Jumping from the Surface of Water by the Long-Legged Fly Hydrophorus (Diptera, Dolichopodidae)

1973

RESEARCH ARTICLE Jumping from the surface of water by the long-legged fly Hydrophorus (Diptera, Dolichopodidae)

Malcolm Burrows Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK and Department of Psychology and Neuroscience, Dalhousie University, Halifax, Nova Scotia, Canada, B3H 4R2 [email protected]

SUMMARY The fly Hydrophorus alboflorens (4mm long, 4.7mg mass) moves around upon and jumps from water without its tarsi penetrating the surface. All six tarsi have a surface area of 1.3mm−2 in contact with the water, but they did not dimple its surface when standing. Jumping was propelled by depression of the trochantera of both hind and middle legs, which are 40% longer than the front legs and 170% longer than the body. As these four legs progressively propelled the insect to take-off, they each created dimples on the water surface that expanded in depth and area. No dimples were associated with the front legs, which were not moved in a consistent sequence. The wings opened while the legs were moving and then flapped at a frequency of 148Hz. The body was accelerated in a mean time of 21ms to a mean take-off velocity of 0.7ms−1. The best jumps reached velocities of 1.6ms−1, and required an energy output of 7μJ and a power output of 0.6mW, with the fly experiencing a force of 140g. The required power output indicates that direct muscle contractions could propel the jump without the need for elaborate mechanisms for energy storage. Take-off trajectories were steep, with a mean of 87deg to the horizontal. Take-off velocity fell if a propulsive tarsus penetrated the surface of the water. If more tarsi became submerged, take-off was not successful. A second strategy for take-off was powered only by the wings and was associated with slower (1degms−1 compared with 10degms−1 when jumping) and less extensive movements of the propulsive joints of the middle and hind legs. No dimples were then created on the surface of the water. When jumping was combined with wing flapping, the acceleration time to take-off was reduced by 84% and the take- off velocity was increased by 168%. Jumping can potentially therefore enhance survival when threatened by a potential predator. Supplementary material available online at http://jeb.biologists.org/cgi/content/full/216/11/1973/DC1 Key words: surface tension, kinematics, flight, escape strategies. Received 4 December 2012; Accepted 4 February 2013

INTRODUCTION et al., 2003). Some powerful propulsive strokes may lift the body Living on or near water presents many hazards to an animal that clear of the water, thus resembling a jump, the distance of which breathes air. For a small insect the problem is accentuated by its may be prolonged by sliding on the low frictional surface of the size, which means that it risks being trapped by the surface tension water (Moller Andersen, 1982). By contrast, pygmy mole crickets of the water, or its fragile wings may become wet. Insects that have jump from water by propelling their hind legs through the surface aquatic larval stages, such as mosquitoes or caddis flies, need to and pushing downwards a sufficient volume of water by the use of move from the surface of water when they emerge as adults. This spring-loaded tibial paddles and spurs, which increase the surface risk of entrapment or drowning is apparently offset by the availability area of the tibiae (Burrows and Sutton, 2012). Larger animals propel of food from others that have failed to avoid a similar fate. The fly themselves by pushing a turbulent flow of fluid down with their Hydrophorus skates on the surface of water searching for a mate feet, which must not become wet. This, for example, enables basilisk or predating upon other insects that have become trapped by the lizards (Basiliscus) to run for a few metres in a bipedal gait across surface tension. While clearly at ease on the water surface, it may the surface of water at a velocity of 1.5ms−1 (Rand and Marx, 1967) need to move to other sites or escape from predators within or above before sinking (Glasheen and McMahon, 1996; Hsieh, 2003; Hsieh the water and thus launch into flight. Jumping enables it to launch and Lauder, 2004), and frogs to jump from the water (Nauwelaerts more quickly into flight and avoid the risk of the flapping wings and Aerts, 2006; Nauwelaerts et al., 2004). touching the water. Few insects have transferred their jumping abilities on land to Solutions to the problem of moving around on water depend upon such compliant surfaces as water. On land, a few insects, such as whether the properties of the surface tension are used, or whether bush crickets, extend their long jumping legs by direct muscular the legs are propelled into the body of the water (Bush and Hu, contractions (Burrows and Morris, 2003). The time taken to extend 2006). Pond skaters make use of the surface tension to move around these long legs, and hence the period over which the body is on the water surface and catch prey, propelled by rapid and accelerated, distributes the ground reaction forces that they exert synchronous rowing movements (Bowdan, 1977; Murphey, 1971) over a longer time, but they are not reported to jump from the surface of their elongated and water-repellent middle legs (Gao and Jiang, of water. Most hemipteran leafhoppers have hind legs that are as 2004) that shed hemispherical vortices (Goodwyn et al., 2008; Hu much as 230% longer than the front legs, but a closely related group,

