HBW 7 - Family text: Indicatoridae (Honeyguides)

Family text: 

Class AVES
Order PICIFORMES
Family INDICATORIDAE (HONEYGUIDES)

  • Medium-small, rather nondescript arboreal birds with small head, short bill, nostrils often raised, and generally rather drab plumage with white outer-tail markings.
  • 10-20 cm.
  • Sub-Saharan Africa and southern Asia.
  • Forest and woodland, including streamside trees in near-desert; from lowlands to near tree-line in mountains.
  • 4 genera, 17 species, 33 taxa.
  • No species threatened; none extinct since 1600.

Systematics

Despite their superficially passerine-like appearance, the 17 mainly green or olive honeyguides of the family Indicatoridae are members of the order Piciformes, allied with the  other, more typical-looking piciform birds, the barbets (Capitonidae), the toucans (Ramphastidae) and the woodpeckers (Picidae). Their relationships with other groups within the Piciformes are, however, unclear. Various anatomical aspects (see Morphological Aspects) have led some authors to place the honeyguides near the barbets, whereas others have suggested that they are more closely related to the woodpeckers. P. J. K. Burton, for instance, found their structural bases for feeding to be similar to those of barbets. Through DNA-DNA hybridization studies, however, C. G. Sibley and J. E. Ahlquist concluded that the honeyguides are closer to the woodpeckers than they are to other piciforms. Nevertheless, their displays, including aerial displays, along with other aspects of their behaviour, and their vocalizations seem more like those of barbets than those of woodpeckers.

Perhaps the major point is that the Indicatoridae are distinctive, and not particularly close to one or another of the piciform families. Many of the species are poorly known, inconspicuous birds of tropical forest. The Dwarf Honeyguide (Indicator pumilio) was described in 1958, and the Yellow-footed Honeyguide (Melignomon eisentrauti) as recently as 1981, and the biology of both remains largely unknown. The mysterious Lyre-tailed Honeyguide (Melichneutes robustus), famed for sounds produced in its aerial display, indeed is known from some countries and large regions of Central Africa only thanks to those very sounds. Most of what is known about honeyguides comes from investigations of five or six species, and even for those the information is incomplete. There are few fossils of honeyguides, dating back only to the Pliocene of South Africa.

The Indicatoridae can be divided into two subfamilies, perhaps better thought of as tribes. These are the thin-billed Prodotiscinae, with three species of Prodotiscus and two species of Melignomon, and the heavier-billed, typical honeyguides of the subfamily Indicatorinae, comprised of the Lyre-tailed Honeyguide in Melichneutes and the closely related genus Indicator with its eleven species. So far as is known, all are nest parasites, using as hosts other Piciformes, other cavity-nesters, and several avian species that build deep or covered nests. All but one of those honeyguides for which the eggs are described lay white eggs. The exception is the Eastern Green-backed Honeyguide (Prodotiscus zambesiae), which lays either white or blue eggs, the latter matching those of one host group, the white-eyes (Zosterops). Both that species and the Western Green-backed Honeyguide (Prodotiscus insignis) also have a fully white outer tail; all other honeyguides have a variable amount of dark tipping of the outer tail feathers, less prominently so in juveniles, which show more white in the tail than do adults. The Prodotiscinae have a gizzard with thicker walls than that of the Indicatorinae, and the skeletal sternum is more deeply notched. The small species of Prodotiscus have more rounded nostrils, softer feathers, thinner skin, and a deeper keel of the sternum than do other honeyguides, as well as only ten tail feathers, and a white patch on the border of the flanks and rump, these feathers being erectile. Melignomon tends towards the Indicatorinae in its thicker skin, its rougher feathering, and the fact that it possesses twelve rectrices, long slit nostrils, and a less deep sternal keel; the two species may take some honeybee (Apis) wax, as well as deriving wax from insect coverings (see Food and Feeding).

It is likely that the Indicatorinae depend upon beeswax in their diet, at least during part of the year. The nostrils are raised with membranous sides on a stouter, broader bill, and the gizzard is thin-walled. Three species of Indicator are sexually dimorphic in plumage, and two others of the eleven species are sexually dimorphic in the colour of the gape. These include some of the best-known members of the family, such as the Greater Honeyguide (Indicator indicator), which leads humans to bees' nests (see General Habits). Males of these species sing in trills, series of double notes, or series of melodic phrases. Hosts of Indicator honeyguides are mainly piciform birds such as barbets and woodpeckers, but the Greater Honeyguide util­izes 40 or more hosts of a diverse range of species. The genus Melichneutes, closely related to Indicator, contains only the Lyre-tailed Honeyguide, notable for its highly modified tail: the central two tail feathers curve outwards, the long central undertail-coverts project between these lyre-shaped feathers, and the four outer pairs of rectrices are short and spiky, all these features being apparently related to the species’ circling, diving flight display. Lyre-tailed Honeyguides are flat-bodied, with a deeper sternum and a barely thicker gizzard than the other honeyguides.

Most honeyguides are Afrotropical, but two species of ­Indicator, the Yellow-rumped Honeyguide (Indicator xan­thonotus) and the Sunda Honeyguide (Indicator archi­pelagicus), occur in tropical Asia, the former along the southern Himalayas, and the latter in the Malay Peninsula, Sumatra and Borneo. It is reaso­nable to assume that their ancestor reached Asia from Africa, and that the two species then diverged from one another. They do not meet, and, reflecting the absence of other honeyguides in their ranges, the white in the outer tail is muted. Both show a feature otherwise shared only with the African Greater Honeyguide, namely the presence of  bright yellow in the plumage: the rump patch in the case of the Yellow-rumped Honeyguide, and the “ shoulder” of the male Sunda Honeyguide.

