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First published online October 5, 2007
Journal of Experimental Biology 210, 3579-3589 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.009092
Kinematics of jumping in leafhopper insects (Hemiptera, Auchenorrhyncha, Cicadellidae)
Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
e-mail: mb135{at}hermes.cam.ac.uk
Accepted 26 July 2007
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Key words: locomotion, kinematics, motor pattern, muscle
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Introduction |
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; Burrows,
2006a). They achieve these feats, although they have only short
hind legs, by storing energy in advance of the jump and then releasing it
suddenly in a catapult action. This jumping strategy
(Alexander, 1995) contrasts
with insects such as bush crickets that have long hind legs and use mostly
direct muscle contractions acting on these long lever arms to generate their
jumps (Burrows and Morris,
2003).
The Auchenorrhyncha, to which the froghoppers belong, contains many
families and a huge diversity of insects, but jumping is a behavioural
characteristic that most of them share. One of these families, the
Cicadellidae or leafhoppers, differs from the others in that most of its
members have long hind legs and one species is reported to reach take-off
velocities of 1.3 m s–1
(Brackenbury, 1996). The family
is one of the largest insect families, containing 22 000 known species
distributed world wide (Dietrich,
2004), and totalling more than those of all birds, mammals,
reptiles and amphibians combined. The body design is typically characterised
by long hind legs, a wedge-shaped head, and a thorax and abdomen that are
streamlined by being encased by the folded front wings. The long hind tibiae,
with several prominent rows of spines, are used in jumping and walking, and as
combs to distribute brochosomes over the integument. These are 0.3–1.4
µm spheres of a protein–lipid complex with an intricate surface
structure (Rakitov, 2000),
secreted by specialised regions of the Malpighian tubules, which may act as a
protective and waterproof coating. The larval stages are free-living on plants
and can jump, unlike the larvae of froghoppers, which either develop
underground, or in masses of foam above ground.
This paper analyses the jumping performance of leafhoppers to determine
what sorts of movements and mechanisms might be involved and how these are
influenced by having long hind legs. It shows that in the best jumps by some
species of leafhoppers, the body is accelerated at 1055 m s–2
in under 3 ms to a peak take-off velocity of 2.9 m s–1. On
average the acceleration period is 5–6 ms and the take-off velocity is
1.1–1.6 m s–1. The performance, while matching that of
fleas (Bennet-Clark and Lucey,
1967; Rothschild and Schlein,
1975; Rothschild et al.,
1972), locusts (Bennet-Clark,
1975) and some flea beetles
(Brackenbury and Wang, 1995),
falls short of that of their close relatives the froghoppers, despite the
extra leverage of the long hind legs and their similar body shape, size and
mass.
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Materials and methods |
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Sequential images of jumps were captured at rates of 1000–5000 frames s–1 with a Photron Fastcam 512 or 1024 PCI camera [Photron (Europe) Ltd, Marlow, Bucks., UK] that fed images directly to a computer. High-speed videos of jumps by Graphocephala, with images captured at 4000 frames s–1 and each with an exposure time of 0.125 ms, and Cicadella (5000 frames s–1 and 0.05 ms) are included as Movie 1 and Movie 2 in supplementary material. Spontaneous jumps and jumps encouraged by delicate mechanical stimulation with a fine paintbrush or a 100 µm silver wire, were performed in a chamber of optical quality glass 80 mm wide, 80 mm high and 25 mm deep with a floor of high density foam. All jumps by the small Empoasca were spontaneous and were performed in a circular chamber (diameter 15 mm, depth 8 mm) with a glass floor and roof. Selected image files were analysed with Motionscope camera software (Redlake Imaging, San Diego, CA, USA) or with Canvas X (ACD Systems of America, Miami, FL, USA). The time at which the hind legs lost contact with the ground and the insect therefore took off and became airborne was designated as time t=0 ms, so that different jumps could be aligned and compared. The time at which the hind legs first moved is also marked on the figures, therefore defining the time over which the body was accelerated. The acceleration was calculated as the average over this period. A detailed analysis was performed on 52 jumps by 12 Empoasca, 43 jumps by 9 Aphrodes, 33 jumps by 7 Cicadella, and 17 jumps by 4 Graphocephala.
Measurements are given as means ± standard error of the mean (s.e.m.). Temperatures in all experiments ranged from 24–30°C unless otherwise stated.