THE JOURNAL OF EXPERIMENTAL BIOLOGY 1974 The Journal of Experimental Biology 216 (11) the Ulopinae, has hind legs that are no more than 10% longer than Tucson, AZ, USA) or with Canvas 12 (ACD Systems of America, the other legs. Both groups have similar take-off velocities, but there Miami, FL, USA). The time at which the hind legs lost contact with are marked differences in their acceleration times and hence ground the water surface and became airborne was designated as time t=0ms reaction forces (Burrows and Sutton, 2008). The advantage of their in Figs 2, 3, 4 and 6, so that different jumps could be aligned and long legs may again lie in distributing ground reaction forces over compared. The time at which the middle or hind legs started to move a longer time, thus reducing energy losses when taking off from and propel the jump was also labelled and the time between these compliant surfaces such as thin and pliable leaves, or even water. two events defined the period over which the body was accelerated Slow movements of long legs will thus produce lower ground in a jump. A one-frame error in estimating both the first movement reaction forces. of the hind legs and the take-off time would result in a 10% error By contrast, most insects, including grasshoppers (Bennet-Clark, in measuring acceleration time. Measurements are given as means 1975), fleas (Bennet-Clark and Lucey, 1967; Sutton and Burrows, ± s.e.m. Temperatures within the experimental chamber ranged from 2011) and many families of bugs within the Hemiptera [e.g. 22 to 24°C. froghoppers (Burrows, 2003; Burrows, 2006), leafhoppers (Burrows, Photographs of live flies were taken with a Nikon D90 camera 2007) and planthoppers (Burrows, 2009a)] use catapult mechanisms fitted with a 100mm Nikon macro lens. The anatomy of the legs for jumping in which power is applied in a very short time. Again, was examined in intact flies, and in those fixed and stored in 70% none are reported to be able to jump from water, but different species alcohol or 50% glycerol. Dried specimens were mounted on can jump from surfaces of different compliances by having specimen holders, sputter coated with gold and then examined in propulsive legs of different lengths. an XL-30 FEG scanning electron microscope (Philips, Eindhoven, This paper reports on an analysis of a fly that successfully jumps The Netherlands). Lengths of the legs of fixed specimens were from the surface of water. Hydrophorus has much longer legs, and measured to an accuracy of 0.1mm on images captured with a digital feet with a large surface area in contact with the water, in contrast camera attached to a Leica MZ16 microscope (Wetzlar, Germany) to flies such as Drosophila, which jump from land (Card and and projected onto a large monitor. Body masses were determined Dickinson, 2008; Trimarchi and Schneiderman, 1995; Zumstein et to an accuracy of 0.1mg with a Mettler Toledo AB104 balance al., 2004). The middle and hind legs act together to provide the (Beaumont Leys, Leicester, UK). propulsive force for jumping and their contribution can be gauged by the dimpling of the water surface that they each cause. The tarsi RESULTS do not penetrate the surface. Jumping increases the velocity of take- Behaviour off and hence a launch into flight by 168%, and decreases the time Hydophorus alboflorens (Fig.1) was observed in its natural to take-off by 84% compared with an alternative strategy of flying environment flying low over calm lagoons, ponds and puddles of accompanied by leg movements that do not cause dimples in the water surface. A