Assuming that the thick, tough skin, the upraised nostrils, and the guiding behaviour are derived features, it follows that the ancestral honeyguide was a small, barbet-like bird similar to species of Prodotiscus, but perhaps with a heavier bill, for excavating nesting cavities. Alternatively, the nest parasitism may have evolved very early in the family, with no recent ancestor a nest-excavator. In relation to the honeyguides’ wax “predation” and the co-evolution of honeybees and honey­guides, it is significant that beeswax utilization by African honeyguides involves only one bee species of the genus Apis, namely A. mellifera; and, according to L. Garnery and colleagues, that species’ ancestor probably entered Africa from the Middle East not much more than one million years ago. The thick skin and the nostril modifications of most honeyguides are not required for any purpose other than protection against the honeybee. The implication is that Melignomon, Indicator and Melichneutes evolved relatively recently. Wax can be obtained from colonies of sweatbees (Trigona), which are incapable of stinging, but such nests are less accessible to honeyguides than are those of the frequently absconding honeybee; Trigona nests are often in the ground, their entrances are small, and the wax may be deep inside. Thus, there are intriguing questions and puzzles regarding the evolution of the honeyguides.

Morphological Aspects

The Indicatoridae are difficult to characterize in terms of their morphology. Their characteristics become apparent only upon close observation, as the birds investigate honeybee nests, or flash the dark-tipped white outer tail in chases of or pursuits by their hosts, with which they interact frequently (see General Habits, Breeding). All honeyguides seek wax as a major food, either from the waxy covering of insects such as scale insects (Coccidae), or from the wax structures of honeybees' nests. Species favouring beeswax have a thickened skin, presumably as some protection from bee stings, although attacks by honeybee swarms are at times fatal to the honeyguides. Enzymes capable of digesting the wax seem well to be developed in the Indicatoridae, and A. R. Place and others have found similar protein substances in seabirds and various landbirds; such enzymes have so far not been found in other piciform birds.

As with many of the barbets, at least some of the species of Indicator have a finely fringed or brushy tongue that may be bifid, and rictal and chin bristles are present, even if short. The stronger-billed honeyguides have a notch along the sides of the bill tomia, a trait exhibited among allies only by the barbets. Hypotarsal scuted “heels” are well developed in the naked, blind young honeyguides, as are the membranous bill hooks with which they kill any of the host’s young, or destroy its eggs. There are other internal morphological attributes involving the oil-gland, muscle ligaments and the skeleton. Honeyguides have a smaller head in relation to the body when compared with the large-headed barbets, toucans and woodpeckers, which also have a larger, more specialized bill.

Rather long, narrow wings give power to the thrust of the honeyguide’s body in flight, and permit an array of flight di­splays. These nest parasites rather readily evade their hosts, and are able to outfly them in most instances. The female honeyguide may soon tire the hosts, enabling her to gain access to their nest to lay an egg. The wings have nine functional primaries and a small tenth primary, which is vestigial or absent in species of Prodotiscus. All genera except Prodotiscus have six pairs of rectrices, as do the woodpeckers; Prodotiscus has five pairs, as do the barbets and toucans. The outermost tail feather is mildly to considerably reduced in the larger honeyguides.

The thick skin of most honeyguides is likely to have evolved in response to bee stings. In addition, however, it preadapts the birds, affording them added protection, in confrontations with hosts, as well as in conflicts with other honeyguides at wax sources. Despite the protection provided by this thick skin, honeyguides are not immune to bee stings. An excessively bold action around a bees' nest can precipitate an attack by the venomous insects; bodies of honeyguides have been found with up to 300 or more stings, particularly about the eyes, around the base of the bill, on the legs, and indeed all over the body.

The bill is rather generalized, and is suitable for fly-catching forays, for probing in the bark of trees, and for pulling away pieces of beeswax. The rictal and chin bristles may prevent deb­ris from insect parts and sticky wax from contaminating the fea­thers of the head. The legs of honeyguides differ in length from species to species, and are used by the birds in somewhat diffe­rent ways while feeding on beeswax. The Scaly-throated Honeyguide (Indicator variegatus) crouches over wax that is of large bulk, perching and pulling; it often holds a larger piece of wax between its legs, toes clamped about the front end, with the body touching the wax. Greater Honeyguides have longer, less feathered legs; they peck from side to side in a generally upright posture, not crouching. Lesser Honeyguides (Indicator minor) sometimes crouch, but they do not generally clasp the wax. The more or less notched bill of adults of these species may help in freeing wax, as well as in aggressive “biting”. The Greater and Scaly-throated Honeyguides, when under pressure from numbers of others at a wax source, often pick off a piece of the material and fly with it to a secluded spot; they are often chased by others, but can lift and fly with pieces as heavy as 14 g. Lesser Honeyguides and Pallid Honeyguides (Indicator meliphilus) rarely fly with large pieces of wax, but they do at times carry away a tiny fragment.

K. E. Stager demonstrated that the olfactory lobe of the brain is well developed in the Indicatoridae. Although olfaction may play some role in the locating of beeswax or bees' nests, it is not thought to be of great importance. Field experience indicates that bee colonies are generally known to the honeyguides of the area in question. These birds’ eyesight is keen, as is their hearing; indeed, they may be able to track individual honeybees to a nest. Moreover, most honeybees' nests are located in situations previously occupied by honeybees, and hence they are regularly checked by the honeyguides, which also monitor humans and their activities. It is possible, however, that olfaction assists the birds in locating bees' nests in heavily forested areas.

