BIOLOGY insight into the birds’ different modes of life. THE BONES IN THE TOES Birds’ feet are not only used for n almost all birds, the number of bones locomotion (walking or running, Iin each toe is preserved: there are two swimming, climbing), but they bones in the first toe (digit I), three bones serve other important functions in in the second toe (II), four in the third (III) perching, foraging, preening, re- and five in the fourth (IV). Therefore, the production and thermoregulation. identity of a toe (I to IV) can be determined Because of this, the structure of a quite reliably from the number of bones in bird’s foot often provides insight it. When evolutionary toe-loss occurs, this into the species’ ecology. Often, makes it possible to identify which digit distantly related species have con- has been lost. verged on similar foot types when adapting to particular environ- ments. For example, the four fully demands of a particular niche or The first, and seemingly ances- webbed, forward-pointing toes environment. The arrangement tral, configuration of birds’ toes – called totipalmate – of pelicans, of toes in lovebirds, barbets and – called anisodactyly – has three gannets and cormorants are an ad- cuckoos, for example, is differ- digits (numbered II, III and IV) aptation to their marine habitat. ent from that in passerines (such orientated forwards and digit I The closely related Shoebill as finches, shrikes or starlings) in (the ‘big toe’, or hallux) pointing does not have webbed feet, per- the same environment. The func- backwards. This arrangement is haps because of its wetland habi- tional reasons for differences in shared with theropod fossils and The toes of penguins tat, but the tropicbirds, which foot structure can be difficult to is the most common, being found (below left) and gan- fancy form their own relatively ancient explain. in more than three-quarters of nets (below) are both evolutionary lineage, are also toti- In an attempt to organise and bird species, including the webbed anisodactyl, but have palmate. Albatrosses, petrels and better understand the observed feet of ducks and penguins, most different webbing shearwaters, however, only have differences among avian feet, songbirds (such as sparrows and patterns (palmate three forward-pointing toes (dig- biologists have named five gen- weavers) and pigeons, buzzards, and totipalmate footwork its II to IV; digit I is vestigial) that eral categories that describe the vultures, eagles and gamebirds. respectively). Both are webbed – or palmate – as do arrangement of birds’ toes: aniso- The anisodactyl toe orientation is groups are adapted penguins, ducks and geese. These dactyly, zygodactyly (including well suited to perching and grasp- to an aquatic envi- species are all adapted to aquatic semi-zygodactyly), heterodactyly, ing, especially when the hallux > ronment. environments where webbed syndactyly and pamprodactyly. feet are clearly beneficial for However, like many concepts in locomotion. biology, there are exceptions, vari- III III Different foot types can be ations and intermediates that vio- IV II II IV DAVIDE GAGLIO equally suited to the functional late these ‘rules’. The dazzling diversity of avian feet I I TEXT LISA NUPEN ANISODACTYL The many different sizes and shapes of birds’ bodies, the astonishing variety of coloration in their plumage and bills and the functional precision of their wings have long intrigued and delighted nature enthusiasts. Perhaps distracted by the bold and beautiful features of avian form, one could be forgiven for overlooking another fascinating aspect of birds’ evolution: their feet. he fact that birds’ feet have digits on each limb – in other by the evolution of the dinosaurs’ a dinosaurian jizz is no words, were tetra dactyl – whereas forelimbs into wings, this diver- coincidence, since birds living reptiles (chameleons, lizards sification is no less significant. III III IV II II IV DAVIDE GAGLIO Tevolved from a group of reptil- and geckos) most often have five. And notably, the structure of III III The long toes of ian ancestors called theropod From this four-toed origin there birds’ feet, especially the orienta- IV II II IV I I African Jacanas rep- (‘beast-footed’) dinosaurs. Like has been a remarkable diversifica- tion and number of digits, or toes, TOTIPALMATE resent an anisodactyl most amphibians and birds to- tion in avian hind-limb structure. shows great variation at multi- arrangement. day, theropod dinosaurs had four Although overshadowed perhaps ple taxonomic levels, providing PETER RYAN I I PALMATE 34 AFRICAN BIRDLIFE SEPTEMBER/OCTOBER 2016 BIRDs’ feet 35 III II II III IV I I IV ZYGODACTYL left Cuckoos exhibit zygo- dactyly, the second most common toe arrangement among birds. below Semi-zygodactyly – the ability to rotate the outer toe forwards and backwards – occurs in owls. III II II III V V IV I I IV SEMI-ZYGODACTYL IV III III IV I II II I HETERODACTYL III III IV II II IV – described as semi-zygodactyly are many intermediate examples rollers. Similarly, among passer- or ectropodactyly. of birds with partly fused