Jumping and kicking in the false stick insect Prosarthria teretrirostris: kinematics and motor control
1 Department of Zoology, University of Cambridge, Cambridge CB2 3EJ,
UK
2 Abteilung Neurobiologie, Universität Ulm, Ulm D-89069,
Germany
* e-mail: mb135{at}hermes.cam.ac.uk
Accepted 18 March 2002
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Summary |
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During jumping, the tibiae of the hind legs are extended in 30 ms with maximum rotational velocities of 11.5° per ms, but during kicking, when there is no body weight to support, extension is complete in 7 ms with rotational velocities as high as 48° per ms. The short time available to accelerate the body indicates that the movements are not powered by direct muscle contractions and that there must be storage of elastic energy in advance. The motor patterns responsible for generating the necessary forces in the hind legs for jumping and kicking are similar and consist of three phases; an initial flexion of the tibia is followed by a co-contraction of the small flexor and large extensor tibiae muscles lasting several hundred milliseconds while the tibia remains fully flexed. Finally, the flexor motor neurons stop spiking so that the tibia is able to extend rapidly. The small semi-lunar processes at the femoro-tibial joints are not distorted, so that they cannot act as energy stores. Some 7% of the energy is stored transiently by bending the thin tibiae during the initial acceleration phase of a jump and releasing it just before take-off.
The jumping and kicking mechanisms of Prosarthria teretrirostris have features in common with those used by locusts but also have their own characteristics. The evolution of jumping in Orthoptera is discussed in this context.
Key words: locust, motor neuron, motor pattern, joint mechanics, false stick insect, Prosarthria teretrirostris
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Introduction |
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Jumping height, however, is almost the same for small and large animals if
the same percentage of body mass is invested in the muscles used in jumping.
The jump of the tarsier is achieved by an investment of some 10% of body mass
in muscles used in jumping (Alexander,
1995) rather than the 4-5% invested by locusts
(Bennet-Clark, 1976
). In
insects, the overall design of the small body has resulted in mechanisms that
store elastic energy from muscle contraction in advance of the movement,
usually by the deformation of cuticular elements. To generate the high
acceleration needed for jumping, this stored elastic energy is then released
rapidly.
Locusts generate and store the 9-11 mJ of energy needed to accelerate their
body in 30 ms and achieve a take-off velocity of 3.2 m s-1 for a
jump that can displace them by as much as 1 m
(Bennet-Clark, 1975;
Brown, 1967
). Locusts have
evolved specific mechanisms that involve structural specialisations of the
hind legs and specialisations of the neural machinery in the central nervous
system that generates a detailed and appropriate sequence of muscle actions
(Burrows, 1995
;
Burrows and Morris, 2001
;
Godden, 1975
;
Heitler and Burrows, 1977a
).
In preparation for a jump, the tibiae are first flexed and fully apposed to
the femur, and the flexor and extensor muscles of the tibia then co-contract
(Heitler, 1974
;
Heitler and Burrows, 1977a
).
The energy from the co-contraction of the muscles is stored by bending the
spring-like semi-lunar processes at the femoro-tibial joint and in the
extensor tendon and femoral cuticle
(Bennet-Clark, 1975
). The
stored elastic energy is released when the flexor tibiae motor neurons are
inhibited rapidly, allowing the tibia to extend.
To determine whether these structural and neural specialisations for
jumping are a common evolutionary thread, we have analysed jumping and kicking
in an unusual orthopteran from South America. Prosarthria
teretrirostris walks slowly and shows freezing behaviour (thanatosis)
like a stick insect (Schultz,
1981; Wolf et al.,
2001
), thereby readily disguising itself amongst the vegetation
upon which it feeds. Like a locust, but unlike a stick insect, it jumps
powerfully for considerable distances and shows strong and rapid kicking
movements, which it uses to deter adversaries. We show that there are few
specialisations of the femoro-tibial joints in the large hind legs that
distinguish them from the front and middle legs, so that the joint mechanics
and the way energy is stored are different from those in a locust. These
insects, nevertheless, use the same motor patterns as locusts to generate the
jumping and kicking movements. As a member of the proscopiid family, P.
teretrirostris probably has relatively primitive jumping legs. Comparison
of the features of a P. teretrirostris hind leg with those of more
advanced and specialised jumping legs may illustrate a path the evolution of
the specialised jumping legs of grasshoppers and locusts could have taken.
