2362

The Journal of Experimental Biology 214, 2362-2374 © 2011. Published by The Company of Biologists Ltd doi:10.1242/jeb.056689

RESEARCH ARTICLE Jumping mechanisms and performance of snow fleas (Mecoptera, Boreidae)

Malcolm Burrows Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK [email protected]

Accepted 11 April 2011

SUMMARY Flightless snow fleas (snow scorpion flies, Mecoptera, Boreidae) live as adults during northern hemisphere winters, often jumping and walking on the surface of snow. Their jumping mechanisms and performance were analysed with high speed imaging. Jumps were propelled by simultaneous movements of both the middle and hind pairs of legs, as judged by the 0.2ms resolution afforded by image rates of 5000framess–1. The middle legs of males represent 140% and the hindlegs 187% of the body length (3.4mm), and the ratio of leg lengths is 1:1.3:1.7 (front:middle:hind). In preparation for a jump the middle legs and hindlegs were rotated forwards at their coxal joints with the fused mesothorax and metathorax. The first propulsive movement of a jump was the rotation of the trochantera about the coxae, powered by large depressor muscles within the thorax. The acceleration time was 6.6ms. The fastest jump by a male had a take-off velocity of 1ms–1, which required 1.1J of energy and a power output of 0.18mW, and exerted a force about 16 times its body weight. Jump distances of about 100mm were unaffected by temperature. This, and the power per mass of muscle requirement of 740Wkg–1, suggests that a catapult mechanism is used. The elastic protein resilin was revealed in four pads at the articulation of the wing hinge with the dorsal head of the pleural ridge of each middle leg and hindleg. By contrast, fleas, which use just their hindlegs for jumping, have only two pads of resilin. This, therefore, provides a functional reference point for considerations about the phylogenetic relationships between snow fleas and true fleas. Supplementary material available online at http://jeb.biologists.org/cgi/content/full/214/14/2362/DC1 Key words: kinematics, resilin, energy storage.

INTRODUCTION 1972; Evans, 1973; Kaschek, 1984). In some ants (Baroni et al., The flightless adults of snow fleas (or snow scorpion flies), Boreus, 1994; Tautz et al., 1994) and a stick insect (Burrows and Morris, are active only during the colder winter months and will often walk 2002), movement of the abdomen adds to the propulsion from the or jump on snow, or on the underlying moss on which they feed, legs. at temperatures of –3 to +3°C. Marshall notes that they ‘often jump Where the legs are used, it is most commonly the single pair of straight up when you approach them for a close look, landing back hindlegs that propel jumping, although small flies such as in the snow with their appendages folded against the body so that Drosophila use their middle legs (Zumstein et al., 2004). The they resemble inanimate specks of dirt on the snow’ (Marshall, hindlegs of jumping insects are arranged mechanically in one of 2006). Their ability to jump is said to be unique among Mecoptera two ways; in locusts and fleas the hindlegs move in planes laterally (Whiting, 2002), but it enables them to escape from predators and displaced on either side of the body, whereas froghoppers, to traverse snow, upon which walking is difficult. An analysis of leafhoppers and planthoppers (Hemiptera, Auchenorrhyncha) use their jumping mechanisms is, however, lacking despite their being an undercarriage arrangement in which they move in the same plane thought to be the closest extant relatives of the fleas (order beneath the body. The mechanics of these different arrangements Siphonaptera). This close relationship is indicated by molecular impose particular constraints upon the jumping mechanisms, studies of four genetic markers (Whiting, 2002; Whiting et al., 2008) resulting, for example, in the elevation and azimuth directions of a and by anatomical and other phenotypic features (Grimaldi and jump being controlled in different ways (Sutton and Burrows, 2008; Engel, 2005). To the criteria that can be used to support this inferred Sutton and Burrows, 2010). phylogenetic relationship, this paper now adds details of the jumping A further difference in the jumping mechanisms results from the mechanisms of Boreus. Some of these mechanisms are clearly in use of different sets of leg muscles to generate the required forces. common with those of fleas (Bennet-Clark and Lucey, 1967; In insects such as locusts (Bennet-Clark, 1975; Heitler and Burrows, Rothschild and Schlein, 1975; Rothschild et al., 1975; Rothschild 1977) and flea beetles (Brackenbury and Wang, 1995), the extensor et al., 1972; Sutton and Burrows, 2011), while the intriguing tibiae muscles in the hind femora generate the force, but in fleas differences suggest a clear evolutionary line. (Bennet-Clark and Lucey, 1967) and in plant-sucking bugs Jumps in insects are usually propelled by the rapid movements (Auchenorrhyncha), force is generated by the trochanteral depressor of a pair of legs, although other parts of the body may be used by muscles within the thorax (Burrows, 2007b; Burrows, 2007c; some groups. For example, in Collembola a jump is propelled by Burrows and Bräunig, 2010). The power in the first example comes extension of an abdominal appendage (Brackenbury and Hunt, 1993; from rotation of the tibiae and in the second from rotation of the Christian, 1978; Christian, 1979) and a click beetle jack-knifes its trochantera. Whichever muscles are used, the same demands exist body at the joint between the prothorax and mesothorax (Evans, for high take-off velocities and short acceleration times, and this

