instantaneous power output. This value was divided by the mean lateral axial
muscle mass to obtain an estimate of muscle mass-specific instantaneous
power.
Statistical analysis
Intervertebral joint angles were compared between aquatic and terrestrial
escape responses using a two-way analysis of variance (ANOVA). In this
analysis, intervertebral angle was the dependent variable, and individual and
substrate (aquatic versus terrestrial) were factors. A total of 29
segment angles were compared for six individuals with 23 trials per
individual per environment (a total of 25 trials). Post-hoc Tukey HSD
tests were used to identify differences between intervertebral joint angles
along the body for the distinct behaviors. In addition, bending values,
curvature coefficients and overall movement patterns were qualitatively
compared with published values for other fishes performing fast-starts.
To test for potential multivariate differences in the overall performance of aquatic and terrestrial escape responses, a multivariate analysis of variance (MANOVA) was used with 18 total trials for six individuals in aquatic escapes and 17 total trials for seven individuals in terrestrial escapes. Six variables were chosen as potential indicators of individual escape response performance and included in the model. These variables were: (1) duration of stage 1 (time from first movement to maximum curvature), (2) duration of stage 2 (time from maximum curvature to straightening of body), (3) time to maximum velocity (time from first movement to peak velocity of the center of mass), (4) ratio of duration of stage 1 to duration of stage 2, (5) maximum velocity and (6) maximum acceleration. After we determined if aquatic and terrestrial escapes were different overall, we used post-hoc ANOVA to identify the variables contributing to differences between behaviors.
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Results |
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In a minority of aquatic escape responses, the fish appeared to perform a terrestrial escape response in the water (described in detail below). In these responses, the fish pushed off the bottom of the aquarium to accelerate out of the water. Similarly, a few of the terrestrial escape responses appeared to have similar kinematics to aquatic escape responses, with a curve of fairly constant radius at the end of stage 1. However, these responses were rare and were not included in the quantitative analysis.
Terrestrial escape responses
Terrestrial escape responses began when the fish lifted its caudal fin off
the substrate (Fig.1B). The
caudal fin was then brought around to form a `J' shape, in which the caudal
fin lay next to the body, just behind the head and near the center of mass.
Maximum bending occurred approximately two-thirds of the way down the body
(Fig. 2). The anterior portion
of the body, including the head, typically did not move during this phase of
the response. This is the preparatory phase and roughly corresponds to stage 1
of the aquatic escape response.
The preparatory phase was followed by a slight lifting of the head, apparently produced by the pelvic and pectoral fins, and a rapid unfolding of the body, which straightened the tail. The straightening of the body occurred via both lateral and ventral movements of the tail (i.e. it pushed to the side and down) that lifted the center of mass off the substrate and propelled it in the direction that the fish was pointing at the beginning of the behavior. This movement roughly corresponds to stage 2 of a fish escape response (Fig.1). The caudal fin was consistently the last part of the fish to leave the ground, and the take-off angle ranged from 27 to 59° above horizontal. Take-off angle was a good predictor of jump range, with higher take-off angles producing longer jumps (N=7, r2=0.78), similar to predictions of a simple ballistic model of movement. However, take-off angle did not predict any other performance variables (such as maximum acceleration; N=7, r2=0.03).
In general, mudskippers performing terrestrial escape responses formed a J-shaped curve with a very sharp bend or fold in the caudal portion of the body and a slight re-curvature in the anterior portion of the body. The values of curvature coefficients for mudskipper terrestrial escape responses were smaller (0.24±0.01; mean ± S.E.M.) than observed in aquatic escape responses (0.55±0.02), indicating greater lateral bending in the terrestrial environment. Mean intervertebral bending angles ranged from small negative values (slight bending of the anterior portion of the body away from the major axial bending of the fish) to large positive values (sharp bending along the posterior two-thirds of the fish; Fig.2).ANOVA for intervertebral angle by location along the body showed a significant difference among intervertebral joints (29 intervertebral joints, 13 trials). Tukey HSD post-hoc tests indicated that the intervertebral segments in the anterior part of the body did not differ from one another, but segments in the posterior portion of the body differed greatly. This suggests that there is little variation in bending among anterior joints, but the caudal portion is bent to a much greater degree and does not form a constant arc (Fig. 2).