The distinctive outer-tail markings of honeyguides are rather uniform among the Afrotropical species. Observations suggest that this pattern, or “flag”, is a useful cue for immature honeyguides, allowing them to “tag along” after an adult, of either their own or another species, to sources of wax. Further, in all species except those of the genus Prodotiscus, the tail of immatures is much whiter, less dark-tipped, than that of adults. This rather constant diffe­rence in the tail pattern between adults and immatures seems to be part of the signalling system that allows immatures dominance at food sources (see General Habits).

The bare area around the eye is smaller than the corresponding naked orbital area shown by the barbets and the toucans. The orbital skin is thick and heavy, and not likely to be of much signal importance, except that immatures have a brighter, lighter orbital area than do adults. In immature Greater Honeyguides the orbital skin is blue, this colour extending on to the crown beneath the feathers; it is yellow in young Scaly-throated Honeyguides, and pale grey in young Lesser Honeyguides. Adults of the last species appear bigger-eyed than immatures, because the orbital area is black and is seen as part of the eye by an observer; the immature shows a small-looking dark eye, the surrounding skin being pale grey and contrasting with the eye colour.

In immatures of the Scaly-throated Honeyguide, as well as those of the Spotted Honeyguide (Indicator maculatus), the gape, which is used in aggression, with bill held wide open, is fully pink. In adult males it is shiny black, whereas females have a pink gape that gradually gathers grey shadow marks with age. With the striking gape colour, along with plumage markings of the crown and throat, and the colour of the orbital skin, the young of these species are dominant at food sources. The immature Greater Honeyguide has a unique yellow-gold, cream and olive-brown plumage quite different from that of adults, and indeed unlike that of any other honeyguide. These immatures instantly become “superdominant” when arriving at a bees' nest, where an individual may feed for 20-30 minutes (see General Habits). When two or more immatures appear together at a food source, the older, less juvenile bird gives way to the other or others.

Apart from those species with a wholly distinct immature plumage, such as the Greater Honeyguide, there are others with markings that are more or less indicative of immaturity, such as the Scaly-throated and Spotted Honeyguides with their barred juveniles. Otherwise, the immature plumage can be distinguished in general terms by the whiter outer tail feathers, the colour of the orbital skin, and several other features, including the more pointed tail feathers; the overall colour is often darker and greener than that of adults, and the facial and other markings are muted. For example, the loral area of the Lesser Honeyguide is white in adults, but grey in immatures, and the malar stripe is less marked in young Least (Indicator exilis), Dwarf, Lesser and Thick-billed Honeyguides (Indicator conirostris) than it is in adults of those species. Recently fledged young honeyguides have creased, wrinkled belly skin, and the hypotarsal “heel” with spiky projections may still be evident. Remnants of the gape “wattle” at the corner juncture of the upper and lower mandibles are visible on juveniles for a period of several months after they leave the nest.

Habitat

Honeyguides are predominantly forest and woodland species of the tropics of Africa and Asia. Always bound by their need for suitable hosts, they range into montane woodland, and to the fringes of temperate woods in parts of South Africa, on high African mountains, and along the Himalayas, where Yellow-rumped Honeyguides occasionally reach the timber-line. The Greater and Lesser Honeyguides, the most broadly distributed members of the family, extend into dry woodland, and into wooded Sahelian grassland, while Scaly-throated Honeyguides occupy dense streamside thickets in near-desert areas of southern Somalia. Although Lesser Honeyguides, in particular, have invaded dry regions as their host barbets, mainly the Acacia Pied Barbet (Tricholaema leucomelas), have extended their ranges, barbets nevertheless occur in some arid bushland parts of Namibia, Somalia and the northern Sahel beyond the range of any honeyguide.

The planting of trees by humans is an important aspect of the dynamics of honeyguide populations. Fruiting trees are especially attractive to barbets, which are major hosts of honeyguides. In the Sahel, such trees may favour honeyguide hosts and, in consequence, the honeyguides themselves, perhaps offering a significant argument against the elimination of trees in man’s never-ending quest for fuelwood. Forest clearance has benefited honeyguides of more open country, especially in West Africa, where forest species are experiencing drastic loss of habitat. In the case of the rather strictly forest-dwelling Thick-billed Honeyguide and its very close relative, the adaptable Lesser Honeyguide of open wooded habitats and edges, the latter is expanding its range throughout formerly forested, recently cleared areas, leading to its replacement of the Thick-billed.

Beeswax can be regarded as a primary source of food for most honeyguides. Afrotropical western honeybees, the source of the “Africanized”, so-called “killer” bees in the Americas, abscond from nests frequently, and more often use holes with larger entrances than do European races of the species; they also migrate under certain conditions. Wax may thus become accessible directly to the honeyguides if the entrances to nests are sufficiently large. In dry regions of Africa, the honeybees sometimes migrate when conditions are severely dry; where bees' nests are in rocks or otherwise in the ground they may be inaccessible, and once bees are gone from such an area, and honey is therefore unavailable, human honey-hunting activities may cease, rendering the habitat marginal even for Greater and Lesser Honeyguides. As a result, very dry zones occupied by some xeric-adapted barbets, such as the Black-throated (Tricholaema melanocephala), Acacia Pied and Yellow-breasted Barbets (Trachy­phonus margaritatus), can, at least seasonally, be devoid of honeyguides. The importance of this critical wax resource is such that its absence, or its inaccessibility, can render the habitat unsuitable for honeyguides. Under less severely arid conditions, that is, for most honeyguides in most places, insects are usually available as food, and the honeybees’ activities do not force large-scale movements of the honeyguides, but they may influence the local concentrations of honeyguides and their foraging habits.