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The hind legs are much longer than the front or middle legs so that the
ratio of front to middle to hind leg lengths in Empoasca is
1:1.1:2.1, rising to 1:1.2:2.9 in the larger Graphocephala
(Table 1,
Fig. 1). These ratios increase
through successive larval stages. In Iassus, for example, the small
nymphs have a ratio of 1:1.2:1.6, which increases in later and larger nymphs
to 1:1.2:2.0, finally reaching 1:1.2:2.3 in adults. The hind legs are
82–84% of overall body length in Empoasca, Aphrodes and female
Cicadella, rising in male Cicadella to 93%. Their long
length also means they have a greater mass that represents 3.8±0.09%
(N=5) of the total body mass in Cicadella, even excluding
the huge coxae (Burrows,
2007a), and thus almost twice that of froghoppers
(Burrows, 2006a).
The increased length of the hind legs relative to the body is due to a
greatly enlarged tibia and a longer femur. For example, in Aphrodes,
a hind tibia was 3.8±0.06 mm long and 125% longer than a middle tibia
and 202% longer than a front tibia, while a hind femur was 2.2±0.03 mm
long and therefore 69% longer than both the front and middle femora. The hind
legs are therefore much longer relative to the other legs and to the body
compared with those in the Cercopidae and Aphrophoridae families of
froghoppers (Burrows, 2006a;
Burrows, 2006b).
Kinematics of the jump
Jumping is powered by the rapid and simultaneous movements of both hind
legs moving in the same plane underneath the body. The movements occurred in a
distinctive and repeatable pattern divisible into three phases
(Fig. 2).
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Third: a rapid jump phase, in which both hind legs were simultaneously depressed about their coxo-trochanteral joints and extended at their femoro-tibial joints (Fig. 2B,C). These movements of the hind legs provided the major propulsive force for the jump as the front and middle legs had left the ground before the depression of the hind legs was completed. Across all the species examined the average time from the first movement of a hind leg until take-off was 5.0±0.1 ms (N=138). This time therefore represents the period during which the body was accelerated to its take-off velocity. The shortest acceleration period was 2.75 ms in the best jumps by Aphrodes (average 4.4±0.18 ms, N=43) and the longest was 8 ms (average 6.4±0.21 ms, N=20) in Cicadella (Table 2).
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Movements of the hind legs in jumping
The detailed movements of the hind legs powering a jump were determined by
analysing sequential images taken from a side, a frontal and a ventral view
(Figs 3,
4,
5).
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Viewing a jump ventrally, showed clearly the angular changes of the coxo-trochanteral and femoro-tibial joints and the simultaneous actions of both hind legs (Fig. 5). When the legs were first drawn into their fully levated positions, the tibio-tarsal joints of each hind leg touched each other beneath the ventral midline of the abdomen (Fig. 5A). From this starting position the first movement of a hind leg in the jump phase was a depression of the trochanter about the coxa and an extension of the tibia about the femur. Capturing images at 4000 frames s–1, giving a time resolution of 0.25 ms, revealed that trochanteral movements of both hind legs occurred at the same time. No recordings revealed any differences in the relative timing of the movements by the two hind legs at this time resolution. While the tarsi remained at the same position on the ground, the progressive depression of the two hind trochantera about their respective coxae resulted in a backwards movement of the two femora and, together with the extension of a tibia about a femur, resulted in the acceleration of the body forwards (Fig. 5A,B). Take-off was achieved when the trochantera were fully depressed and the tibiae almost fully extended (Fig. 5C). The two tarsi remained apposed throughout the progressive depression and extension movements and only drifted apart when they lost contact with the ground after take-off. Once airborne, the extended hind legs were trailed beneath and behind the body.
Plotting the movements of the legs and the body, as viewed from the side, against time (Fig. 6A) or as their positions on the x and y coordinates (Fig. 6B) emphasised the following features of the jump. First, the initial movement in the jump phase was a trochanteral depression by the hind legs. Second, the front and middle pairs of legs both lost contact with the ground at least 2 ms before take-off, so that the final power for the jump was delivered only by the hind legs. The time at which the front and middle legs lost contact with the ground varied from jump to jump and was correlated with the attitude assumed by the body. In the example shown in Fig. 6, the middle legs were the first to lose contact at –3.75 ms followed by the front legs at –2.5 ms (Fig. 6A). Third, the trajectories illustrate the rotation of the femur that resulted from the depression of the trochanter (Fig. 6B). The path of the femoro-tibial joint was initially backwards relative to the body as the trochanter progressively depressed. It then moved forwards relative to the ground as the trochanteral depression and tibial extension movements accelerated the body forwards, before assuming the same trajectory as the other parts of the body after take-off. The wings did not open before the insect became airborne and thus did not contribute any force to the take-off.
