HBW 14 - Family text: Buphagidae (Oxpeckers)
Family Buphagidae (OXPECKERS)
- Medium-sized passerines with heavy, flattened bill; plumage coloration dull brownish and buff, with contrastingly bright eye wattle and bill.
- 20 cm.
- Savanna and farmland with large ungulates.
- 1 genus, 2 species, 3 taxa.
- No species threatened; none extinct since 1600.
The name Buphaginae, as a subfamily within the starling family (Sturnidae), was introduced by the French ornithologist R. Lesson in 1828. This placement of the oxpeckers was followed by G. R. Gray, R. B. Sharpe and A. Reichenow, whereas W. L. Sclater placed the starlings and the oxpeckers in a single family without further comment. Subsequently, D. Amadon noted that the oxpeckers were so aberrant that their membership of the Sturnidae was questionable, and he cited only "the wing structure and other morphological resemblances, the harsh, unpleasant calls, and the habit of nesting in holes of trees" as characters common to the two groups; these features, however, clearly do not constitute strong evidence of a relationship in a phylogenetic sense. Amadon later suggested merely that they were "probably of common ancestry with other starlings", and in 1962, in J. L. Peters's Check-list of Birds of the World, he retained them as a subfamily of the starlings. A couple of decades thereafter, H. E. Wolters, in his treatment of the Sturnidae, placed the two Buphagus species first, followed by the monotypic Asian starling genus Scissirostrum, implying a primitive position within the family, but not in a separate subfamily. The melanin granules in the feathers were found, on microscopic investigation, to be round and solid, typical of the presumed "primitive" condition shared with many starling species, but also with other birds. The karyotype of the Red-billed Oxpecker (Buphagus erythrorhynchus) resembled that of several Sturnus species, but no detailed comparisons were made with members of other bird families. C. G. Sibley and J. E. Ahlquist, in their phylogenetic analyses based on DNA-DNA hybridization, did not include Buphagus among the species that they examined, and Sibley and B. L. Monroe, in their 1990 checklist, placed the oxpeckers closest to the genus Scissirostrum in the tribe Sturnini, evidently influenced by morphological similarities. Some authors, such as P. A. Clancey, have preferred to recognize a separate family, Buphagidae, and this decision, published in Clancey's 1980 checklist of southern African birds, was followed by most southern African authors until the most recent revision of Roberts Birds of Southern Africa, in 2005, which incorporated Buphagus in the Sturnidae. For the rest of Africa, the oxpeckers were generally retained in the family Sturnidae following the checklist for East Africa, by P. L. Britton, and the Afrotropical list of R. J. Dowsett and A. Forbes-Watson, and C. Feare and A. Craig's included the two oxpecker species in their monograph of the starling family, a decision based on a preliminary phylogeny of the African genera that utilized the available morphological and biological characters. Nevertheless, volume VI of the major avifauna The Birds of Africa, published in 2000, accorded the oxpeckers full family rank, as the Buphagidae. No new data were produced in support of any of these decisions. Three independent molecular phylogenies have now placed the oxpeckers as basal to a group which includes the mockingbirds (Mimidae) and the starlings. The consensus view is to assign separate family rank to each of the three groups. A tentative date for the divergence of the Buphagidae, based on a molecular clock, is 22 million years ago, but there are at present no known fossils which could provide independent confirmation of the age of the group. The two extant species are clearly sister-taxa, and hybrids between them have been reported from Zimbabwe in free-living populations in which one species greatly outnumbers the other. As with many other African birds, a plethora of subspecific taxa has been described, the great majority based on minor differences in size and plumage; most of these differences seem not to be biologically informative in terms of defining populations between which there is reduced gene flow. Thus, the common ancestor of the oxpeckers and the starlings would have exhibited some of the morphological traits described above, which have been cited previously as evidence of relationship. In cladistic terms, however, these are shared primitive characters, and thus uninformative in comparison with derived features. In Africa, the savanna habitat has been the centre of evolution for a number of bird families, and also for the ungulates, so that there would have been a long association between the birds and the mammals. Several modern starlings include ectoparasites in their diet, and have been seen to remove ticks (Ixodoidea) from both domestic and wild ungulates. In the case of the Red-winged Starling (Onychognathus morio) and the Pale-winged Starling (Onychognathus nabouroup), a regular grooming association with the klipspringer (Oreotragus oreotragus) has been recorded at several localities in Africa (see pages 000-0 00). Dietary specialists could well have evolved from such opportunistic generalists.