So far as is known, bearing in mind that information on fully half the species of Indicatoridae is very scant, the honeyguides exhibit their ancestral tree-cavity dependence by using hosts that are cavity-nesters. These nests can be in the ground, or in termite mounds, or carton-ant nests, if not in a tree. Since honeybees principally use tree cavities for their nests, this enforces a cavity relationship of honeyguides: most honeyguides seek beeswax, and insect prey as well, in cavities. Females, employing cavity-nesting birds as hosts, must search for and gain entrance to these cavities to lay their eggs. In a real sense, then, and unlike most barbets and woodpeckers but like almost all toucans, the honeyguides are secondary users of nest-cavities. They gain the advantage of primary cavity-nesters, including a clean nesting substrate and fewer parasites, by utilizing primary ­cavity-nesters as hosts. The presence of trees suitable for nest-excavation, usually partly rotten, decayed trees or stubs, is therefore essential for the honeyguides, as well as for their hosts.

General Habits

Tough and aggressive, if inconspicuous birds, the honeyguides do not take kindly to aggression by other birds of less than large size. This perhaps reflects their thick, tough skin, but only to a degree, as all their piciform relatives are, after all, also aggressive. Faster than their hosts, which naturally react aggressively to the parasites’ close approach to their nests, they are often chased by host birds; before the chase ceases, however, the honeyguides are seen to be chasing the host. At least the Lesser Honeyguide, during interactions with barbet hosts engaging in duets and group pre-duet choruses, such as the Black-collared Barbet (Lybius torquatus), seems to utilize its speed in following and, indeed, coming to a perch with the calling group; this causes a breakdown in the normal chorus-duetting, and possibly disrupts breeding, even resulting in renesting and thus allowing another chance for parasitism by the honeyguides.

Their aggression is vital in the gatherings of honeyguides that congregate about any beeswax source. Over 50 honeyguides of four species have been attracted to beeswax feeders in one day, with as many as 37 of them netted in that period. At a source of wax, there are more or less strongly fixed dominance hierarchies within any species. Usually immatures are dominant, followed by females, and then adult males. Of course, the relative hunger of various individuals results in some reversals. More complex are the interspecific hierarchies. In observations in Kenya, Scaly-throated Honeyguides have usually been found to be dominant over the two or three accompanying species, namely the Greater and Lesser Honeyguides and, at times, the Pallid Honeyguide. The very distinctly plumaged immature Greater Honeyguide, however, is superdominant, readily driving off all other honeyguides. Although much smaller, immature Lesser Honeyguides are able on occasion to chase Scaly-throated and some adult Greater Honeyguides from the beeswax. As is often the case in the avian world, very aggressive, dominant honeyguides may become so occupied in attacking and chasing one another that lower-ranking species and individuals in the hierarchy may obtain the opportunity to eat some wax. Another tactic adopted by the Greater and Scaly-throated Honeyguides is to make off with a piece of wax, and to find a quiet nook where they can eat undisturbed. More often than not, however, the honeyguide carrying wax is chased in flight, and, being awkward and ungainly, is forced to drop the material, which may then become the focus of a squabble.

Although the habit of leading humans and other mammals to bees' nests is responsible for the name “honeyguide”, it is believed that only the Greater Honeyguide actually “guides”, and apparently guides only humans, to nests. In more than 15 years of close work with hundreds of Scaly-throated and Lesser Honeyguides, no instance has ever been found involving behaviour by those two species that could be associated with guiding. That is not to say that they, and others, including various forest honeyguides, do not attend humans; they do. Any humans making noise, as when cutting wood or building fires, act as attractants to honeyguides. The birds follow people engaged in such tasks, often approaching them closely, and even fly to tents and vehicles, which they may inspect. Their attention is often overlooked by the humans. Scaly-throated and Greater Honeyguides have a “search-flight”, an unduly slow, very undulating, up-and-down, somewhat circular flight over people and their disturb­ances. Those species, and others, follow one another as well; when wax is found, an avian “bush telegraph” seems to draw in numbers of honeyguides. It is extremely probable that at least adult honeyguides in a given area know the location of many bee colonies. Why should they not? The bees frequently abscond, and nests are used over and over again by bee swarms for so long as the cavities remain usable.

The guiding Greater Honeyguides, the bulk of which are immatures and females, perch, not necessarily conspicuously, in the vicinity of a human being, and call repeatedly (see Voice). If no attention is paid to the bird, it may call off and on, cease after several calls, or continue for up to an hour; one individual called at intervals to the observers, as they moved about a small area, paying no heed to it, for a period of some three hours. If one follows the honeyguide for a short distance and then stops, the bird may call very frequently, move to several different perches, and may then change its direction (see also Relationship with Man). By knowing the location of bees' nests in an area, a person can readily guess to which occupied nest he or she is being guided. In one instance, a female led the observers to four separate nests in less than one hour. No special displays are associated with guiding; the repetitive, insistent calling and the frequent moves, rendered conspicuous by the spread tail and bounding, upward flight to a perch, are seen also in other contexts. Experience shows that, in the vicinity of the bees' nest, the Greater Honeyguide is silent and looks on at the humans. Honey-hunters would then build a smoky fire, and climb to the nest; traditionally, they leave a large chunk of honeycomb for the guider, but it is the opening of the nest and the moving away of the honeybees that reward the individual guider and other attentive honeyguides attracted by the activities.

Guiding is not a predictable activity. In months of working with and among honeyguides, handling Greater Honeyguides almost daily, one of the two researchers would be guided on one day, perhaps several times; several days or a week would then pass with no guiding. A more common feature was incipient guiding, whereby more or less guiding calls were uttered, but not persis­tently, and for only a short time before ceasing. Indeed, some immature, would-be guiders appeared not to know the mode, as they would not lead an observer away, but only called, apparently at the two people, and then disappeared. This long-term study found that encounters with “ investigating” Scaly-throated Honeyguides were more frequent than were incidents of guiding by Greater Honeyguides. The Scaly-throated Honeyguides flew, usually inconspicuously, over the observers, perched nearby, watched, came to the fire, and perched on the vehicle or went inside it; the birds were regularly netted by stringing a net beside the fire, the fire being a device for keeping away large mammals, as well as for boiling water for morning beverages. The disappearance of the guiding phenomenon of Greater Honeyguides in suburbs of metropolitan centres such as Nairobi, in Kenya, suggests that guiding is not a genetically deeply embedded, very highly evolved aspect of behaviour, but that it is, rather, a relatively recent “add-on” to the wax-seeking and wax-acquiring habits of this species.

