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scaphognathites, which draw water and , the largest terrestrial . Giant trashcan crab also ’ – Zoology 137, 125710. doi:10.1016/j.zool.2019. air over the crab s against hard 125710 makes creepy noises panels in the channels. The work by Oka and his team suggests that rather than Noah Bressman (0000-0002-2916-3562) developing a new organ, coconut Wake Forest University [email protected] use a behavioural modification of existing organs to produce sound. However, what are these sounds for? Wing swing, not shape, When in the water, produce is key to bird flight sounds mainly to deter predators, court mates and ward off competitors for resources. The purpose of the sounds made by the crustaceans when on land COMMUNICATION was largely mysterious, but we now have Imagine relaxing on an Indo-Pacific some possible explanations, thanks to tropical island beach under a palm tree with Oka and his team. They recorded sounds a coconut drink in your hand. You hear a from male and female crabs during mating mysterious tapping noise above you, so and at other times. Oka found that both you look up and see a meter-wide crab at sexes produce sounds regardless of the top of the palm tree, tearing a red- whether they are trying to attract the most footed booby apart with its big, meaty desirable mate with their devastatingly CONTROL FLIGHT claws. Sorry for the nightmares, but this is attractive clicks, suggesting that that they Be it finches flapping, hummingbirds the coconut crab (Birgus latro), the largest use sound for more than just casual sex. hovering or seabirds soaring, birds are terrestrial crustacean in the world, which Additionally, both sexes produced a capable of achieving all manner of became famous a few ago after a variety of sounds by adjusting the pitch aerobatic approaches to flight. It would photo of one climbing a trashcan went and sound intervals between their clicks, not be unreasonable to assume that these viral. These giant, omnivorous hermit demonstrating a potential ‘multi-word specialised flight behaviours would be crabs are known for a variety of odd vocabulary’. Some of these ‘words’ likely associated with specific wing types, but, behaviours, including producing eerie serve a courtship role to woo mates, as the in fact, many birds with similar flight clicking sounds. However, nobody knew crabs’ sounds changed throughout the styles possess wings of varying shapes how or why they produce sounds, until a mating process. However, the rest of the and sizes. One theory for this recent study published in Zoology by a coconut crab language is still a mystery. inconsistency between form and function team of scientists led by Shin-ichiro Oka of is that traditional 2D wing shape the Okinawa Churashima Foundation in Many crustaceans communicate using measurements are a poor representation of Japan. The researchers figured out the odours underwater, but these giant crabs the way birds actually use their wings coconut crab’s means of sound production, spend most of their lives on land, so some during flight. By focusing instead on the along with providing some explanations of their aquatically adapted senses may not wing’s 3D movements, or their ‘range of for how they use these sounds. function so well in the air. While they have motion’, a team of researchers from the evolved a strong sense of aerial smell, University of British Columbia, Canada, As crustaceans, coconut crabs are covered odours are carried differently through the led by Doug Altshuler recently revealed in hard segments, which show up well in atmosphere. Therefore, the coconut crab’s that when it comes bird flight behaviour, X-rays. Therefore, Oka and his team had a diverse acoustic vocabulary may it’s less about the wings you’ve got and straightforward way of determining how complement their odour repertoire to more about how you use them. the crabs produce sound: filming the crabs communicate a variety of messages to with X-ray videography while recording other crabs on land. The work by Oka and To clear up the conflicting relationship the sounds they make. By looking at his team highlights just how little we know between wing morphology and flight which body parts were moving only when about some of the biggest, most behaviour, the team started by acquiring noises were audible, Oka was able to conspicuous on our planet and examples of 61 bird species and measured determine the parts used for sound why we need to develop a ‘Rosetta shell’ to the area, shape and the ratio between production. Unlike many crustaceans that understand these overgrown hermit crabs. length and width (known as aspect ratio) use their claws and to of the extended wing. Next, the team produce sound, coconut crabs produce doi:10.1242/jeb.211433 identified each wing’s full range of sound by beating hard parts of their Oka, S., Kobayashi, N., Sato, T., Ueda, K. and motion by marking locations on the wing, mouth structures – known as the Yamagishi, M. (2019). Sound production in the such as the elbow and wrist joints, before

