© 2016. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2016) 219, 609-611

INSIDE JEB

Water-skiing beetles get a limb back into the water ready for Fish hearts get O boost departure. Once balanced on the tips of all 2 bumpy ride four legs, the beetles open the wing case on from carbonic anhydrase their backs and beat the wings a couple of times to unfurl them before switching into flight mode, where they flap the wings in a characteristic figure-of-eight pattern at around 115 Hz to thrust themselves forward. However, instead of gliding Time-lapse image of Galerucella nymphaeae smoothly across the glassy surface, the flying on the water surface. Photo credit: insects looked as if they were careering Haripriya Mukundarajan. along a roller coaster as they flew across the ripple ridges that they generated as they Blink and you’ve missed it: Manu A salmon heart blood vessel collapsed into a moved. ‘Almost like going on a road full of heart shape. Photo credit: Sarah Alderman. Prakash from Stanford University, USA, potholes’,saysMukundarajan,‘Although describes how one moment a waterlily Fish plumbing is contrary. As the heart these potholes are being generated by the beetle (Galerucella nymphaeae)issaton is the last organ that blood passes insect itself’, laughs Prakash. the surface of a pond and the next it has through before it returns to the gills, and vanished. ‘The phenomenon is so with little direct blood supply to the incredibly fast that you don’tsee Puzzled by the beetles’ unexpectedly ceaselessly contracting muscle, there are anything’, says Prakash, describing the bumpy ride, Mukundarajan and Prakash occasions when it could be on the verge ripples that remain on the surface, which analysed the forces acting on them as they of failure. ‘We know this can happen are the only evidence that the insect was slide across the surface and realised that under certain conditions like exhaustive ever there. Having observed the beetles’ the insects were playing a finely tuned exercise in combination with hypoxia or remarkable disappearing act, Prakash balancing act between surface tension elevated water temperature’, says Sarah knew he had to find out how they pull off clinging to their tarsus claws and the lift Alderman from the University of the stunt. ‘Initially, I filmed them without generated by their wings, with surface Guelph, Canada. Added to the challenge confining them in my kitchen…because it tension keeping them firmly anchored at of keeping the heart supplied with is hard to find them [when they get loose] the surface. And when Mukundarajan oxygen, Alderman explains that the in the lab’, he chuckles, recalling that assembled a series of equations that haemoglobin that carries oxygen in fish dinner plates of water provided ideally described the insects’ movements, they blood is finely tuned to blood pH: the sized ponds when filming. And when he explained how the tell-tale ripples – the more acidic the red blood cells, the less saw the first movie, he knew that he was only visible indication of the insects’ able haemoglobin is to carry oxygen, on to something exceptional. The beetles high-speed performance – were produced. which could prevent the red blood cells looked as though they were water skiing, According to Prakash each wingbeat of exercising fish from picking up but travelling at incredible speeds of up to generates a force that momentarily pushes oxygen at the gills if they didn’thavean 0.5 m s−1 – equivalent to a human the insect down, making it bounce along effective pump to remove acid from the travelling at around 500 km h−1 – the surface of the water. An additional set cells and restore the pH balance. propelled by their wings alone, as if they of waves – known as capillary gravity were flying while remaining attached to waves – are also generated spontaneously But Alderman and her colleagues, Till the surface. Prakash was hooked and as the insect reaches a specific speed. The Harter, Tony Farrell and Colin Brauner knew he had to learn more about the duo adds that there are only a narrow from the University of British Columbia, mysterious beetles’ interfacial flight. range of situations where an insect can fly Canada, also knew that fish can take along the surface of a pond and remain advantage of a sudden drop in red blood ‘It was incredibly difficult to image these attached without popping off into the air. cell pH to release oxygen rapidly at tissues guys’, says Prakash, who worked with Prakash is also optimistic that the new – such as red muscle and the retina – when summer interns Thibaut Bardon and Dong mathematical model could explain how required urgently. An enzyme called Hyun Kim, and graduate student Haripriya other exotic species skate, including carbonic anhydrase – which combines marine flies that are content bobbing Mukundarajan, filming the beetles’ antics CO2 and water to produce bicarbonate and with a high-speed camera. Mukundarajan about on the waves. acidic protons, and vice versa – lies at the describes the insects’ movements, saying, heart of this mechanism. Normally there ‘They have an elaborate way of preparing 10.1242/jeb.138990 is no carbonic anhydrase in blood plasma; ’ for flight , before outlining how the insects Mukundarajan, H., Bardon, T. C., Kim, D. H. and however, the enzyme has been found in initially raise the middle pair of legs – to Prakash, M. (2016). Surface tension dominates salmon red muscle capillaries, where it prevent them from impeding the wings insect flight on fluid interfaces. J. Exp. Biol. 219, facilitates the reaction of protons – that during flight – before drying each leg and 752-766. have been extruded from the red blood gently dipping the claw at the end of the Kathryn Knight cell – with bicarbonate to produce CO2,