Wax-eating requires water, and readily available water is a feature at most of the study sites at which there is a great deal of honeyguide activity. Those individuals seen regularly for much of a morning, and feeding frequently, appear to drink every hour or so. Most, however, show no interest in bathing, even when observing the bathing activities of other avian species.

While non-social generally, honeyguides usually come into frequent contact with others of their own species or with other species of Indicatoridae. Any beeswax source attracts small to large numbers of honeyguides, and aggressive interactions are commonplace. Away from these sites, and otherwise except when breeding, honeyguides are solitary birds. Immatures will at times approach adults without aggression, and will even perch above an active feeding site without entering into interactions. Fledglings may beg from adult conspecifics, as well as from their foster-parents or any bird resembling the fosterers. Comfort activities, especially preening of the wings and tail, are important, and are performed in the same way as in other piciforms.

Of the comparatively few displays described for the Indicatoridae, that of the Lyre-tailed Honeyguide is by far the most interesting. This species, rather than singing from a perch, employs a fantastic aerial display. After giving several introductory “pee” notes, it goes into a steep, fast dive with the modified tail feathers spread. It is presumably the air passing through these feathers that produces the “kwa-ba, kwa-ba” series of sounds that are so characteristic of the forest areas inhabited by the Lyre-tailed Honeyguide. Lest this be considered overly distinctive within the family, far less spectacular aerial displays, with sound at considerably lower volume, are known for the Greater, Lesser, Scaly-throated and Pallid Honeyguides; and the three Prodotiscus species also have aerial displays during which they call, in at least two cases over their territories. The male Greater Honeyguide, either on or off the singing territory, sometimes performs a “winnowing” display-flight in which it flutters in one or more circles over a female, making wing sounds; occasionally, it mistakes an older immature of either sex for a female.

Little is known of the roosting behaviour of honeyguides. Radio-telemetry studies of male Scaly-throated Honeyguides have shown that the birds do not roost in cavities, but instead use dense trees and bushes. Territorial males may roost in one of their song trees, a dangerous ploy, perhaps, for at least one such male was killed, probably by a Verreaux’s Eagle-owl (Bubo lacteus), in his main song tree. Most males roost within their territory or close by, although not always at the same site every night. One singer regularly roosted 5 km downstream from its singing territory. Subordinate males around a territory are more mobile. They may roost near a particular territory on one night, several kilometres away from it on the next night, and in yet another direction on the following night. At one major wax-feeding site which was not within or even near any territory, feeding birds left the area one hour or, less often, as little as half an hour before dark, presumably to reach a favourite roosting site.

Forest honeyguides fly directly or in undulating flight, and usually not very far, although they may move about rather constantly throughout the day. They do not cross large open areas. Even woodland and thicket species, such as the Scaly-throated Honeyguide, prefer to stay within or near cover, using streamside vegetation through which to move from one site to another. On the other hand, Greater, Lesser and Eastern Green-backed Honeyguides do at times fly over open areas even as wide as a kilometre or more, often undulating their flight in the manner of some barbets and woodpeckers; through even wider areas of grassland, they may perch briefly in a shrub, herb or bush, before continuing across the opening.

Voice

Songs are known for all but one of the well-studied honeyguides, the exception being the Yellow-rumped, which appears to lack a song. The songs are often musical, unlike any woodpecker vocalizations, and are delivered in barbet-like postures that include arching of the neck, bill pointing downwards, rump fea­thers loosely fluffed, and tail twitching slightly with the notes. In the Scaly-throated and Spotted Honeyguides, a simple, fast trill for several seconds constitutes the song. The Lesser, Thick-billed and Least Honeyguides emit a “wew” introductory note, followed by a trill that is slower than in the previous two species, while the Sunda Honeyguide sings a fast trilled song preceded by a cat-like, rising “miaaw” note. The Greater Honeyguide begins its song with a bow and a soft “peew”, followed by a varied number of double notes transcribed as “Victor” or, rather, “TOR-VIK”, or “Burr-wit”; this is the only honeyguide species in which the female is known occasionally to utter, aggressively, the same song as that of the male.

Among the smaller species of Indicator, Willcocks’s (Indicator willcocksi) and Pallid Honeyguides sing similar songs of repetitive, triple-noted phrases, the former sounding like “ wa-will-it”, and the Pallid “wa-wee-it”. Apart from the Brown-backed Honeyguide (Prodotiscus regulus), which sings a soft trill, the rest of the small honeyguides are poorly known. The songs of the Western Green-backed, Yellow-footed and Dwarf Honeyguides are unknown. The Eastern Green-backed sings, but its song has not been described, while recent recordings of Zenker’s Honeyguide (Melignomon zenkeri) reveal its song to be a long series of slow “psee” to “pseep” notes.

There remains the Lyre-tailed Honeyguide, which, instead of a song delivered from a perch, uses an aerial display with introductory “pee” notes followed by “kwa-ba, kwa-ba” sounds (see General Habits). The latter are presumably produced by the tail feathers, and are characteristic sounds of the forest areas where this poorly known honeyguide lives.

