Ravignani, A.

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OUTSIDE JEBUnborn wasps fumigatetheir dinnerSELF-DEFENCEWhen the leftover food in my fridge turnsinto a microbiology experiment, I simplythrow it out and get a fresh mealelsewhere. But not all animals have thisluxury. Some only get a single meal and,if it rots, the animal starves and dies. Suchis life for the larva of the Europeanbeewolf, whose parent provides it with asingle paralysed bee to literally eat aliveas it develops. The problem is that thelarva and the bee are buried in anunderground chamber surrounded bymicrobes that are as eager to eat the bee asthe larva is. So how do beewolves keeptheir food clean? As elegantly shown byErhard Strohm from the Universityof Regensburg in Germany and hiscolleagues from Mainz and Jena, theyfumigate it.If a paralysed bee is placed into a beewolfbrood cell, it quickly turns into a fuzzytennis ball covered with fungus. But thisrarely happens if a beewolf properly doesits job before abandoning its offspring.Strohm and his colleagues have shownover many years that beewolves use aseries of antiseptic strategies to keep theirlarval resource fungus-free. First, theyembalm the bee in awaxy resin that delaysfungal growth. Second, they inoculate thebrood cell with symbiotic bacteria thatproduce a potent antifungal drug. Butthese do not cover all eventualities,because the wax is only partially effectiveand the bacteria only protect older larvaein cocoons.The hint that something more was at playcame from the conspicuous odour of thebrood cells themselves, notably cells thatalso contained a wasp egg. The teamtested eggs and found that they secretehuge quantities of a pungent, andhighly toxic, volatile gas called nitricoxide. Nitric oxide is used industriallyto fumigate fruit against fungalcontamination, so the team hypothesizedthat the eggs were using it in the samewayto protect their bee prey. To test this, theyplaced bees with and without an egg into abrood cell and counted how many rotted.As predicted, the bees with individualeggs were protected from fungi. And, ifthey added a second bee – not in contactwith the egg – this was decontaminatedtoo, proving that protection was due to thevolatile gas.A nitric oxide fumigant is the perfectsolution to the problem faced by thesewasps. It fills all spaces in the brood cellwhere fungi hide and can dissolve intothe water droplets on the surface of thebee, giving rise to nitrogen dioxide, yetanother antimicrobial agent. It canalso linger after a well-timed pulse ofproduction, much like an unfortunateodour in a car with the windows up.Finally, its effects are general becausenitric oxide can prevent the growthof a broad range of possible fungalcontaminants.But these advantages have to work in thecontext of the wasp’s other defences –and it seems they do. When the teamcombined waxy embalming with eggfumigation of their unfortunate beevictims, they found that the combinationworked better than either alone. Andimportantly, although for unknownreasons, nitric oxide does not inhibit thegrowth of the symbiotic bacteria thatmake up the beewolf’s third line ofdefence. The authors speculate that thebacteria may be protected in the brood cellor may have evolved resistance. Anotherpossibility is that nitric oxide may be lessactive against bacterial spores, but thisremains to be tested.Parents go to great lengths to protect theiroffspring, but kids eventually have tofight their own battles. This amazingsystem shows that the unborn can also getin on the action of self-defence. Even eggswant a clean meal.doi:10.1242/jeb.192997Strohm, E., Herzner, G., Ruther, J., Kaltenpoth,M. and Engl, T. (2019). Nitric oxide radicals areemitted by wasp eggs to kill mold fungi. eLIFE 8,e43718. doi:10.7554/eLife.43718Daniel E. Rozen (0000-0002-7772-0239)Leiden Universityd.e.rozen@biology.leidenuniv.nlSinging seals imitatehuman speechSOUND PRODUCTION Have you ever wondered which animalslearn to communicatewith sounds and how?We can precisely control our vocal tract andvocal cords when learning new sounds. Butthe capacity for ‘vocal learning’ is extremelyrare; fewer than 100 attested species withonly a dozen mammals are capable oflearning how to produce sounds forcommunication. For example, cats, dogs andchimpanzees cannot learn vocalizations.Amanda Stansbury and Vincent Janik fromthe University of St Andrews, UK, testedwhether grey seals (Halichoerus grypus) canbe trained to learn new sounds by imitation.The researchers trained a grey seal, namedZola, to copy three sounds played througha loudspeaker. To make the task easierfor Zola, these sounds were recordings ofher own calls, which had been shifted infrequency to sound higher or lower. Everytime Zola reproduced one of the soundsat the correct pitch, she received a fishreward. After training, Zola could copysequences of up to 10 sounds varying inpitch, most of which she had not heardbefore. However, when the team analysedOutside JEB reports on the most exciting developments in experimental biology. The articles are written by a team of active research scientistshighlighting the papers that JEB readers can’t afford to miss.1© 2019. