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First published online October 5, 2007
Journal of Experimental Biology 210, 3590-3600 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.009100
Anatomy of the hind legs and actions of their muscles during jumping in leafhopper insects
Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
e-mail: mb135{at}hermes.cam.ac.uk
Accepted 30 July 2007
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Key words: kinematics, muscle, motor pattern
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). These
movements of the hind legs accelerate the body in an average of 5–6 ms
to a peak take-off velocity of 1.1–16 m s–1, though in
the best jumps the performance can be considerably better with the
acceleration lasting less than 3 ms and the take-off velocity reaching 2.9 m
s–1. The jumping performance is, however, less than that of
their close relatives the froghoppers (Hemiptera, Auchenorrhyncha, Cercopidae)
(Burrows, 2003;
Burrows, 2006a), despite their
proportionately longer hind legs. The key movements in the jumping of insects
in both families is the rapid depression of the trochanteral joints of the
hind legs about the coxae. The difference in performance therefore raises the
question of whether there are different structural arrangements of these
joints in leafhoppers and different mechanisms of neural control of the
muscles moving these joints.
In general, insects with short legs have to store energy in advance of a
jump and then release it suddenly in a catapult action because the direct
action of the muscles cannot generate enough energy in the short acceleration
times available (Alexander,
1995). Fleas (Siphonaptera, Pulicidae)
(Bennet-Clark and Lucey, 1967;
Rothschild and Schlein, 1975;
Rothschild et al., 1972) and
froghoppers (Hemiptera, Auchenorrhyncha, Cercopidae)
(Burrows, 2003;
Burrows, 2006a) are examples of
insects with short legs that use a catapult mechanism. Insects with long legs,
such as bush crickets (Orthoptera, Ensifera, Tettigoniidae)
(Burrows and Morris, 2003),
power their jumps by direct action of the muscles acting on the long levers.
Some insects, such as locusts (Orthoptera, Caelifera, Acrididae)
(Bennet-Clark, 1975), combine
the storage of energy with the extra leverage provided by long legs.
An analysis of the jumping mechanisms used by leafhoppers with long hind legs should therefore reveal their particular specialisations that enable jumping compared with their shorter legged close relatives and with other insects. This paper shows that the structure of the coxa of a leafhopper hind leg is different from that of froghoppers and apparently has no mechanism that enables it to lock the femur in place when preparing to jump. The anatomical arrangement of the antagonistic muscles also indicates that their lever arms are similar when fully levated in preparation for jumping. Recordings from the muscles moving the trochanter indicate that there is only a short period of co-contraction and that the frequency of depressor spikes rises while that of the levator falls just before the trochanter is moved rapidly.
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The anatomy of the hind legs and metathorax was examined in intact insects and in leafhoppers preserved in the following ways: fixed in 5% buffered formaldehyde and stored in 70% alcohol; fixed and stored in 70% alcohol; preserved in 50% glycerol; cleared by boiling in 5% potassium hydroxide. Drawings of the legs, joints and muscles were made with the aid of a drawing tube attached to a Leica MZ16 stereo microscope. Individual colour photographs were taken with a Nikon DXM1200 digital camera attached to the same microscope. Dried specimens were also mounted on specimen holders, sputter coated with gold and then examined in a Philips XL-30 Scanning Electron Microscope.
To record the electrical activity of muscles generating jumping, a
leafhopper was restrained on its back in PlasticeneTM with the hind legs
free to move. Rapid and co-ordinated movements of the two hind legs occurred
spontaneously or could be induced by the same mechanical stimuli used to
promote unrestrained jumping. As in froghoppers
(Burrows, 2006a), the sequence
of movements of the hind legs was the same as that observed in unrestrained
jumping. Pairs of 30 µm steel wires, insulated but for their tips, were
inserted through small holes in the sternal plates of the metathorax and into
the trochanteral depressor and levator muscles of the hind legs. The positions
of the electrodes were confirmed by dissection of the muscles at the end of
the recording session. Movements of a hind leg were recorded at the same time
as the electrical activity of the muscles, by capturing images at rates of 250
frames s–1 with a Photron Fastcam 512 or 1024 PCI camera
[Photron (Europe) Ltd, Marlow, Bucks., UK] attached to a Wild M7A microscope
viewing the insect ventrally. The captured images were stored on one computer.