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Materials and methods |
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A high-speed camera and associated computer (Red Lake Imaging, San Diego, CA, USA) enabled images of jumping and kicking movements to be captured at a frame rate of 1000 s-1 and with a shutter speed of 1/2000 s. Selected images were stored on a computer for later analysis with Motionscope (Red Lake Imaging) or with Canvas (Deneba Systems Inc, FL, USA) software. Jumps were performed by unrestrained insects and kicks by both free and restrained insects in which the hind femora were fixed in Plasticine but the tibiae and tarsi were free to move. Eleven jumps by three adult males at right angles to the optical axis of the camera were captured. With this orientation, the legs project laterally from the body at angles that change as the coxae are rotated at the joints with the thorax. This may lead to error in measurements of the absolute femoro-tibial angle, but the analysis of this joint concentrated on its angular changes during a jump. Eight kicks by four insects were also analysed in detail.
Body size and the proportions of legs were compared with those of locusts Schistocerca gregaria and stick insects Carausius morosus and Cuniculina impigra. The anatomy of the femoro-tibial joint was examined in intact insects, in legs preserved in 50% glycerol so that the joint was still moveable and in legs in which the cuticle was cleared by boiling in 5% potassium hydroxide. Drawings of the hind legs and the femoro-tibial joint were made with the aid of a drawing tube attached to a Zeiss stereo microscope. The centre of gravity was determined by suspending insects from a nylon filament attached first to the tip of the abdomen and then to the metathorax just behind the coxae of the hind legs. The intersection of these two lines projected beyond the nylon filaments (read from superimposed photographs) marked the centre of gravity.
Lever ratios of the flexor and extensor tibiae muscles were measured in freshly autotomized hind legs of females glued by the anterior surface of the femur to a vertical cork board so that the tibia was free to move at the femoro-tibial joint. The tibia could then be rotated in the vertical plane of the cork board, the axis of rotation of the femoro-tibial joint running perpendicular to the board in the horizontal plane. The flexor and extensor tendons were exposed by opening the posterior surface of the femur, and one tendon was then clamped to a force transducer. The measurements were then repeated with the other tendon. The transducer was mounted on a small micromanipulator that allowed fine adjustment of the tension exerted on a tendon. This whole apparatus could be rotated in the vertical plane around the axis of the femoro-tibial joint. Weights of 1 or 1.5 g were attached to the tibia 10 mm from the femoro-tibial joint with a nylon filament. When the extensor tendon was attached to the transducer, the weight was suspended from the ventral side of the tibia to exert a flexion force; when the flexor tendon was attached, the weight was suspended from the dorsal surface to exert an extension force. By adjusting the force applied to the flexor or extensor tendon, respectively, the tibia was maintained in a horizontal position. The femur and attached force transducer were rotated through the whole range of femoro-tibial joint angles, and the force applied to a tendon to keep the tibia horizontal was determined.
To record the activity of the muscles during jumping and kicking, pairs of
stainless-steel wires 50 µm in diameter, insulated but for their tips, were
inserted into the extensor and flexor tibiae muscles of one hind leg. The
wires were waxed to the dorsal thorax and suspended from the roof of a Faraday
cage in which the insect was free to move. Movements of the right hind leg
were monitored by attaching to the proximal end of the tibia, a small piece of
foil that reflected a light beam focused onto a position-sensitive diode
(von Helversen and Elsner,
1977). Muscle activity and the movement recordings were digitised
at 5 kHz (Cambridge Electronic Design, 1401) and written to CDs for later
analysis with Cambridge Electronic Design Spike2 software.
Significance levels between measurement samples were assessed using the U-test after Wilcoxon, Mann and Whitney (significance level 5 %); data are given as mean values ± standard errors of the mean (S.E.M.).
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Results |
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The feature common to both jumping and kicking movements was the rapid extension of the tibiae of the hind legs. During jumping, both tibiae were extended at the same time, and the posture of the body was adjusted to give an appropriate take-off angle. It is important that the centre of gravity is just behind the hind-leg coxae, where the force exerted by the legs accelerates the body. This allowed the take-off angle to be adjusted appropriately by changes in body posture but avoided destabilisation as the body was accelerated. Kicking typically involved the movement of just one hind leg, although on occasion both were used. The hind leg(s) was rotated at the joint with the body so that the kick was aimed at its target.
Jumping performance
The most powerful jumps were completed in 30±2.1 ms (N=11)
measured from the time when the joints of the hind legs first began to move
until the insect became airborne (Fig.
2). Different jumps by the same insect took different times to
complete and propelled it different distances. The highest takeoff velocity
was 2.5 m s-1, with the body being accelerated at up to 165 m
s-2 for 30 ms or less, and the take-off angle, measured from the
centre of gravity, ranged from 20 to 50° (mean 40.7°, N=11).