Inside JEB highlights the key developments in Journal of Experimental Biology. Written by science journalists, the short reports give the inside viewof the science in JEB. Journal of Experimental Biology

609 INSIDE JEB Journal of Experimental Biology (2016) 219, 609-611 which then diffuses back into the red anhydrase in the lumen of salmon heart that may to see the leggy solitarious locusts outstrip blood cell. The CO is then converted enhance oxygen delivery to the myocardium. their stumpier gregarious counterparts, 2 J. Exp. Biol. 219, 719-724. back into bicarbonate and protons in the recording impressive 1.1 m-long leaps, in blood cell, causing the pH to plummet and Kathryn Knight comparison to the gregarious locusts’ release a burst of O2 from the modest 0.85 m-long bounds. And when haemoglobin. Could salmon take Riley and Brighton filmed the take-offs advantage of this mechanism to boost Long legs drive solitarious with a high-speed camera, they could see oxygen supplies to the heart when the the solitarious locusts hurl themselves animals are working full out? Possibly, locusts’ powerful leaps forward at speeds that were 23% faster but only if carbonic anhydrase was (3.26 m s−1) than the gregarious locusts’ accessible to blood passing through the 2.65 m s−1 take-off – although the heart. solitarious insects pay a higher price for their impressive leaps, consuming twice Alderman and Jonathan Wilson began as much energy per jump as the searching for the enzyme in salmon gregarious locusts. hearts. Using cobalt sulphide to stain sites where the enzyme accumulated, So, the solitarious locusts’ longer legs Alderman could clearly see the enzyme propelled the insects faster and farther, in on the surface of the heart chambers. She contradiction of what was already known also identified the gene that was Male gregarious locust (Schistocerca gregaria) about spring-loaded leaps. Burrows and expressed to produce the protein. Then, jumping. Photo credit: Malcolm Burrows. Greg Sutton had previously shown that to be sure that carbonic anhydrase could recoil speed due to elastic energy stored contribute to dumping residual oxygen Of all the biblical plagues, locusts are in the limb was the major factor that out of the blood in the heart, Alderman probably the most infamous. Stripping affected the speed of spring-assisted and Harter had to figure out a way of vegetation bare and devastating crops, an leapers, not leg length. So why were the directly measuring pH inside the heart advancing swarm can decimate solitarious locusts packing so much more chambers to see whether the enzyme thousands of hectares in a single day. of a punch than their shorter limbed altered it. This type of experiment is Explaining that locusts exist in one of cousins? usually performed using ground-up two forms – the benign solitarious locust ’ and the voracious gregarious locust – tissue in a test tube, but that wouldn t Rogers looked inside the locusts and all Stephen Rogers from Arizona State confirm that carbonic anhydrase in the became clear. Measuring the dimensions University, USA, says that field workers heart chamber walls could alter blood of the leg, he realised that the solitarious ‘ monitor how far solitarious locusts have pH, So we decided to modify the assay locusts’ hind limbs were longer to progressed on their transformation into and use the heart itself as the reaction accommodate the bulging muscle that is ’ swarming gregarious locusts by vessel , Alderman recalls. required to wind up the elastic energy measuring the length of the insects’ hind storage structures. And when Rogers legs: adult solitarious locusts have longer Working closely together, the duo scrutinised these springs – known as femurs than adult gregarious locusts. painstakingly developed a technique semi-lunar processes – on either side of Recalling a discussion during a meeting where they could measure the pH in the the locust’s knee joint, they were 25% less when he was in Malcolm Burrows’ lab in beating heart with pH probes that were stiff than the gregarious locusts’ and the Cambridge, UK, Rogers says, ‘We were thinner than a human hair. Eventually, the muscle tendon was also less stiff, ’ mulling over things to do and we said, duo s persistence paid off and the pH in allowing the two structures to store more “We have these morphological the heart plummeted as they fed CO2 into elastic energy. He suspects that solitarious differences that are used by the field the pulsating chambers. And when they locusts invest more in their powerful leaps workers, but we have no idea why they added a carbonic anhydrase inhibitor to evade danger when a threat looms, (produced by Claudia Supuran) to the are there and what they mean for the biology of the animal’”. So, the team while gregarious locusts prefer to plod fluid, the pH fall slowed dramatically. along en masse. ‘You could even argue if Carbonic anhydrase was responsible for decided to get to grips with why solitarious locusts are leggier. you are a super athlete in a locust swarm, the drop in pH. and you stand out, it is a bad thing’, laughs Rogers, who suggests that getting ‘The take-home message for our study is Rogers explains that solitarious locusts and gregarious locusts are genetically ahead of the crowd is no advantage for that the salmonid heart has an ace up its gregarious locusts. sleeve to help it overcome adverse identical and the solitarious insects only transform into threatening gregarious conditions’, says Alderman, who is now 10.1242/jeb.138982 eager to find out whether the fish play this locusts when thrust into the company of card during their marathon upstream others, so they have to be reared in Rogers, S. M., Riley, J., Brighton, C., Sutton, individual cages in the lab while the G. P., Cullen, D. A. and Burrows, M. (2016). migration to spawn. Increased muscular volume and cuticular gregarious animals are raised specialisations enhance jump velocity in 10.1242/jeb.138974 communally. Rogers, Joanna Riley and solitarious compared with gregarious desert Caroline Brighton then built an insect locusts, Schistocerca gregaria. J. Exp. Biol. 219, Alderman, S. L., Harter, T. S., Wilson, J. M., 635-648. Supuran, C. T., Farrell, A. P. and Brauner, C. J. athletics stadium to measure the length of