The electrical signals from the muscles were digitised at sampling rates of 25
kHz with a CED (Cambridge Electronic Design) interface running Spike 2 version
5 software and were then written directly to a second computer. The data files
of images and muscle recordings were synchronised on the two computers to a
resolution of 4 ms, by feeding a 0.5 ms long electrical pulse to a separate
channel of the CED interface, and that simultaneously triggered a light flash
of a miniature LED in the visual field of the camera. Eighty two jumps by five
Aphrodes were analysed in which both muscle recordings and images of
the movements were captured. Temperatures in all experiments ranged from
24–30°C.
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). They have
other structural differences that distinguish them from the front and middle
legs.
The arrangement of the hind coxae is quite different to those of the front
and middle legs. The coxae of the front legs are widely separated at the
ventral midline with the sucking mouthparts projecting posteriorly between
them, and can rotate laterally and medially about the prothorax. The coxae of
the middle legs are closer to each other at the ventral midline, but still do
not touch. They are again able to rotate about the mesothorax in a plane that
results in a forwards and downwards movement and a backwards and upwards
movement of the whole middle leg. By contrast, each hind coxa is huge and
extends from the ventral midline to the lateral edge of the metathorax, and is
largely immobile relative to the metathorax
(Fig. 1A,D). The coxae
therefore move only with the metathorax. This contrasts with the design of the
hind legs in froghoppers where each coxa can rotate about the metathorax
(Burrows, 2006b). A further
feature of the hind coxae is their close apposition to each other at the
midline. They are linked by particular structures (see below), which ensure
that both coxae move as a single unit with the rest of the metathorax. This
arrangement provides a stable base for the movements of the more distal
segments of the hind legs. A hind coxa, unlike that in froghoppers
(Burrows, 2006b), also has no
ventral protrusion from its more lateral part that could engage with the femur
when the hind leg is fully levated. Furthermore, the dorsal surface of the
proximal femur has no structural specialisations that would allow engagement
with the coxa.
The trochanter is heavily sclerotised on its medial rim where the tendon of the large trochanteral depressor muscle inserts and at the two points of its articulation with the femur. Its articulation with the coxa consists of a ventral and a dorsal pivot, with curved horns of the trochanter engaging with sockets in the coxa (Fig. 1A). The coxo-trochanteral joint can move through some 130°. In its fully levated position the femur rests in a hollowed part of the ventral coxa so that proximally it is pressed against a hair row on a ridge in the coxa (Fig. 2A,C). The femoro-tibial joint and its associated femoral spines fit into a sculpted region of the head just behind a compound eye (Fig. 2A,B). This recess allows the hind femur to move further medially so that in turn the trochantero-femoral joint can be fully levated. In its fully levated position, a hind leg therefore comes to lie in a position bounded dorsally by the thorax and ventrally by the front and middle legs.
The femur articulates with the trochanter at a ventral and a dorsal pivot by projections from the femur inserting into sockets on the trochanter. The movement is in a plane almost orthogonal to that of the coxo-trochanteral joint but is restricted to a small arc of some 15–20°. The femoro-tibial joint consists of a double pivot articulation with a lateral covering plate and has no distinct semi-lunar process or other heavily sclerotised structure that could store energy (Fig. 1B). The joint allows the tibia to be flexed and extended about the femur through an arc of 160–170° in the same plane as that of the coxo-trochanteral joint.
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The tarsus consists of three segments with two terminal pads (arioli) (Fig. 1C) and can be levated and depressed about the tibia through an angle of 40–50°. This movement is again in the same plane as that of the femoro-tibial and coxo-trochanteral joints. This arrangement means that during a jump three of the main joints of the leg move in the same plane.
Proprioceptors
There are many arrays of hairs associated with the proximal joints of a
hind leg that would appear to be positioned to act as proprioceptors, rather
than as exteroceptors, monitoring the movements of these joints during jumping
(Figs 1,
2,
3).