The plumage of oxpeckers is dull, lacking any of the iridescence displayed by the starlings, and there is no sexual dimorphism in coloration. Males of both species are, on average, slightly larger than the females, although considerable overlap in measurements exists. The tail is graduated, with the individual rectrices stiff and pointed, and it is used as a prop to support the bird in the posture of a woodpecker (Picidae) on a tree trunk. Indeed, an observer at a Red-billed Oxpecker nest in a tree-hole reported that, when one young left the nest prematurely and fluttered to the ground below, the adults led it back to the nest by running up the trunk in a manner reminiscent of a woodpecker. The moult is very protracted, the Red-billed Oxpecker taking more than 300 days to replace the primary remiges in South Africa. As a consequence, some overlap between breeding activity and moulting will occur, although, with such a slow rate of moult, this is unlikely to be stressful for the birds. On the evidence of museum specimens, an extended moult period is likely to be typical for all populations of both oxpecker species. Although the two species differ in bill shape, the Yellow-billed Oxpecker (Buphagus africanus) having a flatter and deeper lower mandible than that of its congener, there is no clear evidence that this is associated with different feeding methods. Nestlings of both species have a greenish-yellow bill colour, which changes to dark brown when they fledge, and they have a yellow wattle around the eye, which darkens to dull brown in the immature. In the case of the Red-billed Oxpecker, the eye wattle changes again, to yellow, in the adult, although this is not so with the Yellow-billed Oxpecker. Juveniles younger than 60 days of age still have a yellow bill, while the bill of the young Red-billed Oxpecker becomes dark brown from about 60-120 days. Adult bill colour is acquired at about seven months by the Red-billed Oxpecker, and certainly within the first year of life by the Yellow-billed Oxpecker. Further, juveniles have a dark brown iris, which, in the case of the Red-billed Oxpecker, starts to turn yellow at about four months and changes to yellowish-red by the time the birds are 6-7 months old. The timing of this iris-colour change has not been recorded for the other species, and the morphological basis of the eye coloration is not known. The possible signal value of these changes in eye and bill colours has yet to be studied. J. P. Chapin reported that the eye colour of a captive oxpecker varied, and he speculated that it might be dependent on blood flow, in which case spontaneous changes in the intensity of eye coloration would be possible. P. R. Lowe commented in a footnote that his dissection of the jaw musculature of Buphagus suggested that the latter was a starling in the broad sense, but that the maxillo-palatine and vomer bones in the skull differed sufficiently from those of other starlings to imply that it should be placed in a separate subfamily. W. J. Beecher also examined the jaw muscles of the starlings, and noted that, in the Red-billed Oxpecker, both the protractor of the quadrate and the pterygoid and palatine muscles were enlarged, a development typical of the woodpeckers and apparently associated with the buffering of the brain against the shocks resulting from blows delivered by the bill. In other respects, he found the jaw musculature to be similar to that of the primitive starling condition, as opposed to the derived state found in those starling species that are specialized for probing. Oxpeckers spend most of the day perched on the top or side of large mammals (see General Habits), and the buphagid leg musculature reflects this fact. Studies of the hind-limb musculature of the oxpeckers showed that the basic arrangement of the leg muscles resembled that of true starlings, the only differences affecting muscles which increased the grasping power of the feet. The legs are relatively short compared with those of either perching or ground-dwelling birds of similar body weight. The claws of oxpeckers exhibit the structure and curvature typical of climbing birds such as woodpeckers, treecreepers (Certhiidae) and nuthatches (Sittidae), whereas the Common Starling (Sturnus vulgaris) has the claws of a typical perching bird. In contrast to members of the starling family, the oxpeckers' hind claw is shorter than the claw on the middle toe, the reverse of the pattern found in perching birds. Oxpeckers also have a very fine constricted tip on the claws, which may be an adaptation for penetrating the substrate at the tip while maintaining claw strength along the rest of its length. One collector commented that, if a freshly killed oxpecker was placed on the skin of an ox, the feet and claws immediately grasped the substrate, and it was difficult to disengage them.