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 (2020) 223 manually flexing and extending the wings maybe one day soon, this area of research anterior (mouth to stomach) and – while filming the motion of the markers will influence the shape of wings to come. the posterior (intestine) gut, the authors from multiple angles to reconstruct the separated the sections and compared the motion in 3D. In order to compare doi:10.1242/jeb.211441 bacteria species in each at both life stages. these hand-made range of movement Baliga, V. B., Szabo, I. and Altshuler, D. L. (2019). Initially, the team found that bacteria measurements with the ’sfree Range of motion in the avian wing is strongly known as Firmicutes, Spirochaetes and movements, the team also filmed two of associated with flight behavior and body mass. Fosobacteria – which are involved in Sci. Adv. 5, doi:10.1126/sciadv.aaw6670 the 61 species, pigeons (Columba livia) fermentation, breakdown of plant and zebra finches (Taeniopygia guttata), Alex Evans (0000-0002-5655-012X) products and immune protection – occur flying from various angles. After University of Leeds in both life stages of the white cachama. researching in the literature what was [email protected] However, Fusobacteria dominated the already known about bird flight, the team front section of juvenile intestines, while then assigned each of the 61 species to at Spirochaetes dominated in the posterior. least one of 12 distinct categories of flight In contrast, Fusobacteria and Firmicutes styles, including different combinations Guts and microbes: a dominated the population of the entire of hovering, gliding, soaring and flapping revolution in aquaculture adult gut. As members of the Fusobacteria flight. Finally, to investigate how wing family produce vitamin B12 during shape and flight behaviour varied digestion, the authors suggested that their between related species, the team presence could eliminate the need to constructed a family tree from the DNA supplement the fish diet with vitamin sequences of 220 bird species and paired B12, therefore cutting down costs to each species with their flight styles. the fish farmer.

The team’s experiments confirmed the In addition, the team found that probiotic theory that the flight style of a bird is bacteria, which boost the immune much more strongly linked to the wing’s system to fight infections, occurred in range of movement than its static shape, in the fish guts, although they were more addition to finding that the wings’ range dominant in the adult intestines than in of movements were almost twice as likely MICROBIOME those of the juvenile fish. However, to correctly predict a bird’s flight Take some guts, a few bacteria species the researchers also discovered behaviour than their wing shape or body and throw in some brains while you are at Proteobacteria in the guts of all farmed mass. These results reveal that bounding it…and what does that give you? One of fish, which can cause infections if the and gliding birds tend to have a greater the most unexplored interactions that has animals are stressed. They suggested that range of wing movement and lower body scientists all riled up: how the bacteria manipulating the ‘good’ probiotic mass, allowing for a wider adaptability of population in the gut, known as the gut bacteria in the fish digestive systems wing motion, while soaring birds, such as microbiome, interacts with the brain to could allow them to outcompete the ‘bad’ eagles, tend to possess rigid wings with a allow the animal to grow and adapt to ones, as well as boosting the immune much more restricted range of movement. stress in its environment. And this system to reduce infection and promote The team also report that pigeons and interaction could not be more relevant growth. zebra finches rarely fully extend their than it is for farmed fish, where wings when flying freely, further overcrowding, waste generated by the The idea of an interaction between the suggesting that wing shape does not animals and increasing global microbiome and the brain is not new, accurately represent a bird’s true range of temperatures are just some of the stressors but how they interact and to what degree flight styles. that the fish can endure. How can fish bacteria in the gut can influence how the farmers increase production in a brain responds to stress is still a mystery To explain these findings, the team then sustainable way, yet minimize the adverse that we are only now beginning to turned to their evolutionary tree and conditions that the fish may encounter? Is unravel. Exploring this question in the realised that 2D wing shape is much more it possible to manipulate the diversity of context of aquaculture opens new similar between related species than the the gut microbiome to improve the overall possibilities for food production. Can we wing’s range of movement, suggesting health and growth of fish in aquaculture? improve the health of the fish by simply that bird species are more likely to vary Can we make them bigger, faster, manipulating the population of the their flight behaviours through 3D wing healthier – and do it at a lower cost? bacteria growing in their intestines? Can motion than by adapting the shape of their we improve the taste of the meat? Can we wing. Not only do these results help to Victor Alfonso Castaneda-Monsalves make fish grow faster, reproduce sooner improve our understanding of bird flight from Universidad Nacional de Colombia and at high rates, to increase production? behaviours and the evolutionary in Medellin and his colleagues set out to These are just some of the questions processes behind them, they also show identify the species of bacteria living in that are worth exploring, as the human promising applications for our own the gut of the third most cultured fish in population continues growing and aeronautical ambitions. For drones and Colombia, the white cachama (Piaractus the global demand for fish is ever crewed aircraft, overcoming turbulence brachypomus). For their work, the group increasing. and strong winds are issues that could be compared both juvenile and adult addressed by morphable wing shapes, and fish. Wanting to differentiate between the doi:10.1242/jeb.211417 Journal of Experimental Biology