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Plotting the angular changes of the coxo-trochanteral, and the femoro-tibial joints from images captured from a ventral view, showed that the coxo-trochanteral joint was rotated at 44 000 deg. s–1 and the femoro-tibial joint at 47 000 deg. s–1 during the jump phase of the movement (Fig. 7). These plots further indicated that the movements of both joints started at the same time as each other in both Cicadella (Fig. 5) and Aphrodes (Fig. 7). In the other species the joint rotations were slower: in Cicadella the average values were 19 000 deg. s–1 for the coxo-trochanteral joint and 20 000 deg. s–1 for the femoro-tibial joint; in Empoasca they were 26 000 and 28 000 deg. s–1, respectively; and in Graphocephala 21 000 and 23 000 deg. s–1, respectively.
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This jump gave a clear indication of the separation of actions between the different pairs of legs; the body attitude was set initially by the front and middle legs and take-off was propelled by the hind legs. In other jumps, the front and middle legs may have contributed to the thrust for take-off, but they always lost contact with the ground a few milliseconds before the hind legs and thus did not contribute to the later stages of propulsion.
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By contrast, in Empoasca, wing movements commonly accompanied or even preceded the leg movements of a jump (Fig. 9). In the examples shown, the wings started to spread laterally 6 ms (Fig. 9A) or 7 ms (Fig. 9B) before take-off and 2 ms before the first movement of a hind leg was detected. The wings then progressively unfolded and were elevated as the trochantera of the hind legs were depressed about the coxae (Fig. 9B). At take-off, the wings were still being elevated and the first depression movement began only after take-off. The wing movements therefore allow a smooth transition from the jump to the assumption of flapping flight.
Jumping in larvae
The free-living larvae lack functional wings but nevertheless still jump.
The jumps by nymphs of Iassus, for example, showed many of the
features of jumps by the adults of the species already described
(Fig. 10A–C). The
acceleration for the jump was applied in 2–2.5 ms by the rapid movements
of the hind legs and involved depression of the trochantera about the coxae
and extension of the tibiae about the femora. A notable difference was the
placement of the hind tarsi lateral to body and not touching each other
beneath it as in adults (see Figs
4,
5). This was seen most clearly
in jumps away from (Fig. 10B)
or toward (Fig. 10C) the
camera. From this lateral position, the two hind tarsi became apposed to each
other only after take-off and not during the application of thrust that
powered the take-off.
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After take-off the body was rarely observed to spin, indicating that little energy was lost by conversion to rotational kinetic energy of the body. There is still rotational kinetic energy in the legs, but calculations indicate that this is only 0.5–2.% of the total energy expended. By contrast, many jumps were assisted by flapping movements of the wings once the insect was airborne. The height or distance achieved after a jump is thus the product of the forces exerted during a jump itself and those generated by the wing movements during flight. Empoasca with a mass of 0.86 mg and a body length of length of 3.5 mm (Table 1) reached an average height of 47±6.3 mm (N=58 jumps) and a horizontal distance of 53±5.5 mm. Jumping performance declined with repeated attempts to encourage an individual to jump so that these averages underestimated jumping performance. Individual best performances were almost three times better, reaching heights of 180 mm or 51 x body length, and distances of 170 mm.
Assuming that a jump was not assisted by the wings and that the body did
not experience any slowing due to wind resistance, then the height and
distance achieved are given by Eqn
1 and Eqn 2:
 | (1) |
 | (2) |
=take-off angle,
g=acceleration due to gravity (9.81 m s–2).
In the best jumps, Aphrodes should therefore reach a height of 156 mm
(or 18 times its body length) and a distance of 825 mm, Iassus nymphs
102 mm and 407 mm, Cicadella 41 mm and 243 mm, and
Graphocephala 42 mm and 300 mm, respectively. Assuming that
Empoasca takes off at an angle of 35°, it will reach a height of
42 mm and reach a distance of 245 mm. For Empoasca, these equations
are a good predictor of the real height achieved in a jump but not of the
distance, suggesting that the latter is more strongly influenced by flapping
the wings. The wind resistance experienced by these differently sized insects,
which is not considered in these equations, is likely to curtail the real
distances achieved (Bennet-Clark and Alder,
1979; Vogel,
2005).