THE JOURNAL OF EXPERIMENTAL BIOLOGY Jumping in snow fleas 2363 means that a catapult mechanism has to be used because the legs time at which the hindlegs and middle legs lost contact with the are short. A catapult mechanism allows the power-producing ground and the insect became airborne was designated as t0ms. muscles to contract slowly and store energy in distortions of the The time at which these legs started to move and propel a jump skeleton, which can then be released suddenly to power the jump. was also determined so that the time between these two events The energy stores are diverse but a role for the elastic protein resilin defined the period over which the Boreus actively accelerated. Peak (Weis-Fogh, 1960) has been implicated in fleas (Bennet-Clark and velocity was calculated as the distance moved in a rolling 3 point Lucey, 1967) and demonstrated in froghoppers (Burrows et al., 2008) average of successive frames. One-hundred and nineteen jumps by and planthoppers (Burrows, 2010). A known exception to the use 18 Boreus (12 males and 6 females) were captured at temperatures of a catapult mechanism is in bush crickets, which have very long of 23–24°C and analysed to determine jumping performance. hindlegs that provide sufficient leverage for direct muscular Measurements are given as means ± s.e.m. contractions to propel a jump (Burrows and Morris, 2003). The external anatomy of the legs was examined in intact Boreus This paper analyses the jumping mechanisms of the snow flea, and after fixation in 70% alcohol or 50% glycerol. Dried specimens Boreus, to understand how it fits into the emerging picture of the were mounted on specimen holders, sputter coated with gold and general principles that underlie jumping in insects. Of particular then examined in a Philips XL-30 scanning electron microscope. interest is whether these mechanisms can also shed light on the To reveal the presence of the rubber-like protein resilin, dissected evolutionary relationships between this group of insects and the fleas. Boreus were viewed through Olympus Mplan 10ϫ/0.25 NA, and A brief report (Edwards, 1987) has suggested some of the LUCPlanFLN 20ϫ/0.45 NA objective lenses, under ultraviolet (UV) mechanisms that might be used. The anatomy of the thorax of Boreus or white epi-illumination on an Olympus BX51WI compound (Fuller, 1954) shows that the legs are arranged at the sides of the microscope. UV light from an X-cite series 120 metal halide light body and details of its thoracic musculature (Fuller, 1955) indicate source was conditioned by a Semrock DAPI-5060B Brightline series that large trochanteral muscles in the thorax may power jumping. UV filter set (Semrock, Rochester, NY, USA) with a sharp-edged Both features are shared by true fleas. High speed images of jumping (1% transmission limits) band from 350 to 407nm. The resulting presented here show that the two middle legs and the two hindlegs blue fluorescence emission was collected at wavelengths from 413 move together to power jumping. Paralleling the use of four legs, to 483nm through a dichroic beam splitter. four resilin pads are revealed that are associated with each middle leg and hindleg, but not with the front legs. In contrast, in fleas the RESULTS hindlegs are the sole provider of power for jumping and only two Adult Boreus are flightless, so their forms of locomotion are pads of resilin are found associated with them. restricted to walking and jumping. Walking was affected by the low temperatures at which Boreus lives in the winter. At 8°C walking MATERIALS AND METHODS speeds of 14mms–1 were measured but at 3°C speeds fell to as low Adult male and female Boreus hyemalis (Linnaeus 1767) were as 1mm s–1. In adult females, both pairs of wings are greatly reduced, caught in January and February of 2008–2010 in pit fall traps laid and in adult males they are modified to form dorsally protruding in sandy soil beneath moss near Santon Downham and Lakenheath, and backwardly curved hooks (Fig.1) which are used to grab a Norfolk, England. They were maintained in the laboratory for a few female in mating. All parts of the body are darkly coloured. The days feeding on their host moss at temperatures of 4–5°C. They head in both sexes has a large ventrally pointing rostrum, or beak, belong to the order Mecoptera (scorpion flies) and to the family with biting mouthparts at the end, and prominent articulated Boreidae that consists of 24–26 species in three genera of Holarctic antennae (64±2.9% of the body length, mean ± s.e.m., N6 males) insects (Grimaldi and Engel, 2005). Colloquially they are known that are often rested on the ground, particularly at the start of a jump. as snow fleas, but so too are springtails (Collembola) such as Females have a large curved ovipositor protruding prominently from Hypogastrura nivicola. They are also, and less confusingly, known the posterior of the abdomen. Females weighed 4.2±0.37mg (N9), as snow scorpion flies. The results are based on an analysis of 28 whereas males weighed only 2.9±0.28mg (N10) (Table1). Females adult Boreus. had a body length of 3.6±0.26mm (N7), excluding the length of Sequential images of jumps were captured at rates of 5000s–1 the ovipositor, compared with males at 3.4±0.2mm (N13). Females with an exposure time of 0.1ms using a single Photron Fastcam are therefore significantly heavier (t-test, t172.881, P0.01) than 1024PCI high speed camera [Photron (Europe) Ltd, West Wycombe, males but are not significantly longer (t-test, t180.574, P0.73), Bucks, UK], and were fed directly to a laptop computer. The camera, when the ovipositor is discounted. with a 100mm micro Tokina lens, pointed directly at the middle of a glass chamber 80mm wide, 80mm tall and 10mm deep at floor level and widening to 25mm at the top. The floor of the chamber was of high density foam. Boreus was free to jump in any direction (see supplementary material Movies1–3 for jumps viewed from the side, above and behind, respectively) but the shape of the chamber constrained most jumps to the image plane of the camera. Measurements of changes in joint angles and distances moved were made from jumps that were parallel to the image plane of the camera, or as close as possible to this plane. Jumps that deviated to either side of the image plane of the camera by ±30deg were calculated to result in a maximum error of 10% in the measurements of joint or body angles. Sequences of images were analysed with 1 mm Motionscope camera software (Redlake Imaging, Tucson, AZ, USA), or with Canvas 11 (ACD Systems of America, Miami, FL, Fig.1. Photograph of a side view of a male snow flea, Boreus hyemalis,on USA). To allow different jumps to be aligned and compared, the moss, its natural host plant.

THE JOURNAL OF EXPERIMENTAL BIOLOGY 2364 M. Burrows

Structure of the legs 0. 33 The mesothorax and metathorax are fused to form a strong

B u rrow s , and rigid cuticular box supporting the middle legs and hindlegs, 3 .1 4. 3 4.5 3 .6 2. 3 1.7 2.9 7.9 1. 8 3 . 4.2 10 whereas the prothorax supporting the front legs is separately Hindleg length

(mm)/m ass (mg) articulated (Fig.2A, Fig.3A). The boundary between the episternum and epimerum of both the mesothoracic and 4 2.7 8 90

10 8 112 metathoracic segments is marked by an indentation. This represents the pleural ridge that extends from the wing hinge dorsally to the articulation of the coxa ventrally. The surfaces B u rrow s a nd Su tton, 200 8 ; 3 9 4 8 61 1 3 5 8 474 38 66 703 57 1 8 2 55 65 of the thoracic cuticle and the legs have a dense covering of 112 157 140 1 83 107 144 fine hairs ranging from 15 to 35m in length. The front legs are the shortest and in a male are 3.5mm long, whereas the middle legs are 4.4mm long and the hindlegs are the longest Leg length (% b ody length) B u rrow s , 2007 a ; 8 5 40 3 54 29 50 46 38 3 7 8 2 8 110 of all at 5.4mm (Table1). Relative to the front legs this gives Front Middle Hind   a ratio of leg lengths in males of 1:1.3:1.7 (front:middle:hind) and in females of 1:1.2:1.7. In males, the middle legs represent 140% and the hindlegs 187% of the body length, while in u mping in s ect th a t h ve their prop l ive leg either the ide of B u rrow s , 2006; .2 7 1.9 1.5 2.1 1.7 females the values are smaller when the length of the ovipositor is excluded. Proportional to each other, to the length of the body and to the body mass, this makes the leg lengths of the 1 1 snow flea similar to those of a flea (Table1). B u rrow s , 2009 a ; 6 The legs move in two separate planes on each side of the

a tio of leg length s body with the body slung between them. The middle and hind R 1 1.21 2.7 2.1 4.5 1 1 1. 3 1 1. 33 1 11 1. 3 1.2 1.7 coxae of a male are each about 0.6mm long and 0.2–0.25mm Front Middle Hind wide and articulate with the fused mesothoracic and metathoracic box (Fig.2B,C and Fig.3A,B). These articulations ome other j u mping in s ect s ome other 8 b ody form i s comp a red with th t of other j allow small forward and backward rotations of these coxae. B u rrow s a nd Wolf, 2002; 1 7 4 5 a nd 6.6 1.1 1.1 1.7 1 1.2The front 2.2 coxa, in contrast, is somewhat shorter. The hind and T a r sus middle trochantera of a male are each about 0.2mm long and articulate through an angle of about 140deg with their respective coxa (Fig.2D). The anterior and posterior hinges b i a 3 . 8 16.4 4.9 1 1.1 2.9 6 3