Both members of this family are savanna species, being absent from deserts and from closed evergreen forest. Their habitat choice, however, is further constrained by preferences for particular host mammals, and for the main tick species on which they feed. The favoured ticks are limited by humidity, and evidently cannot survive in some open grassland or scrub habitats; these regions would also lack suitable nesting sites for the oxpeckers. In South Africa, C. J. Stutterheim showed that the historical records of the Red-billed Oxpecker coincided closely with the distribution of the two commonest tick species, namely Boophilus decoloratus and Rhipicephalus appendiculatus, recorded in the stomach contents of wild birds, and favoured in feeding trials with two captive individuals. Both of these tick species, however, extended into the winter-rainfall region of the southern coast, whereas the western limit for the Red-billed Oxpecker was at the boundary of the summer-rainfall region. The Yellow-billed Oxpecker, too, feeds extensively on R. appendiculatus, with ticks of the genus Amblyomma apparently its second choice. The ticks are again a good predictor of this oxpecker's distribution in north-eastern South Africa, but this buphagid seems never to have occurred so far south as does its congener. Through much of eastern Africa the two species are extensively sympatric, and there is no obvious separation between them in habitat selection; both have been recorded at up to 3000 m in Kenya, with some indication that Yellow-billed Oxpeckers are more often found above 1000 m and Red-billed Oxpeckers at lower altitudes. For other regions of Africa, data on tick distribution are too incomplete for any correlation with the distribution of the birds to be assessed. Considerable overlap in host choice between the two oxpecker species is evident, and the two can sometimes be seen side by side on the same mammal. There have been no systematic observations of their interactions in this situation, although there is little indication that either of the two buphagid species is influenced in its choice of host animal by the presence of the other species. Under captive conditions, Yellow-billed Oxpeckers were constantly dominant over Red-billed Oxpeckers, although there were relatively few direct confrontations. Some mammal species appear to be avoided. Savanna elephants (Loxodonta africana) do not tolerate oxpeckers and quickly chase them off. A few reports from Zimbabwe of oxpeckers on elephants were during a severe drought, when the elephants were in very poor physical condition and appeared totally indifferent to the presence of the birds. It has been suggested by several observers that elephants are sensitive to the sharp claws of oxpeckers, one ornithologist describing them as being thin-skinned animals with a trunk. On the other hand, through much of western Africa, elephants are commonly seen with Piapiacs (Ptilostomus afer), a corvid having much blunter claws and a different foot structure, perched on them. Bushbucks (Tragelaphus scriptus) and common waterbucks (Kobus ellipsyprimnus) have been seen actively to dislodge oxpeckers which landed on them; the lechwe (Kobus leche) and the puku (Kobus vardonii) are not exploited by the birds, either, nor are southern reedbucks (Redunca arundinum). The impala (Aepyceros melampus) seems to be the only smaller antelope regularly patronized by oxpeckers, whereas there are no reports for any of the duikers (Cephalophinae) being so used. This may be explained by the fact that impalas are found in bushy habitat, which leads to a high load of immature ticks, and live in a herd structure, which provides a number of individual hosts in close proximity. In Zambia, the large-bodied Lichtenstein's hartebeest (Alcelaphus lichtensteinii) seemed to be avoided by oxpeckers, although it was reported as a host for Yellow-billed Oxpeckers in Mali, while the tsessebe, or topi (Damaliscus lunatus), is also utilized much less frequently than would be expected. Many observers have provided lists of the host mammals on which oxpeckers have been sighted. In current national parks these may often be biased by the availability and relative abundance of particular game species, and this may account for some of the apparent regional differences observed. Nevertheless, there is a general consensus concerning the ungulates which are utilized most frequently under natural conditions. These are the African buffalo (Syncerus caffer), white rhinoceros (Ceratotherium simum), black rhinoceros (Diceros bicornis), giraffe (Giraffa camelopardalis), hippopotamus (Hippopotamus amphibius), greater kudu (Tragelaphus strepsiceros), eland (Taurotragus oryx), roan antelope (Hippotragus equinus), sable antelope (Hippotragus niger), Burchell's zebra (Equus burchellii), blue wildebeest (Connochaetes taurinus), impala, and desert warthog (Phacochoerus aethiopicus). Cattle arrived in north Africa at least 8000 years ago, and there were certainly herds of domestic animals north of the equator for thousands of years, although the herdsmen are thought to have moved southwards only some 2500 years ago, reaching the current southern limit of the oxpeckers' distribution about 2000 years before the present. Today, cattle are the primary hosts of oxpeckers in many regions. G. Archer noted that oxpeckers were rare in Somalia not only because of the general absence of wild ungulate hosts, but also because of the widespread replacement of cattle and donkeys by camels (Camelus), which were evidently not favoured by the buphagids. Single-humped domesticated camels, known as dromedaries (Camelus dromedarius), are thought to have reached Africa from Asia only within the last 1000 years. Nevertheless, other observers do report instances of oxpeckers feeding from camels. Horses will usually not tolerate oxpeckers according to some observers, but others have reported having recorded these birds as perching on horses, often feeding at wounds, as well as on donkeys and mules. Oxpeckers occasionally perch on goats or sheep, and sometimes on domestic pigs.