It requires 850 µJ of energy to lift the body with a mass of 0.28 g
(Table 1) off the ground with
this velocity.
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Males jumped an average horizontal distance of 66±6.7 cm (N=5), reaching a height of 13-15 cm. The longest jump we observed was 90 cm. The larger and heavier females jumped shorter distances, averaging 49±8.4 cm (N=7). These values are close to those calculated assuming non-ballistic conditions with no air resistance or aerodynamic effects of the body. With a take-off velocity of 2.5 m s-1 and a take-off angle of 40°, a male would be predicted to jump a distance of 63 cm and to a height of 13 cm.
In preparation for a jump, the tibiae of the hind legs were flexed to their maximum extent about the femur, but the curved tibiae could not be apposed to the femora along their length (Fig. 2A). The coxae were also rotated forward so that the femora were pointing upwards at an angle of 90° to the body. The tibiae of the hind legs then started to extend at the same time as their coxae were depressed, so that the net effect was to raise the body higher from the ground. The continuing depression of the coxae resulted in the further elevation of the body so that, eventually, the two femora of the hind legs were below the body. Similarly, the continuing extension of the two tibiae both elevated the body and moved it forwards. The same joints in the front and middle legs also underwent similar movements, resulting first in the tarsi of the front pair of legs and then, approximately 5 ms before take-off, the tarsi of the middle legs leaving the ground. When the tibiae of the hind legs reached full extension, the insect became airborne. The tibia moved about the femur with a peak rotational velocity of 11.5° per ms.
Considerable bending of the hind-leg tibiae occurred during the acceleration phase of the jump. As the body was raised, the tibiae bent progressively so that they were maximally bowed when the femora were parallel with the ground. The bowing was quantified as the radius of curvature of the tibia, which decreased from its natural value of 41 to 25 mm in this example of a male jumping, and by the distance between the centre of the tibia and a line (chord) linking the femoro-tibial and tibio-tarsal joints. This doubled from its natural value of 1.7 mm to a maximum of 3.5 mm (Fig. 2B). As the tibiae were progressively extended, the bowing progressively diminished so that, at the point when the tarsi left the ground, the tibiae were almost straight (the radius of curvature was 96 mm and the distance as above was now only 0.6 mm). Once the insect was airborne and the hind legs were no longer bearing any load, the tibiae resumed their natural bowed shape. The force acting on each hind leg to bend a tibia in this way, estimated from the acceleration of the body mass during a jump, was approximately 23 mN.
The spring constants (Young's modulus) for a tibia at moderate static deformation were measured to estimate the larger transient deformations observed in normal jumping. Force was applied to a tibia of five males, and the amount of bending was measured. The speed of bending and recovery was critical because, when the force was applied more slowly than observed in the high-speed images, the tibiae showed gradual (semi-) plastic deformation well before the amount of bending observed during jumping was reached. The change, however, fully reversed within minutes of the force being released. Experiments with transient bending at rates and for periods of approximately 100 ms, similar to those observed during jumping, showed that elastic deformation was possible. The measured spring constants were approximately 20 mN mm-1 for axial compression (along the chord indicated in Fig. 2B, although bending perpendicular to this axis yielded similar results). With a typical amount of bending of 1.8 mm observed in jumping which corresponds to an axial compression of approximately 1.2 mm the elastic energy stored in one tibia was approximately 29 µJ. The elastic energy stored in the bent tibiae of both hind legs will, therefore, be approximately 7% of the total kinetic energy requirement for a jump.
Kicking performance
Kicks by an individual hind leg occurred when the tarsus was lifted from
the ground and aim was directed by rotation of the leg at the coxa. In
restrained insects with no external load to work against, the extension
movements of a tibia were very rapid (Fig.
3). The fastest full extension was achieved in 7 ms (mean 8 ms,
N=7, range 7-11 ms), with maximum velocities of tibial rotation more
than four times higher than during jumping at 48° per ms. The velocity and
consequent inertial forces were sufficiently high that the tibia was
over-extended at its extreme position and rebounded, often through several
cycles of progressively slower and smaller flexion and extension movements.
Close-up images of the femoro-tibial joint showed no bending of the semi-lunar
processes either preceding or accompanying tibial extension. Similarly, no
distortions in the cuticle of the femur or tibia around the femoro-tibial
joint were observed.