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Castañeda-Monsalve, V. A., Junca, H., Garcıa-́ while they were caring for their offspring. Erin McCallum (0000-0001-5426-9652) Bonilla, E., Montoya-Campuzano, O. I. and The team collected female birds that were Swedish University of Agricultural Moreno-Herrera, C. X. (2019). Characterization Sciences of the gastrointestinal bacterial microbiome of keeping their eggs warm in nest-boxes at a farmed juvenile and adult white Cachama field site near Turku, Finland. They took a [email protected] (Piaractus brachypomus). Aquaculture 512, small blood sample containing cells with 734325. doi:10.1016/j.aquaculture.2019.734325 mitochondria for later analysis and Oana Birceanu (0000-0002-3345-8769) returned the mother to continue McMaster University incubating her eggs. The team then Mouse neurogenous [email protected] returned 10 days later to collect blood zone doubles during once again when the eggs had freshly hatched and the mothers were scrambling puberty A consistently performing to care for their chicks, allowing them to mitochondrion for every test whether there was a change in mitochondria number or performance season given the task at hand. The blood samples allowed the researchers to measure two things. First, they measured the number of mitochondria in each bird’s blood cells by comparing the amount of genetic material that came from mitochondria to the amount of genetic material from the rest of the cells. Second, they measured how

efficient or high performing a bird’s BRAIN REMODELLING mitochondria were by testing how well Puberty is often accompanied by making they produced ATP given the amount of dumb decisions. Yet, despite its fuel available. reputation, Michael Brecht and