Since oxpeckers spend most of their days perched on the host mammals, relatively few activities take place away from the host. Nevertheless, oxpeckers have been observed to dust-bathe, as well as indulging in conventional bathing in water. The birds will leave their mammalian hosts briefly and fly to water-holes in order to drink or bathe, but more often they are passengers when the mammals go to drink. Sometimes the oxpeckers simply run down the animal's leg to reach the water, and take a few sips without actually "detaching" themselves from the mammal. After bathing, they preen the wet plumage while perched on the host. In addition, captive Red-billed Oxpeckers adopted typical sun-bathing postures while perched on a wall within their enclosure, and they were also photographed while sunning, with the wings and tail spread out, on the back of a rhinoceros. When moving about on the host mammal, oxpeckers generally hop, moving both hind limbs simultaneously, but when stalking flies or during courtship they will also "walk", moving the limbs alternately. They seem invariably to hold the head held up, and they move forwards or sideways and even backwards, but seldom hang suspended underneath the animal. When defecating, oxpeckers lean forward, raise the tail, and generally spray the excrement well away from the host's body. Throughout their range, Red-billed Oxpeckers leave the host animals in the evening and fly off to roost in small groups, or as large flocks from several sites, in trees or reedbeds. These roost-sites may be shared with Lamprotornis starlings, and in some areas even buildings are used for roosting. Similar behaviour has been reported for Yellow-billed Oxpeckers in Nigeria, where the birds roosted in trees, but in Zambia this species was seen to sleep on buffaloes at night, in Zimbabwe observers reported the oxpeckers as sleeping while perched on kudus, elands and sable antelopes, and in Uganda a group was found to be sleeping on a giraffe. There is one report from Zambia of Red-billed Oxpeckers on buffaloes at night. How widespread this behaviour is remains unclear, and it is not known which local conditions may determine the birds' choice of sleeping place. Molecular techniques were employed in order to determine the sex of Red-billed Oxpeckers in Zimbabwe. The results revealed that the sex ratio among regular group-members was balanced, but that the composition of non-breeding social groups was quite fluid over time. Although the overall sex ratio was 52 males to 108 females, this appeared to be an artefact of the restricted sampling area and the apparent greater mobility of females in all age-classes.
Oxpeckers hardly rate a mention as songsters, and the vocalizations which have attracted most attention are the alarm calls given while the oxpeckers are perched on their mammalian hosts, and the flight calls emitted by the birds when startled or on their way to or from roost-sites. These are the diagnostic calls for human observers in the field. W. Neweklowsky, however, described two song types for the Red-billed Oxpecker in the Zurich Zoo, in Switzerland. One consisted of a string of soft calls, interspersed with trills and whistles, which were uttered by both male and female of a pair when they were temporarily separated; and the second type was a series of drawn-out whistling notes used in courtship, and seemingly given by the male alone. Clearly, we are most likely to discover the full repertoire of oxpecker vocalizations from observations of individuals in captivity, where a close approach is possible, and the host animals are also habituated to the presence of humans. Currently, more attention is being paid to the songs produced by female birds, and it is evident that, with many passerine species, the females do sing, often in the same contexts of territorial defence or courtship as those which elicit song from the males. Future studies of oxpecker vocalizations should, therefore, focus on individually marked birds of known sex.
