Preening power: red-billed woodhoopoes go on the defensive

Red-<strong>billed</strong> Woodhoopoes <strong>go</strong> on the defensivePREENINGPOWERText by Ross WanlessIn the wild, every day is a struggle betweenlife and death. P<strong>red</strong>ators lurk in the shadows,hunting by night, using the minutest sounds and fainttrails of scents that waft through the branches, undetectedby human noses, to locate their prey.In the woodlands and forests of Africa, one species has hit upon animpressive way of defending itself from the denizens of the dark. Chris van Rooyen

The Red-<strong>billed</strong> Woodhoopoe Phoeniculuspurpureus is an intriguing species.Because it lives in groups, itssociety is a rich tapestry of inter actions,alliances, betrayals and secrets. Its life isplayed out in the forests and woodlandsof sub-Saharan Africa, where it is one ofthe more conspicuous birds. Its noisycalls echo and resound across valleys,while territorial disputes between neighboursachieve impressive crescendos. Onewould struggle not to see these birdswhen walking through any reasonablylarge tract of forest or well-wooded habitat.The species’ raucous cackling givesrise to its Xhosa name, Hlekabafazi, whichmeans ‘laughing women’.For almost 30 years biologists havebeen studying these somewhat bizarre,but ingratiatingly endearing birds. Theirintricate lives are unique among birdsin a number of ways and, despite animpressive volume of research, theycontinue to surprise.An unusual strategyOne of the Red-<strong>billed</strong> Woodhoopoe’smore unusual traits is its need to roostin cavities (usually in trees), a situationcomplicated by the fact that the birdscannot excavate their own holes. Thisreliance on other animals’ (or nature’s)handiwork places them under tremendouspressure. In many areas, thereis enormous competition between severalcavity-roosting species, and <strong>woodhoopoes</strong>are always on the lookout for aback-up cavity in their territory.Woodhoopoes breed communally. Inmost recorded cases of breeding attempts,the alpha pair breed, and any other membersof the group help in the rearing ofthe brood. The business of helping othersto raise young rather than breeding oneselfis quite intriguing. At first glance itmight not make much sense to expend alot of time and energy helping to rearanother pair’s young. Why don’t thesehelpers <strong>go</strong> off and breed themselves?Firstly, some year-old birds do manageto establish territories and breed. Theirsuccess rate is, however, generally ratherlow. By contrast, helpers seem able tolearn what to do, and when they establishthemselves as breeders, they tend todo much better than others. It takes a lotof practice and skill to forage in thewoodlands for oneself, let alone for aChris van rooyenLeft and right Communalliving has advantages for the<strong>woodhoopoes</strong> – increased numbersmean a better defence systemand more helpers to feedthe young.brood of highly demanding, growingchicks. A second reason is that moreoften than not, helpers are ‘family’; eitheroffspring from earlier breeding attemptsor related (typically siblings) to one of thealpha pair. It makes biological sense toinvest in one’s family, even if the youngbeing ca<strong>red</strong> for aren’t one’s own. Becauseof this ‘blood connection’ or relatedness,helpers invest their efforts in ensuringthat their sha<strong>red</strong> genes are passed on tothe next generation. This co-operativebreeding strategy is employed by a diversityof animals, ranging from honey-beesand ants to naked mole-rats.A third reason is that in some circumstancesroosting cavities and territoriesare hard to come by, and even harder todefend. A larger group can usually defenda cavity or maintain a large territory, andwhen times are tough, for example intimes of drought, territories are oftenexpanded to improve foraging. Underthese circumstances, small groups runthe risk of being displaced completely.This can be an utter disaster for <strong>woodhoopoes</strong>,which have to find safe roostingcavities every night. It seems thatthe best option, unless another territorycan be found immediately, is to joinanother group.The disadvantage of joining anothergroup is that newcomers always start atthe bottom of the ladder. A very strongpecking order is present in most grouplivingbirds and in <strong>woodhoopoes</strong> thistakes on added significance. Should oneof the alpha pair die, the male or femalenext in line in the pecking order willtake over as breeders. For newcomersthis can mean a very long wait for thechance to reproduce.Threats from p<strong>red</strong>atorsNo one is really too sure why <strong>woodhoopoes</strong>always roost in a cavity. Some evidencesuggests that during winter, grouphuddling in cavities can result in a considerablesaving of energy. This does notexplain why, on warm nights, cavi- Brendan Ryan56 <strong>red</strong>-<strong>billed</strong> WoodHoopoesfebruary/march 2001<strong>red</strong>-<strong>billed</strong> WoodHoopoes57