3 ye a r period. Boreus of these articulations mean that levation of the joints swings 1.5±0.05 2.0±0.06 the more distal segments of each leg dorsally and forwards Hindleg length (mm) Boreus hyemalis (Fig.3A). Accordingly, when fully levated, as in preparation B u rrow s a nd Morri , 200 3 ; 4 20 19. 3 0.5 0.6 3 .1 2.7 0.5 0.9 0.4 1 1 1.4 41 44 57 1.4

17. 3 22.1 25.5 for a jump, both femora are pressed against the lateral surfaces Fem u rTi of the fused epimera and episterna, with the femoro-tibial joints pointing dorsally. The movements of the coxo-trochanteral joint would appear to be monitored by arrays of proprioceptive

3 hairs (Fig.2D, Fig.3B–D). One group of 8–10 hairs, 40–50m 0.4 10.9 1.6 1.7 0.5 2.6 1 1 1.2 1. 8 1 1 1.2 5 3 3 .2 T a r sus long is associated with a dorsally pointing cuticular protrusion B u rrow s a nd Picker, 2010; 3 (Fig.2D). Other groups are associated with the two articulations of each of the middle legs and hindlegs. On the middle leg, .1 5.1 b i a 0.4 0.7 0. 8 1.70.61. 8 0.7 0. 3 2.2 10.7 there is a group of about 20 hairs, 10–12 m long on both sides

1.1±0.05 1.5±0.05 1.4±0.0 3  of each articulation (Fig.3B,C). On the hindlegs, there is a T ab le 1. Body form in s now fle as

Middle leg length (mm) similar arrangement of hairs though some of them may be up

0.4 7. 38 0. 8 1. 3 0.5 to 20m in length (Fig.3B,D). Fem u rTi 1.1±0.0 8 M.B. ( u np ub li s hed d a t ); 2 The joint between the trochanter and femur consists of a c au ght d u ring J a n ua ry nd Fe b r in the sa me loc tion over dorsal and ventral articulation that allows the femur to move through only a small angle. The hind femur of a male is 1.4mm .1 1. 8  6 1 1.1 0.7 1.1 1. 8 4 3 3 .5 8 .5 3 .2 (mm) ( N = 1 3 ) 3 .4±0.2

3 .6±0.26 0.9±0.06 1.0±0.04 1.0±0.04 1.2±0.09 1.4±0.26 1.7±0.0 long but only 0.12mm in diameter at its widest point, and the Body length

Boreus hyemalis middle femur is 1.1mm long and about the same diameter (Fig.2E). There is therefore little space in either the middle 2 0.7 1. 8 6.7 5.2 1.42.1 1.2 0.5 420 21.4 5.9 5.7 276 66.4 9. 8

12. 3 1 8 .4 2 3 . 88 or hind femora in which to accommodate an extensor tibiae (mg) 1250 1600 46 7.5 7.4 5.2 2 3 .1 21.9 Su tton a nd B u rrow s , 2011; ( N = 9) 1 ( N = 10) 2.9±0.2 8 4.2±0. 3 7

Body m ass muscle capable of generating force that might make a substantive contribution to jumping movements. The femoro- tibial joints of both hindlegs and middle legs consist of a lateral

3 and a medial articulation that allow movements of some

5 170deg. A hind tibia is 1.5mm long but only 0.07mm wide. 1 4 10 The longest parts of the middle legs and hindlegs are the tarsi, 7 8 9 6 which in a male are 1.5 and 2.0mm long, respectively. Arrays 2 2 of ventrally pointing spines are present at the articulation of b ody or u nderne a th it. D t from: 2009 b . Archaeopsyllus erinacei Schistocerca gregaria (greg a rio us m le) Schistocerca gregaria ( s olit a rio us m le) Xya capensis Pholidoptera griseoptera (m a le) Saldula saltatoria Philaenus spumarius Aphrodes makarovi Ulopa reticulata Issus coleoptratus Prosarthria teretrirostris (m a le) m a le ( N = 9) fem a le ( N = 7) D a t were o b ined from 9 m le nd 7 fem Loc us t Loc us t Pygmy mole cricket s B us h cricket Froghopper Le a fhopper Le a fhopper Pl a nthopper In s ect with le gs underneath body S hore bu g In s ect Boreus hyemalis Boreus hyemalis F a l s e tick in ect In s ect with le gs at ide of body Hedgehog fle a the five tarsal segments.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Jumping in snow fleas 2365

Fig.2. Scanning electron micrographs of the A Meta Meta Meso Meso Spiracle Pronotum epimerum episternum epimerum episternum right side of a male Boreus. (A)The head and thorax to show the fusion of the mesothorax and metathorax and the articulation of the large mesothoracic and metathoracic coxae. The front legs are separate from this rigid part of the thorax. Abdomen The black arrows point to the articulation of a pleural ridge with a wing. (B)The articulation of the right hind coxa with the metathorax. (C)The articulation of the right middle coxa. (D)The coxo-trochanteral joint of the right middle leg. Hair plates associated with this Front joint are shown at higher magnification in the coxa two insets (arrows). (E)The femoro-tibial joint Hind Middle of the right middle leg. coxa coxa Beak