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The femur of a hind leg was oval in cross section and not hexagonal like that of a locust. At its proximal end, where it contains the main bodies of the extensor and flexor tibiae muscles, the femur of females measured 2.2±0.09 mm (N=5) in the dorso-ventral axis (males 1.5±0.03 mm, N=7), but narrowed distally, where it contains only muscle tendons, tracheae and branches of nerve 5, to 1.0±0.06 mm (males 0.6±0.02). The most distal fibres of the main body of the extensor muscle of a female inserted some 13 mm short of the femoro-tibial joint, with only the few fibres of the accessory extensor muscle closer to the joint. The extensor tibiae muscle in females had a mass of 22.7±3.0 mg (N=6) and in males a mass of 7.7±0.17 mg (N=4). The flexor tibiae muscles were smaller, with a mass of 5.2±0.4 mg in females and 1.6±0.2 mg in males. The maximal cross-sectional area of the extensor tibiae muscle was approximately 3.3 mm2 in females and 0.9 mm2 in males.
The tibia was thin, with a diameter of 0.8±0.01 mm (N=5), in adult females (males, 0.5±0.02, N=7). In females, it was 34.8±0.6 mm long (N=18) and in males 26±0.3 mm (N=11) so that in both it was some 2 mm longer than the femur. The tibia was bowed so, when the insect was standing, the convex surface was lateral. In females, the radius of curvature of the tibia was 52±0.2 mm (N=16) and in males 41±0.2 mm (N=14).
The tibia could move about the femur by some 140° from a minimum flexed
angle of 30-35° to a maximum extended angle of approximately 170°
although, at the end of a kick, over-extension by a further 10-20° often
occurred. Externally, the femoro-tibial joint is characterised by thin,
recessed semi-lunar processes, two black spines on the distal dorsal rim of
femur and a sculptured anterior coverplate
(Fig. 4). The semi-lunar
processes, one on the anterior and one on the posterior face of the femur, are
set in deep grooves and are only some 0.07 mm wide and 0.9 mm long
(Fig. 4A). The articulation of
the femur with the tibia is very similar to that of a locust hind leg
(Burrows and Morris, 2001). The
most distal ends of both semi-lunar processes turn inwards, and each has flat
distal edges that form the femoral half of the hinge joint with the tibia
(Fig. 4C). Ventral to the
semi-lunar processes, the lateral and medial walls of the femur bulge outwards
to form cavities into which the lateral and medial projections, or horns, of
the tibia respectively locate (Fig.
4A). The anterior coverplate is sculptured so that the anterior of
the two horns of the tibia is visible as it rotates in the bulge of the femur,
but covers the ventral part of the tibia when it is fully flexed. The proximal
part of the tibia consists of two flat edges that hinge with the flat edges of
the inward projections of the femoral semi-lunar processes
(Fig. 4A,C) and are held
together with tough membrane. On the proximal ventral tibia are two rows of
hairs each containing 5-6 short and prominent hairs
(Fig. 4A,B) that are deflected
by contact with the ventral femur when the joint is fully flexed.
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Lever arms of hind-leg flexor and extensor tibiae muscles
To estimate the forces that muscles could exert the throughout the range of
femoro-tibial joint positions of a hind leg, the lever arms of the flexor and
extensor tibiae muscles were analysed in two ways.
First, lever arms were determined from scale drawings of hind legs (Fig. 5A,B) dissected to reveal the attachment sites of the muscle tendons. At extended joint angles, the extensor muscle has a much larger lever than the flexor muscle because it attaches to the tibia at a position that is dorsal and proximal relative to the pivot of the joint. The flexor tendon runs almost through the pivot because of its ventral and more distal attachment to the tibia. At flexed joint angles, by contrast, the flexor tendon has a larger lever arm than the extensor because its tendon runs over, and is deflected by, the cuticular invagination, or lump, in the distal ventral femur (Figs 4B, 5B). In this way, the flexor tendon pulls on the tibia at angles close to 90° when the tibia is flexed. At the most flexed joint angles into which the tibia can be forced, the flexor and extensor tendons run close to each other over the femoral lump so that the extensor tendon crosses the axis of rotation and, therefore, goes over centre.
Determining lever arms from morphological inspection does not take into account that both flexor and extensor tendons attach as membranous and highly flexible structures to U-shaped sclerotised rims on the tibia (Figs 4A,B, 5A). The effective attachment site to which force is applied may therefore vary with femoro-tibial angle. For example, when the joint was extended, the extensor tendon seemed to pull mainly at the base of the U-shaped attachment; when it was flexed, the primary force appeared to be exerted on the two tips. This means that, when the joint was flexed, the effective point of attachment for the extensor moved into a more proximal (ventral) position on the tibia (compared with Fig. 5B) and that the extensor tendon did not cross the axis of rotation. Furthermore, in a morphological analysis, it remains unresolved whether the extreme joint positions are ever attained in natural movements. Indeed, our high-speed images of natural jumping and kicking movements showed that the tibia did not flex to angles of less than 35-40°. For both these reasons, it is doubtful that, in normal usage, the extensor acts over centre.