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2019) 222JournalofExperimentalBiologythe audio recordings, they discoveredthat instead of modifying the vibrationfrequency of her vocal folds – as humansdo when singing – Zola was altering theshape of her vocal tract, similar to the waywe change the shape of our mouths whengoing from ‘bath’ to ‘boot’. She couldeven imitate motifs such as the ‘StarWars’ theme and ‘Twinkle little star’; thevideos are a must-watch. So, Zola the‘singing seal’ could imitate tunes byperforming vocal tract movements that wehumans usually make when speaking.Stansbury and Janik then trained two moreseals, Janice and Gandalf, to imitate fivevowel sounds – similar to those found in(British English) ‘bath’, ‘may’, ‘meet’,‘thought’ and ‘boot’ – to assess theanimals’ ability to control their vocal tracts.To make the task more manageable,Stansbury and Janik produced the vowelsounds by modifying the seals’ own callsand trained Janice and Gandalf to matchthese modified calls. Eventually, both sealscould reliably imitate the five vowels byemphasizing either the lower or higherfrequencies. The seals had changed theirvoices to sound deeper (as in ‘boot’) ormore acute (as in ‘meet’), so that they nolonger sounded like other seals. They hadlearned how to produce new sounds insteadof ‘recycling’ sounds they could alreadyproduce.Why is this story scientificallyinteresting? Stansbury and Janik provideexperimental evidence that it is possiblefor some mammals other than humans tolearn to produce new sounds viamodifications of their vocal tracts. This issomething we humans do constantlywhen learning our mother tongue or a newlanguage. Currently, many researchersstudy bird song production to help usunderstand human speech, but now amuch closer relative – seals, with theirhuman-like vocal tracts and learning abilities– could be a perfect alternative modelspecies for learning about human speechand song thanks to our similar anatomy.In addition, it is possible to measurethe brain activity of seals, potentiallyallowing us to identify which areas of thebrain are key for seal vocal imitation.In brief, seals may have much to teachus about human speech and song. Sealscientists are beginning to listen and youare all welcome to join in too.doi:10.1242/jeb.208447Stansbury, A. L. and Janik, V. M. (2019). Formantmodification through vocal production learningin gray seals. Curr. Biol. doi:10.1016/j.cub.2019.05.071Andrea Ravignani (0000-0002-1058-0024)Vrije Universiteit Brussel & SealcentrePieterburenandrea.ravignani@gmail.comSun and wind cues guidedung-rolling beetlesacross the savannahNSEWNAVIGATIONSouth African dung beetles competefiercely for the chance to eat the poopof other animals. When a beetle comesacross a pile of dung in the savannah, itquickly cuts off a piece, rolls it into a ball,and heads off in reverse with its stinkyprize, away from other hungry beetles. Toefficiently escape with their trophy, thebeetles move in a straight line, orientingthemselves with celestial objects such asthe sun or moon. However, new researchfrom Marie Dacke and colleagues fromSwedish, German and South Africanuniversities suggest that the beetles canalso steer based on changes in winddirection.First, Dacke and colleagues testedwhether beetles in their natural habitatsteer dung balls in a straight line usingcues from the wind in addition to thecelestial cues they are known to use. Theresearchers tested the beetles when thesun was at three different positions abovethe horizon – low (15–30 deg), medium(45–60 deg) and high (>75 deg) – andobserved whether they continued to rolltheir dung balls in the same direction inresponse to a 180 deg artificial change inwind direction. When the sun was at itshighest elevation and the experimentersswitched the direction of the wind, thebeetles started rolling their dung balls inthe opposite direction. However, whenthe sun was at the lower elevations, thebeetles kept rolling their balls in the samedirection no matter how the windchanged. This suggests that the beetlesorient themselves based on a single cue ata time, either the sun or the wind, and thatthey might, in fact, have a ‘wind compass’they use when the sun is high in the sky.The team then took the beetles back tothe lab to better understand how theycoordinate using wind and sun cues. First,the scientists changed the number ofsensory inputs the beetles receivedbetween each roll of their dung ballsforward: they provided the beetles withmultiple inputs on their first rolls (windfrom a fan and a bright light to mimicthe sun, set perpendicular to each other).They then removed one of the inputsduring the