MATERIALS AND METHODS Hydrophorus alboflorens (Walker 1849) were collected from lagoons, ponds and puddles in forest tracks around Halifax, Nova Scotia, Canada, during September to November 2010. They belong to the order Diptera, sub-order Brachycera, super-family Empidoidea, family Dolichopodidae and sub-family Hydrophorinae. Sequential images of jumps were captured at rates of 5000s−1 and an exposure time of 0.1 or 0.2ms, with a single Photron Fastcam 1mm 512PCI camera (Photron Europe, High Wycombe, Bucks, UK), B fitted with a 100mm micro Tokina lens. Images were fed directly to a portable computer for later analysis. All jumps occurred spontaneously from the water contained within a glass chamber measuring 80mm wide, 80mm high and 25mm deep. Some spontaneous jumps were also from the walls of the chamber. The camera pointed either at an angle above the surface of the water or directly at the meniscus of the water in the middle of the front face of the chamber. Measurements of changes in joint angles and Femur distances moved were made from jumps that were, as close as possible, parallel to the image plane of the camera. Jumps that deviated from this plane by ±30deg were calculated to result in a Tibia maximum error of 10% in the measurements of joint or body angles. Peak velocity was calculated as the distance moved by a point on the thorax just dorsal to the middle legs and measured from such Tarsus sequences. A rolling three-point average of successive images was 1mm taken during the final 3ms before take-off. Other jumps in which the insect was viewed from behind or in front were also captured. A total of 60 jumps by six adult H. alboflorens were captured, with Fig.1. Photographs of Hydrophorus alboflorens. (A)Side view of the fly standing on a hard surface. The right middle leg is held raised from the a minimum of three jumps by each fly. Two jumping sequences are ground. (B)Dorsal view of the fly standing on the surface of the water. The included as supplementary material Movies1, 2. Selected image files whole lengths of each of the six tarsi are in contact with the surface of the were analysed with Motionscope camera software (Redlake Imaging, water.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Fly jumping from water 1975 fresh water, occasionally alighting briefly on the surface of the water, –16.2 ms –4.2 ms and then standing or moving about on the water for prolonged periods. When on the surface of the water, the body and the wings did not become wet. In response to a shadow or a vibrational stimulus to the water surface they would jump and launch into flight with a wingbeat frequency of 148±1Hz (grand mean ± s.e.m. of six H. LM alboflorens). Many jumps, however, appeared to be spontaneous or LH LH at least not in response to any discernible stimulus. The same flies RH LF RH LM would also alight upon, and take-off from, the surrounding RM RF RM vegetation. –14.6 –2.8 Body form First movement Adult H. alboflorens had a body length of 4.4±0.2mm and a mass of 4.7±0.6mg (N=8). There were no apparent size classes within the flies studied and thus they were not divided into males and females. The body was narrow with a maximum width of 1mm and the wings projected posteriorly over the body and beyond the tip of the abdomen when folded (Fig.1A,B). All the legs were longer than the body, thus fulfilling the common name of this family of –10 –1.2 flies – long-legged flies; the front legs were 5.3±0.1mm long, the middle legs 7.1±0.1 and the hind legs 7.3±0.1, so that the ratio of leg lengths was 1:1.4:1.4 (front:middle:hind). The front legs were 122% longer than the body, the middle legs 165% longer, and the hind legs 170% longer. Expressing the length of the hind and middle leg against the cube root of the body mass gave a ratio of 4.4. When standing on water, reflections indicated that the entire length of all six tarsi were in contact with, but did not penetrate, the surface (Fig.1B). The tarsus of the front leg was 1.6mm long, –8 0 the middle 2mm and the hind 2.1mm long. This means that for each leg the tarsus was long relative to both the femur and tibia; the front leg tarsus was 127% longer than front tibia and 114% longer Take-off than the front femur, for the middle legs the values were 93 and 97% and for the hind legs 91 and 89%. All tarsi had a width of 120–125μm, as measured from images captured in the scanning electron microscope, so that all six tarsi provide a contact area of 1.3mm−2 (0.2mm−2 for a front, 0.21mm−2 for a middle and 0.25mm−2 for a hind tarsus) when on the surface of the water –6 +2.2 (Fig.1B).

Kinematics of jumping High-speed images of jumps from the surface of the water were captured from different angles by a single camera (Figs2–4) so that LF+RF the orientation and movements of the legs could be interpreted in LH LH+RH all three dimensions. The majority of the jumps were viewed from LM+RM LM the side (Fig.2, supplementary material Movie1), augmented by 2mm RH RM views from behind (Fig.3) and in front (Fig.4). Some jumps were performed from the front glass wall of the chamber, allowing the Fig.2. Side view of a jump by Hydrophorus alboflorens from the surface of leg movements to be seen from underneath. For most jumps, the the water. Images were captured at 5000s−1. The front legs (left LF, right camera pointed at an angle down onto the surface of the water to RF) are indicated by yellow arrows, the middle legs (LM, RM) by white record any dimples created by forces applied by individual legs. To arrows and the hind legs (LH, RH) by pink arrows in this and subsequent determine whether any leg penetrated the surface of the water, the figures. The middle and hind legs created dimples on the surface as they camera was also pointed in the plane of the water surface. The were depressed and extended to propel the jump. The wings began to following description combines information from all views and open and flap as soon as the legs moved. In this and Figs3, 4 and 6, the bottom left-hand corner of each image represents a constant reference applies to all jumps that occurred spontaneously and after variable point. periods of standing on the water. When standing on the water in advance of a jump, all six tarsi were in full contact with the surface of the water but none caused marked dimpling. Jumping was propelled by the depression of the consistent pattern of movement from jump to jump that indicated trochantera of both middle and both hind legs that usually preceded they were contributing to propulsion. Typically, they were lifted opening and then flapping movements of the wings (Figs2–4). The from the surface of the water before take-off occurred and while first movements of the middle and hind legs were synchronised to the middle and hind legs depressed at their coxo-trochanteral joints. within 1ms of each other. The front legs, by contrast, showed no At no stage during a jump did the front tarsi create dimples in the

