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First published online December 16, 2008
Journal of Experimental Biology 212, 106-115 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.024448
Jumping strategies and performance in shore bugs (Hemiptera, Heteroptera, Saldidae)
Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
Author for correspondence (e-mail: mb135{at}hermes.cam.ac.uk)
Accepted 10 November 2008
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Summary |
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2.1 mg and are 3.5 mm long. The hind legs
that propel jumping are 180% longer than the front legs and 90% of body
length, but non-jumping species in the same family have longer hind legs
relative to the lengths of their bodies. Jumps were powered by large
trochanteral depressor muscles in the thorax in two different strategies. In
the first (used in 24% of jumps analysed), a jump was propelled by
simultaneous extension of the two hind legs powered by rapid depression
movements about the coxo-trochanteral joints, while both pairs of wings
remained closed. In the second strategy (74% of jumps), the wings were opened
before the hind legs began to move. At take-off, the position of the wings was
variable and could be 8–21 ms into either elevation or depression. When
the hind legs alone propelled a jump, the body was accelerated in
3.97±0.111 ms at a take-off angle of 52±6.5° to a take-off
velocity of 1.27±0.119 m s–1; when the wings also
moved, the body was accelerated in 3.86±0.055 ms at a take-off angle of
58±1.7° to a take-off velocity of 1.29±0.032 m
s–1. These values are not different in the two jumping
strategies. In its best jumps the take-off velocity reached 1.8 m
s–1 so that Saldula experienced an average
acceleration of 529 m s–2, equivalent to almost 54g, expended
3.4 µJ of energy, while exerting a force of 1.1 m N. The power requirements
for jumping indicate that a catapult mechanism must be used in which the
trochanteral depressor muscles contract and store energy in advance of a jump.
These jumps should propel it to a height of 105 mm or 30 times its body length
and distances of 320 mm. The two jumping strategies achieve the same jumping
performance.
Key words: kinematics, Heteroptera, locomotion
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INTRODUCTION |
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).
The wings can either start to move before take-off, or their movements are
delayed until take-off has been achieved
(Brackenbury and Wang, 1995;
Card and Dickinson, 2008;
Hammond and O'Shea, 2007;
Pond, 1972). The propulsion
for jumping in insects is typically provided by rapid movements of the legs,
or less often by movements of other parts of the body, all involving extensive
mechanical, muscular or neural specializations to accomplish this demanding
form of locomotion. Accomplished exponents, which propel jumping by rapid
movements of their hind legs, are found in the Siphonaptera, fleas
(Bennet-Clark and Lucey, 1967;
Rothschild and Schlein, 1975;
Rothschild et al., 1975;
Rothschild et al., 1972);
Orthoptera, bush crickets (Tettigonidae)
(Burrows and Morris, 2003) and
locusts (Acrididae) (Bennet-Clark,
1975; Godden,
1975; Heitler,
1977; Heitler and Burrows,
1977a; Heitler and Burrows,
1977b); Coleoptera, flea beetles (Alticinae)
(Brackenbury and Wang, 1995);
and Phasmatodea, stick insects (Burrows,
2008). By contrast, in the Collembola, springtails jump by rapidly
extending their terminal abdominal appendages
(Brackenbury and Hunt, 1993),
whereas movements of the whole abdomen are used in the Hymenoptera by some
ants (Baroni et al., 1994;
Tautz et al., 1994), in the
Phasmatodea by a stick insect (Burrows and
Morris, 2002) and in the Archaeognatha by Petrobius
(Evans, 1975). In the
Coleoptera, click beetles (Elateridae) move the prothorax against the
mesothorax (Evans, 1972;
Evans, 1973;
Kaschek, 1984), and in
Hymenoptera trap-jaw ants (Odontomachus) rapidly close their
mandibles against the ground, or an approaching object, to propel themselves
upwards or backwards (Patek et al.,
2006).