Food and Feeding
The main food item of the Buphagidae is ticks, with a clear preference apparent for particular species and also for certain stages in the ticks' life-cycle. The Red-billed Oxpecker, especially, feeds primarily on the immature stages of ticks. Lice (Anoplura), fly larvae (Diptera) and leeches (Hirudinea) are also removed from the host's body surface, while flying insects such as dipterans, particularly horseflies (Tabanidae) and blackflies (Simuliidae), are caught in the air. As engorged ticks are in essence small bags of blood, the oxpeckers will also feed directly on blood from wounds, and sometimes on other body fluids such as mucus from the nose or eyes, and even on ear wax, which would seem to have little nutritive value. There seem not to be any major differences in food preferences between the two species, except that, on the basis of comparative studies of a small number of captive individuals, Yellow-billed Oxpeckers may catch more biting insects and take larger ticks, such as engorged females of Amblyomma hebraeum, than do Red-billed Oxpeckers. Oxpeckers remove ectoparasites from their mammalian hosts by two different techniques. One of these involves simple pecking and plucking with the tip of the bill, whereas in the other method, known as "scissoring", the bill is laid sideways against the skin and is then opened and closed, as with a pair of scissors. The former approach depends on visual location of the prey, while in the latter technique the prey is detected by touch. The feeding style utilized is correlated with the hair structure of the host, with scissoring not employed on nearly hairless animals, such as rhinoceroses or hippopotamuses, except at wounds or when collecting mucus at the nasal openings. The highest frequency of scissoring is observed when the buphagid is on the longest-haired hosts, such as the kudu and the roan and sable antelopes. The head and ear regions are in many cases the areas where the birds spend the majority of their foraging time, and regular hosts are often most accommodating in allowing what appears to the human observer to be an uncomfortable and invasive process. Studies of the impala's interactions with oxpeckers indicate that the antelope grooms less often when visited by the birds, suggesting that it does benefit from the association. In this case, the oxpeckers clearly focus their attention on areas which the impalas are not able to reach effectively by their own means, and where the highest concentrations of ticks are likely to be found. Two of the common tick prey species, Amblyomma hebraeum and Boophilus decoloratus, have also been recorded as ectoparasites of both adult and nestling Red-billed Oxpeckers. Since these ticks were found much more frequently on the nestlings, it is possible that they represent live food which had escaped after having been brought to the nest. The other ectoparasites noted, two mites (Acarina) and a feather louse (Mallophaga), are specific to the birds in question and would not have been acquired from their mammalian hosts. As mentioned in the preceding paragraphs, oxpeckers often feed at the sites of wounds. This behaviour, when directed at the black rhinoceros, is commonly associated with the skin lesions infested with filariid parasites, which are found in this species but not in the white rhinoceros. The possible role of the oxpeckers in delaying the healing of such wounds or in the transmission of the parasites has yet to be clarified; there is a current research project on this topic. Hippopotamuses frequently have wounds resulting from intraspecific fighting, and these are favoured feeding sites for buphagids. Several observers have reported that the birds, as well as taking blood, will remove fragments of tissue from the wounds. There are observations also of oxpeckers feeding on carrion, including the dressed carcases of animals. Oxpeckers held in captivity are routinely maintained on a diet in which the main component is raw minced meat. Despite the implication that oxpeckers may actively feed on the flesh of their hosts, this may be exceptional under natural conditions. Observations on captive rhinoceroses suggested that abrasions healed despite the attentions of the birds. As a final point of interest, a tame oxpecker fed eagerly on blood from a cut in a human finger, nibbling at the area in order to increase blood flow, but apparently not causing any further damage. During the translocation of Red-billed Oxpeckers in South Africa, the captured birds were initially held in bomas (livestock enclosures), with donkeys as hosts. This led to problems when the birds opened wounds on the donkeys, such that the latter had to be changed on a regular rotational basis. A simple solution proved to be that of feeding the oxpeckers directly with blood, which was collected from a culled animal and treated with an anticoagulant, along with lean minced meat to which vitamin and mineral supplements had been added. Buphagids on this diet often gained weight during the quarantine period before being released at a new locality, and it was found to be unnecessary to enclose a mammalian "host" with them.
At least in the Kruger National Park, in South Africa, the breeding season is closely linked to rainfall, which influences both the grazing activity of the ungulates and the prevalence of ticks. Courtship and copulation take place on the host animal, further illustrating the closeness of the association of these birds with large mammals. In observations of captive birds, the selection of the nest-site appeared to be determined by the male. The two species of oxpecker normally nest in tree holes, although they have been reported as using other sites, including holes in walls, and J. Vincent even found a nest at the base of a cleft in a large boulder. The cavity is lined with dry grass, and often with the addition of hair plucked from the host mammals; in farming areas this can include wool from sheep (Ovis), which the birds seemed to visit for this purpose only. Dung and rootlets may also be added to the interior. Both members of the family lay clutches of two or three eggs, the Red-billed Oxpecker sometimes laying up to five. The latter's eggs have a white to creamy, or occasionally very pale blue or pale pink, ground colour heavily speckled with reddish-brown and lilac-grey, or sometimes with pink and maroon speckles on grey and lavender blotches; they measure 22·5-26·5 × 15·8-18·6 mm. Yellow-billed Oxpeckers' eggs are similar, but the speckling is sometimes less heavy or even lacking altogether, and a small sample had dimensions of 23·4-26·6 × 16·6-18 mm. For both species, the incubation period is approximately 13 days. The nestling period of the Red-billed Oxpecker is 27-30 days, whereas that of its less well-known congener appears to be about 25 days. In captivity, male and female Red-billed Oxpeckers shared incubation duties, and it is likely that this applies to both species under natural conditions. Similarly, the feeding of the young is a joint venture. As with most passerine birds, brood patches develop only on the females. Co-operative breeding is a regular feature of the social organization of oxpeckers, most helpers apparently being older siblings of the nestlings. In one captive group, other, unrelated adults also assisted in the feeding of the young. Helpers sometimes contribute nesting material during the nest-building stage, but their primary role is that of feeding the young, both nestlings and fledglings.