THE JOURNAL OF EXPERIMENTAL BIOLOGY 1976 The Journal of Experimental Biology 216 (11)

First movement –21.2 ms –3.8 ms –16.2 ms –6 ms

LM RM LH LM RM RH LM LH RH LH RH RM –14 –2.4 RF LF

–13.6 –4.2 First movement

–11.4 –0.8

LM RM –11.6 –2 LH RH

–8 Take-off 0

RH LF

RM RF LH LM –6.2 +1.8 –9.8 Take-off 0

2mm

Fig.3. Hydrophorus alboflorens jumping from the surface of the water viewed from behind. Images were captured at 5000s−1. When standing the six legs made only small indentations in the surface. As soon as the middle and hind legs started to depress and extend they created large dimples that expanded progressively. –7.2 +1.6 water. By contrast, the movements of the middle and hind legs created dimples around their tarsi that increased in depth and diameter the further the body was raised from the water (Figs2–4). These dimples indicate that these four legs – two middle and two hind – were applying force to the water surface. When jumping was viewed in the same plane as the surface of the water, the following features of the movements of the tarsi became apparent (Fig.5). First, the tarsi of the hind and middle legs 2mm did not penetrate the surface of the water when creating large dimples (Fig.5A–C). A tarsus could be seen below the meniscus of the chamber but still above the indented surface of the water. Air could Fig.4. Hydrophorus alboflorens jumping from the surface of the water viewed from the front. Images were captured at 5000s−1. The front legs sometimes be seen to be present surrounding the tarsus (Fig.5B). lost contact with the water surface earlier than the middle and hind legs In other sequences the indentation of the water below the meniscus and, unlike the middle and hind legs, did not cause indentations in the could be seen to change in depth and in shape as force was applied surface of the water.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Fly jumping from water 1977

A CD0ms 0ms Fig.5. Surface tension and the tarsi of Hydrophorus alboflorens. Images were captured at 5000s−1. (A)Two frames 4ms apart from a jump in which the two middle (white arrows) and two hind legs (pink arrows) made four dimples in the water, which increased in diameter as greater thrust was applied by these legs. (B)A frame from a fly jumping from the surface in which the tarsus of LH LM the left middle leg is visible below the meniscus (black RM RH arrow) with air above it. It has created a large dimple in RM the water surface but has not penetrated the surface of +0.8 the water. (C)Four frames starting at time 0 ms, taken +4 RH from a jump by another fly, in which an indentation in the surface (white arrow) caused by the right middle leg first increased and then decreased as the insect took off. None of the legs penetrate the surface. (D)Four frames again starting at time 0 ms, from another jump in which the right hind tarsus (pink arrows) did penetrate the surface. This tarsus was progressively swept backwards through the water and then withdrawn from the water.

+2 +6

B +5.6 +8

5mm 5mm and then reduced as the leg was progressively lifted from the water in the best jumps. The power output ranged from 0.1 to 0.6mW, (Fig.5C). These observations indicate that the tarsi normally and the force exerted in the best jumps was 0.8mN. The mean take- remained above the surface of the water. off angle was a steep 87±7deg relative to the horizontal. The wings In normal jumps, in which no legs penetrated the surface of the were usually being depressed at take-off, but the relationship water, the time taken to accelerate the body to take-off was between the leg and wing movements was variable, and take-off 21.1±0.2ms (grand mean for six flies with a minimum of three jumps could occur at the start or end of depression within either the first by each; Table1). The mean take-off velocity was 0.7±0.06ms−1, or second wingbeat cycle. with the best performance by an individual fly achieving 1.6ms−1. In some jumps, one of the middle or hind legs did penetrate the In the best jumps, the applied accelerations were 140ms−2 so that surface of the water and was then moved in the water (Fig.5D). the forces experienced were approximately 14g. The energy required The fly nevertheless still managed to take-off, but at a lower velocity. to achieve take-off ranged from 1.2μJ in average jumps to 7.2μJ For example, in a jump in which at least one leg penetrated the

Table1. Performance of Hydrophorus alboflorens when jumping from the surface of water Body mass Body Time to Take-off v Take-off Acceleration Energy Power Force (m) length take-off (t) elocity (v) angle (f) g force (E)(p)(F) Formula f=v/t g=f/9.81 E=0.5mv2 p=E/tF=mf Units mg (10−6kg) mm ms (10−3s) ms−2 deg ms−2 g μJ (10−6J) mW (10−3W) mN (10−3N) Jumping and flying 4.7±0.6 4.4±0.2 21.1±1.4 0.70±0.06 87±5 33.3 3.4 1.2 0.1 0.2 Best 5.3 4 11.6 1.64 80 141.4 14.4 7.2 0.6 0.8 Flying only 4.7±0.6 4.4±0.2 32.4 0.38 68 11.7 1.2 0.4 0.01 0.1 Best 5.4 4 25.2 0.43 17.1 1.7 0.5 0.02 0.1 The first row gives the mean of means take-off performance for 6 flies when jumping and flying, and the second the best performance of an individual. The third row gives the mean performance for 6 take-offs by the same 6 flies when flying alone was used and there was no disturbance of the water surface; the last line gives the best performance by an individual.