The ability of insects to jump reaches its zenith in the Auchenorrhyncha,
one of the four sub-orders of the Hemiptera, and in particular by members of
one of its numerous families, the Cercopidae. Froghoppers (spittle bugs) have
the best jumping performance of any insect described so far, accelerating
their bodies in less than 1 ms to a take-off velocity of 4.7
ms–1, experiencing a force of some 550 g
(Burrows, 2003;
Burrows, 2006a). This
outstanding performance is achieved by using a catapult mechanism in which
force is developed by the slow contraction of huge thoracic muscles and the
stored force is then released rapidly
(Burrows, 2007c). A second
family, the Cicadellidae or leafhoppers, are also accomplished jumpers
(Burrows, 2007a;
Burrows, 2007b) with one group
having long hind legs and another short hind legs although both achieve
comparable take-off velocities (Burrows
and Sutton, 2008), but which are considerably slower than those of
froghoppers. The other three sub-orders of the Hemiptera also contain
proficient jumpers. In the basal Coleorrhyncha at least one extant species
jumps (Burrows et al., 2007).
In a second sub-order, the Sternorrhyncha, one family, the pysllids or jumping
plant lice, are, as their colloquial name implies, well known for their
jumping but their performance is only currently being investigated (M.B.,
manuscript in preparation).
The fourth sub-order of hemipterans, the Heteroptera, contains a wide
diversity of bugs, but only two families have species that are reported to
jump. This paper analyses the jumping mechanisms of Saldula
saltatoria, a member of one of these families, the Saldidae
(Polhemus, 1985), which lives
on the muddy banks of freshwater and is known colloquially as a shore bug. Its
hind legs, which it uses to propel jumping are shorter than those of other,
supposedly non-jumping species in the same family, and have few
specialisations compared with froghoppers. Two distinct jumping strategies are
used. First, the hind legs are accelerated rapidly about the coxo-trochanteral
joints while the wings remained closed. Second, the same rapid movements of
the hind legs are used, but before they lose contact with the ground, the
wings are opened and begin to move in the wing beat cycle. This study
therefore investigated whether the early opening of the wings will increase
drag and therefore slow the take-off velocity, or can contribute power and
therefore increase the take-off velocity. Are jumping and flying co-ordinated
to achieve the highest take-off velocity or the most stable trajectory after
take-off? What therefore are the relative benefits of these two jumping
strategies?
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MATERIALS AND METHODS |
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) who commented
`Much hunting yields but few Saldas (= Saldula), and he who desires
to cultivate the virtue of patience, cannot do better than try a day's
Salda-hunting'. They belong to the order Hemiptera, sub-order Heteroptera and
to the family Saldidae. Sequential images of jumps were captured at rates of 5000 frames s–1 and with an exposure time of 0.05 ms with a Photron Fastcam 1024PCI high speed camera [Photron (Europe) Ltd, Marlow, Bucks., UK]. The images were fed directly to a laptop computer. The insects were manoeuvred with a fine paint brush into position in front of the camera pointing directly toward the middle of a chamber 80 mm wide, 80 mm tall and 10 mm deep at floor level and widening to 25 mm at the top. The floor, which was horizontal or a few degrees from the horizontal, was of high density foam. Within the chamber, Saldula was free to jump in any direction but the shape of the chamber meant that most jumps were in the image plane of the camera. Detailed measurements of changes in joint angles and distances moved were made from jumps that were parallel to the image plane of the camera, or as close as possible to this plane. Calculations show that jumps that deviate to either side of the image plane of the camera by ±30° would result only in a maximum error of 10% in the measurements of leg joint, or body angles. Sequences of images were analysed with Motionscope camera software (Redlake Imaging, Tucson, AZ, USA), to determine the position of points on the body or hind legs, or with Canvas X (ACD Systems of America, Miami, FL, USA) to determine angular changes. A point on the body that could be recognized in successive frames and was close to the centre of mass, as determined by balancing the insect on a pin, was selected for measurements of the velocity and trajectory of the body and is indicated in Fig. 7D. The time at which the hind legs lost contact with the ground and the insect became airborne was designated as t=0 ms so that different jumps could be compared and aligned. The time at which the hind legs started to move and propel the jump was also labelled and the time between these two events therefore defined the period over which the body was accelerated in a jump. Peak velocity was calculated as the distance moved in a rolling three point average of successive frames (a 0.6 ms moving time window). Acceleration was also measured from a rolling three point average during the acceleration period, with the peak value given in Table 3. Photographs and anatomical drawings were made from both live and preserved specimens. Data are based on 34 jumps by seven Saldula saltatoria recorded at 24°C. Seven museum (University Museum of Zoology, Cambridge, UK) specimens of each of the following five species of saldidids were measured to determine their leg and body lengths: Saldula littoralis (Linnaeus 1758), Saldula scotia (Curtis 1835), Saldula pallipes (Fabricius 1794), Saldula c-album (Fieber 1859) and Chiloxanthus pilosus (Fallen 1807). Measurements are given as means ± standard error of the mean (s.e.m.). Movies, captured at 5000 frames s–1 and with an exposure time of 0.05 ms, of a jump by Saldula with wings closed and of a jump with wings open are available as supplementary material Movie 1 and Movie 2, respectively.