Honeyguides have a broad repertoire of vocalizations other than song. Some have an aggressive, song-like trill or squeaks, or piping notes. The Scaly-throated Honeyguide, as an example of a reasonably well-studied indicatorid, has a variety of such sounds: a piping, whistled “ wee” series uttered aggressively by males; a song-like trill but with “pyew” sounds in it, also given by males; loud chattery calls given repeatedly by females in aggression; buzzy skizz notes; a post-copulatory wavering whistled series or a floppy aerial display with “wup, wup” sounds; and three distinct calls of the young, namely chatters, yelps and wails. Loud rustling wing sounds accompany aggressive calling and chasing by this species. It is likely that the other honeyguides have a more or less equivalent repertoire of calls, and the Lesser, Greater and Pallid certainly do.

Immature Greater Honeyguides utter an aggressive “feeeer” that drives away other honeyguides in a feeding situation, this becoming an ear-splitting “pseeeeaar” from trapped birds held in the hand. In aggression, adults and older immatures of this species utter peeping to piping and chattering series of notes, often wavering in pitch, and resembling the begging calls of young Greater Honeyguides.

Similar calls to the last are also used as guiding calls. These consist of a chatter made up of “tya” notes compounded with peeps or pipes, thus double-noted, and varying in pitch. No calls have been heard from guiding Greater Honeyguides that differ from variations of the calls just described, which are emitted also by aggressively interacting, chasing Greater Honeyguides.

Food and Feeding

Beeswax, chiefly the wax of honeybees of the genus Apis, forms the major element of the diet of most honeyguides. Noteworthy among other foods are scale insects (Coccidae), which essentially replace beeswax in the diets of the slender-billed species of the genus Prodotiscus. They are also important to Zenker’s Honeyguide and, probably, to the Yellow-footed Honeyguide. All honeyguides are known to eat insects and spiders. Other than scale insects, insects are represented in the diet by honeybee eggs and larvae but few adults, aculeate Hymenoptera, sweatbees, and caterpillars, including waxworms and eggs of Galleria that infest beeswax, along with beetles, termites, flies, mayflies, winged and wingless ants, aphids, homopterans, hemipterans and orthopterans. Diverse spiders include those of the Thomisidae and Oxyopidae. Plant fibres and some fruits, including figs (Ficus), are eaten. Honeyguides are occasionally noted as taking bird eggs and nestlings, but this must be rare; they are not mobbed by other birds. Since their young are raised at least to the fledging stage by diverse host species, they eat the foods of the hosts, generally insects and fruits.

Those species using beeswax secure it wherever it is accessible and not defended vigorously by honeybees, the stings of which, in numbers, readily kill a honeyguide, despite its thickened skin. In Africa, the entrances to most bees' nests are accessible to honeyguides, especially of the smaller species. When the cavity is full to its entrance with comb, the comb may be eaten by honeyguides in the cool hours of morning, before honeybees become active. For most honeyguides, in most areas, it is the recently vacated nests that yield the resource to the birds, which squeeze in, and work over the walls of the nest and its ceiling, scraping off bits of left-over comb. The stubby bill of species of Indicator smaller than the Greater and Scaly-throated Honeyguides may in fact be adapted to enable them to carry out such scraping more efficiently. The Yellow-rumped Honeyguide may be forced to scrape left-over bee comb from cliff faces after giant or rock honeybees (Apis dorsata or A. laboriosa) have moved off to a new site for their open colony.

All the species of honeyguide that are moderately to well known indulge in fly-catching, in which they sally from perches after insects or spiders. Small honeyguides, such as the Pallid and the two green-backed species, hover when fly-catching, at times in front of flowers such as those of Erythrina, Rubus and Gymnosporia. Other insects are obtained by gleaning from the bark of tree branches and foliage, and larger honeyguides sometimes work over tree trunks. Greater Honeyguides will also on occasion follow a woodpecker, snapping up insects flushed by the creeping picid. Most honeyguides, but especially those of the genera Prodotiscus and Melignomon, will at times join mixed-species foraging flocks of insectivorous birds. When alate termites swarm, all honeyguides abandon other foraging activities and sally for these insects. So far as is known, there are no reports of honeyguides foraging for, and eating, fruits, but stomach contents of adult specimens of, for example, the Eastern Green-backed and Lyre-tailed Honeyguides have been found to include fruits such as figs and mistletoe (Loranthus) berries.

Newly fledged honeyguides almost immediately commence gleaning on branches and inspecting crevices in search of food, even as they beg from their foster-parents. They follow the honeyguide “ signals”, the white marks on the spread outer tail, to wax sources, tagging after adults and older immatures. In very rare instances, a begging fledgling has been fed by an adult of its own species, the reported cases involving young Western Green-backed and Yellow-rumped Honeyguides.

Breeding

All honeyguide species that are sufficiently well known are brood parasites, and it is thought likely that the others also will prove to be so. Information relating to hosts, especially, is lacking for both species of Melignomon, for both Asian honeyguides, and for the little Dwarf and Willcocks’s Honeyguides. Meagre, suggestive information regarding hosts is known for the Least, Thick-billed, Spotted and Lyre-tailed Honeyguides. Most of the available data on nest parasitism among the Indicatoridae refer to the Eastern Green-backed, Brown-backed, Lesser, Scaly-throated and Greater Honeyguides.

Breeding seasonality is clear-cut in the near-temperate Yellow-rumped Honeyguide, and in populations of Greater, Lesser and Scaly-throated Honeyguides at corresponding latitudes, all of which breed in the hemispherically equivalent spring and summer. Elsewhere, in the tropics, seasonality is far less evident. Of course, the breeding seasons of the honeyguides are attuned to those of their hosts. In addition, rainfall is a critical factor in breeding seasonality. In forests which experience an extended wet season, or where it is more or less wet all year, some individuals may have a protracted breeding period, while others may breed at one particular time of year, and others at other times; in unusually wet years, with rainfall extending into all months in woodland that is normally dry and wet seasonally, the honeyguides may follow the same regime. Conversely, when prolonged drought occurs, honeyguides may cease breeding activity for the year.