THE JOURNAL OF EXPERIMENTAL BIOLOGY 1978 The Journal of Experimental Biology 216 (11)

−1 surface (Fig.5D), the take-off velocity of 0.43ms was 63% lower –35.4 ms –7.4 ms than the average.

Take-off into flight without jumping In eight of the 60 sequences of taking off by H. alboflorens, the LM RM middle and hind legs did not cause any indentations in the surface of the water, indicating that they were not applying much force

(Fig.6, supplementary material Movie2). The wings were, however, LH RH still flapped at the same frequency (Figs2–4). With this strategy, it –23.4 –4 took longer to accelerate the body to take-off (35±4ms, mean of First movement six take-offs), compared with a mean of 19±2ms for a further six take-offs accompanied by jumping by the same individual H. alboflorens. The take-off velocity was also lower (0.38±0.16ms−1 −1 LM compared with 1.02±0.15ms , for those assisted by jumping). RM These values are statistically significantly different (t-test with equal variance not assumed: acceleration time t6.292=3.66, P=0.01; take- LH RH off velocity t5.125=4.29, P=0.007). The longer acceleration time also –17.2 –2 meant that the wings could complete more cycles of flapping movements before take-off. The differences between the movements of the middle and hind legs in these two strategies became clearer when angular changes were plotted for two joints of a hind and a middle leg (Fig.7). When jumping, the angle through which the femur was moved relative to the body, and by the tibia relative to the femur, in both the middle and hind legs ranged from 60 to 100deg. By contrast, when flying alone appeared to power take- –11.4 0ms off, the joints moved through less than 50deg. The rate of angular Ta k e - o f f changes in the joints was also much lower. For example, when jumping the rate of angular movement by the right and left middle femora about the body was approximately 10degs−1, but fell to only 1degs−1 when flying alone was used.

Landing on the surface of water When alighting on water, H. alboflorens also had to ensure that its body and especially its wings did not become wet, to avoid the risk –9.4 +3.4 of becoming trapped by the surface tension. A small number of landings were captured when they fortuitously happened in the focal plane of the camera (Fig.8). The fly approached the water with all six legs outstretched, the front legs pointing anteriorly and the middle and hind legs sideways. In the example shown, the body was tilted sideways in such a way that the distal tips of the tarsi of the left 2mm middle and hind legs were the first to contact the water (Fig.8). The wings were in the elevated phase of the flight sequence. The left middle and hind tarsi, together with the wing movements, were able Fig.6. A take-off from the surface of the water by the same Hydrophorus to support the mass of the body and did not penetrate the surface. alboflorens as in Fig.4. In this take-off none of the legs created indentations in the water surface, but the wings were flapped. Acceleration The body then tilted to the right so that the entire lengths of the time was longer and take-off velocity lower. The surface of the water middle and hind tarsi contacted the surface of water and the tip of remained still. Images were captured at 5000s−1. the abdomen indented the surface, but did not penetrate it. The right middle and hind tarsi next contacted the water and finally the front tarsi touched down. Throughout this sequence the hind wings were the two behavioural strategies produce take-offs that differ in the held above the surface and at no time did any part of the fly penetrate time it takes to become airborne and in the take-off velocity. Jumps the surface. The result was that only the under-surfaces of the were accompanied by, or followed by, flapping movements of the abdomen and the tarsi contacted the water surface. The wake caused wings and thus represent a mechanism for launching into flight. by the impact of the fly then spread out, with the fly coming to rest The key to successful jumping was that the fly made use of the with all tarsi in contact with the water but not associated with any surface tension of the water. If the tarsi of the propulsive legs dimpling of the surface. penetrated the surface, take-off velocity was either reduced or failed completely, with the attendant risk of the body either becoming wet DISCUSSION or entrapped by the surface tension. This study has demonstrated that to jump successfully and rapidly from the surface of water H. alboflorens uses three morphological Structural specialisations specialisations and two behavioural strategies. The body structure The three key specialisations used in jumping from water are the spreads the propulsive forces over a large area of contact between way that the propulsive (ground reaction) forces are applied. First, the legs and the water surface in both space and time. In addition, the simultaneous contribution of the middle and hind legs distributes