Front femur 200 µm Middle femur Trochanter B Metathorax C Mesothorax

Episternum

Hind Middle coxa coxa 100 µm 100 µm

D 10 µm E

10 µm Femur Coxa

Trochanter Tibia Femur 100 µm 100 µm

Kinematics of jumping levation movements moved the femora into either a vertical or a High speed images of jumps were captured from different angles slightly forward-pointing position so that proximally their medial by a single camera (Figs4–7) so that the orientation and movements surfaces were closely pressed against the epimera and episterna of of the legs could be interpreted in all three dimensions. The majority the fused mesothorax and metathorax (Figs4 and 5). The femora of the jumps were viewed from the side (male in Fig.4, female in of the middle legs and hindlegs were parallel to each other and were Fig.5; supplementary material Movie1), supplemented by views sometimes splayed laterally from the body (Figs 6 and 7). Their from above (Fig.6 and supplementary material Movie2) and behind femoro-tibial joints protruded above the dorsal surface of the thorax (Fig.7 and supplementary material Movie3) to give further (Figs4 and 5) and were flexed so that the tibiae and tarsi were drawn information about the angles of femora relative to the body and of forward. The degree of flexion of the femoro-tibial joints varied in the femoro-tibial angles. The following description combines different jumps indicating that full flexion was not a pre-requisite information from all views, while the angular changes of the leg for jumping. The front legs, in contrast, adopted different angles joints during a jump are plotted in Fig.8. The sequence of leg prior to different jumps. The antennae were usually held elevated movements in jumping was observed to be the same in males and before a jump so that they pointed anteriorly. In preparation for females. most jumps they were moved downwards so that the distal third of Jumps occurred from a standing start, or followed a period of their segments rested on the ground (Figs4 and 5). The whole body walking after a short and variable pause. All were preceded by adopted a curved position. movements of the middle legs and hindlegs into their most levated At the start of a jump, the hind tarsi were level with, or just behind, positions by rotation about the coxo-trochanteral joints. These the tip of the abdomen and lateral to each side of the body. The

THE JOURNAL OF EXPERIMENTAL BIOLOGY 2366 M. Burrows

Fig. 3. Scanning electron micrographs of the ventral Anterior  A Hind surface of a female Boreus. (A) The proximal joints of femur  Trochanter the middle legs and hindlegs are closely apposed, but separated from those of the front legs. Anterior is Coxa Coxa to the right. (B)The joints between the coxae and trochantera of the middle legs and hindlegs. Hair plates are indicated by white arrows. Anterior is to the top. (C)The left middle coxo-trochanteral joint from another Boreus showing the hair plates associated with the anterior articulation of this joint Coxa (white arrows). (D)The right hind coxo-trochanteral joint of the Boreus in B, showing hair plates Coxa associated with the anterior articulation.

Middle femur Front Trochantera femur 200 µm

B Anterior Middle coxa

Trochanter

Hind coxa

Trochanter 200 µm

C Left middle coxa D Right hind coxa

Trochanter Trochanter

50 µm 20 µm middle legs adopted a similar but more anterior position, with their extension movements of the coxo-trochanteral and femoro-tibial femora and tibiae parallel to the respective segments of the hindlegs joints of the middle legs and hindlegs then raised the front of the (Fig.6). The first detectable propulsive motion of a jump, as viewed body further so that the curvature of the antennae became less from the side, was a simultaneous backwards movement of the four pronounced as fewer of their segments contacted the ground. The middle and hind femora (Figs4 and 5). These changes were movements of the middle legs and hindlegs proceeded in unison produced by depression of the coxo-trochanteral joints with little with all the particular segments of one leg moving in parallel with rotation evident at the trochantero-femoral joints, with the result the corresponding segment on the other leg joints until they reached that a trochanter and a femur seemed to act as a unit. The tibiae almost full depression and extension. At this stage, the middle and were then extended about the femora so that the body was hind tarsi were level with, or behind, the tip of the abdomen. The progressively raised from the ground and the insect was propelled tarsi remained in their same positions outside the lateral limits of forwards. The antennae initially remained in contact with the ground the body. The front legs made no obvious movements that could as the middle legs and hindlegs depressed and extended, pushing apparently contribute substantive force to the jump. Indeed, the front the body upwards and forwards. The continuing depression and legs lost contact with the ground only 1–3ms after the first

THE JOURNAL OF EXPERIMENTAL BIOLOGY Jumping in snow fleas 2367

Fig. 4. Jump of a male Boreus viewed from –13 ms  LH Take-off 0 ms the side. The frames are arranged in two columns at the times indicated, with the take- LM off time designated as 0ms. The middle legs and hindlegs both began to move at –7.5ms. The right front leg (RF) is indicated by LM vertical, yellow arrows, the middle legs (LM RH RM RF and RM) by horizontal arrows with white LH heads, and the hindlegs (RH and LH) by First movement diagonal, pink arrows. This convention is also –7.5 RH RM RF of middle legs used in Figs5–7. and +1 hindlegs

–5 LM LF LH

LM

LH RM RF RH –2 +2

LH

RH RM RF LF –1 LM

RH RM RF LH 2 mm

movements of the other legs and sometimes as much as 4ms before sustained extension of the tibia about the femur was delayed by take-off (Fig.5). Take-off was marked by the middle and hindlegs 2–3ms relative to the start of the coxo-trochanteral joint movements. losing contact with the ground. After take-off, the tibiae of both the Then the femoro-tibial joints of the four middle legs and hindlegs middle legs and hindlegs crossed over and during the initial part of were extended in parallel until take-off (Fig.8B,D). After take-off, the trajectory trailed behind the body. there was sometimes (Fig.8D) a slight initial flexion of these joints. The parallel movements of the middle legs and hindlegs were In contrast, the femoro-tibial joints of the front legs, in addition to revealed clearly when changes in the angles of their joints were their coxo-trochanteral joints, showed no changes consistent with plotted (Fig.8). The analysis given here is of a jump that was close their contributing substantially to propulsion in any jumps. to the mean performance by male snow fleas. The coxo-trochanteral joint was the first to move, as indicated by changes in the angle of Jumping performance the femur relative to the body in dorsal views (Fig.8A), or by the The acceleration period of a jump, measured from the first coxo-trochanteral joint itself when viewed from the side (Fig.8C). observable trochanteral depression to the time when all legs had The first movements of these joints in the hindlegs and middle legs lost contact with the ground, was 6.6±0.33ms in males and occurred within the same frame (resolution 0.2ms) in all jumps 6.6±0.17ms in females (mean of means of 8 males and 6 females analysed. Changes in the angle of this joint in the two middle legs performing 87 jumps) (Table2). These values are not significantly and the two hindlegs then proceeded in parallel until they reached different (t-test, t120.164, P0.872). full depression at take-off. In contrast, the angle of this joint in a The angle of the body relative to the ground was set by movements front leg changed little throughout the acceleration period of a jump of the front legs that preceded any propulsive movements by the (Fig.8A). The initial depression of the coxa was also followed by middle legs and hindlegs. At take-off the body angle, represented by changes in the femoro-tibial angles as the thrust was applied by the a line joining the tip of the abdomen with the dorsal surface of the tarsi to the ground in moving the insect forwards (Fig.8B). A head, was 14.0±2.58deg (range 11–33deg) in males and 16.2±2.33deg