The principal hosts of the oxpeckers do not undertake long-distance migrations, and the birds are not, therefore, obliged to follow migratory herds of game. Red-billed Oxpeckers do make regular flights each night to roost-sites in reedbeds or trees, but colour-marked individuals which were tracked visually in the Kruger National Park, in South Africa, moved less than 10 km from the capture site, and two individuals had circular home ranges calculated at about 27 km² over a nine-month period. This is likely to be typical in areas with dense game populations and permanent water supplies, but where the game undertake significant seasonal movements one could expect that the oxpeckers would follow. There is one record from Zambia of a Red-billed Oxpecker found 64 km from the ringing site after 16 months, and some individuals appeared to have moved up to 50 km from the point of release within a year of their reintroduction to reserves in Zimbabwe. Since Yellow-billed Oxpeckers may sleep while perched on the host animals (see General Habits), they could be passively carried by herds of buffaloes, which will occasionally travel up to 8 km in a day. Despite these indications that oxpeckers are largely sedentary, there are some ringing records which suggest long-distance dispersal or vagrancy. A translocated Red-billed Oxpecker in South Africa returned to the site where it had been captured, 170 km away, and another was found 87 km from the release site. Still in South Africa, prior to the reintroduction of Red-billed Oxpeckers in the Eastern Cape, a single individual was reported from Cape Recife Nature Reserve, near Port Elizabeth, in 1960, and two were sighted on cattle near Kenton-on-sea in 1989. No escapes from captivity had been reported, and the nearest wild populations at that time were more than 1000 km away. There have been no studies of the dispersal of buphagids, nor of any interchange between different groups, but among co-operative breeders such as the oxpeckers the young birds generally leave the natal group in order to attain breeding status. The apparent female-biased sex ratio found in Red-billed Oxpecker groups in a study in Zimbabwe (see General Habits) strongly suggests that females are the dispersing sex, and that, when a breeding female is lost from a group, she is replaced by one of the "floaters" which associate temporarily with different social units. In this study, lone individuals which were resighted after having been ringed, and having had their sex determined (see General Habits), were more likely to be female than to be male.
Relationship with Man
For our hunting forebears, oxpeckers would have been simply a nuisance, since they must often have alerted grazing animals to the approach of human hunters, especially before man had developed weapons which could kill at an appreciable distance. Later, hunters with rifles still found that the birds regularly alerted their quarry to the approach of a human. The nineteenth-century natural-history collector J. A. Wahlberg noted in his journals two occasions on which rhinos escaped his sights after oxpeckers gave the alarm, while on two other rhino hunts the call of an oxpecker first alerted him to the probable presence of the mammals. Wahlberg's contemporary and sometime travelling companion A. Delegorgue wrote of oxpeckers warning buffaloes and elands, as well as rhinoceroses, and commented that, as a hunter, he had cursed the oxpeckers more than he had any other birds. A. R. Maclatchy, a twentieth-century hunter of big game in Gabon, credited the oxpeckers with bringing to his attention the position of a wounded buffalo before the concealed animal charged him, and he considered them a help, rather than a hindrance. He noted also, incidentally, that these birds would return to a wounded buffalo, or even to a freshly killed one. Conflicting views were evident with regard to the nature of the relationship between oxpeckers and domestic livestock. At the start of the twentieth century, T. Ayres, a transport rider in South Africa, stated that the birds dug large holes in the back of transport oxen and fully merited their name of "buphaga", which means "ox-eater". Later, A. Vincent noted that, in his experience, oxpeckers within a herd of cattle were seen most often on the bulls, which were probably dipped less often and therefore carried a heavier tick burden. This would have been long before the days of artificial insemination. Sclater