THE JOURNAL OF EXPERIMENTAL BIOLOGY Fly jumping from water 1979

AB Fig.7. Movements of leg joints during the 200 Hind legs Take-off Take-off two strategies used for take-off. (A)Jumping and flying. (B)Flying alone. The top graphs plot the changes of the Right femoro-tibial angle femoro-tibial angles of the left (open Left femoro-tibial angle 150 circles) and right (filled circles) hind legs and of the angle between the femur and the body (left hind leg, open triangles; right hind leg, filled triangles). The bottom 100 graphs plot the same angles with the same symbols for the left and right middle legs. Right body–femur angle Left body–femur angle 50

200 Middle legs Joint angle (deg)

150

100

50 Middle and hind legs start Middle and hind to move legs start to move 0 –50 –40 –30 –20 –10 0 +10 –50 –40 –30 –20 –10 0 +10

Time (ms) these forces between four points of tarsal contact with the water. and the wings in flapping; and second, by the flapping movements Second, the long middle and hind legs (165–170% longer than the of the wings at the same frequency, but with a lesser contribution body) distribute the forces over a mean acceleration time of 21ms. from the middle and hind legs – their rate of angular movement This is because it takes longer to extend longer legs, and therefore was tenfold less, and the angles through which particular joints the forces exerted on the water at any one time will be lower than moved were halved. The combination of these two resulted in leg if the legs were shorter. Third, each tarsus is long and covered in movements that took longer to accelerate the fly to take-off. They numerous fine hairs so that the surface area of contact of the four also resulted in a reduction of the ground reaction forces exerted, propulsive tarsi is 0.92mm−2. The front tarsi are longer than the as deduced from the absence of dimpling of the water surface front femur or tibia and the propulsive middle and hind tarsi are normally associated with the tarsi of each of these legs when almost as long as their respective femora and tibiae. All of these jumping. The two strategies were not used by an individual fly in factors combine to ensure that the forces applied by the propulsive any particular sequence, but in the experimental chamber used to legs are distributed widely. The importance of not penetrating the capture high-speed images, combined jumping and flying was the surface tension is emphasised by the consequences that result when, predominant mechanism in all flies analysed. Because all the jumps on rare occasions, a leg is pushed into the water. The take-off were spontaneous, it is not clear whether specific stimuli elicit, as velocity is then reduced by half even if the other legs remain on they do in Drosophila (Card and Dickinson, 2008), different the surface. If more than one tarsus penetrates the surface the jumping performances. remaining ground reaction forces may not be able to raise the body The contribution of jumping was to reduce the time taken to sufficiently from the water to allow the wings to move without become airborne (the acceleration time) by 84% and to increase the contacting the water and becoming entrapped. The same take-off velocity by 168%. Both effects should markedly increase specialisations also allow the fly to land on the surface of the water survival chances in escaping from a potential predator approaching without becoming wet. from below the water surface, or from above. There is a balance, however, between speed of escape and the risk that too much force Behavioural strategies applied too rapidly will result in the tarsi penetrating the water; this Hydrophorus alboflorens used two distinct strategies to take-off would reduce take-off velocity, or lead to a possible failure of take- from the surface of water and launch into flight: first, propulsion off altogether. Both strategies, coupled with the length of the middle by the combined actions of the middle and hind legs in jumping and hind legs, ensure that the body is raised high enough above the

THE JOURNAL OF EXPERIMENTAL BIOLOGY 1980 The Journal of Experimental Biology 216 (11)