THE JOURNAL OF EXPERIMENTAL BIOLOGY 2368 M. Burrows

LH –31 ms –1 Fig.5. Jump of a female Boreus viewed from the side. Before the jump the antennae were raised but during the jump they were lowered to the ground and were bent as the thrust was applied by the middle legs and hindlegs, which both RH RM RF began to move at –5ms. The front legs lost –20 contact with the ground at –4ms. Take-off 0 ms

LH First movement –5 RF of middle legs LH LM and RH hindlegs RM

+1 RH RM RF –4

–3

+2

–2 RF RH RM LM LH RH LM LF LH 2 mm RM RF

(range 10–26deg) in females (mean of means of 9 males and 6 females Once airborne the body remained quite stable. In the pitch plane performing 83 jumps) (Table2). These values again are not the rate of rotation, measured from 2ms before take-off to 2ms –1 significantly different (t-test, t130.58, P0.572). The initial trajectory after take-off, was 5.4±0.61Hz or 1900degs (mean of means of the jump in males was 39.6±2.06deg (range 32–47.5deg, mean of 12 Boreus performing 40 jumps with a minimum of 3 jumps of means for 7 males performing 29 jumps) and in females was by each, range 2.1–9.5Hz or 750–3400degs–1). In a 100mm long 52.2±4.55deg (range 41.6–65.5deg, mean of means for 5 females jump with a take-off velocity of 1ms–1 and an elevation of 40deg performing 19 jumps). These figures are significantly different (t-test, describing a parabolic trajectory, the body is predicted to rotate t102.81, P0.018). The take-off velocity, measured as a three-point a maximum of 0.7 times (or by 250deg, range 100–450deg) before rolling average in a 2ms period preceding take-off, was 0.8±0.02ms–1 landing. Only four jumps were recorded with rotation in the roll in males (mean of means of 29 jumps by 7 males, range plane (mean 43Hz, range 13–62Hz) and only one jump yawed 0.72–0.85ms–1) and 0.7±0.04ms–1 in females (mean of means of 19 at 1Hz. jumps by 5 females, range 0.64–0.85ms–1). These values are not significantly different (t-test, t101.827, P0.98). The fastest jump was Muscles made by a male that achieved a take-off velocity of 1ms–1 with an From the kinematic analysis of the jumping movements, the key acceleration of 161ms–2, which required an energy output of 1.1J movements of both the middle legs and hindlegs were a levation and a power output of 0.18mW, and exerted a force of 0.35mN or followed by a rapid depression of the coxo-trochanteral joints that about 16 times its body weight (Table2 gives figures for mean and provided the propulsive power. Most of the space within both the best performances of both sexes and the formulae used in the mesothorax and metathorax is occupied by huge trochanteral calculations). depressor muscles [dvm II – musculus dorsoventralis mesothoracis; The maximum distances jumped at 21.5°C and at less than 10°C dvm III – musculus dorsoventralis metathoracis (Fuller, 1955)], were not significantly different (paired sample t-test, t51.963, which are the largest muscles in the body (Fig.9A,B). These muscles P0.107). The time taken to prepare for a jump has, however, been arise from the mesothoracic and metathoracic notum, and attach to reported to be longer at lower temperatures (Edwards, 1987). The tendons that extend through their respective coxae to insert on the mean distances jumped by males at 21.5°C were 100mm in males dorsal rims of the trochantera. In contrast, the homologous muscles and 85mm in females (mean of means for 20 jumps by 4 Boreus moving the trochantera of the front legs are much smaller. Muscles of each sex). levating the trochantera into their cocked position ready for jumping

THE JOURNAL OF EXPERIMENTAL BIOLOGY Jumping in snow fleas 2369

First movement –6 ms –1.2 –8.8 ms –2.8 of middle legs LH RH and LM LF LM LF hindlegs LM RM LH LH

RF RF RM RM LF RF RH RH –8 –4 –0.8 –2

–6.8 –3 –0.4 –1.4 LF LM LH

RF RM First movement –5.6 RH of middle legs and –2 Take-off 0 ms hindlegs

LF –0.8 LM LH

RF –4.8 RM RH

–1.6 +2

LF Take-off 0 ms

LM RH –4 RF LH RM 2 mm

Fig.6. Jump of a male Boreus from the vertical rear wall of the chamber, 2 mm viewed dorsally. All the legs project laterally from the body. The middle legs and hindlegs rotate simultaneously about their coxo-trochanteral and femoro-tibial joints to propel the jump, but the front legs do not move.

Fig.7. Jump of a male Boreus viewed from behind as it moved away from are smaller than the depressors used for propulsion and are located the camera. The sequence shows how the body is slung between the middle legs and hindlegs that propel the jump, while the front legs lift from in the coxae (Fuller, 1955). the ground before take-off. The yellow vertical arrows point to the femoro- tibial joints of the front legs; the upper, horizontal arrows with white heads Energy storage point to the femoro-tibial joints of the middle legs and the lower ones to the Assuming that the depressor muscles generating the propulsive middle tarsi; the upper diagonal pink arrows point to the femoro-tibial joints movements of a jump represent about 11% of body mass, as in of the hindlegs and the lower ones to the hind tarsi. froghoppers (Burrows, 2007c), the power per mass of muscle ranges from 450Wkg–1 for the best jumps of females to 740Wkg–1 for the best jumps of males (Table2). In Boreus, the muscle mass may be energy must be stored before a jump and then released rapidly in greater than in froghoppers because two pairs of legs (the middle a catapult-like action. and hind) propel jumping. Nevertheless, these values are close to A search was therefore carried out for sites where energy might the maximum active contractile limits of striated muscles, which be stored, with a particular focus on the occurrence of resilin, which range from 250 to 500Wkg–1 when operating at high temperatures in fleas (Bennet-Clark and Lucey, 1967) has been implicated in (Askew and Marsh, 2002; Ellington, 1985; Josephson, 1993; Weis- energy storage for jumping. In froghoppers (Burrows et al., 2008) Fogh and Alexander, 1977). In contrast, Boreus jumps readily at and planthoppers (Burrows, 2010), resilin has been clearly shown temperatures near 0°C, suggesting that direct contractions of the to be present at the sites where energy is stored for jumping. Under muscles would be unlikely to be able to power jumping. Some illumination with specific wavelengths of UV light, four patches of