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RESULTS |
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Structure of the legs
The front legs of Saldula were 1.8±0.08 mm long
(N=7), the middle legs 2.0±0.06 mm, and the hind legs
3.2±0.08 mm, so that the ratio of leg lengths was 1 front: 1.2 middle:
1.8 hind (Table 1). In total
the hind legs represented 89.6±3.26% of the body length whereas the
front and middle legs represented 50.3±3.32% and 58.2±3.24%
respectively. The longer hind legs resulted largely from their tibiae which at
1.6±0.02 mm (N=7) were 93% longer than the middle and 138%
longer than the front tibiae. By contrast, their femora were 1.0±0.04
mm (N=7) and only 25% longer than the middle and 46% longer than the
front femora. Expressed as the cube root of body mass, the hind legs have a
ratio of 2.5, similar to that of long-legged leafhoppers
(Burrows and Sutton,
2008).
The legs of S. saltatoria were compared with those of five other species within the family Saldidae that apparently do not jump but have a similar body shape and length (Table 1). The ratios of the lengths of the three pairs of legs were similar to those of S. saltatoria, but relative to the length of the body all had longer hind legs. This suggests that the length of the hind legs does not predict jumping ability.
Jumping was powered by the rapid and simultaneous depression of both hind legs about their coxo-trochanteral joints, with the large depressor muscles located in the thorax. Each hind coxa of S. saltatoria was large relative to the size of the metathorax (Fig. 1B, Fig. 2) and could rotate forwards and backwards through a small angle relative to a reference point on the mesothorax. The coxae of the two hind legs were apposed to each other at the midline (Fig. 2A). The ventral surface of a hind coxa was sculpted to accommodate the femur when the trochanter was levated and the hind leg was swung forward into its preparatory position for jumping (Fig. 2A,B).
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A hind trochanter pivoted with the coxa about a ventral
(Fig. 2) and a dorsal
articulation in which curved horns of the trochanter inserted into sockets on
the coxa. It could be levated (flexed) and depressed (extended) through an
angle of 140° in a plane approximately parallel with the underside of
the body. The large tendon of the trochanteral depressor muscle attached to
the medial rim of the trochanter. The main body of the depressor muscle was
located in the thorax and was large relative to the trochanteral levator
muscle, which was entirely within the coxa.
A hind femur could move through a small angle about the trochanter. Its
femoro-tibial joint showed no outward specialisations for jumping
(Fig. 2A). A hind tibia was
longer than the femur and had a semi-circular array of spines on its ventral
surface at the tibio-tarsal joint. A tibia could extend and flex through an
angle of 160–170° in the same plane as the levation and
depression movements of the trochanter about the coxa. A tarsus also had
arrays of spines pointing ventrally (Fig.
2A), which, like those at the tibio-tarsal joint, seem
appropriately placed to increase traction with the ground when jumping.
Jumping movements
Saldula used two strategies for jumping. In nine of the 34 jumps
analysed (26%), the wings remained closed and were not moved either before or
at take-off (Figs 3,
4), and in 25 jumps (74%) they
were opened before take-off and then flapped (Figs
5,
6). The jumping data (take-off
velocity, acceleration, take-off angle and body angle at take-off) from the
seven individuals were normally distributed and analysed using parametric
statistics.
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Jumping with wings closed
In this first strategy for jumping, the hind legs executed three distinct
phases of movement while the wings remained firmly closed and were not used
either during the launch into take-off in a jump or initially when airborne
(Figs 3,
4). The three phases of
movements by the hind legs were:
First, in preparation for a jump, the hind legs were drawn fully forwards by levation of their coxo-trochanteral joints so that the femora lay firmly pressed into the hollowed regions of the ventral coxae. The tibiae were also flexed about the femora but the two segments were not closely apposed to each other along their length. The result of these movements, which lasted up to a few hundred milliseconds, was that the tips of the tarsi of the two hind legs were placed on the ground just outside the lateral edges of the body and therefore did not touch each other (Fig. 4).
