© 2021. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2021) 224, jeb235168. doi:10.1242/jeb.235168

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Buzzing bees grab and go weighing just 0.2 g, to measure the doi:10.1242/jeb.235168 vibrations. They collected bees and Vallejo-Marın,́ M. and Vallejo, G. C. (2020). while leisurely hoverflies hoverflies from around Scotland and Comparison of defence buzzes in hoverflies and lunch returned to the lab to identify the . buzz-pollinating bees. J. Zool. doi:10.1111/jzo. They then held the insects gently against 12857 the exquisitely sensitive apparatus, just Christopher Basu (0000-0002-2357-9516) firmly enough to cause the insects to buzz Imperial College London with alarm and vibrate the sensor. Overall, [email protected] the duo tested 299 insects, split evenly between bees and hoverflies, and measured over 4000 buzzes. Socialites boosted but Surprisingly, the hoverflies were just as capable of producing flower-shaking loners set back in a crowd vibrations as the bees. Vallejo-Marin and Vallejo found that larger insects produced

POLLINATION larger and louder buzzes, but the buzzing produced by similarly sized bees and Take a walk around the Scottish hoverflies were otherwise Highlands in summer and you’ll be indistinguishable. They should both be wowed by the wildflowers that light up able to buzz out pollen. the landscape. Bees and hoverflies are also attracted by the flowers, to collect But buzzing a sensor is one thing; pollen. But these two groups of buzzing Vallejo-Marin and Vallejo wanted to see insects use different behaviours to get to for themselves whether the hoverflies’ this protein-rich food source. Bees often defensive buzzes were capable of buzz the pollen out of the flower, by releasing pollen from flowers. They COSTS clamping their mouthparts onto the anther repeated the previous experiment, but this People’s responses to social situations and speedily shaking it with their time using a natural sensor – a flower – varies considerably according to their vibrations. Buzzing pollination has because buzzing against an anther personality type. We span the spectrum evolved 40 times in over half of the should cause it to release pollen. While from loners to social butterflies and 20,000 bee species, yet just one species of pressing the buzzing insects against the everything in between. And the same is hoverfly is known to buzz flowers; anthers of two plant species, the true of other . Depending on their instead, the rest silently and slowly rub the researchers collected the pollen that lifestyle, they may either be stressed or pollen off with their legs and body. tumbled out, and in most cases the fulfilled by socializing. Megan Currier bees and hoverflies released over 2000 and colleagues from Widener University Mario Vallejo-Marin and Gillian Vallejo grains of pollen each time: a veritable in Pennsylvania, USA, aimed to better are no strangers to Scotland. Working at feast. understand this idea in wild animals by the University of Stirling and at Natural measuring the energy costs associated Power, Stirling, UK, they are situated Yet despite their apparent ability, with movement in cooperative, socialite right at the gateway to the Highlands and hoverflies for the most part decline to use fish or antagonistic, loner fish. are fascinated by pollinating insects. They buzzing to collect pollen. The were curious to know why bees and researchers have ideas of why this might Currier and colleagues suspected that the hoverflies go about it in different ways. be. A big clue lies in what bees and high energy investment needed to achieve hoverflies actually do with the pollen: the movement may push some animals to First, the duo wondered whether hoverflies eat it themselves, sometimes maximize their efficiency through the hoverflies are incapable of producing even tucking in while they’re still at the generations. Using a fish species that is large enough vibrations to shake off the flower, but the bees are there for take- social (bluegill sunfish Lepomis pollen, so they set out to measure the away, rushing the pollen home to their macrochirus) versus a competitive fish bodily accelerations of bees and larvae. Buzzing quickly exfoliates large with strong social hierarchies that can be hoverflies during their defensive buzzes. amounts of pollen, which is a lot more found swimming alone (rainbow trout Greater acceleration means more vigorous effective, but more energetically Oncorhynchus mykiss), the researchers buzzing and more pollen. But how to expensive, than the hoverflies’ relaxed set about figuring out how these animals measure the vibrations of a tiny ? and economical approach. With hungry maximize efficiency as they move Use an even tinier sensor. Vallejo-Marin mouths to feed, buzzing bees are through their habitat. Individuals could and Vallejo used an accelerometer certainly busier. use what is known as ‘entrainment