–4 ms RF +4 jumping insects, such as grasshoppers (Bennet-Clark, 1975) and RM hemipteran hoppers (Burrows, 2006), a jump is powered only by LF RH the two hind legs with the mass of their jumping muscles representing approximately 10–11% of total body mass. If the jumping muscles of H. alboflorens follow the same proportional relationship, a power output of some 120Wkg−1 of muscle, as +8 calculated from the kinematics, would be needed to generate one LH LM of the best jumps. Because two pairs of legs propel a jump, the proportion of jumping muscle mass may be higher, further lowering the power output required. The maximum active contractile limits of normal muscle range from 250 and 500Wkg–1 (Askew and –6 Marsh, 2002; Ellington, 1985; Josephson, 1993; Weis-Fogh and +12 Alexander, 1977), so that the calculated values for H. alboflorens LF RF are therefore well within this range. Direct contractions of the appropriate trochanteral muscles in the hind and middle leg muscles should be capable of propelling a jump. It follows, therefore, that RM these flies do not need to store energy and then release it suddenly in a catapult-like mechanism, and elaborate energy storage LM LH RH mechanisms are not required. +2 2 The overall jumping performance nevertheless matches those of some other insects that jump from land by the direct contractions 0 ms Touch-down of muscles. For example, Drosophila reaches an initial velocity of RF 0.5ms−1 in an acceleration time of 5ms when jumping from land LF (Card and Dickinson, 2008). Similarly, snow fleas (Mecoptera, Boreidae) use direct contractions of middle and hind legs muscles +32 to propel themselves to take-off velocities of 1.0ms−1 in RH approximately 6ms, again when jumping from land (Burrows, 2011). LM RM With this method of jumping, performance can be improved by increasing the length of the hind legs and thus their leverage. This option is exploited by bush crickets that can achieve take-off LH 5mm velocities of 2ms−1 but at the expense of much longer acceleration times (Burrows and Morris, 2003). Fig.8. Landing of Hydrophorus alboflorens on the surface of the water. The jumping performance of H. alboflorens approaches that Images were captured at 5000s−1.The left middle and hind legs touched of jumping insects that do use a catapult mechanism, even though down first (time 0ms). The tip of the abdomen then hit the surface of the water but did not penetrate it. The body was gradually raised so that the H. alboflorens is jumping from a compliant surface. Two insect came to rest on the tarsi of all six legs. hemipteran bugs, Hackeriella (Coleorrhyncha: Peloridiidae) (Burrows et al., 2007) and Saldula (Heteroptera: Saldidae) (Burrows, 2009b), reach take-off velocities of 1.5 and 1.8ms−1 but accelerate in only 2–4ms so that the energy requirements are surface of the water to enable a full depression and elevation cycle  much higher. The champion jumping insects in terms of take-off of the flapping movements of the wings before the fly becomes velocity are some froghoppers (Burrows, 2003; Burrows, 2006) airborne. They both enable escape from the surface of the water without the wings becoming wetted and the body subsequently and some planthoppers (Burrows, 2009a), which achieve their becoming entrapped by the surface tension. prowess by transferring energy stored in a catapult in less than 1ms. A consequence of this is that the ground reaction forces are Jumping performance unsuitably high for jumping from a compliant surface such as A jump by H. alboflorens required the coordinated action of four water; the propulsive legs would penetrate the surface. Pygmy legs, which all started to move within 1ms of each other, as measured mole crickets that also use a catapult deliberately penetrate the from the high-speed images, and their movements paralleled each surface of the water with their propulsive tibiae, but have spring- other during the acceleration phase of a jump. This level of loaded tibial paddles that flare out to increase the tibial surface synchrony between the legs is similar to that seen in grasshoppers area and enable a sufficient volume of water to be pushed and locusts, where the legs, like those of the fly, move in separate downwards (Burrows and Sutton, 2012). planes parallel to the sides of the body (Sutton and Burrows, 2008). In insects where the propulsive hind legs are arranged beneath the ACKNOWLEDGEMENTS body and move in the same plane as each other parallel to the under I am most grateful to Dr Scott E. Brooks (Diptera Unit, Invertebrate Biodiversity Agriculture and Agri-Food Canada, Ottawa, ON, Canada) for identifying this fly. I surface of the body, much closer synchronisation is necessary to would like to thank Ian Meinertzhagen for his hospitality and for making laboratory control jump trajectory in the azimuth plane (Sutton and Burrows, facilities available to me at Dalhousie University where the experimental work was performed. Many thanks also to Steve Shaw, who helped me collect these flies 2010). and provided many insights during the course of the work. Marina Dorosenko Can direct contractions of the trochanteral depressor muscles helped enormously with analysis of the data. generate sufficient force during the acceleration period to lift the fly from the surface of the water, or must some form of energy COMPETING INTERESTS storage and a power amplification mechanism be used? In most No competing interests declared.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Fly jumping from water 1981