Second, the hind legs were held motionless in this fully levated position for periods up to 400 ms. During this time, movements of the front and middle legs adjusted the angle of the body relative to the ground and also changed the azimuth orientation of the body, thus determining the azimuth direction of the jump.
Third, the rapid jump movement itself resulted from a powerful depression of the coxo-trochanteral joints of both hind legs at the same time, and an accompanying extension of the femoro-tibial joints (Figs 3, 4). The movements of the coxo-trochanteral joints could most clearly be seen in the ventral views of the body (e.g. Fig. 4). No differences in the start of the movements of the two hind legs could be detected with the resolution (0.2 ms) available in these sequences captured at 5000 frames s–1. The movements will thus be called synchronous within this constraint of resolution. The time from the first movements of the hind legs until they lost contact with the ground at take-off, a period that defined the time over which the insect was accelerated in a jump, was 3.97±0.111 ms (N=9). During this period a trochanter progressively depressed at rotational rates of 25,000 deg s–1 with the result that the femur moved downwards and backwards relative to the body (the most obvious movement of the hind leg when viewed from the side, as in Fig. 3), and with the tibia also extending progressively. The continuing thrust generated by these movements moved the body forwards and raised it progressively from the ground. The consequence of the body being raised was that both the front and middle legs lost contact with the ground before the hind legs. During the latter part of the jump, propulsion could therefore only be provided by the hind legs. Even in the earlier part, the middle and front legs showed no consistent movements to suggest that they were providing much propulsive force. Take-off occurred when the coxo-trochanteral and femoro-tibial joints of the two hind legs were almost fully depressed and extended, respectively. After the tarsi had lost contact with the ground the momentum of the movements of these two joints resulted in the tibiae crossing beneath the abdomen (Fig. 4).
Jumping with wings open
The same sequence of movements of the hind legs also characterised this
second strategy for jumping, but it was preceded by opening movements of both
pairs of wings at variable times before take-off. The wings were first held
elevated and after a variable period were depressed and elevated in a flight
pattern which began 12.8±0.58 ms (range 8.4–21 ms; N=25)
before take-off (Figs 5,
6). By contrast, the time from
the first movement of the hind legs until the insect became airborne was
3.86±0.055 ms (N=25) and these movements were always
accompanied by a forward and upwards displacement of the body. To compare this
acceleration time with that in jumps when the wings were not moved, a single
sample t-test was used because the sample sizes for the two jumping
strategies was different (Table
2). Comparing the smaller sample of jumps when the wings were
closed with the mean of larger sample when wings were opened shows that times
are not different at the 5% level (t7=1.5,
P=0.177). There is thus no significant difference in the acceleration
times of Saldula when jumping with or without the contribution of
wing movements. At the point of take-off in different jumps, the wings were in
the depression (Fig. 5) or
elevation (Fig. 6A) phase of
the wing beat cycle and at different positions relative to the body in either
phase (Fig. 6B). This indicates
that there was no strict temporal relationship between the cycle of the wing
beat and the timing of the propulsive movements of the hind legs in a
jump.
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Jumping performance
Jumping using the first strategy in which propulsion is generated by the
hind legs while the wings remain closed, propelled Saldula to a
take-off velocity of 1.28±0.119 m s–1 (nine jumps by
four Saldula; Fig. 7A,
Table 2). In the second
strategy in which the wings were opened and moved, the take-off velocity
achieved was 1.29±0.032 m s–1 (25 jumps by the same
four Saldula) (Fig.
7B, Table 2). The
best performance in either strategy was a take-off velocity of 1.8
ms–1. The peak velocity was attained just before take-off but
was usually maintained for the few milliseconds that the insect remained in
the frame of the camera (Fig.
7A,B).
The take-off angle when the wings remained closed and the jump was powered only by leg movements was 52±6.5 degrees (N=9) and when wing movements were also used the take-off angle was 58±1.7degrees (N=25; Table 2). The attitude of the body relative to the ground was 47±4.7 degrees (N=9) when legs alone were moved compared to 54±2.6 degrees (N=25) when the wings were also moved. Using the same statistical test as used above in comparing the acceleration times, none of the parameters of the jumps in the two strategies differed significantly at the 5% level [take-off velocity (t6=0.962, P=0.373), take-off angle (t5=1.377, P=0.227) or body angle at take-off (t5=1.304, P=0.249)]. The initial trajectories of the jumps were also similar when either strategy was used (Fig. 7C,D), but would be expected to diverge because the wings should enable greater heights and distances to be achieved.