A prominent hair row and two hair plates on the coxa are likely to be stimulated when a hind leg is fully levated in preparation for a jump. The leg movements associated with walking on a horizontal surface do not bring the femur into contact with these arrays of hairs. The hair row on the medial edge of the ventral hollow of the coxa consists of some seven stout hairs, only 10 µm long but 5 µm wide at their base (Fig. 2A,C,D). The femur abuts against this hair row only when a hind leg is fully levated. The two hair plates in the ventral hollow of the coxa each consist of some 15 hairs, with the medial hairs 30–45 µm long and the more lateral ones 60–70 µm long (Fig. 3A,B). These hairs will be stimulated by the dorsal surface of the femur as it locates into the coxal hollow during levation of the coxo-trochanteral joint, and then presses on them while it remains in the fully levated position.
The coxa and trochanter also have a number of prominent hairs that are longer than the more numerous surrounding hairs. The coxa has a group of 2–4 hairs (the number depends on the species) 125–150 µm long on its posterior ventral surface that point posteriorly (Fig. 1A, Fig. 2A, Fig. 3A). They are likely to be deflected by the trochanter as it moves in its most depressed position. The trochanter also has two prominent hairs 200 µm long on its dorsal surface that point laterally and slightly anteriorly (Fig. 3D,E). They may be deflected by the coxa as the trochanter is levated.
The ventral horn of the trochanter that engages in a socket in the coxa, and thereby forms one of the two joint articulations, has a prominent hair plate on its lateral surface (Fig. 3A,C). The plate consists of a group of some six slender hairs, 25–30 µm long and 2.5 µm wide at their base but tapering to their tip. As the trochanter is fully levated the rotation of the horn in its coxal socket will progressively deflect the hairs.
Ribbed and articulated spines that are some 200 µm long and 35 µm in diameter at their base project distally from the femur close to the femoro-tibial joint (Fig. 1A, Fig. 2A,B). Typically there are five spines, but both the number and their arrangement differs between species. In Cicadella, two pairs of spines point forwards toward the joint while a fifth is set more proximally and points ventrally. Aphrodes also has five spines, but one of the four pointing toward the joint is smaller. Iassus has three spines that all point toward the joint. In all species, these spines will be distorted when the hind leg is fully levated in preparation for a jump and the distal end of the femur engages with a recess in the lateral head capsule.
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).
A structure involving a protrusion from the coxa of one hind leg engaging
with a socket on the other hind leg is clearly bilaterally asymmetrical. In
some leafhoppers the protrusion was from the left coxa
(Fig. 4) and in others, of the
same or different species, from the right coxa
(Fig. 5). To determine whether
there was bias in favour of the protrusion arising from one particular side,
101 leafhoppers of several different species and of either sex were analysed.
Pooling the data from all these insects showed that 45 protrusions were from
the left coxa and 56 from the right. A 
2 test gave a value of
1.198 and a P value of 0.27, indicating therefore that there was no
statistical difference in the frequency of left or right protrusions. If data
were separated into individual species, there was again no statistical
difference in the frequency of left or right protrusions within a species [for
example, Empoasca (N=24) left=12, right=12: Iassus
(N=32) left=18, right=14, 2=0.5,
P=0.48].
Muscles involved in jumping
Movements of the trochanter are powered by large muscles that occupy most
of the space within the coxa (Fig.
6). The large depressor muscle arises from the anterior and
ventral wall of the metathorax and inserts on the sclerotised medial rim of
the trochanter (Fig. 6A). The
two parts of the levator are both more lateral and of similar mass to the
depressor (Fig. 6A,B). The more
medial part arises from the anterior and ventral wall of the metathorax just
lateral to the origin of the depressor and the lateral part from the lateral
wall of the metathorax. They both insert on the lateral edge of the
trochanter.