Outside JEB reports on the most exciting developments in experimental biology. The articles are written by a team of active research scientists highlighting the papers that JEB readers can’t afford to miss. Journal of Experimental Biology

1 OUTSIDE JEB Journal of Experimental Biology (2021) 224, jeb235168. doi:10.1242/jeb.235192 swimming’, in which they essentially buddies) and inanimate objects (think of Science and Technology in Trondheim hitch a free ride by swimming in the rocks) in its environment. Like humans, set out to determine whether zebrafish can turbulence kicked up by obstacles such as some animals will be more or less social evolve heat tolerance fast enough to help rocks or chunks of wood in the flow. naturally and, as such, will be more or less them survive as temperatures soar. Alternatively, the fishes could take inclined to use sociality to enhance their advantage of the benefits of swimming in own efficiency. Social distancing in the Receiving zebrafish captured by local schools, when the leader of a group ongoing COVID-19 pandemic is fishermen in West Bengal, India, the essentially generates comparable becoming a prolonged way of life and this team allowed the new arrivals to mate turbulence through the swishing of its tail, study shows that keeping your distance backinNorway.Theythenplacedthe which fishy followers can exploit to likely impacts some individuals (like the progeny in a tank and slowly increased reduce their own energetic costs when social butterflies) more than others (such the water temperature until the fish lost moving. as the loners). So, some species achieve their balance to identify the highest more together, but being in a crowd can temperature that each individual could To test these ideas, Currier and colleagues set others back. cope with. Next, the team allowed the employed a swim tunnel, also known as a fish that could stand the heat to breed fish treadmill. This contraption allowed the doi:10.1242/jeb.235200 together, while allowing the least researchers to pump up the water flow to Currier, M., Rouse, J. and Coughlin, D. J. (2020). resilient fish to breed with others like test how the fish optimize their swimming Group swimming behaviour and energetics in themselves. Repeating the process over a Lepomis macrochirus efficiency, by measuring the amount of bluegill and rainbow trout total of six generations, the scientists Oncorhynchus mykiss. J. Fish Biol. doi:10.1111/ energy they consumed and the rate of tail jfb.14641 tried to rear a hardy group that were bred swishing. For the social bluegill sunfish, to withstand high temperatures and a they compared the swimming efficiency of Lauren Nadler (0000-0001-8225-8344) feebler population that could only cope Nova Southeastern University groups of three fish with that of individual [email protected] with cooler conditions. The team also swimmers, at 4 different swim speeds placed a group of the hardy zebrafish in (ranging from 25.5 to 51 cm s–1 for the warmer water for 2 weeks before 17 cm long fish). For the competitive measuring the highest temperature that rainbow trout, they examined the Climate change may push each fish could tolerate to find out swimming efficiency of individuals versus zebrafish to the brink whether these robust animals were 4 group sizes (composed of 2–8 fish), capable of adapting to even hotter testing the fish’s swimming efficiency conditions, which might further increase with and without a cylindrical obstacle in their heat tolerance and help them deal the flow – for the fish to shelter behind – at better with a heatwave. a swim speed of 63 cm s–1 for the 21 cm long fish. The researchers suspected that Having bred at least 20,000 fish in the fish would use whichever strategy (either Herculean series of experiments, Morgan schooling or entrainment swimming) that and colleagues found that zebrafish are best suited their lifestyle. only able to increase their thermal tolerance at a rate of 0.04°C per Andtheywereabsolutelyright.Themore generation. In addition, the team found cooperative and social sunfish greatly that as zebrafish evolved to endure higher reduced both the energy consumed and TOLERANCE temperatures, they reduced their ability to their rate of tail swishing when they could For species living near their thermal increase their heat tolerance to the same do it together in a school, rather than alone, limits – the highest temperatures an extent, using physiological changes to regardless of how fast the flow pumped. can tolerate – climate change deal with thermal stress. These results For the more competitive and reclusive threatens to push them over the edge. suggest there is a limit to how much trout, group swimming actually increased Although zebrafish seem to be zebrafish can increase their heat tolerance. their energy use when moving around, everywhere, with hundreds of investigators instead of making their movement more experimenting on different lab strains, this The main question is whether the fish can efficient, possibly because of the stress species may be in trouble in the wild. adapt fast enough to keep up with the induced by the social setting. On the flip Zebrafish are a tropical species that live a unprecedented rates of climate change side, rainbow trout reduced their movement couple of degrees below the highest that we are currently seeing and the costs by sheltering behind a static obstacle temperatures at which they can survive. researchers conclude it is very unlikely. in the flow, taking up positions in the They live in shallow freshwater that heats Like many of the things that we have eddies generated by the water’sflow up quickly, in India, Bangladesh and learned from this model species, these around the obstacle. This strategy allowed Nepal. Climate change scenarios predict zebrafish may be warning us of what is to the trout to reduce both their energy that maximum temperatures in India are come for other tropical species living near consumption and rate of tail swishing. expected to surpass 44°C by 2100, leaving their upper thermal limits. it unclear whether zebrafish will be able to Studies like this highlight the importance adapt to these new conditions or if they doi:10.1242/jeb.235192 of taking an animal’s lifestyle into will perish. With this chilling possibility in Morgan, R., Finnøen, M. H., Jensen, H., Pélabon, account when speculating how it will mind, Rachael Morgan and a team of C. and Jutfelt, F. (2020). Low potential for respond to animate objects (like its colleagues from the Norwegian University evolutionary rescue from climate change in a Journal of Experimental Biology