ENERGY BUDGET ENERGY colleagues from Humboldt University of Tucked into almost every cell of an Stier and colleagues found that the birds Berlin, Germany, recently discovered that animal’s body there are fierce little had fewer mitochondria while they were the awkward period of adolescence engines that turn food into energy. These tending to their nestlings compared to coincided with parts of the brain getting little power plants, called mitochondria, when they were incubating the unhatched bigger in rats (doi:10.1016/j.cub.2015.11. fuel animal activities by generating ATP eggs. However, the mitochondria 041). Appropriately enough, the region (adenosine triphosphate) that animals use performed more efficiently (produced that expands during puberty is called the to contract their muscles or send nerve more ATP with less fuel available) while ‘genital cortex’, a part of the brain that’s impulses so they can get moving and do the birds were busy wrangling their active when its namesake region is things. For any species, some individuals nestlings. A female’s ‘energy budget’ is aroused. The scientists made this discovery will be high performers – you know the likely much tighter when she has by comparing snapshots of the brain taken type – they run the fastest or jump the nestlings, because she has to feed both from different rats before, during and after highest, others are more ho-hum and herself and a nest full of hungry, puberty. However, comparing the same average, and some drag their heels not begging chicks. brain cells in the same region of the doing well at all. Scientists already know same animal across development would be that this range or variation in animal The researchers also found the birds were a more reliable way to compare how performance is partly caused by the consistent across contexts: those with the puberty remodels the brain. number of mitochondrial engines animals most and the highest performing have and how effective their mitochondria mitochondria during incubation, also had Following up on this study, Johanna Sigl- are at turning food into energy. We also the most and the highest performing Glöckner, also from Brecht’s laboratory, know from lab studies that couch potatoes mitochondria during the nestling phase. turned to another lab animal, the house can actually increase their performance Overall, the team’s findings suggest that mouse (Mus musculus), for which there is when faced with energetically demanding wild animals may have some wiggle room a wide range of fancy molecular tools that situations. Yet, it is unclear whether the to modify the amount and performance of allow scientists to flag specific brain cells. number of mitochondria or how effective their mitochondria across contexts. Using this technology, she and her they are at pumping out energy can However, they are also stuck with the colleagues spied on brain cells in the change over time within wild animals. cards they were dealt and are consistently genital cortex of individual mice several either ‘high’ or ‘low’ performers in all times during their development, as This is an important question because scenarios. recently reported in Current Biology. some stages in life require more energy than others; for example, reproduction is doi:10.1242/jeb.211409 First, the team determined if, like rats, male infamous for being energetically draining. and female mice grew more touch- Antoine Stier, Pierre Bize, Bin-Yan Hsu Stier, A., Bize, P., Hsu, B. and Ruuskanen, S. sensitive brain cells in the genital cortex and Suvi Ruuskanen from universities in (2019). Plastic but repeatable: rapid adjustments during puberty. While mice have other cell of mitochondrial function and density during Finland and the UK set out to address this reproduction in a wild bird species. Biol. Lett. 15, types in their genital cortex, since sex is all very question by studying pied flycatchers 20190536. doi:10.1098/rsbl.2019.0536 about touch, the team focused on tallying Journal of Experimental Biology

3 OUTSIDE JEB Journal of Experimental Biology (2020) 223 touch-sensing cells as they play a more Sigl-Glöckner tweaked her designer age, but also their sex and sexual obvious role. To accomplish this, Sigl- mice so that the touch-sensitive cells experience. Glöckner brought in specially designed would glow even brighter when they mice that produce glow-in-the-dark tags were activated: the brighter the cell, the These findings by Sigl-Glöckner and her only within brain cells receiving touch more responsive to touch. Then, the team colleagues expand our understanding of information from the thalamus, the brain’s turned on a tiny vibrating device, the how different factors drive brain sensory relay station. This allowed the same one that makes your cell phone remodelling across development and team to peek in on the mice periodically buzz, to sexually stimulate mice while reveal that just as hormonal pre-teens and count how many new touch-sensitive measuring how bright their brain cells increase in size and sensitivity during cells were born in the genital cortex as the glowed. Despite having a similar number puberty, so too does the mouse genital mice grew up. Following puberty, both of cells in the genital cortex, the male cortex, thus stimulating more questions to male and female mice doubled the size of mouse cells shone brighter than the be answered about how puberty changes their pre-pubertal genital cortex and female cells – both pre- and post-puberty the brain. added nearly two new touch-sensitive – suggesting that male mice have a more cells a day across adolescence. sensitive erogenous zone across doi:10.1242/jeb.211425 Therefore, mice, like rats, expand the size development. However, if female mice Sigl-Glöckner, J., Maier, E., Takahashi, N, of their genital cortex during sexual mated with a male before puberty or if Sachdev, R., Larkum, M. and Brecht, M. (2019). Effects of sexual experience and maturation. However, while (brain) size females were abstinent and just reaching puberty on mouse genital cortex revealed by matters, it wasn’t clear how responsive to adulthood, their genital cortex cells chronic imaging. Curr. Biol. doi:10.1016/j.cub. touch these new cells were. became more responsive to stimulation 2019.08.062 compared with pre-puberty. Taken Daniel M. Vahaba (0000-0003-2960-3756) In order to measure how genital together, the changing response to sexual Smith College cortex cells respond to stimulation, stimulation depends not only on mouse [email protected] Journal of Experimental Biology

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