THE JOURNAL OF EXPERIMENTAL BIOLOGY 2370 M. Burrows

Body/femur angle Fig.8. Angular changes of middle leg and ACTake-off Coxo-trochanteral angle 160 Take-off hindleg joints during jumping. The angles measured are shown superimposed on 140 RH frames from the jumps. (A,B)Jump of a 120 male Boreus viewed from above (Fig.6). 100 (A)Changes in the angles of the femora relative to the body start at the same time LF 80 RH (open vertical arrow) in the middle legs LH 60 RM (black lines and symbols, RM and LM) and hindlegs (pink lines and symbols, RH 40 LM RM and LH). The middle legs and hindlegs 20 RH then move together during the 0 acceleration phase of the jump, but the same angle of the left front leg (green line Femoro-tibial angle 180 BDFemoro-tibial angle and symbols, LF) changes little. 160 (B)Changes in the femoro-tibial angle

Joint a ngle (deg) also occur at the same time in the middle 140 legs and hindlegs, but occur after those at 120 RM the coxo-trochanteral joints. The same 100 angle of a front leg shows little change. RM (C,D)A jump to the right by another male 80 LH Boreus. The coxo-trochanteral (C) and LM 60 femoro-tibial (D) angles of the right middle RH legs and hindlegs change at the same 40 LF RH RM time. –6 –4 –2 0 +2 –8 –6 –4 –2 0 +2 Time (ms) bright blue fluorescence were found, two in the mesothorax and the front legs are separate. Both the middle legs and hindlegs are two in the metathorax, each associated with a particular middle leg longer than the body, with the middle legs representing 140% and and hindleg (Fig.10). No blue fluorescence was found at the the hindlegs 187% of the body length in males. How do these equivalent sites in the prothorax associated with the front legs. The relationships compare with those in other insects that propel jumping fluorescence emanated from a crescent-shaped area of cuticle with their legs (Tables1 and 2)? Jumping insects can be divided (Fig.10B) at the articulation of the heavily sclerotised dorsal head into two broad functional categories according to the way the of the pleural ridges of the mesothoracic and metathoracic segments hindlegs are oriented. These different arrangements have significant (indicated externally by the black arrows in Fig.2A) with the wing mechanical consequences for the way force is delivered to the ground hinge. The fluorescence was highly localised and was not present and the control of jumping (Sutton and Burrows, 2008; Sutton and in surrounding skeletal structures or other tissue. The blue Burrows, 2010). fluorescence diminished in intensity if the pH of a saline solution In the first group are insects such as froghoppers, leafhoppers was made acidic and recovered when it was returned to its normal and planthoppers, with their legs slung beneath the body. All their pH. In alkaline saline the intensity increased but subsided to its jumps are powered by trochanteral depressor muscles. In this group previous level when returned to a saline at its normal pH. Such the proportions of the hindlegs relative to the other legs are low specific, blue fluorescence and its reversible pH dependence are except in the long-legged cicadellids. Relative to body length, the two key signatures of the elastic protein resilin (Andersen and Weis- hindlegs are much shorter than those of snow fleas and relative to Fogh, 1964; Burrows et al., 2008; Neff et al., 2001). body mass they have a lower index. In the second group are insects such as snow fleas Boreus, true DISCUSSION fleas, locusts and bush crickets, which all have legs that move at Snow fleas, Boreus, propel their jumps by rapid depression and the sides of the body. Power for jumping is generated by trochanteral extension movements of their middle legs and hindlegs, achieving depressor muscles in snow fleas and fleas, but by extensor tibiae take-off velocities of up to 1ms–1 (mean of 0.8ms–1 in males and muscles in Orthopterans and flea beetles. In fleas such as the 0.7ms–1 in females) and forward distances of about 100mm, hedgehog flea Archaeopsyllus erinacei (Table1) the proportions of equivalent to some 30 times their body length. Once airborne, the the legs relative to each other and relative to the length or mass of body remains relatively stable with only low rates of rotation in the the body are similar to those in snow fleas. In Orthoptera the hindlegs pitch plane. Jumps are often strung together in a sequence, each are proportionately longer than the other legs, but relative to body with an erratic shift in direction and ending in a cataleptic posture, length they are shorter, and relative to body mass they have indices suggesting that they subserve an escape function. Jumping also gives in the same range as snow fleas. The exceptions are bush crickets, a marked improvement to the speed of locomotion when compared which have hindlegs that are much longer relative to body length, with natural walking speeds, particularly at low temperatures. In and male Prosarthria, which have a much higher index relative to these insects, jumping is all the more remarkable because the adults body mass. only live for a few weeks, emerging in the middle of a northern What sets snow fleas apart from all other members of this second hemisphere winter and often jumping from the surface of snow. group is that all 119 of jumps recorded in this study were propelled by the middle legs and hindlegs acting together. No jumps were Actions of the legs during jumping observed in which the hindlegs acted alone. The first movements The middle legs and hindlegs are slung from the sides of a strong of the four legs appeared to occur at the same time, as determined box formed by the fusion of the mesothorax and metathorax, while by the capture rate of the images, which gave a resolution of 0.2ms.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Jumping in snow fleas 2371

No detectable pattern emerged to suggest that one pair of

m ) legs moved consistently before the other pair, or that one 1 –1 leg of a particular pair moved before the other. During the 3 50 450 4 3 0 740 6000 6 8 00 6500 2200 4400 1900 m ass W kg 14,000 3 5,500 14,000 114,500 /(0.11 acceleration phase of a jump, the angular changes of the p Power/m us cle coxo-trochanteral joints, which are key to the propulsion, were matched in all four legs. Similar and progressive angular changes in the femoro-tibial joints also followed N) – 3 4 mf in all four legs. No observations indicated that the timing 9 8 66 11 19 0.7 1.1 160 0.46 0.40 0. 33 0. 3 5 0.5 3 F = of the movements of the four legs had to be as closely controlled as for the hindlegs in planthoppers (Burrows, 2010). The mechanics of the legs also do not suggest that uncontrollable spins would result, as in planthoppers, if W) mN (10 – 3 / t

1 the legs did not act precisely at the same time. Delivering 4 83 1 3 2 8 1.5 0.5 155 333 3 15 0.4 3 0.16 0.17 0.14 0.1 8 0.2 3 p = e closely timed movements of four legs nevertheless poses challenges for the underlying neural control mechanisms, and there is no possibility that simple mechanical linkages 2 J) mW (10 –6 mv between the legs could simplify the coordination as in 8 8 . 5 8 77 0.6 1. 8 1.1 1. 3 0.9 1.1 0.2 3 .4 155 9000 planthoppers. e = 0.5 u J (10

Why use four legs?