Jumping performance was calculated from the data obtained from the
high-speed images (Table 3).
The average acceleration over the whole of this period was 335 m
s–2 (average of 32 jumps with wings open or closed) rising to
529 m s–2 in its best jumps so that it would experience
forces up to 54 g. The energy required to achieve these
performances (mean or best) was 1.8–3.4 µJ, the power output was
0.5–1.0 mW and the force exerted was 0.7–1.1 mN. Assuming that, as
in froghoppers (Burrows,
2007c) the mass of the muscles generating propulsive movements of
the hind legs represents about 11% of body mass, then the power per mass of
muscle is 4500 W kg–1. This far exceeds the power that muscle
could produce by direct contraction
(Alexander, 1995;
Vogel, 2005b) and indicates
that contractions must begin before the jump with energy being stored and then
released suddenly.
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Performance relative to other jumping insects
Where does the jumping performance place Saldula among other
Hemipterans and amongst other insects that power jump by movements of the
legs. Saldula accelerates its body in 4 ms to a take-off velocity in
its best jumps of 1.8 m s–1. The acceleration of froghoppers
(Auchenorrhyncha, Cercopidae) is more than four times higher and the take-off
velocity (4.7 ms–1) 2.6 times greater. In long-legged
leafhoppers (Auchenorrhyncha, Cicadellidae), which like Saldula have
hind tibiae that are longer than the femora, the mean acceleration times range
from 4.4 to 6.4 ms. Saldula matches the best take-off velocities of
four species of cicadellids that range from 1.6 to 1.85 m
s–1, being bettered only by Aphrodes at 2.9 m
s–1 (Burrows,
2007b). Its performance also exceeds that of Hackeriella
(Coleorrhyncha, a sister sub-order to the Heteroptera), which has a mean
acceleration time of 2 ms and a best take-off velocity of 1.5 m
s–1 (Burrows et al.,
2007).
Compared with other insects, the acceleration time of Saldula is
longer than that of a flea (Siphonaptera) but its take-off velocity is higher
(Bennet-Clark and Lucey, 1967).
Its best take-off velocity is comparable to that achieved by flea beetles
(Coleoptera, Alticinae) (Brackenbury and
Wang, 1995) and many bush crickets (Orthoptera, Ensifera,
Tettigoniidae) (Burrows and Morris,
2003), but falls short of that achieved by heavier insects such as
the false stick insect Prosarthria teretrirostris (Orthoptera,
Caelifera, Proscopiidae) with a mass of 280 mg and which takes 30 ms of
acceleration to achieve a take-off velocity of 2.5 m s–1, and
1–2 g locusts (Orthoptera, Caelifera, Acrididae) which accelerate in
20–30 ms to a take-off velocity of 3.2 m s–1
(Bennet-Clark, 1975).
It was not possible to determine by direct observation the height and
distance achieved by jumps. A camera position (or particular lens) that
resolved the movements of the individual legs was not able to record the full
trajectory of the jump, or even its apogee. Similarly, a camera position that
recorded the complete trajectory failed to show whether the movements were
also influenced by flapping movements of the wings. An alternative method was
therefore to calculate, from standard equations (Eqns
1 and
2 below) for the motion of an
inert body (Alexander, 1968),
the distance and height achieved in a jump that did not involve wing
movements, and assuming there was no drag on the body:
 | (1) |
 | (2) |
is the
take-off angle and g is the acceleration due to gravity (9.81
m s–2).
Saldula should jump a distance of 170 mm and reach a height of 50
mm when there is no contribution from active wing movements when using its
mean take-off velocity of 1.3 m s–1 and its mean body angle
at take-off of 52°. These distances would rise to 320 mm and 105 mm,
respectively, if it used its best take-off velocity of 1.8 m
s–1. This indicates that Saldula could jump to a
height equivalent to 30 times its body length. On this measure it is again
outperformed by both froghoppers and fleas (both more than 100 times body
length), but almost matches the 40 times achieved by a short legged cicadellid
(Ulopa) of similar mass and length
(Burrows and Sutton, 2008).