Walking
The size and the key role of the hind legs in powering jumping has an
impact on other behaviour of leafhoppers, most notably walking
(Fig. 11). All legs
participate in walking on a horizontal surface, unlike those in froghoppers
(Burrows, 2006a), and are
coordinated in an alternating tripod gait. Each time that a hind leg executes
a stance phase, however, the body is displaced laterally in addition to
forwards. The alternate action of the two hind legs thus results in a sideways
oscillation of the body so that the overall path of the insect involves
rhythmical deviations to the left and to the right instead of being in a
straight line. The hind legs are thus responsible for the characteristic
waddling gait of these insects when walking.
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), almost reaching the proportionate length of locust hind
legs (102–107%) but falling well short of those of bush crickets (180%)
(Burrows and Morris, 2003).
They are also proportionately longer than the front and middle legs by a
factor of 1.9–2.9, the same as in fleas, greater than in froghoppers
(factor of 1.4–1.6) but less than in grasshoppers (3.2). Their increased
length is also reflected in their mass, which at 3.8% of body mass, is almost
twice that of froghoppers, but much less than the whole hind legs of locusts
which represent 14% of body mass
(Bennet-Clark, 1975). The light
weight of the hind legs of froghoppers
(Burrows, 2007b), leafhoppers
and presumably fleas, suggests that the force exerted by the extensor tibiae
muscles is not great, and that the key movements in jumping are the depression
of the trochantera about the coxae powered by muscles in the thorax. The
high-speed images of leafhoppers jumping do not give any indication of whether
the tibial movements are under active muscular control, or the passive result
of the forces exerted by the depression of the trochantera. By contrast, in a
locust the muscles generating the power for jumping are those that move the
tibiae and which are located in the femora. The design of the hind legs of leafhoppers therefore differs significantly from that of their close relatives the froghoppers in that their longer length should provide greater leverage with their acceleration, only marginally curtailed by their greater mass. The length of the hind legs also has an impact on other locomotion. When flying, the hind legs are held depressed and extended to trail behind the body and are moved in ways that suggest they are used as rudders to adjust steering. When walking horizontally, the extension of one hind leg in a stance phase pushes the body laterally, only for the movement to be reversed when the opposite high leg is extended, thereby imparting a waddling gait.
Jumping performance
The high-speed images taken from different perspectives show that the main
thrust for jumping is provided by the rapid depression of the trochantera of
both hind legs at the same time. The front and middle legs adjust the take-off
angle by raising or lowering the front end of the body before a jump, but as
the hind legs unfurl and lift the body they typically lose contact with the
ground some 2–4 ms before take-off. The movements of the hind legs in
jumping occur in a distinctive pattern of three phases. First, the hind legs
are moved in 15–30 ms from a standing placement lateral to the body to
one directly underneath the body at the midline where the two tarsi touch each
other. This involves a levation of the trochanter and the accompanying forward
movements of the rest of hind leg so that the femoro-tibial joint may engage
with a sculpted region of the head capsule and the femur sits in a ventral
depression of the coxa. The whole hind leg is thus bounded dorsally by the
body and ventrally by the front and middle legs on the same side. In the
second, holding phase the hind legs remain stationary in their fully levated
positions for 10–200 ms. The durations of the first two phases suggest
that there is little time for contractions of the muscles to distort skeletal
elements and thus store energy. In the third and final jump phase, the hind
legs are rapidly depressed at the coxo-trochanteral joints and extended at the
femoro-tibial joints in movements that lead to take-off. The movements in this
phase last 5–6 ms on average across the different species analysed, but
in the best jumps can be accomplished in 2.75 ms. This period therefore
represents the time over which the body is accelerated in a jump and is up to
seven times slower than the time taken by froghoppers in their best jumps
(Burrows, 2006a). As a
consequence, the acceleration of 1055 m s–2 and the peak
take-off velocity of 2.9 m s–1 that they experience in their
best jumps are less than in froghoppers (5400 m s–2 and 4.7 m
s–1, respectively).