and R. E. Moreau wrote that, in Tanzania, oxpeckers were "credited with performing services of the utmost value in cleaning cattle of ticks, and they have been heartily damned for making, and keeping open, wounds". These authors commented that local people had a generally favourable opinion of the birds, whereas European stock-owners considered them a pest. Moreau examined the stomach contents of 58 Red-billed Oxpeckers from Tanzania, and found 2291 ticks in 55 of the birds; one stomach was empty, and two others contained only Diptera. He concluded that the birds were probably beneficial to healthy cattle exposed to ticks, and suggested that stock in poor physical condition were the most likely to suffer damage. V. D. van Someren came to a similar conclusion on the basis of a questionnaire distributed to European farmers in Kenya after the dipping of cattle had become a regular practice. R. E. Cheesman and Sclater described the Red-billed Oxpecker in Ethiopia as "A bird of evil habits, a mule with a saddle gall has little chance of healing, as these birds keep the wound open daily by pecking the live flesh and drinking the blood, and will pick holes for themselves in the skin of a weak or sick donkey." F. J. Jackson, writing of Red-billed Oxpeckers in Uganda, balanced their positive services to cattle and big game against the damage caused to pack-donkeys and mules "in the old caravan days", and claimed that many donkeys died through the aggravation of sores by the oxpeckers. Once again, the damage was associated with existing injuries and poor condition of the animals. Some 40 years later, however, Y. A. Mengesha stated that oxpeckers in Ethiopia visited animals with sores more often than they did those with ticks, and he observed the birds as they opened wounds on a cow which had no existing skin lesions. According to his informants, many cattle-owners in the region considered the birds to be pests, and took special measures to keep them off the stock. Some traditional cattle-herders still regard the buphagids more favourably in a region with many tick-borne diseases which affected domestic stock prior to the advent of veterinary services. Even in the twenty-first century, in the Mbulu highlands of Tanzania, there was a social prohibition against the harming of oxpeckers, since these birds' important role in reducing the numbers of ticks was familiar to the community. Studies undertaken by P. Weeks in Zimbabwe suggested that the relationship between Red-billed Oxpeckers and cattle in this region was not beneficial to the cattle, since "wound-feeding" by the oxpeckers was rife, and there was no detectable increase in tick loads on cattle from which the birds had been experimentally excluded. He noted also, however, that cattle are not the hosts with which the birds have co-evolved, and that their relationship with wild game may represent a genuine symbiosis. Observations of captive oxpeckers and black rhinoceroses at Zurich Zoo, in Switzerland, demonstrated that the birds did open new wounds on their hosts, and that the rhinos were intolerant of the birds feeding at wounds and regularly attempted to dislodge them. This was an unnatural situation, especially since the captive rhinos were tick-free, but it suggests that field studies of oxpeckers should focus on the frequency of feeding at wounds, and monitor the frequency with which new wounds are created on game animals. Although Reichenow quoted South African observers who reported that oxpeckers on cattle flew up when people approached, and were apparently disconcerted at the animals' failure to react to the birds' alarm calls, both Jackson and Archer noted in eastern Africa, some 30-40 years later, how different the oxpeckers' behaviour was when the birds were exploiting domestic stock. In the latter situation, they always moved swiftly to the other side of the animal, away from the human observer, but did not fly up or give alarm calls. Yet within a few kilometres of the cattle herds, oxpeckers on wild game immediately gave alarm calls when people approached. Do oxpeckers foraging on cattle learn to imitate the mammals' indifference to the presence of herdsmen and, as a consequence, stop responding? Do these birds still alternate between foraging on wild animals and exploiting domestic animals, or are there "specialist" populations which favour one host category above the other? At this stage, we have no clear answers to these questions.