second revolution of the dungball – leaving the insects to navigate eitherby artificial ‘wind’ or a fake ‘sun’ alone.In response, the beetles continued rollingtheir dung balls in straight lines despiteswitching from multiple to individualsensory inputs, which was surprising, asunder natural conditions in the savannahthe beetles seemed to position themselvesbased on one sensory input at a time.However, the beetles’ ability to continuemoving in a straight line suggests that theystore directional information from boththe wind and the sun in their internalcompass systems. The researchers thentested whether orientation informationfrom the sun and wind sensory systemscan be stored and exchanged betweendifferent brain areas. They realised thatthe beetles were able to depend ondirectional information from the sunand moon collected at different times,suggesting that information from the twosystems is shared somewhere in the brain.Dacke and colleagues are the first to showthat wind is important for helping SouthAfrican dung beetles roll away fromhungry competitors with their dinner.Additionally, their research highlightsthat information from the wind and thesun might be stored in the same placein the beetles’ brains. For an animalthat feasts on other animals’ poop, theSouth African dung beetle has quite asophisticated navigation system.doi:10.1242/jeb.193003Dacke, M., Bell, A. T. A., Foster, J. J., Baird, E. J.,Strube-Bloss, M. F., Byrne, M. J. and el Jundi,B. (2019). Multimodal cue integration in the dungbeetle compass. Proc. Natl. Acad. Sci. USA116, 14248-14253. doi:10.1073/pnas.19043081162OUTSIDE JEB Journal of Experimental Biology (2019) 222JournalofExperimentalBiologyGina Mantica (0000-0001-5329-3896)Tufts Universitygina.mantica@tufts.eduPain insensitivity: subtlechanges make a hugedifferenceNOCICEPTIONSome years ago, after putting out therecycling, I had the unpleasant discoverythat my dog had got into my bag ofjalapeño potato chips and thrown up allover the floor. They obviously hadn’t satwell with him. As I cleaned up the mess,I pondered why my dog was so quick toexpel the snacks, whereas I could happilyeat a whole bag in a single sitting.Evidently, the same question occurred toOle Eigenbrod of the Max DelbrückCenter, Germany, who teamed up with agroup of international collaborators toexplain why some animals tolerate certainsubstances, whereas others do not.The nervous system perceives pain viaspecialized neurons (nociceptors) thatrespond to substances ranging from lethalvenom to benign pepper. However, evenclosely related species do not respondwith equal intensity to the samecompounds, thanks to their differentevolutionary trajectories. For this reason,Eigenbrod and colleagues studied paininsensitivity in nine species of relatedAfrican burrowing rodents, which areseparated by 7–55 million years ofevolutionary history, by evaluating theirreactions to three noxious molecules:capsaicin (which makes jalapeños spicy),hydrochloric acid (found in acidic fruits)and AITC (a pungent molecule in manyroot vegetables). After dabbing a stingingmolecule onto each animal’s footpad, theauthors assessed how much pain theyexperienced by measuring the time eachrodent spent licking its paw. They alsoinvestigated the molecular components ofthe rodent’s pain neurons, to identify thespecific differences that underlie paininsensitivity.The researchers initially found that thepain neurons of all nine rodent speciespossess the receptor molecules that shouldallow them to detect the three noxiousmolecules. However, some of the speciesdid not exhibit pain in response to thesecompounds. For instance, highveld mole-rats did not feel AITC dabbed onto theirpaws, even though there are neuronreceptors that should bind the noxiouschemical and potentially trigger pain. Theteam attributes this insensitivity to theoverexpression of a gene for a sodiumleak ion channel that short circuits thepain neurons and prevents them fromtransmitting signals. The team suspectsthat AITC resistance stems from thehighveld mole-rats sharing their burrowswith aggressive Natal droptail ants,whose excruciatingly painful stingsactivate the AITC receptor. Clearly, it wasadvantageous for the rodents to evolveimmunity to the stings.The team also observed that East Africanroot-rats,Capemole-rats andnakedmole-ratswere completely oblivious to thehydrochloric acid dabbed onto their paws.The authors found that the pain neurons ofthese three species possess a sodium ionchannel with the same two amino acidalterations. These changes preventhydrochloric acid from activating the ionchannel, rendering the neurons insensitive tothe acid and unable to trigger pain.Considering that the three species areseparated by40million years of evolutionaryhistory, thesemodifications are a classic caseof convergent evolution, allowing all threespecies to tolerate hydrochloric acid.Finally, the researchers noted that Nataland