Wing movements do not appear to assist the leg movements in jumping by
leafhoppers, and indeed the free-living larvae that lack functional wings are
proficient jumpers. In the adults of three species examined, the wings always
remained folded during preparations for a jump and during take-off. Only in
Empoasca did the wings unfold and elevate before take-off so that
they are unlikely to contribute greatly to the forces at take-off. The jump is
too rapid for a single cycle of wing movements to be completed before
take-off. It is clear, however, that many jumps represent a launch into
flight. The flapping movements of the wings take over from the propulsion
provided by the legs once airborne, and thus contribute to the height and
particularly to the distance achieved. For this reason few reliable
measurements of the heights and distances achieved by jumping alone were
obtained. Instead, estimates of the heights and distances that might be
achieved simply by jumping and ignoring the likely considerable impediment
caused by drag (Bennet-Clark and Alder,
1979; Vogel,
2005), were made from measurements of the take-off angle and
velocity. These estimates suggest that in its best jumps, Aphrodes
should reach a height of 156 mm (or 18 times its body length) and a distance
of 825 mm.
The jumping performance of leafhoppers is impressive when compared to other
insects. The take-off velocity is higher than in fleas and the force of 100
times body mass that is exerted is comparable
(Bennet-Clark and Lucey, 1967;
Rothschild and Schlein, 1975;
Rothschild et al., 1972). The
much heavier locusts take 20–30 ms to accelerate their body
(Brown, 1967) to a comparable
take-off velocity (Bennet-Clark,
1975). This analysis of the movements involved in jumping and the
resulting jump performance poses a key problem. Leafhoppers and froghoppers
have a similar body shape and mass, but despite having longer hind legs,
leafhoppers fail to outperform froghoppers when jumping. Do leafhoppers have
different mechanical features of the joints in the hind legs, different
arrangements of muscles, and different neuronal strategies for activating
these muscles in jumping? Alternatively do both use catapult mechanisms in
which the length of the hind legs is not critical. These issues will be
analysed in the accompanying paper
(Burrows, 2007a).
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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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Alexander, R. M. (1995). Leg design and jumping technique for humans, other vertebrates and insects. Philos. Trans. R. Soc. Lond. B Biol. Sci. 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.
Bennet-Clark, H. C. and Alder, G. M. (1979).
The effect of air resistance on the jumping performance of insects.
J. Exp. Biol. 82,105
-121.
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.
Brackenbury, J. (1996). Targetting and visuomotor space in the leaf-hopper Empoasca vitis (Gothe) (Hemiptera: Cicadellidae). J. Exp. Biol. 199,731 -740.[Abstract]
Brackenbury, J. and Wang, R. (1995). Ballistics and visual targeting in flea-beetles (Alticinae). J. Exp. Biol. 198,1931 -1942.[Medline]
Brown, R. H. J. (1967). The mechanism of locust jumping. Nature 214,939 .[Medline]
Burrows, M. (2003). Froghopper insects leap to new heights. Nature 424,509 .[CrossRef][Medline]
Burrows, M. (2006a). Jumping performance of
froghopper insects. J. Exp. Biol.
209,4607
-4621.
Burrows, M. (2006b). Morphology and action of
the hind leg joints controlling jumping in froghopper insects. J.
Exp. Biol. 209,4622
-4637.
Burrows, M. (2007a). Anatomy of hind legs and
muscle actions during jumping in leafhopper insects. J. Exp.
Biol. 210,3590
-3601.
Burrows, M. (2007b). Neural control and
co-ordination of jumping in froghopper insects. J.
Neurophysiol. 97,320
-330.
Burrows, M. and Morris, O. (2003). Jumping and
kicking in bush crickets. J. Exp. Biol.
206,1035
-1049.
Dietrich, C. H. (2004). Phylogeny of the leafhopper subfamily Evacanthinae with a review of neotropical species and notes on related groups (Hemiptera: Membracoidea: Cicadellidae). Syst. Entomol. 29,455 -487.[CrossRef]
Rakitov, R. A. (2000). Secretion of brochosomes during the ontogenesis of a leafhopper, Oncometopia orbona (F.) (Insecta, Homoptera, Cicadellidae). Tissue Cell 32, 28-39.[CrossRef][Medline]
Rothschild, M. and Schlein, J. (1975). The jumping mechanism of Xenopsylla cheopis. Exoskeletal structures and musculature. Philos. Trans. R. Soc. Lond. B Biol. Sci. 271,457 -490.[Medline]
Rothschild, M., Schlein, Y., Parker, K. and Sternberg, S. (1972). Jump of the oriental rat flea Xenopsylla cheopis (Roths.). Nature 239,45 -47.[CrossRef]
Vogel, S. (2005). Living in a physical world II. The bio-ballistics of small projectiles. J. Biosci. 30,167 -175.[Medline]
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