Status and Conservation
In both southern and eastern Africa, the reduction in size of the herds of wild game and, in particular, the displacement of the rhinoceros and buffalo have removed favoured oxpecker hosts. Game control, a euphemism for large-scale attempts to eradicate wild animals from areas selected for stock-farming, was frequently linked to campaigns to eliminate the tsetse fly (Glossina), the insect vector of trypanosome parasites which killed the imported animals but left the indigenous wildlife unaffected. Although domestic cattle are acceptable replacement hosts for the oxpeckers, rinderpest epidemics at the end of the nineteenth century seriously reduced the populations of both cattle and buffaloes. Soon after this, a regular animal-dipping regime was introduced in many farming areas in an effort to reduce stock losses from tick-borne diseases. Not only were tick populations greatly reduced by dipping, but the early arsenical dips were highly toxic to the birds, and this led to the rapid disappearance of oxpeckers from areas under the influence of European colonists. Thus, whereas C. Belcher had reported pre-1920 observations indicating that Yellow-billed Oxpeckers were common on cattle at Chiromo, in Malawi, this buphagid had virtually disappeared from the country when C. W. Benson reviewed the Malawi avifauna, in 1977, and it is now confined to game reserves according to the most recent atlas data. The Red-billed Oxpecker, too, is largely restricted to protected areas with wild ungulates, and in the past 50 years there have been only two reports of this species from Malawi, in both cases on cattle. Commercial farmers in the Makonde district of Zimbabwe noted the return of Red-billed Oxpeckers to the area some 50 years after they had last been reported in the district. This was apparently associated with the cessation of tsetse-fly control programmes, which had involved both elimination of wild game and pesticide-spraying, followed by the re-establishment of game on many properties. When Stutterheim reviewed the historical distribution of oxpeckers in South Africa, he concluded that the Red-billed Oxpecker had disappeared from the southern part of its range in the Eastern Cape province coincidentally with the widespread introduction of cattle-dipping early in the twentieth century, while it survived in the north-east of the country primarily in game reserves or in tribal lands, where cattle were not dipped regularly. The Yellow-billed Oxpecker seems always to have been less common in the region, and was restricted to the north-eastern sector. It was considered extinct in South Africa by 1965, and may have disappeared as a breeding species much earlier than that. In 1979, however, Yellow-billed Oxpeckers reappeared in the Kruger National Park, in the north-east part of South Africa, where there had been no confirmed records of the species since 1896, and juveniles were sighted in 1984. This oxpecker had evidently colonized the area from north of the Limpopo River, which forms the northern boundary of the park, since there were still Yellow-billed Oxpecker populations in southern Zimbabwe. It was suggested that the breakdown in the regular dipping of cattle and in control over the movements of both cattle and game during the later phases of the war in Zimbabwe facilitated the dispersal of these birds through this region. In 2000, the number of Red-billed Oxpeckers in the Kruger National Park was estimated at more than 32,000 individuals, whereas the estimated population of Yellow-billed Oxpeckers in this park was about 500. The latter species clearly remains an uncommon bird there. The first attempts at reintroducing oxpeckers in areas from which they had been extirpated were made in Zimbabwe. In 1962, after heavy tick loads had been noted on newly established wild game in McIlwaine National Park, oxpeckers of both species were captured in Hwange National Park (at that time known as Wankie National Park), and two days later released in McIlwaine. Observers recorded that Burchell's zebras stampeded on the approach of the oxpeckers, and blue wildebeest also refused to allow the birds to settle on them; an eland cow even rolled in attempting to dislodge the oxpeckers. In contrast, a giraffe immediately accepted the birds. Nonetheless, the buphagids failed to establish themselves in this park. Then, in 1975, totals of 47 Yellow-billed and twelve Red-billed Oxpeckers, again having been captured in Hwange, were released in the Matobo National Park (then known as the Rhodes Matopos National Park). This exercise was successful in the case of the Yellow-billed Oxpeckers, but the number of Red-billed Oxpeckers was presumably too small to facilitate the establishing of a viable population. Subsequently, however, Red-billed Oxpeckers were reintroduced successfully at other Zimbabwe localities. Both species of oxpecker have now been reintroduced successfully in South Africa. In 1986, 43 Yellow-billed Oxpeckers from Namibia were transported to the Umfolozi Game Reserve, in KwaZulu-Natal, where breeding in the wild was reported within two years. Red-billed Oxpeckers returned to the Eastern Cape in 1990, with releases made in the Addo National Park, in the Great Fish Reserve, and on a private game farm. Sightings of dark-billed juveniles confirmed that the oxpeckers were breeding successfully, and individuals of both species were also breeding in captivity in holding aviaries. Subsequently, more oxpeckers have been released at these locations, at other protected areas and on farms in this province, and on cattle ranches and reserves elsewhere in the country. Farmers have been encouraged to view oxpeckers as allies in the struggle to control tick burdens on cattle, in conjunction with new chemical agents which are "bird-friendly" and can be used with reduced frequency once the oxpeckers are well established. If this programme is a success, it will offer a much wider distributional range to oxpeckers than merely large game reserves with adequate populations of wild ungulates. Nevertheless, it is clear that the contribution of oxpeckers should not be overemphasized, and they are best seen as one element of an integrated pest-management programme for tick populations. Since oxpeckers are dependent on hollow trees for nesting, but cannot make their own nest-holes, both veld fires and firewood-collecting reduce their nesting opportunities. This may force them to use less suitable sites, those more accessible to predators, and this often results in lower breeding success. Both drought and fire also have a clear impact on tick populations, and these factors were considered responsible for a decline in the population of Yellow-billed Oxpeckers in the Caprivi region of Namibia. Fire is commonly employed as a management tool in protected areas, and it is increasingly being recognized that the timing and consequent intensity of fires are important in determining the maintenance of dead trees, which provide a habitat for many birds, mammals and other organisms.
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