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). The following
descriptions of jumps recorded in this experimental arrangement all carry the
above caveats. The first movements in preparation for a jump were a levation of the trochantera of both hind legs. The jump may follow this initial levation or there may be a delay lasting several hundred milliseconds before simultaneous recordings from the levator and depressor of one trochanter showed that both muscles were activated at the same time (Fig. 8). The actions of both muscles resulted in a forward movement of the coxae, as indicated by the horizontal lines on the first two frames of Fig. 8. Just before the jump occurred there was an increase in the frequency of spikes in the depressor muscle, while the frequency of spikes in the levator muscle declined. The total duration of the electrical activity in the two muscles was 79.3±14.8 ms (N=23 jumps, range 12–222 ms) as measured from the start of their joint activity until the jump movement. The different durations of activity in a trochanteral depressor muscle was seen in different Aphrodes and during different jumps by the same one (Fig. 9).
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Simultaneous recordings from the depressor muscles of the right and left hind legs showed that spikes occurred at the same time in each muscle before a jump movement of both hind legs (Fig. 10A). The activity in each muscle appeared to result from the activity of more than one motor neuron. The spikes of an individual motor neuron could not be readily distinguished so that the summation and interactions of these spikes in the myogram recordings precluded determination of spike frequencies. Viewing the spikes on an expanded time scale indicated that the spikes on the two sides were not closely coupled and simultaneous spike occurrences did not appear to be common to the muscles on each side (Fig. 10B).
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Mechanical specialisations
The most obvious specialisation of the hind legs of leafhoppers is their
long length relative to their body and to the other pairs of legs. This
increased length is due largely to an increase in the length of the tibiae
with their longitudinal arrays of spines. Leafhoppers, like froghoppers, have
arrays of small spines on the distal tibia and on the tarsal joints that
should increase traction when jumping.
Each coxa can move only with the metathorax at its articulation with the
mesothorax. In jumping this is manifest as an anterior movement of the two
halves of the metathorax during the holding phase (see
Fig. 8). The rigidity of the
two coxae and their simultaneous movements are further enhanced by an unusual
mechanism that links them both. This consists of a protrusion from the medial
surface of one coxa that inserts in a matching socket on the other coxae,
which has been described briefly before
(Emeljanov, 1987;
Gorb, 2001). The linkage is
reinforced by two arrays of microtrichia on each coxa that engage with each
other. Microtrichia are typically found in insects where two surfaces need to
be held together under certain circumstances but still capable of release
under different circumstances (Gorb,
2001). The protrusion can arise from either coxa and there is no
statistical preference for one side in the different species or within a
particular species. The protrusion and the corresponding socket are, however,
absent from larvae where the medial coxal walls are smooth and also lack the
microtrichia. The larvae are nevertheless proficient jumpers
(Burrows, 2007a), thus posing
the question as to whether the linkage between the two coxae is an essential
specialisation for jumping. Perhaps there are subtle differences between the
jumping mechanisms or performance of larvae and adults that have yet to be
revealed.
Leafhoppers lack a mechanical mechanism that could restrain movements of
the hind legs during the holding phase of the jump. Froghoppers have a ventral
protrusion from a coxa that is covered in microtrichia and which engages with
a protrusion from the dorsal surface of a femur, also covered in microtrichia,
when a hind leg is fully levated in preparation for a jump
(Burrows, 2006b). Disengagement
of this lock precedes the release of the leg in rapid jumping movements.
Leafhoppers do not have a ventral protrusion from a coxa or a dorsal
protrusion from the proximal femur that could engage with each other to
provide a lock. Instead the femur fits into a hollow on the ventral coxa when
the hind leg is fully levated, but this would not restrain a depression
movement.
Muscular specialisations
The levator and depressor muscles that operate the coxo-trochanteral joint
are of similar size and mass. The levator muscle has a mechanical advantage
over the depressor when the hind legs are fully depressed, but when the legs
are fully levated their lever arms are the same. This contrasts with the
arrangement of the equivalent muscles in froghoppers, where the huge depressor
muscle occupies most of the metathorax but the much smaller levator muscles
are restricted to the coxa (Burrows,
2007b). Moreover, the small levators have a mechanical advantage
over the large depressor when the trochantera are fully levated.