The second method of analysis was to simulate the forces acting on the joint by replacing the flexor and extensor muscles with weights and force transducers. This allowed the lever arms of the two muscles to be determined directly by measuring the forces needed at the two tendons to balance the joint in different positions (Fig. 5C). The lever arms of the two muscles were equal at a joint angle of 55°. If balanced and constant loads were applied to the two tendons at this angle, the tibia extended further when moved beyond 55° and flexed further below 55°. The extensor muscle showed consistently larger lever arms in the force measurements compared with the morphometric measurements. This indicates that the morphological identification of the attachment site of the extensor tendon was not appropriate in functional terms. The effective attachment point appeared to be located more proximally on the tibia so that the extensor tendon did not cross the axis of rotation of the joint even in the most flexed joint position. Similarly, the force measurements indicate that the morphometric data underestimate the flexor lever in extended leg positions and overestimate it in flexed positions. This again suggests a shift in the effective site at which force is applied to the distributed attachment on the U-shaped rim of the tibia.
Muscle activity during jumping and kicking
To understand how the muscles generate the necessary forces during jumping
and kicking, myograms were recorded from one hind leg and related to the
movements of the tibia of that leg. The motor patterns and muscle actions that
underlie jumping and kicking had the following features in common
(Fig. 6A,B).
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First, the flexor tibiae motor neurons spiked so that the resulting contraction of the flexor tibiae muscle pulled the tibia into its most flexed position. Second, the extensor and flexor tibiae muscles then co-contracted. In some electrode placements, it seemed as if additional flexor motor neurons were active from those that initially flexed the leg. In the 29 kicks analysed, the duration of the co-contraction averaged 416 ms (range 220-1003 ms), and in the 19 jumps the average was 333 ms (range 147-585 ms). The prominent feature of recordings from the extensor tibiae muscle were the large potentials resulting from spikes in a single motor neuron presumed to be the fast extensor tibiae motor neuron. During kicks, there were an average of 24 of these spikes (range 12-56, N=29) and during jumps there were 19 (range 12-23, N=19) at a mean frequency of almost 60 Hz. The differences in the number of spikes during kicks appeared to correlate with the power and speed of tibial extension and during jumps with the distance that the body was propelled. The large muscle potentials showed a marked decrement in amplitude as the co-contraction progressed. This could be caused by a frequency-dependent change in neuromuscular transmission or by the powerful contraction moving the electrodes.
Third, activity in the flexor muscle stopped on average 20 ms before a tibial movement could be detected during a kick or a jump. Spikes in the extensor continued after those in the flexor ended, but also stopped before the rapid extension of the tibia began. At the end of a kick or a jump, the flexor muscle was active, often with a low level of co-activity in the extensor, so that the tibia was moved slowly to a more flexed position.
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Discussion |
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Comparison with locust jumping
The jumping performances of P. teretrirostris and locusts are
similar but, because the locust has to propel a much heavier body, it needs to
generate much higher forces. During jumping, locusts extend the tibiae of
their hind legs fully in 20-30 ms (Brown,
1967) to achieve take-off velocities of 3.1 m s-1
(Bennet-Clark, 1975
), while
P. teretrirostris takes 30 ms to extend its hind legs and reaches
take-off velocities of 2.5 m s-1. These data fit with the energy
requirements of the jump, which are almost 1 mJ in a male P.
teretrirostris with a body mass of 280 mg, and almost 10 mJ in a male
locust with a mass of 1.6 g. Similarly, there is much overlap in the kicking
performances of the two species, but the fastest kick observed in a locust
took only 3 ms with the tibia rotated at a maximum rate of 80° per ms
(Burrows and Morris, 2001
),
whereas the fastest kick in P. teretrirostris took 7 ms during which
the tibia achieved maximal rotational velocities of 48° per ms.
This similarity in jumping performance results from the investment by both
species of a similar muscle mass relative to body mass for use in jumping; the
muscles used by P. teretrirostris in jumping account for 4-6 % of the
body mass and in the locust 4-5 %
(Bennet-Clark, 1976). This will
allow similar jumping performance in animals of similar size, regardless of
whether the jump is directly powered by muscle contractions or muscle energy
is stored as elastic energy (with similar efficiency). Even animals of
different mass will produce jumps of comparable absolute size because the
mechanical energy delivered by a muscle scales almost linearly with muscle
mass (Bennet-Clark, 1976
) and,
thus, with body mass if similar proportions of body muscle are used for
jumping.