8 There are at least three possible reasons why snow fleas g 9 8 11 12 12 16 5 8 3 41 54 160 550 102 2 8 64 10 8 g force Energy ( e ) Power ( p ) Force ( F )

g = f /9. 8 6 need to use both middle legs and hindlegs to propel jumping. First, the use of four legs will distribute the ground

–2 reaction forces over a larger area provided by the four tarsi. ( f ) 960 115 121 161 106 56 8 33 5 529 1 8 01 f = v / t 1600 5400 1 33 0 2 8 00 1055 m s These forces are further reduced by the 6 times longer Acceler a tion

s now fle as acceleration time of a snow flea jump compared with that of a flea. Lower ground reaction forces should enable jumping either from more compliant surfaces or from soft 3 3 9 27 14 deg a nce of ( N = 9) ( N = 6)

t a ke-off surfaces such as snow. A similar outcome is found for 33 ( N = 1) 3 6.7±5.0 14.0±2.5 8 16.2±2. 33

Body a ngle t jumping leafhoppers, a few species of which have long g force, energy, power a nd force re ll bas ed on the me n v l u e s given in t ab le for m ass , cceler tion time (time to ke-off) hindlegs while others have short hindlegs (Burrows and B u rrow s , 2009 a .

5 Sutton, 2008). Both use a catapult mechanism for jumping 92 45 5 8 50 deg a ngle ( N = 7) ( N = 5) and achieve similar take-off velocities, but it takes longer 52±6.5 47±4.7 T a ke-off 3 9.6±2.06 52.2±4.55 3 7.1±4.40 to accelerate long hindlegs, so they will exert lower ground reaction forces. Like the snow flea, this should enable take-

B u rrow s , 2007 a ; off from more compliant surfaces. 4 –1 s 1 1. 33 1.9 0.9 4.7 2.9 1. 8 3 .2 Second, using four legs gives a stable platform for take- 8 ±0.10 46. 8 ±2.0 2 8 ±1.9 ( N = 7) ( N = 5) . T ab le 2. J u mping perform T a ke-off 0. 8 ±0.02 0.7±0.04 2.5±0.09

velocity ( v ) off. If the centre of mass is between the middle legs and hindlegs, their torques will be in opposition. A consequence B u rrow s , 2006;

3 of this is that the rate of spin of the body once airborne )m s )m – 3

3 0 should be low. The kinematic analysis confirmed this by 12 1.4 1.2 7.4 6.2 3 .4 2.75 off ( t ) ( N = 8 ) ( N = 6) 0. 8 75 20– showing that the mean rate of rotation in the pitch plane 6.6±0. 33 6.6±0.17 3 .9±0.05 1. 3 ±0.0 Time to t a ke was only 5Hz and rotation in the roll plane was rare. In contrast, fleas spin in the pitch plane at rates as high as 40Hz (G. P. Sutton and M.B., unpublished observations), m) m s (10 – 3 froghoppers at up to 80Hz (Burrows, 2006) and pygmy 1. 8 2.0 3 .5 ( N = 7) .5±0.22 4.4±0.1 8 ( N = 1 3 ) 3 .4±0.2 3 .6± 0.2 6.1±0.0 8 3 .5±0.09 mole crickets at 190Hz (Burrows and Picker, 2010). Bennet-Cl a rk nd L u cey, 1967; 2 Third, two pairs of legs may be the only way of , comp a red with th t of other j u mping in s ect . The v l e for cceler tion, generating enough power to launch a snow flea into the air. The legs are thin and the femora contain little muscle kg) mm (10

–6 mass so that most of the power must come from the 0.7 1.0 3 .5 2.2 2.1 0.45 1 1 50 ( N = 1) ( N = 9) 8 .4±1. 38 ( N = 10) 2.9±0.2 8 4.2±0. 3 7 2.1±0.09

Boreus hyemalis trochanteral muscles in the thorax. Again, the volume of 12. 3 ±0.74 1500–2000 mg (10

Body m ass ( ) Body length one segment of the thorax may mean that the mass of muscle that can be accommodated is insufficient to Su tton a nd B u rrow s , 2011; 1 generate the necessary power. Only a few other insects and some spiders use two pairs

a nce of s now fle as , of legs to propel jumping, and the advantages in doing so 1 spumarius makarovi

3 are probably similar to those of snow fleas. The ant, 4 2 5 , m a le , fem a le Myrmecia nigrocincta, propels its jumps by extension of 6 (greg a rio us ph as e) its middle legs and hindlegs (Tautz et al., 1994), judged a nd velocity. D t from: Archaeopsyllus erinacei Me a n ( N = 10) Be s t Be s t Boreus Me a n ( N = 9) Be s t Boreus Me a n ( N = 7) Be s t Spilopsyllus cuniculus Philaenus Me a n ( N = 3 4) Aphrodes Me a n ( N = 4 3 )1 Saldula saltatoria Me a n ( N = 3 2) Schistocerca gregaria Be s t Be s t R abb it fle a Hedgehog fle a Form u l a Unit s S now fle a S now fle a Froghopper Le a fhopper S hore bu g Loc us t J u mping perform to be simultaneous by images captured at intervals of

THE JOURNAL OF EXPERIMENTAL BIOLOGY 2372 M. Burrows

(Baroni et al., 1994) to 0.7ms–1 (Tautz et al., 1994), but it is unclear Right hindleg Right middle leg Right front leg A how either value was measured. Similarly, the calculations of Trochanter Femur acceleration and energy requirements are not clear enough for comparison (Baroni et al., 1994). The stick insect Sipyloidea sp. ‘Thailand 8’ throws the mass of its abdomen forward and pushes off the ground with its thin middle legs and hindlegs in a jump that reaches a take-off velocity of between 0.6 and 0.8ms–1 (Burrows and Morris, 2002). Some jumping spiders such as Salticus scenicus (Parry and Brown, 1959) and Cupiennius salei (Weihmann et al., 2010) also use two pairs of legs to propel jumping.