Neural specialisations
Arrays of hairs appear to be positioned to act as proprioceptors, which
could monitor the positions and movements of the hind legs that are adopted
and used in jumping but not in walking. One of the most obvious movements in
jumping but not walking is the full levation of the trochanter that engages
the femur with the hollowed ventral region of the coxa, and the femoro-tibial
joint with the sculpted region of the head. A hair row and two hair plates on
the ventral coxa and the femoral spines at the femoro-tibial joint should all
signal when this movement occurs and the final fully levated position
achieved. A hair plate on the ventral horn of the trochanter that inserts into
a socket in the trochanter and thereby forms one of the two articulations of
this joint should also signal the more extreme levation movements. Long hairs
on the coxa and trochanter should also be stimulated when the trochanter moves
into in most levated and depressed positions. Froghoppers also have an array
of proprioceptors that could monitor their specific jumping movements, but the
arrangement is different reflecting the different organisation of the joints
(Burrows, 2006b).
The motor pattern underlying the jump consisted of an initial co-activation of the trochanteral levator and depressor muscles that resulted in a full levation of the leg and a forward movement of the coxa and metathorax. Once in the fully levated position the two muscles have a similar mechanical advantage so that a co-contraction of the two muscles should not result in a movement of the trochanter. Instead their combined contractions move the coxa and metathorax forward with the potential to store energy in skeletal structures.
The duration of the muscle activity was very brief with the whole pattern
lasting on average about 80 ms (range 12–222 ms). This contrasts with
the several seconds of contraction by the depressor muscles preceding jumps by
froghoppers and which are accompanied by little activity in the levators
(Burrows, 2007b). The low
mechanical advantage of the depressor when the hind leg is fully levated and
the presence of a mechanical lock prevent depression of the hind legs during
this period. In leafhoppers, storage of energy could occur during the much
briefer holding period. The final burst of spikes in the depressor when the
levator activity has declined must generate sufficient force to depress the
trochanter, at the same time rapidly releasing any force stored by the
preceding muscle contractions.
The spikes in a trochanteral depressor muscle appeared to result from the
activity of more than one motor neuron. The spikes of an individual motor
neuron could not be readily distinguished so that the summation and
interactions of these spikes in the myogram recordings precluded determination
of spike frequencies. The motor spikes in the depressor muscles on the two
sides do not appear to be tightly coupled, to the extent that the spikes
cannot be matched in a one to one fashion. This again strongly contrasts with
the activity of the left and right depressor muscles of froghoppers during
jumping, in which the spikes in the two muscles were synchronous with only a
few exceptional failures on one side
(Burrows, 2007b).
The resulting jump of leafhoppers is much slower than that produced by
froghoppers. The hind legs take on average 5–6 ms to be fully depressed
and extended (Burrows, 2007a)
compared to less than 1 ms in froghoppers
(Burrows, 2003;
Burrows, 2006a) and the
take-off velocity of 2.9 m s–1, although impressive, falls
well short of the 4.7 m s–1 achieved by froghoppers. The
energy expended by leafhoppers in their best jumps is, however, only about a
third of that expended by froghoppers
(Burrows, 2006a;
Burrows, 2007a). A comparison
of jumping between two different groups of insects with similar body designs
– leafhoppers with froghoppers, and bush crickets with locusts –
indicates a potential trade-off between movements that are energetically more
expensive but which can deliver better performance. In locusts, the
power-producing extensor tibiae muscle of a hind leg co-contracts with the
antagonistic flexor tibiae muscle without moving the leg but stores energy in
distortions of the cuticle (Burrows,
1995; Burrows and Morris,
2001; Heitler and Burrows,
1977). By contrast bush crickets, which like leafhoppers also have
proportionately longer hind legs, power their jumps
(Burrows and Morris, 2003),
and crickets their kicks (Hustert and
Gnatzy, 1995), by muscle contractions moving long levers. The
energy that bush crickets expend in jumping is also less than that expended by
locusts, but their performance is inferior.
Many members of the other families of Auchenorrhyncha are also prolific jumpers. This offers the opportunity to explore the way that different families have adapted specific elements from this panoply of jumping mechanisms to meet their own behavioural needs. For example, some cicadellids do not have long hind legs like those described here but are said to be proficient jumpers.
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Acknowledgments |
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