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tropical fish. Proc. Natl. Acad. Sci. USA 117, socket located on the surface of the Domna-Maria Kaimaki 33365-33372. doi:10.1073/pnas.2011419117 insects’ skin. (0000-0002-6104-1442) Andrea Murillo (0000-0003-4793-708X) Imperial College London McMaster University Next, the Japanese researchers focused [email protected] [email protected] on male ladybirds, setting out to identify how actin contributes to the development of each disc and needle-shaped hair. Using a dye that specifically targets Freshwater snails’ stinky Tool-shaped ladybird actin, Kimura and Hosoda observed that hairs guarded by protein 12 hours after moulting the footpads environment could kill initially appeared flat, like terraces, with their babies the hair sockets, hair shafts and finally hair tips progressively forming over the next 30 hours. The team was also curious to investigate the structure of the hairs beneath the insects’ skin, suspecting that they might be linked to neurons, as previously reported for some fruit fly hairs. This time using a dye that reveals neurons, the scientists found that there are in fact two types of hair: one

TTACHMENT associated with a neuron, which is A thought to act as a sensor and give Insects are champions of climbing even on feedback to the insects as they move, and INHERITANCE the smoothest of surfaces thanks to their another without a neuron. Growing up, an animal’s environment can sticky footpads. The pads, found on influence its personality. But researchers different parts of their legs, can be smooth Knowing that actin is a key player in the also want to know whether the parents’ or hairy but both types allow the insects to formation of the tip structures of environment can influence the attach equally well via a thin film of a liquid Drosophila sticky hairs, Kimura and personalities of their offspring too. Recent they secrete. Looking closely at the hairy Hosoda wondered whether the protein work by Juliette Tariel and colleagues pads, scientists have identified four distinct was also significant in the growth and from the Université Claude Bernard in designs of hair tip, resembling spatulas, development of the ladybird’s attachment Lyon, France, suggests that this is the case discs, lances or needles. But how do these hairs. Comparing the growth of normal for the offspring of freshwater snails tool-shaped hairs develop their different hairs with that of hairs that had been (Physa acuta). An animal’s response to forms? Having previously investigated the injected with a drug that prevents actin predators is just one behaviour that could hairs on the feet of fruit flies (Drosophila) molecules from assembling and forming be affected by the parents’ environment. and found that fibres of the protein actin long chains, the duo revealed that in both So Tariel and colleagues wanted to see form a scaffolding that contributes to their cases there were bundles of the protein in how snails would respond to a predator, spatula-shaped hair tips, Ken-ichi Kimura the hair shaft. However, while actin and whether the youngsters’ responses to and Naoe Hosoda, extended their research bundles branched out to form a scaffold at a predator varied – from relaxed to to the sticky structures on ladybird the hair tip in untreated ladybirds, in the terrified – if their parents were familiar (Harmonia axyridis) limbs. insects that had been injected with the with the predator’s smell. interfering drug, the scaffolding bundles After collecting samples of legs from failed to assemble, leading to significant The researchers took adult snails from the adult ladybirds and youngsters at specific malformations of the hair tips. river Rhône in Lyon back to the lab. They life stages after moulting, the researchers then put the snails into plastic containers examined them under a microscope. The Fruit flies and ladybirds both depend on filled with either freshwater or water resulting images