ties are prefer<strong>red</strong> over safe roosts inthorn bushes or high up in trees. Whatis known for sure, how ever, is thatroosting in cavities can be downrightdangerous. Cavity raiding by nocturnal,arboreal p<strong>red</strong>ators such as genets, treecivets, African wild cats and feral domesticcats, and possibly a number of snakespecies, is well known and in some areasis a significant cause of death. Whereverthere are strong forces (for example,high levels of p<strong>red</strong>ation) acting onpopulations, there are equally strongforces of natural selection that act toalleviate those pressures. Group-livingand cavity roosting seem to have set thestage for a strong selective pressure for<strong>woodhoopoes</strong> to evolve some mechanismthat would counteract the highrisk of p<strong>red</strong>ation.DefenceMany organisms use chemicals in a varietyof ways to defend themselves againstp<strong>red</strong>ators. They do it by being malodorous,tasting really bad, or actually beingpoisonous. Skunks do it. Butterflies doit. Frogs do it. Fish doit. But birds? Surprisingly, chemicaldefence has been documented in morethan 120 species of birds. Two wellknownsouthern African gamebird species,the Common Quail Coturnixcoturnix, and the Spur-winged GoosePlectropterus gambensis are so poisonousthat they can kill. Luckily they are nottoxic during the time they spend insouthern Africa. The quail eats nastyEuropean plants like hemlock shortlybefore its seasonal migration in Europe,and if eaten at this stage the birdcan cause an illness known in medicalparlance as ‘coturnism’. (Despite this,hunting and eating quail remains anational pastime in much of southernEurope.) Another migrant, the SpurwingedGoose spends much of its timein The Gambia, where it eats a particularlypoisonous beetle not found insouthern Africa. Both these species, andindeed all other known examples ofchemically defended birds, take the toxinsthey use from their diet.The exact nature of chemical defenceis known in relatively few bird species,with the most recent evidence comingfrom the genus Pitohui. Three species ofPitohui, endemic to New Guinea, havebeen shown to have a toxic compoundof a class found only in one other taxonomicallyand geographically distantgroup, the neotropical poison-dart frogsof the genus Phyllobates. The chemicalcompounds found in the skin and musclesof Pitohui species are believed to bestrong enough to kill a medium-sizedbird of prey.The way of the <strong>woodhoopoes</strong>All birds have a small preen gland situatedabove the tail, at the base of thespine. In most birds the gland secretes avariety of fatty acids, oils and otherorganic com pounds, which the birdsspread on their feathers during preening.Such preening has two widely recognisedfunctions: in much the same way asregu larly used wood or leather needs oiling,the oils of the gland are conside<strong>red</strong>essential to the maintenance of <strong>go</strong>odfeather condition; the second functionmay be for fungicidal, bactericidal orother hygienic purposes.Woodhoopoes seem to have found athird and unique use for this gland. Theirpreen gland is capable of producing ascent so strong that experiencedre searchers can tell how recently a roostcavity was used, based only on the lingerin<strong>go</strong>dour. Further, the secretion remainsdetectable for several hours on the handsof those who have handled birds (and isextremely unpleasant to taste). In short,<strong>woodhoopoes</strong> smell bad!Yet more compelling, albeit circumstantial,evidence for chemical defencecomes from woodhoopoe behaviour.When disturbed at their roost cavities,<strong>woodhoopoes</strong> do something ratherunusual. Normally, birds will try todefend themselves with their bills, and<strong>woodhoopoes</strong> certainly have bills longenough for us to suppose they