Most male honeyguides of the better-known species maintain a singing territory, a term considered preferable to “songpost” or “studpost”, used chiefly in southern Africa. Territorial male Scaly-throated Honeyguides regularly sing from one of several trees or bushes, using certain sites and certain perches at each site. Particular sites, or trees, are sometimes used for long periods, even years, but much more often the birds shift their sites, and use different trees, so that the territory may, over time, change in shape and size. Singing territories of different males are usually not adjacent; when they are, one bird is gradually forced out. Singing male Scaly-throated Honeyguides on prime territories are usually three or more years old. Territories attract other, subordinate and younger males, some of which are transient, whereas others may be more persistent. A territory can attract up to eight or nine males at a time. The dominant, territorial male sings for long periods, and stays within his territory most of the time, thus monitoring other males and seeking mates. If he leaves the territory, a secondary male may sing tentatively, and then gradually move to occupy a singing site; such males sometimes copulate with a visiting female. Males securing a territory can hold it for as long as seven years, but most are able to do so for only one or two years. Some territories are “traditional”, with examples from South Africa of singing territories of Greater Honeyguides that have persisted for decades. Young males will attempt to establish a territory where none has previously existed, but such territories are usually ephemeral. A male at a less contested, presumably poorer-quality site may be a secondary male at another male’s territory, and may ultimately replace the dominant male there.

Other well-known honeyguide species more or less fit the pattern outlined above for the Scaly-throated. Greater Honeyguide territories are in more open terrain, at woodland edges, or in bushland. These territories are widely spaced and, perhaps partly for that reason, attract fewer secondary males than do those of the Scaly-throated Honeyguide. Male Yellow-rumped Honey­guides do not sing, but defend a territory at a rock face bearing colonies of the rock honeybee. In the breeding season, a territorial male challenges all conspecifics coming to “his” larder, driving off other males, and courting the females that come to the beeswax resource he controls. Subordinate males tend to remain near such a territory, and may at times challenge the dominant male, as well as sneak copulations with visiting females if the territorial male is away. Should the dominant male be taken by a predator, the prime territories, at least, are taken over almost instantly by one of the secondary males; this has been found to be the case for all well-studied honeyguides. Male Brown-backed and Pallid Honeyguides at the extremes of the range, or in poor habitat, tend to initiate a territory, test it out, and then move on to sing at another site; in other words, most sing only temporarily, at various sites. Young male Lesser Honeyguides may do the same.

With the strategy of a male being to gain and hold a favou­rable territory, what do the females do? Breeding female Scaly-throated Honeyguides need to locate suitable feeding sites, especially for beeswax in non-lush settings. They must be able to locate host nests within a radius of travel, and they must find an accessible, suitable male with which to mate. Some females accomplish these goals within a limited area, and are rarely or never found elsewhere; presumably, these areas are optimal sites for their breeding. Other females move about much more in the breeding and non-breeding seasons. Female Scaly-throated Honeyguides seem to fight only at sources of beeswax. In contrast, at least some adult female Greater Honeyguides engage in prolonged encounters during which one or both may sing male-like songs, a phenomenon which, on current knowledge, is unique among the Indicatoridae. It is unknown whether a particular female mates with only one male, at least for one clutch, or whether all females are, as most seem to be, promiscuous, as are males.

The actual egg-laying habits of an individual are almost unknown. R. B. Payne, in his studies of specimens of Greater and Lesser Honeyguides in the well-defined breeding season of southern Africa, found the overall clutch size to be about 20 eggs, laid in distinct sets of four or five each. It is suggested that tropical honeyguides lay perhaps as many, or more, eggs, but in smaller sets of three or four. Within a set, a female lays about every second day; she therefore copulates to fertilize an egg on the day of its ovulation, and then has the next day in which to lay the egg in the nest of an appropriate host. Data are needed on other species, and from tropical populations, to test these generalizations.

Evidence exists that males, as well as females, monitor the activities and nests of their hosts. Most data relate to Lesser Honeyguides, but Scaly-throated and Spotted Honeyguides come to playback of recordings of their host woodpeckers’ calls, and also to calling woodpeckers themselves, triggering aggressive interactions. Males may monitor hosts and nests with regard to the location of their own singing territory, to the occurrence of breeding by their hosts, and to the success of their presumed offspring. They sometimes also act to keep other males away from duetting barbet pairs. A strategem, if hosts already have eggs of their own, is for a male honeyguide to interfere with the hosts, interrupting and disturbing them, thereby causing nest failure and affording a new opportunity for the parasite to lay. Females, of course, monitor the hosts’ nests. There is suggestive evidence that a male Lesser Honeyguide occasionally acts in concert with a female, presumably one with which he has mated, to afford her an opportunity to gain access to the hosts’ nest. An intriguing report exists of two Lesser Honeyguides assisting a host pair of Acacia Pied Barbets in preventing Rüppell’s Parrots (Poicephalus rueppellii) from usurping the barbets’ nest-cavity.

The laying female may puncture or remove one or more of the host’s eggs. There are many cases of Eastern Green-backed Honeyguides indulging in this behaviour, which also occurs in some Greater Honeyguides, and perhaps less often in others. The honeyguides’ own eggs are elliptical, and are white; an exception is provided by some Eastern Green-backed Honeyguides that lay blue eggs, matching in colour those of the frequent host white-eyes. The female must be quick, and may take only 10-15 seconds to lay and leave. Hosts such as barbets can kill or maim a honeyguide caught in the nest, and barbets have been seen to toss and slam a honeyguide against the nest entrance before releasing it. Female honeyguides also receive rough treatment from their partner during copulation; the male clasps the hindneck feathers or even the skin, at times leaving a bare area that may be wounded. Breeding females may require a good rehabilitation period between laying sets of eggs.