A more detailed comparison of data from P. teretrirostris with
that from the locust (Bennet-Clark,
1975) suggests that the properties of the muscles used in jumping
are similar in the two species. The extensor tibiae muscle in male P.
teretrirostris has a mass of approximately 8 mg, and the energy generated
by a slow contraction of these muscles in the two hind legs in preparation for
a jump should amount to some 1.2 mJ, by extrapolation from the 75 mJ
g-1 measured in the locust extensor tibiae. This agrees with the
maximum energy content of almost 1 mJ calculated from the jumping performance
of P. teretrirostris and indicates an efficiency of approximately 70
% for the transformation of muscle energy into kinetic energy of the jump,
including intermediate elastic energy storage. The maximal cross-sectional
area of the extensor tibiae muscle was some 0.9 mm2 in male P.
teretrirostris, which should thus be able to generate forces of
approximately 0.7 N per leg. In the locust, the whole muscle has a
cross-sectional area of 16-17 mm2 and can generate 15 N, or 0.8 N
mm-2. The maximum lever of the extensor tibiae muscle of P.
teretrirostris (Fig. 5C)
is 0.04 times tibia length, and this again agrees with the force requirements
calculated from the maximum acceleration of 165 m s-2 measured
during a jump, amounting to approximately 0.6 N per leg.
It is clear from the above comparison that P. teretrirostris, much
like the locust, has to store elastic energy to generate the brief (but high)
acceleration necessary for the jump. The main reason that stored elastic
energy is required is the short time available for acceleration before
take-off. Tibial extension is complete within 30 ms, yet the extensor tibiae
muscle of the locust needs a few hundred milliseconds to develop peak force
and a minimum of 59 ms to reach peak twitch force
(Cochrane et al., 1972). The
mechanisms used by the locust and P. teretrirostris to transform
muscle energy into the kinetic energy of a jump or a kick and thereby achieve
the comparable performances show many similarities. There are, however,
notable differences.
First, in proportion to body mass but not body length, the hind legs of P. teretrirostris are much longer than those of locusts; in the lighter males, they are proportionately eight times longer, and even for the heavier females they are twice as long. The longer legs allow (lower) acceleration over a longer distance and thus require the generation of proportionately less muscular force. They also require a less sturdy construction of the femoral cuticle. Heavier locusts, therefore, require additional specialisations for jumping; stronger muscles, sturdier cuticle and additional stores for muscle energy to achieve higher acceleration.
Second, in the locust, the tibia of a hind leg, but not of a middle or a front leg, can be flexed fully about the femur so that the two are closely apposed along their length in a groove on the ventral wall of the femur. In P. teretrirostris, the hind leg is similar to the other legs in that it cannot be fully apposed to the femur. The most flexed angle that the tibia was observed to achieve during natural jumping or kicking was 35°. This is in part due to the marked curvature of the tibia and in part because, if the joint were flexed further, the lever arm of the extensor tibiae muscle would go over centre. Instead, the lever arms of the flexor and extensor muscles are such that, at the most flexed angles, that of the extensor is close to zero while that of the flexor is maximal, and at 55° they are balanced. The lever arms then reverse so that, at angles of 90-130°, the extensor lever arm is maximal and that of the flexor is close to zero.
Third, in the locust, the structure of the femoro-tibial joint of a hind
leg is dominated by the presence of large semi-lunar processes that are bent
during a jump or a kick and are estimated to provide almost half the energy
storage for these movements (Bennet-Clark,
1975). By contrast, the semi-lunar processes in P.
teretrirostris are small, and high-speed images show that neither they
nor the distal part of the femur are noticeably distorted during kicking, so
that they cannot act as an energy store. Instead, we assume that most of the
energy is stored in the tendon of the extensor tibiae muscle, in the muscle
itself and in the femoral cuticle. The smaller mass of P.
teretrirostris and the proportionately longer legs mean that less elastic
energy storage is required to provide the acceleration for a jump.