FUNDING Gao, X. and Jiang, L. (2004). Biophysics: water-repellent legs of water striders. This research received no specific grant from any funding agency in the public, Nature 432, 36. commercial, or not-for-profit sectors. Glasheen, J. W. and McMahon, T. A. (1996). A hydrodynamic model of locomotion in the basilisk lizard. Nature 380, 340-342. Goodwyn, P. J. P., Wang, J.-T., Wang, Z.-J., Ji, A.-H., Dai, Z.-D. and Fujisaki, K. REFERENCES (2008). Water striders: The biomechanics of water locomotion and functional morphology of the hydrophobic surface (Insecta: Hemiptera-Heteroptera). J. Bionics Askew, G. N. and Marsh, R. L. (2002). Muscle designed for maximum short-term Eng. 5, 121-126. power output: quail flight muscle. J. Exp. Biol. 205, 2153-2160. Hsieh, S. T. (2003). Three-dimensional hindlimb kinematics of water running in the Bennet-Clark, H. C. (1975). The energetics of the jump of the locust Schistocerca plumed basilisk lizard (Basiliscus plumifrons). J. Exp. Biol. 206, 4363-4377. gregaria. J. Exp. Biol. 63, 53-83. Hsieh, S. T. and Lauder, G. V. (2004). Running on water: three-dimensional force Bennet-Clark, H. C. and Lucey, E. C. A. (1967). The jump of the flea: a study of the generation by basilisk lizards. Proc. Natl. Acad. Sci. USA 101, 16784-16788. energetics and a model of the mechanism. J. Exp. Biol. 47, 59-67. Bowdan, E. (1977). Walking and rowing in the water strider, Gerris remigis. II. Muscle Hu, D. L., Chan, B. and Bush, J. W. M. (2003). The hydrodynamics of water strider activity associated with slow and rapid mesothoracic leg movement. J. Comp. locomotion. Nature 424, 663-666. Physiol. 123, 51-57. Josephson, R. K. (1993). Contraction dynamics and power output of skeletal muscle. Burrows, M. (2003). Biomechanics: froghopper insects leap to new heights. Nature Annu. Rev. Physiol. 55, 527-546. 424, 509. Moller Andersen, N. (1982). The Semiaquatic Bugs (Hemiptera, Gerromorpha); Burrows, M. (2006). Jumping performance of froghopper insects. J. Exp. Biol. 209, Phylogeny, Adaptations, Biogeography and Classification. Klampenborg, Denmark: 4607-4621. Scandinavian Science Press. Burrows, M. (2007). Neural control and coordination of jumping in froghopper insects. Murphey, R. K. (1971). Motor control of orientation to prey by the waterstrider Gerris J. Neurophysiol. 97, 320-330. remigis. Z. Vgl. Physiol. 72, 150-167. Burrows, M. (2009a). Jumping performance of planthoppers (Hemiptera, Issidae). J. Nauwelaerts, S. and Aerts, P. (2006). Take-off and landing forces in jumping frogs. J. Exp. Biol. 212, 2844-2855. Exp. Biol. 209, 66-77. Burrows, M. (2009b). Jumping strategies and performance in shore bugs (Hemiptera, Nauwelaerts, S., Scholliers, J. and Aerts, P. (2004). A functional analysis of how Heteroptera, Saldidae). J. Exp. Biol. 212, 106-115. frogs jump out of water. Biol. J. Linn. Soc. Lond. 83, 413-420. Burrows, M. (2011). Jumping mechanisms and performance of snow fleas Rand, A. S. and Marx, H. (1967). Running speed of the lizard Basiliscus basiliscus on (Mecoptera, Boreidae). J. Exp. Biol. 214, 2362-2374. water. Copeia 1967, 230-233. Burrows, M. and Morris, O. (2003). Jumping and kicking in bush crickets. J. Exp. Sutton, G. P. and Burrows, M. (2008). The mechanics of elevation control in locust Biol. 206, 1035-1049. jumping. J. Comp. Physiol. 194A, 557-563. Burrows, M. and Sutton, G. P. (2008). The effect of leg length on jumping performance Sutton, G. P. and Burrows, M. (2010). The mechanics of azimuth control in jumping of short- and long-legged leafhopper insects. J. Exp. Biol. 211, 1317-1325. by froghopper insects. J. Exp. Biol. 213, 1406-1416. Burrows, M. and Sutton, G. P. (2012). Pygmy mole crickets jump from water. Curr. Sutton, G. P. and Burrows, M. (2011). Biomechanics of jumping in the flea. J. Exp. Biol. 22, R990-R991. Biol. 214, 836-847. Burrows, M., Hartung, V. and Hoch, H. (2007). Jumping behaviour in a Gondwanan Trimarchi, J. R. and Schneiderman, A. M. (1995). Initiation of flight in the relict insect (Hemiptera: Coleorrhyncha: Peloridiidae). J. Exp. Biol. 210, 3311-3318. unrestrained fly, Drosophila melanogaster. J. Zool. 235, 211-222. Bush, J. W. M. and Hu, D. L. (2006). Walking on water: biolocomotion at the Weis-Fogh, T. and Alexander, R. M. (1977). The sustained power output from interface. Annu. Rev. Fluid Mech. 38, 339-369. striated muscle. In Scale Effects in Animal Locomotion (ed. T. J. Pedley), pp. 511- Card, G. and Dickinson, M. (2008). Performance trade-offs in the flight initiation of 525. London: Academic Press. Drosophila. J. Exp. Biol. 211, 341-353. Zumstein, N., Forman, O., Nongthomba, U., Sparrow, J. C. and Elliott, C. J. H. Ellington, C. P. (1985). Power and efficiency of insect flight muscle. J. Exp. Biol. 115, (2004). Distance and force production during jumping in wild-type and mutant 293-304. Drosophila melanogaster. J. Exp. Biol. 207, 3515-3522.

THE JOURNAL OF EXPERIMENTAL BIOLOGY