might dothe same. Curiously, they face away froma threat. Not only do they turn tail, butthey also expose their preen gland.Typically, the emission of a drop of theirextremely pungent se cretion accompaniesthis behaviour. This response tothreat seems to be designed to maximisethe effect of a deterrent odour. Viewed inthis light, their strange reaction to p<strong>red</strong>ators(and biologists) looks remarkablyastute instead of mystifyingly silly.This has led researchers to speculatethat the unpleasant secretion is used inchemical defence. Speculation, conjectureand circumstantial evidence are allvery well, but how does one prove thata bird uses chemicals to defend itselfagainst p<strong>red</strong>ators?The proof of the pudding...The first step was to identify what compoundswere responsible for the smell.Professor Ben Burger of the University ofStellenbosch, together with a student,analysed the chemical composition ofwoodhoopoe preen-gland secretions.They identified a suite of volatile compoundsresponsible for the <strong>power</strong>ful scentassociated with <strong>woodhoopoes</strong>. In factthere were so many compounds that theodours could quite likely be used forother purposes, such as territorial orroost-cavity defence, communication orthe maintenance of social structure, andkeeping ectoparasites such as feathermites and lice at bay.Once the smell-producing compoundshad been identified, they could be synthesisedin relatively large quantities.This meant I could set about testingwhether the woodhoopoe secretion wasin fact a deterrent to p<strong>red</strong>ators. Simplefood-choice tests were performed ondomestic cats, using canned cat foodlaced with the synthetic scent. Theassumptions behind this were that catsare representative of the kind of p<strong>red</strong>atorslikely to investigate tree cavities. Ihad to make sure the cats were hungry, sothat if they left any food uneaten it wasbecause they really didn’t like it. I gavethe hungry cats a choice of two bowls ofcanned cat food, one normal and theother laced with the chemicals found inwoodhoopoe preen glands.... is in the smellThe results of the tests were totallyunequivocal, but not what I hadexpected. P<strong>red</strong>ictably, all the cats <strong>go</strong>bbledthe unscented food. Some tookone sniff at the bowl of smelly food,turned up their noses and went to lickthe untainted bowl clean. Most, however,attempted to eat the food despiteits smell. All gave up after realisingthe food not only smelled bad, buttasted disgusting too. What this simpleexperiment showed is that <strong>woodhoopoes</strong>cent is a <strong>power</strong>ful deterrent top<strong>red</strong>ators. However, because most ofthe cats at least attempted to eat thefood, even though it smelled very bad,I could not conclude that bad smellalone is enough to deter hungry p<strong>red</strong>ators.Woodhoopoes, just like incometaxreturns, are rather complicated.Some of the cats were prepa<strong>red</strong> to tryand eat the food, even though it clearlysmelled bad and tasted even worse. Thissuggests that under natural conditionsat least some p<strong>red</strong>ators are likely toattempt to capture roosting <strong>woodhoopoes</strong>.What probably happens in natureis that the p<strong>red</strong>ator would kill and possiblyeat a woodhoopoe. But it woulddo so without relish, and would learn toavoid in future any cavities that had thetell-tale smell of <strong>woodhoopoes</strong> whichwould serve as a warning that thesebirds are not a tasty meal.Woodhoopoes are the first birds tohave proven chemical defence againstp<strong>red</strong>ators. Further research may revealmore surprises. To date, all other chemicalsused by birds in their defence arethought to have been sequeste<strong>red</strong> fromplants or insects in the diet. The preengland naturally produces a wide rangeof organic chemicals and there is everyreason to believe that <strong>woodhoopoes</strong>are the first birds known to sciencethat synthesise their own defensivecompounds.<strong>Preening</strong> not only enhances feathercondition in the Red-<strong>billed</strong> Woodhoopoe,but it may well be part of the species’defence armoury by making it smell andtaste foul to p<strong>red</strong>ators.chris van Rooyen58 <strong>red</strong>-<strong>billed</strong> WoodHoopoesafrica – birds & birding<strong>red</strong>-<strong>billed</strong> WoodHoopoes59