Performance
One-factor MANOVA on kinetic, or performance, variables indicated an
overall significant difference between aquatic and terrestrial escape
responses (F8,24=6.49, P<0.05). Individual
ANOVA tests for each variable indicated that duration of stage 1
(F1,6=16.05, P<0.05), ratio of duration of
stage 1 to duration of stage 2 (F1,6=28.04,
P<0.05), time to maximum velocity (F1,6=20.93,
P<0.05) and maximum acceleration (F1,6=15.77,
P<0.05) differed significantly between environments. Duration of
stage 2 and maximum velocity did not differ between environments. In general,
terrestrial responses took longer than aquatic escape responses
(Fig. 3). In fact, it took
twice as long to reach maximum velocity in terrestrial escape responses than
in aquatic escape responses. This was due to stage 1 being twice the duration
for terrestrial escape responses than for aquatic escape responses (see
Table 1).
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Instantaneous power was estimated between two consecutive digital images (a 4 ms interval). Mudskipper mass ranged from 0.4 to 2.0 g, and the mass of one set of axial myomeres (from one side of the body) averaged 20% of total body mass. Total acceleration of the body averaged 125.47±11.9 m s-2 (mean ± S.E.M.; in calculations of muscle performance, acceleration due to gravity was included as a factor that the muscles would be required to overcome). Using these values for the power calculations, muscle mass-specific power ranged from 350 to 770 W kg-1.
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Discussion |
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To escape predators, mudskippers must produce effective escape responses in
aquatic and terrestrial environments. We found that these aquatic and
terrestrial escape behaviors are distinct. Mudskipper aquatic escape responses
are similar to those produced by other fishes and fit the stereotyped
kinematic pattern of a C-start escape response
(Domenici and Blake, 1997;
Weihs, 1973
). For example, the
intervertebral joint angles at the end of stage 1 in mudskippers are similar
to those reported for several species of fish
(Brainerd and Patek, 1998
). In
addition, aquatic escapes in mudskippers are rapid behaviors, with similar
durations of stages 1 and 2 of the escape response to other fast-starting
fishes (Domenici and Blake,
1997
).
However, the mudskipper terrestrial escape response differs from aquatic escape responses of mudskippers and those of other fishes in several ways. The escape response takes longer in the terrestrial environment, due to a twofold increase in the duration of the preparatory phase. Thus, it took mudskippers significantly longer to reach the propulsive phase and, in turn, maximum velocity when they were on land. The increased time to maximum velocity suggests that performance is `worse' in the terrestrial environment, although we note that the maximum velocities achieved are the same across the two environments and a larger distance is covered with a single propulsive movement during terrestrial escapes. Additionally, the axial skeleton bends to a greater degree during terrestrial escape responses than during aquatic responses. The pattern of axial bending on land is also different, with flexion restricted to the posterior region of the axial skeleton.
These results are contrary to our initial predictions. We hypothesized that if the underlying musculoskeletal pattern used to produce the behavior were similar across the two environments, then reduced hydrodynamic drag in the terrestrial environment should allow improved escape performance (i.e. a quicker, higher-velocity escape response).
We also hypothesized that intervertebral bending is constrained by the morphology of the vertebral column and that decreased hydrodynamic resistance on land would not generate increased intervertebral flexion. Thus, the observed patterns are not generated as a simple consequence of employing the same behavior across two physically disparate environments.
Instead, these results suggest that mudskippers use distinct behaviors in
the different environments. Several lines of evidence support this conclusion.
First, aquatic responses are rapid behaviors with durations within the range
of Mauthner-initiated escape responses (although it is not known if
mudskippers have Mauthner neurons). By contrast, terrestrial responses appear
too slow to employ this pathway (Hale,
2000). If the aquatic responses use the Mauthner cell system and
the terrestrial responses do not, this would imply that a different neural
pathway is used for each behavior. Second, the axial muscles appear to be
recruited differentially in the different environments. In previous studies of
fish escape responses, all of the myomeres in the axial musculature were
activated near-synchronously (Jayne and
Lauder, 1993
), which produces consistent bending along the
vertebral column. In mudskipper terrestrial responses, most bending occurred
about a particular location on the body. The variable pattern of bending along
the body in the mudskipper terrestrial response suggests that a distinct
subset of myomeres is being recruited to produce the behavior
(Katz et al., 1999
;
Wakeling and Johnston, 1999
).
Finally, when we attempted to stimulate aquatic escape responses, mudskippers
occasionally produced what appeared to be a kinematically `terrestrial' escape
response in the water. All of these results suggest that the observed
differences between response types are not simply passive responses to changes
in the physical environment but instead reflect a novel motor pattern.
It is probable that physical differences between the two habitats
necessitated the evolution of a novel escape behavior. A fish immersed in an
aquatic medium must contend with the viscosity of water but is able to produce
thrust along the entire lateral surface of the body
(Johnston et al., 1995). By
contrast, a fish performing an escape behavior on land must grapple with the
novel challenges of weight and gravity and can produce thrust with only the
ventral surface of the body and tail. We noted two unusual aspects of
terrestrial escapes relative to aquatic escapes terrestrial escapes
require a long preparatory phase and acute posterior axial bending. We suggest
that these aspects of terrestrial escapes have evolved to allow effective
thrust production on land.