These estimates for Saldula, however, take no account of the wind
resistance that is likely to be offered by a small body moving at such high
velocities. Vogel has estimated that the froghopper Philaenus which
has a mean mass of 12 mg and a mean length of 6.1 mm
(Burrows, 2006a) would lose
some 25% of its jumping range because of drag, a smaller flea beetle 40% and
an even smaller flea 80% (Vogel,
2005a). Given its size and mass a shore bug would thus be expected
to achieve only about half its calculated range.
Adaptations for jumping
Saldula has few specialisations for jumping particularly in
comparison with the most adept jumpers within its order, the Hemiptera. The
length of the hind legs themselves is not remarkable when compared with
non-jumping members of its family. Although the proportions of the three pairs
of legs are similar in both jumping and non-jumping species of this family,
the hind legs are shorter relative to the length of the body than those in the
non-jumping species. Saldula has hind legs that are 90% of the body
length and relative to the cube root of body mass, have a ratio of 2.5, close
to the value for long-legged leafhoppers
(Burrows and Sutton, 2008),
but greater than for froghoppers with proportionately shorter hind legs. The
length of the hind legs does not, however, influence take-off velocity when
jumping is powered by a catapult mechanism
(Burrows and Sutton, 2008).
Saldula requires a power output per mass of muscle of 4500 W
kg–1 to jump and this is unlikely to be generated by direct
muscle contractions acting on the long lever arms of the hind legs
(Alexander, 1995;
Vogel, 2005b). Instead the
implication is that the trochanteral muscles must contract slowly in advance
of the jump, store force, probably in skeletal structures, and then release it
suddenly in a catapult action. This is the strategy used by froghoppers
(Burrows, 2003;
Burrows, 2006a;
Burrows, 2006b;
Burrows, 2007c) and
leafhoppers (Burrows, 2007a;
Burrows, 2007b) and by some
other insects as diverse as fleas
(Bennet-Clark and Lucey, 1967)
and locusts (Bennet-Clark,
1975). The advantage of long legs may therefore lie in the lower
ground reaction forces exerted compared with insects that have shorter hind
legs, enabling them to jump effectively from the mud on which they live.
None of the structures found on the proximal joints of the hind legs of
members of two families of auchenorryhnchan bugs so far described and thought
to be specialisations for jumping, were found in Saldula. For
example, the two hind coxae although enlarged and apposed at the midline have
no linking structures similar to the fields of microtrichia in froghoppers
(Burrows, 2006b), or the
press-studs (poppers) in long-legged cicadellids
(Burrows, 2007a;
Emeljanov, 1987). They thus
more closely resemble the coxae of coleorrhynchans
(Burrows et al., 2007) or
short-legged cicadellids (Burrows and
Sutton, 2008). Similarly there are no obvious proprioceptors in
the same positions on the coxa as in either froghoppers
(Burrows, 2006b) or
cicadellids (Burrows, 2007a)
that could signal engagement of a femur with the hollowed ventral region of a
coxa, or movements of the coxa relative to the metathorax. This suggests that
the control of force in the build up to a jump is less critical than in their
relatives that achieve higher take-off velocities. Finally, there are no
structures like those in froghoppers
(Burrows, 2006b) which are
covered in microtrichia and restrain a femur against a coxa while the
trochanteral depressor muscles contracts to generate the force required for a
jump.
Strategies for jumping
Little information is available on the natural ecology of these insects to
suggest why they might jump. They live and forage for food on the exposed
surface of the muddy shores of fresh water ponds and other larger expanses of
fresh water. They feed by sucking out the contents of dead insects trapped in
the mud. This life style may thus expose them to predation by other animals
and in particular birds, from which their camouflaged colouration may provide
insufficient protection. A rapid jump that leads directly to flight may thus
be an important survival strategy. This is supported by the result presented
here that in almost three quarters of the jumps recorded, the wings were
opened and then elevated and depressed in the wing beat cycle before the hind
legs had lost contact with the ground and the insect become airborne. In the
remaining quarter of the jumps the hind legs alone were moved rapidly while
the wings remained firmed closed and covered the body. Neither strategy
produced a faster take-off so what advantage accrues from using one strategy
rather than the other?
Why use wing movements?