revealed all four hair tip the same mechanisms to produce the mixed with the smell of the snail’s designs in the sticky attachment pads of different tip designs that help insects hold predator – crayfish – and allowed the each male’s leg, while the female ladybird on tight. Now that the authors have snails to breed. Finally, the team left some footpads contained only three, missing verified the importance of the actin of the offspring in their original watery the disc-shaped hairs. The duo also scaffolding, they are investigating new homes or transferred them to a container pinpointed the location of each type of avenues, fusing developmental biology with the opposite-scented environment, hair tip on the male footpads; finding and biomimetics in search of the ultimate predicting that offspring of parents spatula and lance-shaped hairs arranged ladybird-inspired adhesive. familiar with the crayfish scent would around the perimeter of the pad, disc- respond faster to the predator and that shaped hairs located at the back of front- doi:10.1242/jeb.235184 there would be more variation in their leg pads and the front of middle-leg pads, Kimura, K. and Hosoda, N. (2021). Crucial role of individual responses. To test this, the and needle-shaped hairs populating the framework with cytoskeletal actin filaments for researchers put an adult snail into a remaining surface of the pads. Further shaping microstructure of footpad setae in the container filled with crayfish water and ladybird , Harmonia axyridis. . imaging of the hairs also revealed that the Struct. Dev. 60, 100998. doi:10.1016/j.asd.2020. counted how many seconds it took for the hair shaft is hollow and surrounded by a 100998 snail to escape and crawl out of the water. Journal of Experimental Biology

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Surprisingly, Tariel and colleagues found Another surprise was that the snails with the scent of fear suggests that the that the parents’ environments didn’t produced by parents that bred in the environment of parents can affect how affect the variation in behaviour of their crayfish-ridden water tended to escape their babies respond to changes in their offspring. All of the youngsters whose more slowly when presented with a own environments. In the case of these parents that had lived with the stink of predatory crayfish; if they tried to freshwater snails, where their parents predators escaped within similar time escape at all. The snails’ slow escape grew up could be a matter of life and frames. might be because the snails are familiar death, if the youngsters have lost their with the odour of crayfish. The scent of edge and don’t know when to make In contrast, growing up with the smell of crayfish usually warns snails when a a speedy getaway. fear did affect the youngsters’ behaviour. predator is at large, but if the snails Individual snails often responded constantly smell crayfish without doi:10.1242/jeb.235176 differently from their brothers and encountering the genuine threat, sisters; there was much more variation in they could well stop responding to the Tariel, J., Plenet, S. and Luquet, E. (2020). How their behaviour. The difference in the scent as they appear to have nothing do developmental and parental exposures to ’ predation affect personality and immediate baby snails responses might be due to to fear. behavioural plasticity in the snail Physa acuta? differences in how they use energy while Proc. R. Soc. B 287, 20201761. doi:10.1098/ developing. For example, some snails While this is the opposite of the rspb.2020.1761 may invest energy into growing thicker researchers’ original prediction, the Gina Mantica (0000-0001-5329-3896) shells for defence rather than building discovery that crayfish odour carried less Boston University muscle for a sprint escape. dread for the offspring of parents living [email protected] Journal of Experimental Biology

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