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Mecoptera, Boreidae) 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 0.2ms resolution afforded by image rates of 5000framess–1. The middle legs of males represent 140% and the hindlegs 187% of the body length (3.4mm), 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 6.6ms. The fastest jump by a male had a take-off velocity of 1ms–1, which required 1.1J of energy and a power output of 0.18mW, and exerted a force about 16 times its body weight. Jump distances of about 100mm were unaffected by temperature. This, and the power per mass of muscle requirement of 740Wkg–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 t0ms. 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 407nm. 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 483nm 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 14mms–1 were measured but at 3°C speeds fell to as low Adult male and female Boreus hyemalis (Linnaeus 1767) were as 1mm 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.
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