Are wing movements used to stabilize the body once airborne or to ensure a
smooth transition from jumping to flying? The bodies of many jumping insects
rotate about either the longitudinal or transverse axes (or sometimes even
both axes) once airborne following a jump. This means that they could
potentially lose energy because of these rotations and also increase the
probability that the jump will end in an uncontrolled landing. The
similarly-sized cicadellid Ulopa loses as much as 13% of its kinetic
energy to rotation as it spins with wings closed at frequencies up to 89 Hz
about the transverse and longitudinal axis of its body after take-off
(Burrows and Sutton,
2008).
Any improvement in stability from opening the wings will, however, be at
the potential expense of increased drag and thus diminished jump height and
distance which may be a costly solution if jumping to escape a predator.
Estimates of the drag likely to result when the wings of Saldula are
opened during take-off indicate that the deceleration would be only about a
tenth of the acceleration provided by the forces generated by the hind legs.
These estimates are made by assuming that the wings are elliptical plates of
known area moved at the maximum take-off velocity measured, through air with a
density of 1.3 kg m3. Because drag is proportional to the square of
velocity, it will be lower at the slower velocities at the start of a jump
when the body is being accelerated. Take-off velocity should not therefore be
reduced by the opening of the wings, as is observed, but stability could be
improved. The body of Saldula is flattened dorsoventrally and may
thus offer resistance to rotation, explaining why a jump with the wings closed
is also stable. Keeping the stiff front wings closed means that they help with
streamlining the body and the reducing drag. This presumably explains why some
insects, including the fastest and most powerful jumpers like froghoppers
(Burrows, 2003;
Burrows, 2006a), tolerate
rotation and a potentially unstable landing. In flea beetles, opening and then
moving the wings stabilises the body against spinning and results in better
targeting and a much higher proportion of jumps ending with a feet-first
landing (Brackenbury and Wang,
1995). For shore bugs, the body was stable and there were no
indications of rotation even when the wings remained closed over the first few
milliseconds of a jump that were available for analysis. Wing movements might,
however, provide more sustained stability later in the trajectory particularly
in the face of cross currents or turbulence.
The movements of the wings during the acceleration of the body in a jump
could provide a smoother and faster translation into flight. If the opening of
the wings were delayed until the insect were airborne, there could be two
impairments to performance. First, the forces experienced at the peak velocity
experienced at take-off might impede the opening the wings, particularly the
membranous hind wings. We know that the drag forces from the wings are small
relative to those exerted on the body by the legs, but we do not know how they
compare with the forces generated by the muscles moving the wings. Second,
opening the wings while airborne might impede the forward and upward momentum
of the jump with a potentially disastrous outcome if the movement is for
escape. The strategy observed in Saldula is to establish the flight
pattern before take-off and then have the jump lead to a smooth transition to
flight and maintenance of forward speed. Wing movements also commonly
accompany or even precede the leg movements of a jump in the small but
long-legged cicadellid Empoasca, but less frequently in larger
members of the same family (Burrows,
2007b). The wing movements of Empoasca, sometimes
preceded the leg movements of a jump, but the first depression movement began
only after take-off. In flea beetles, the downward movement of the wings is
said to be `exactly synchronised with hind-leg extension at take-off'
(Brackenbury and Wang, 1995)
and in mantids strong coupling between leg extensors and wing depressors is
inferred from single still images taken during take-off
(Brackenbury, 1990;
Brackenbury, 1991). A jump also
often launches an adult locust into flight with the wings generally opening
15-35 ms after take-off, but sometimes they open before this
(Camhi, 1969;
Pond, 1972). The implication
is therefore that there should be a close link between the interneurons
initiating and controlling flying and jumping, but few natural stimuli that
elicit jumping or kicking in locusts have been used to test this linkage.
Moreover, many jumps do not lead to flight. Recordings from locust flight
motor neurons show that their activity in a flight pattern is initiated at
variable times before or after the time that a kick (not a jump) by both hind
legs is released (Pearson et al.,
1986). The conclusion from intracellular recordings from
individual neurons is that those interneurons that trigger jumping are not
involved in initiating flying, but those that maintain the linkage between
these two movements remain to be identified. The lack of coupling between the
phase of the wing beat cycle and the release of the power developed by the
hind legs for jumping in both shore bugs and locusts suggests that there is
little aerodynamic advantage in linking the two motor patterns more closely;
it is sufficient that the pattern of wing movements is established around the
time of take-off when the jump is a launch into flight.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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