(2016). Evidence for a plasma-accessible carbonic the insects’ leaps and they were impressed Kathryn Knight Journal of Experimental Biology

610 INSIDE JEB Journal of Experimental Biology (2016) 219, 609-611

Record-breaking mite uses grappling hook tight turns

Looney Tunes would have you believe youngster hit a blistering 323 body slower turn at around 567 deg s−1, where that the fastest animal in California is lengths (BL) s−1, leaving the previous they scuttle around a corner with the outer the aptly named Road Runner, closely world record holder – an Australian legs taking longer strides than the inner pursued by its nemesis, Wile E. Coyote, tiger beetle – in the dust at a trifling legs. Investigating the mites as they but Jonathan Wright from Pomona 171 BL s−1. sprinted from a standing start, Wright and College, USA, would like you to colleagues were also impressed to see the consider a much smaller creature. ‘Mites Impressed by the mite’s agility, the team animals hit a respectable 0.15 m s−1 in just attain some of the fastest relative speeds went on to scrutinise the arachnid’s 15–20 ms, pulling accelerations of documented in the animal kingdom’, footwork, recording the mites’ stride 7.2 m s−2 as they took off and say Wright and his colleagues, and frequency at a remarkable 135 Hz, which decelerations of 10.1 m s−2 when they when the team filmed their local mite, they say is the highest value reported for came to a standstill. Paratarsotomus macropalpis, any weight-bearing muscle. And when scuttling across hot concrete on a they analysed the mites’ turning 10.1242/jeb.139006 driveway close to the college campus, performance, they discovered that the Rubin, S., Young, M. H.-Y., Wright, J. C., they were in for a treat. The tiny animals mites used two strategies: a high-speed Whitaker, D. L. and Ahn, A. N. (2016). racked up top speeds of up to turn at approximately 795 deg s−1, where Exceptional running and turning performance 0.26 m s−1. Scaling the speeds relative they pivot around the third inner leg as the in a mite. J. Exp. Biol. 219, 676-685. to the mite’s diminutive body size, the claw at the end of the limb attaches to the Kathryn Knight team was truly astonished to see one surface like a grappling hook; and a [email protected] Journal of Experimental Biology

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