Dorsal Is a catapult mechanism used? midline There are four reasons for suggesting that a catapult mechanism must be used by snow fleas to propel their jumping. First, the length of the legs and the short period over which acceleration is applied indicate that insufficient energy could be generated by the direct contraction of muscles working against levers. Second, the energy Right requirements for a jump are toward the extremes of what striated Posterior Anterior muscle could generate (Askew and Marsh, 2002; Ellington, 1985; Josephson, 1993; Weis-Fogh and Alexander, 1977). A further factor Left is that snow fleas must often jump at temperatures around 0°C, but µ Left hindleg Left middle leg Left front leg 200 m the quoted estimates of the performance of striated muscle were made at their much higher, optimum operating temperature. It is, B Dorsal however, not known whether the muscles of snow fleas are adapted Posterior Anterior to work more efficiently at low temperatures. If snow fleas were to Ventral operate at 30°C and to have a slightly higher mass of jumping muscle, then energy storage would not be necessary. In snow fleas the energy store could be used to deal with reduced muscle Depressor performance at low temperature, in contrast to other insects that use (dvm II) their energy stores to surmount the problem that even their maximum Depressor possible muscle performance would not be sufficient to propel (dvm III) jumping. Third, jump distance is not greatly affected by temperature, but a jump powered by direct muscle contractions would be Left front leg temperature dependent. For snow fleas, the period during which the catapult is loaded would be expected to be temperature dependent, and this has been reported (Edwards, 1987). Fourth, resilin is present at the junction of the pleural ridges with the hinges of the wings of Trochanter the middle legs and hindlegs, but not of the front legs. This suggests Trochanter that energy is stored by contractions of the muscles powering the Femur movements of the middle legs and hindlegs. The soft and elastic Left hindleg Left middle leg 100 µm resilin together with the hard cuticle of the skeleton could provide a mechanism for storing the energy generated by the slow Fig.9. Muscles that power jumping of Boreus. (A)The thorax of a male was contractions of the trochanteral depressor muscles. The combination opened by a ventral midline incision and the legs of the two sides pulled of these two materials, as in the energy storage mechanisms of apart to reveal large trochanteral depressor muscles of the hindlegs and froghoppers (Burrows et al., 2008), provides a means of bending middle legs, but much smaller ones of the front legs. (B)The left side of the thorax of a male viewed internally following a midline bisection to reveal the the hard cuticle through small distances while the resilin ensures large trochanteral depressor muscles. The head and abdomen are not that it does not shatter under deformation, and that the whole shown. structure returns rapidly to its original shape after a jump. If a catapult is used, then there must be a mechanism that allows the trochanteral muscles to contract and energy to be stored without movements of 2.5ms (400framess–1, or 12.5 times slower than in the present the hindlegs, and which then allows the stored energy to be released study). Another ant, Harpegnathos saltator, is said to use both suddenly. This mechanism is not known in snow fleas. middle legs and hindlegs synchronously to power a jump, but only recordings from leg nerves and muscles, shown at a slow time scale, Fleas and snow fleas are available to support such actions during fictive movements Does this analysis of jumping behaviour and its associated (Baroni et al., 1994). A second analysis, however, showed that the mechanisms illuminate the phylogenetic relationships between fleas hindlegs of this ant moved to full extension while the middle legs and snow fleas, which are currently placed within different orders? remained flexed (Tautz et al., 1994). The middle legs then extended A comparison of the jumping mechanisms of snow fleas, analysed to propel the ant to take-off. It is hard to extract information from in this paper, and true fleas (Bennet-Clark and Lucey, 1967; Rothschild these papers that would allow a direct comparison with the jumping and Schlein, 1975; Rothschild et al., 1975; Rothschild et al., 1972; performance of snow fleas. The acceleration period is given as Sutton and Burrows, 2011) reveals both similarities and differences, 15–25ms and the take-off velocity is estimated to be from 0.49 with the latter indicating adaptations to different habitats. The muscles

THE JOURNAL OF EXPERIMENTAL BIOLOGY Jumping in snow fleas 2373

Anterior Fig.10. Possible sites of energy storage for jumping. A Images taken under bright field and under ultraviolet Right Left illumination have been superimposed. (A)Ventral view Right front leg Posterior Left front leg of the inside of the thorax with the legs pulled apart laterally. Four bilaterally symmetrical areas that Dorsal fluoresce bright blue and that correspond to midline articulations of the hindlegs and middle legs are apparent, but no fluorescence is associated with the front legs. (B)A higher power image viewed only under bright field illumination of the region that fluoresces in the left middle leg. (C)Higher power image of the Right middle leg Left middle leg fluorescent regions associated with the hindlegs and middle legs. The inside surface of the dorsal midline is at the centre of the image and anterior is to the top.

Right hindleg Left hindleg B Left middle leg

100 µm C 50 µm

Right middle leg Left middle leg

Right hindleg Left hindleg

50 µm

that propel a jump are the same trochanteral depressors that lie in the involved jumping. The general principles and mechanisms of jumping thorax. The two insects achieve similar take-off velocities but, once are the same in snow fleas and fleas, even though Boreus uses four airborne, a snow flea spins less than a flea because the use of two legs while fleas use only the two hindlegs. These functional and pairs of propulsive legs provides a more stable platform for take-off. behavioural findings add clear further evidence to support a close The acceleration time of a snow flea in a jump is about 6 times longer relationship between the Boreidae and the Siphonaptera. than that of a flea and this means that it exerts less ground reaction force. Both use a catapult mechanism that requires the storage of ACKNOWLEDGEMENTS energy in advance of the jump. Resilin is present at the articulation I am enormously grateful to John S. Edwards for sharing with me his unpublished of the wing hinge with the heavily sclerotised dorsal head of the pleural data on snow fleas. I am also greatly indebted to Roger Northfield for introducing me to these insects, locating their habitats and catching them. I thank Greg Sutton ridge in both insects and is assumed to play a key role in energy and Steve Rogers for their many helpful suggestions during the course of this storage. The clear difference is that fleas propel jumping with just work and, together with Steve Shaw, for their incisive comments on the the hindlegs whereas snow fleas use both the middle and hind pairs manuscript. Jo Riley provided tremendous support with experiments and analyses. of legs. Fleas have two pads of resilin associated with the two hindlegs, whereas snow fleas have four pads of resilin associated with each of REFERENCES the middle legs and hindlegs. The location of the resilin for each Andersen, S. O. and Weis-Fogh, T. (1964). Resilin. A rubberlike protein in arthropod individual leg is the same in fleas and snow fleas. The question cuticle. Adv. Insect Physiol. 2, 1-65. therefore arises as to whether snow fleas using two pairs of legs Askew, G. N. and Marsh, R. L. (2002). Muscle designed for maximum short-term power output: quail flight muscle. J. Exp. Biol. 205, 2153-2160. represent the ancestral mechanism and fleas have become specialised Baroni, U. C., Boyan, G. S., Blarer, A., Billen, J. and Musthak, A. T. M. (1994). A by the use of just one pair of legs. Alternatively, both mechanisms novel mechanism for jumping in the Indian ant Harpegnathos saltator (Jerdon) (Formicidae, Ponerinae). Experientia 50, 63-71. could be specialisations in different directions from an evolutionary Bennet-Clark, H. C. (1975). The energetics of the jump of the locust Schistocerca common ancestral mechanism of locomotion that may not have gregaria. J. Exp. Biol. 63, 53-83.

THE JOURNAL OF EXPERIMENTAL BIOLOGY 2374 M. Burrows

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