The long preparatory phase with a large degree of posterior axial bending
may facilitate the production of a jumping, or ballistic, behavior. Many
jumping tetrapods (and some invertebrates) are known to use `preloading' of
muscles during the preparatory phase to amplify power production during the
propulsive phase (Aerts, 1998).
During preloading, agonist muscles are activated by the nervous system but are
prevented from shortening by the activity of antagonist muscles. When the
agonists are allowed to contract (because antagonist activity is diminished),
preloaded muscles produce a powerful contraction because the series elastic
and contractile elements work in concert to shorten the muscle
(Pilarski et. al., 2002
). The
long preparatory phase of mudskipper terrestrial escapes may allow a similar
pre-loading of the axial muscles for ballistic propulsion, where muscles are
activated contra-laterally and power is amplified in the propulsive phase.
Additionally, the caudal fin must be placed close to the center of mass during the preparatory phase to lift the fish from the substrate during the propulsive phase. Placing the tail in this position requires a tight bending, or folding, of the body of the fish about a point approximately two-thirds of the way down the body. When the axial musculature straightens, it provides not only forward thrust (as in an aquatic escape response) but also the vertical thrust necessary to lift the center of mass off the ground. Again, this pattern of bending may be necessary to produce an effective ballistic movement on land.
The unusual pattern of bending observed in mudskippers also allows us to
evaluate previous hypotheses about potential morphological limitations on
axial bending in bony fishes. Brainerd and Patek
(1998) studied the relationship
between the number of vertebrae in the axial column and axial bending in
several reef fish species. They found that reef fish produce approximately
8° of bending at each intervertebral joint (i.e. the angle of bending
produced between two adjacent vertebrae), with only minor variation in this
value present among species or joints
(Brainerd and Patek, 1998
;
Jayne and Lauder, 1993
). They
suggested that increased axial bending is produced by increasing the number of
vertebrae, rather than the degree of bending at each joint. Therefore,
vertebral number should be a good predictor of axial flexion (because more
vertebrae will generate more flexion). For instance, elongate fishes produce
extreme axial flexion and form an `O' shape at the end of stage 1 with the
head and tail touching. This bending is produced by a large number of
intervertebral joints rather than acute bending at a small number of joints
(Westneat et al., 1998
).
Mudskippers have similar vertebral joint numbers to some of the fishes used in
the Brainerd and Patek (1998
)
study, and mudskipper aquatic escape responses demonstrate intervertebral
joint angles of approximately 8°. However, mudskipper terrestrial
responses had greater bending in some regions of the vertebral column (up to
20°) than predicted by Brainerd and Patek's model. Thus, data from the
terrestrial responses suggest that vertebral morphology is not what constrains
vertebral bending to 8°.
The maximum instantaneous power produced in a mudskipper jump was similar
to that reported for other poikilothermic vertebrates. The values were similar
to (although generally higher than) values reported for fish performing escape
responses in water, which range from 100 to 500 W kg-1
(Frith and Blake, 1995), and
similar to (although generally lower than) values reported for terrestrial
jumping anurans, which range from 200 to 1000 W kg-1
(Marsh and John-Alder, 1994
).
Although the whole-animal acceleration during the aquatic escape responses was
greater than that observed during terrestrial escape responses
(Table 1), a re-analysis of the
terrestrial escape responses, taking into account the effect of gravity,
revealed that the acceleration due to the axial myomeres was actually the same
in both environments. Thus, although the timing variables were quite
different, the performance measures of maximum acceleration and velocity in
the two different environments were not significantly different. Because
aquatic mudskippers must have some added mass due to water displacement and
adhesion/cohesion of water, we suggest that they actually produce more power
in the aquatic environment to reach the same maximum velocity.
It is interesting to consider the ecological implications of observed performance differences in aquatic and terrestrial escape behaviors. The aquatic escape rapidly accelerates the center of mass of the fish in a variable direction (but always away from the negative stimulus). The unpredictable nature of the resulting escape trajectory, and the speed of the response, should make it difficult for a predator to anticipate a fish's movements, or to overtake it. However, the high viscosity of the aquatic medium means that a fish must keep swimming to achieve significant displacement away from the predator (if it stops swimming, it will rapidly coast to a stop). The terrestrial escape response appears to employ a different strategy. It involves a substantially longer preparatory phase and tends to propel the fish in the same direction it was originally facing. However, because air has very low viscosity, a fish on land can use a single propulsive stroke to create a ballistic movement that will move it a great distance away from the potential predator.
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Acknowledgments |
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