naked mole-rats are impervious to thespicy jalapeño capsaicin and believe therodents’ evolved insensitivity is due tothem inhabiting deep, oxygen-poorburrows, where CO2 levels can reach veryhigh levels. Given that inhaling largeamounts of CO2 can cause a great deal ofpain, it is likely that the mole-rats adaptedto their underground lifestyle by bluntingmost of their pain responses.Although the nine rodent species areclosely related, they each live in verydifferent geographical environments andhave faced different selection pressuresthat have led to their varying degrees ofpain sensitivity. It appears that evolutionhas several lessons to teach us about thevarious molecular mechanisms that canmediate pain.doi:10.1242/jeb.192989Eigenbrod, O., Debus, K. Y., Reznick, J., Bennett,N. C., Sánchez-Carranza, O., Omerbašić, D.,Hart, D. W., Barker, A. J., Zhong, W.,Lutermann, H., Katandukila, J. V., Mgode, G.,Park, T. J. and Lewin, G. R. (2019). Rapidmolecular evolution of pain insensitivity inmultipleAfrican rodents. Science 364, 852-859. doi:10.1126/science.aau0236Ilan Ruhr (0000-0001-9243-7055)The University of Manchesterilanruhr@manchester.ac.ukAndean birds with slowmetabolism live longerPACE OF LIFEMetabolism – the chemical process thatgenerates energy for cells to function – isso fundamental to existence that it has beendubbed ‘the fire of life’. However, thedebate over how the rate ofmetabolism caninfluence an animal’s survival has burnedon for decades. The ‘pace of life’ theorypredicts that species with high metabolicrates accrue more damage and succumbto death earlier than animals with slowermetabolism. Whilst this makes sense intheory – a gently burning flame lastslonger than a firework – experimentallyproving it has been a tricky business.To shed light on how metabolic ratecorrelates with survival in wild tropicalbirds, a team led by Micah Scholer fromthe University of British Columbia,Canada, studied a diverse cohort of37 species in the Peruvian Andes, fromthe humid foothills up to 3000 m altitude.The group caught birds in mist-nets andreleased them, tagged but unharmed, atdifferent sites over several years to assessannual survival. They then combinedthis dataset with previously acquiredmeasurements of basal metabolic rateof the same species from the same fieldsites – achieved by measuring oxygen3OUTSIDE JEB Journal of Experimental Biology (2019) 222JournalofExperimentalBiologyconsumption in resting animals – in asophisticated mathematical model todissect the interplay between metabolism,survival and habitat.Survival varied greatly between differentspecies; in some cases, annual survivalexceeded 70%, whereas in the mostvulnerable species, less than half thisproportion survived each year. The teamfurther revealed that, although metabolicrate was similar between birds inhabitingdifferent altitudes, montane speciesexhibited lower survival than those fromthe foothills. Avian life at high altitudeis something of a double-edged sword;the harsher, drier environment provideschallenges, yet this also discouragespredators. It appears here that the costs ofliving at altitude outweighed the benefitsof lower predation, although the researchteamwas unable to exclude the possibilitythat the high-altitude birds wereemigrating from the study site insteadof perishing.The standout result was that, irrespectiveof altitude, the species with the lowestmetabolic rate – or the slowest pace of life– indeed exhibited the highest rate ofsurvival. Whether annual survival per seequates to evolutionary success isdoubtful, because even the species withthe lowest survival rate are, by definition,successful enough to prosper today.Apparently, they are able to reproduceeffectively in their short but busy lifetime,which may be fuelled by their highmetabolic rate. The fact that specieswith both short and long lifespanspersist suggests that neither strategyis optimal.By revealing a well-defined link betweenmetabolism and survival, this studynot only represents a great advancefor environmental physiology but alsohelps pave a path for future work. Forexample, researchers could measuremetabolic rates in animals’ naturalenvironments, which is tricky buttechnically feasible, to allow us todescribe how metabolism changesseasonally in the different habitats.Ultimately, this will help paint anever-clearer picture of how and whysurvival and metabolism vary betweendifferent species.doi:10.1242/jeb.193011Scholer, M. N., Arcese, P., Puterman, M. L.,London ̃o, G. A. and Jankowski, J. E. (2019).Survival is negatively related to basal metabolicrate in tropical Andean birds. FunctionalEcology 259, R333. doi:10.1111/1365-2435.13375William Joyce (0000-0002-3782-1641)University of Ottawawilliam.joyce@bios.au.dk4OUTSIDE JEB Journal of Experimental Biology (2019) 222JournalofExperimentalBiology

Singing seals imitate human speech

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