toes in ines it can sometimes be difficult There is another configura- this group. Extreme syndactyly to distinguish the syndactyl and I I tion – known as syndactyly – in occurs in the wood-hoopoes and anisodactyl conditions, as they SYNDACTYL which two or more toes (usually hornbills and diminishes progres- intergrade closely. III and IV) are fused to vary- sively through the kingfishers to The final arrangement of toes – The fused toes of birds, such as cuckoos and tura- to zygodactyly and heterodac- ing degrees. Syndactyly has been only minor fusion in Upupa and pamprodactyly – is found among syndactyl kingfishers cos, have this arrangement, but tyly might include increased grip well studied in humans as a con- finally the true anisodactyl feet of some mousebirds and swifts, > may increase grip it is also well suited to grasping, strength for perching resulting genital oddity that arises from strength for perching. as in parrots, and climbing, as in from two pairs of toes oppos- specific genetic mutations, and woodpeckers. These species are ing each other, and better grasp- five types of finger or toe fusion CONVERGENT EVOLUTION OF ZYGODACTYLY ALBERT FRONEMAN (4) not closely related, which sug- ing for similar reasons. Parrots, have been characterised. In the he osteological details of foot structure are different in woodpeckers above Only trogons is elongated, but it is not the only gests that zygodactyly has evolved among other species, routinely avian world, the fleshy sheath Tand cuckoos, indicating that these distantly related groups evolved possess a heterodac- evolutionary ‘solution’ to such multiple times. manipulate their food using their that unites the anterior digits is zygodactyl feet in different ways. In fact, zygodactyly seems to have tyl foot type, which activities. Trogons have a unique ar- feet – there are even left-footed thought to increase grip strength evolved independently in at least four groups of birds: the cuckoos, differs from a zygo- In the second most common rangement of digits – termed and right-footed parrots. Birds when the bird is perching, as it cuckoo roller, parrots and Piciformes (woodpeckers, barbets, honeyguides dactyl arrangement foot type among birds – called heterodactyly – which resembles such as ospreys, owls, mousebirds forces the digits to act in concert. and their allies). Whether it evolved due to some adaptive advantage or in that digits III and zygodactyly – digits II and III zygodactyly except that digits III and some woodpeckers have the Syndactyly is common among through random mutation is unknown. It has recently been suggested IV – not II and III – point forwards and digits I and IV and IV point forwards and I and ability to rotate the outer digit kingfishers, hornbills and bee- that anisodactyly evolved from a state of zygodactyly. point forwards. point backwards. Some perching II backwards. Some advantages (IV) forwards and backwards eaters (Coraciiformes) and there 36 AFRICAN BIRDLIFE SEPTEMBER/OCTOBER 2016 BIRDs’ feet 37 anisodactyl passerine counter- parts (compare bee-eaters, bar- bets and weavers, for example). It is difficult to explain why some aquatic or marine spe- cies are totipalmate and oth- ers have lost the hallux (having only three webbed toes). Or why some kingfishers retained four toes while others down-sized to three. Why is the hallux reduced or lost in many cursorial birds, but the roadrunners, as quintes- sential running ground-birds, IV III II I I II III IV retained the same zygodactyl arrangement that is found in other cuckoos? These questions DAVIDE GAGLIO remain to be answered. IV I I IV and is characterised by all four work by Walter Bock in 1959 sug- The best current understand- PAMPRODACTYL digits being directed forwards, gested that the four perching toe ing is that the different foot types enabling these species to hang configurations seen in modern evolved for perching and have Mousebirds are able their weight on all four toes and birds (anisodactyly, syndactyly, been secondarily repurposed for to hang, supporting even feed upside-down. heterodactyly and zygodactyly) other functions. For example, their entire weight each evolved in response to se- the zygodactyl foot is used for on their feet, thanks rom just this brief look at lection for a strong set of oppos- several different modes of lo- to the pamprodactyl digit orientation we can see able toes for perching rather than comotion (such as running and arrangement of their that foot type varies across for climbing. Interestingly, sev- hopping) and, in general, dif- toes. Fthe avian tree of life. Some early eral types of foot structure have ferent foot types may be equally evolved more than once through suitable for one particular func- convergent evolution; in other tion (perching or grasping). This EVOLUTIONARY TOE-LOSS words, distantly related birds have essentially means that the differ- everal families of birds, including rails, flamingos, evolved similar, but not identical, ent arrangements were a kind of Sgrebes, plovers, sandpipers and their allies, show arrangements of their four toes.