Fourth, in the locust, the lump
(Heitler, 1974) protrudes into
the distal femur for 40 % of the diameter of the femur, but in P.
teretrirostris it extends for only 15 %. In the locust, the flexor tendon
forms a pouch that fits over the lump when the tibiae is fully flexed and
locks it in this position as long as the flexor continues to contract. It is
only when the flexor muscle relaxes and releases the pouch from the lump that
the tibia can extend. In P. teretrirostris, the consequence of having
only a small lump is that the angle of the flexor tendon is altered less at
extreme flexed angles of the joint, and it is probably less effective in
locking the flexor tendon. The ability of the small flexor to restrain the
action of the larger extensor tibiae muscle during the co-contraction phase
must, therefore, depend more on the respective lever ratios determined by the
anatomy of the joint than on the locking mechanism provided by the femoral
lump.
Despite these differences in the structure and operation of the
femoro-tibial joint, the motor pattern that produces a jump or a kick is
strikingly similar in the locust and P. teretrirostris. In both, it
consists of three phases: first, an initial flexion brings the tibia close to
its maximally flexed position; second, a cocontraction of flexor and extensor
tibiae muscles, that can last several hundred milliseconds, allows the force
generated by the extensor tibiae muscle to be built up slowly and stored;
third, the spikes in the flexor motor neurons stop abruptly so that the flexor
muscle relaxes, allowing the stored force to be delivered rapidly. By
contrast, most crickets kick but do not jump, powered by brief contractions of
the extensor tibiae muscle and not by long periods of co-contraction
(Hustert and Gnatzy,
1995).
Evolution of jumping legs
Does the design of the hind legs of P. teretrirostris represent an
ancestral design of orthopteran jumping legs, intermediate between a normal
walking leg and the specialised jumping leg of locusts and grasshoppers?
Alternatively, does this convergent evolution represent two solutions derived
from a more primitive design that has emerged to generate similar
behaviour?
The close resemblance between the structure of all P. teretrirostris legs is striking, particularly in the structure of the femoro-tibial joints, contrasting strongly with the evident specialisation of the hind legs in locusts.
Most notable are: first, semi-lunar processes that are small, with only the hinge area sclerotised; second, the structure of the hinge itself; and, third the structure of the attachment sites of the flexor and extensor tendons. The main specialisations of the hind leg for jumping include: first, a ventral lump in the femur that alters the lever ratio of the flexor muscle at flexed joint angles; second, increased femoral and tibial lengths; third, a larger muscle mass; and, fourth, a more sturdy structure.
Locusts and grasshoppers have carried hind-leg specializations for jumping much further, particularly with regard to heavy sclerotisation of the semi-lunar processes and their use in elastic energy storage, stronger cuticle and sclerotisation of several other parts of the leg, the hexagonal cross section of the femur, a more pronounced ventral lump in the femur and a pouch in the flexor tendon, which locks over that lump.
Even if the main features of P. teretrirostris jumping legs do not represent ancestral traits (i.e. they are symplesiomorphic for the saltatoria), they may illustrate how the ability to jump evolved gradually in the saltatoria and without the need for ad hoc invention of qualitatively new characters. It is possible that the features that enabled jumping evolved gradually with only small proportional changes in different parts of the walking legs. For example, the basic features of angle-dependence of the lever arms at the femoro-tibial joint, which are important for co-contraction, and elastic energy storage are already present in a walking leg. Likewise, the specialised locust hind legs may have evolved from hind legs like those of P. teretrirostris through small and gradual changes. Even novel characteristics such as the pouch in the flexor tendon fit into this scheme. A small pouch, originating from the softer central part of the splaying flexor tendon, would confer the advantage of increased friction during co-contraction. Any further increase in pouch size would increase this advantage, allowing a gradual transition to the pouch with locking function seen in the locust.
The fossil record suggests that P. teretrirostris hind legs
represent primitive jumping legs in the sense outlined above. More basic
extinct groups of orthopterans such as the Oedischidae and Tcholmanvissidae
all appear to have had hind legs that are similar to those of present-day
proscopiids (Sharov, 1961).
The Jurassic Locustopsis germari (Locustopsidae) was more
locust-like, with well-developed and compact jumping legs, although some other
species of that group (Sharov,
1961
) also had proscopiid-like hind legs. Final assessment must
await further completion of the fossil record, since there are no records of
fossil proscopiids, or progress in the molecular approaches to resolve details
of the relationships between the orthopteran groups
(Flook et al., 1999
).
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Alexander, R. McN. (1995). Leg design and jumping technique for humans, other vertebrates and insects. Phil. Trans. R. Soc. Lond. B 347,235 -248.[Medline]
Bennet-Clark, H. C. (1975). The energetics of the jump of the locust Schistocerca gregaria. J. Exp. Biol. 63,53 -83.[Abstract]
Bennet-Clark, H. C. (1976). Energy storage in jumping insects. In Insect Integument (ed. H. R. Hepburn), pp. 421-442. Amsterdam, Oxford, New York: Elsevier Scientific Publishing Company.
Bennet-Clark, H. C. and Lucey, E. C. A. (1967). The jump of the flea: a study of the energetics and a model of the mechanism. J. Exp. Biol. 47,59 -76.[Medline]
Brackenbury, J. and Hunt, H. (1993). Jumping in springtails: mechanism and dynamics. J. Zool., Lond. 229,217 -236.
Brown, R. H. J. (1967). The mechanism of locust jumping. Nature 214,939 .[Medline]
Brunner von Wattenwyl, C. (1890). Monographie der Proscopiiden. Vh. Zool. Bot. Ges. Wien 40, 87-123.
Burrows, M. (1995). Motor patterns during kicking movements in the locust. J. Comp. Physiol. A 176,289 -305.[Medline]
Burrows, M. and Morris, G. (2001). The
kinematics and neural control of high-speed kicking movements in the locust.
J. Exp. Biol. 204,3471
-3481.
Cochrane, D. G., Elder, H. Y. and Usherwood, P. N. R. (1972). Physiology and ultrastructure of phasic and tonic skeletal muscle fibres in the locust, Schistocerca gregaria. J. Cell Sci. 10,419 -441.[Medline]
Dirsh, V. M. (1961). A preliminary revision of the families and subfamilies of Acridoidea (Orthoptera, Insecta). Bull. Br. Mus 10,349 -419.
Evans, M. E. G. (1972). The jump of the click beetle (Coleoptera: Elateridae) a preliminary study. J. Zool., Lond. 167,319 -336.
Evans, M. E. G. (1973). The jump of the click beetle (Coleoptera, Elateridae) energetics and mechanics. J. Zool., Lond. 169,181 -194.
Flook, P. K., Klee, S. and Rowell, C. H. F. (1999). Combined molecular phylogenetic analysis of the Orthoptera (Arthropoda, Insecta) and implications for their higher systematics. Syst. Biol. 48,233 -253.[Medline]
Godden, D. H. (1975). The neural basis for locust jumping. Comp. Biochem. Physiol. 51A,351 -360.
Grzimeks, B. (1979). Grzimeks Tierleben, vol. 12, Saugetiere 3. München, Germany: Deutscher Taschenbuch Verlag.
Hall-Craggs, E. C. B. (1965). An analysis of the jump of the Lesser Galago (Galago senegalensis). J. Zool., Lond. 147,20 -29.
Heitler, W. J. (1974). The locust jump. Specialisations of the metathoracic femoraltibial joint. J. Comp. Physiol. 89,93 -104.
Heitler, W. J. (1977). The locust jump. III. Structural specializations of the metathoracic tibiae. J. Exp. Biol. 67,29 -36.
Heitler, W. J. and Burrows, M. (1977a). The locust jump. I. The motor programme. J. Exp. Biol. 66,203 -219.[Abstract]
Heitler, W. J. and Burrows, M. (1977b). The locust jump. II. Neural circuits of the motor programme. J. Exp. Biol. 66,221 -241.[Abstract]
Hustert, R. and Gnatzy, W. (1995). The motor
program for defensive kicking in crickets: performance and neural control.
J. Exp. Biol. 198,1275
-1283.
Maitland, D. P. (1992). Locomotion by jumping in the Mediterranean fruitfly larva Ceratitis capitata.Nature 355,159 -161.
Rothschild, M., Schlein, Y., Parker, K. and Sternberg, S. (1972). Jump of the oriental rat flea Xenopsylla cheopsis (Roths). Nature 239, 45-47.
Schultz, J. (1981). Adaptive changes in antipredator behaviour of a grasshopper during development. Evolution 35,175 -179.
Sharov, A. G. (1961). Phylogeny of the Orthopteroidea. Trans. Inst. Palaeontology (Akad. Nauk. SSR). Trudy Paleontologischeskogo Instituta (Israel Program of Scientific Translations, 1971) 118,1 -251.
von Helversen, O. and Elsner, N. (1977). The stridulatory movements of acridid grasshoppers recorded with an opto-electronic device. J. Comp. Physiol. A 122, 53-64.
Wolf, H., Bassler, U., Speil, R. and Kittmann, R.
(2001). The femurtibia control system in a proscopiid
(Caelifera, Orthoptera): a test for assumptions on the functional basis and
evolution of twig mimesis in stick insects. J. Exp.
Biol. 204,3815
-3828.
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