In elaborating the hosts utilized by honeyguides, one has to realize that females may have insufficient time to locate a host’s nest that has eggs at the appropriate stage of development. The timing of laying must be such that it will allow close synchrony of hatching of the host’s clutch and the honeyguide’s own egg, or earlier hatching of the latter. Some eggs may therefore be “ dumped” in the nest of a non-host species. Warblers (Sylviidae), flycatchers (Muscicapidae), white-eyes and perhaps sunbirds (Nectariniidae) seem to be the preferred hosts of the small Prodotiscus honeyguides. These are cup-nesters, mainly species constructing deep cups or covered nests, but some cavity-nesters such as petronias (Petronia) and tits (Parus) may possibly be used. Hosts of the Melignomon honeyguides are unknown, but may include barbets of the genus Gymnobucco. Suspected hosts of small species of Indicator are various of the small barbets known as tinkerbirds (Pogoniulus); Pallid Honeyguides are known to use Yellow-rumped Tinkerbirds (P. bilineatus) as hosts, and may parasitize other barbets as well.

The Thick-billed Honeyguide lays in nests of the Grey-throated Barbet (Gymnobucco bonapartei), and probably those of others of that genus. Of the 19 or 20 hosts of the Lesser Honeyguide, the chief victims are barbets, with nine species recorded, six of which are social; the others are three or four woodpeckers and two bee-eaters (Merops), and, perhaps only occasionally, a kingfisher (Halcyon), a swallow (Hirundo), two starlings (Sturnidae) and the Yellow-throated Petronia (Petronia superciliaris). All but the swallow are cavity-nesters, the swallow building a closed mud nest. The Spotted Honeyguide is suspected of using Gymnobucco barbets as hosts, as is the Lyre-tailed Honeyguide. Six woodpeckers, two barbets and a tinkerbird are recorded as hosts of the Scaly-throated Honeyguide. This honeyguide, however, is too large to fit into a tinkerbird cavity and possibly “dumped” the egg, laying it through the entrance; V. G. L. van Someren reported that, remarkably, the tinkerbirds enlarged the nest-chamber and entry tunnel in order to accommodate the nestling honeyguide.

There are about 40 hosts recorded for the Greater Honey­guide. In some areas, the majority of its eggs are laid in the nests of one or two species, especially bee-eaters, kingfishers and starlings. A roller (Coracias), three woodhoopoes (Phoeniculidae), the Hoopoe (Upupa epops), four kingfishers (Alcedinidae), eight bee-eaters, three barbets, six woodpeckers, three swallows, three starlings, two thrushes (Myrmecocichla), two petronias, a tit and a sunbird are the known hosts, these being cavity-nesters or, in a few cases, builders of closed nests. The number and variety of its hosts may be related to the striking sexual and age dimorphism of the Greater Honeyguide, far exceeding that of any other indicatorid species.

So far as is known, honeyguide eggs are not removed from nests by the hosts, except in cases, perhaps of “dumping”, in which the honeyguide lays before the host has commenced laying. The eggs take twelve to 18 days to hatch, an incubation period that is short by comparison with that of many host species, but in fact no shorter than in other piciforms, even including toucans. The honeyguide hatches naked, blind and weak, with a well-developed egg tooth, and small, sharp, curved membranous hooks on the tips of the mandibles; it also possesses spiny hypotarsal “heels”, and it sits on these and on the belly. From this point onwards, the hatchling moves its head about, clinging to and biting anything it touches, except the foster-parents. It punctures and destroys the host’s eggs one by one. If any of the host’s nestlings are present, they are “bitten” and lacerated, and they weaken and die, and are then removed by the parents. There are no known cases of a fosterer’s own young surviving to fledging if a honeyguide is raised in the nest. The membranous bill hooks presumably break off at as early an age of seven days in species of Prodotiscus, but they are present for 14 days or more in larger honeyguides, which occasionally still bear one or both hooks at fledging. On occasions, two or more honeyguide eggs are laid in the same host’s nest, possibly a result of “egg-dumping”; in some such cases, albeit rarely, the hatchling honeyguides, with their thick skin, fail to cause serious injury to one another, and so may be raised together successfully.

Nestling honeyguides beg loudly, and, by securing food intended for a number of the host’s young, they grow rapidly, the larger species gaining up to about 2 g in weight per day. There have been suggestions that nestling Greater Honeyguides mimic the begging calls of their specific hosts, but observations have so far not found this to be the case. The young honeyguides have several calls, and these shift developmentally. Greater Honeyguides, even where favouring one particular host, nevertheless parasitize various other species, and, moreover, the young do not vary in their mouth and facial-skin colours. Nothing in the behaviour of honeyguides suggests that individuals have ­either genetic or imprinted host-specificity. The eyes of the nest­ling honeyguide open at between ten and 20 days, by which time the chick is rather well feathered. The young of the smaller species fledge at about 21 days, while larger ones leave the nest at about 35 days of age. Nestlings do not appear at the nest entrance until a few days before fledging. While at the entrance they may see and hear monitoring adult honeyguides, perhaps their own parents.

At fledging time at a barbet’s nest, the appearance of the flying, emergent honeyguide confounds the foster-parents and their helpers, which may suddenly react as to the presence of an adult, by chasing the fat young honeyguide out of the territory. Whether or not the hosts react aggressively to the young honeyguide, problems usually arise rapidly. These are due partly to the young honeyguide failing to return to roost in the nest with its foster-parents, and partly to the frequently divergent foraging habits exhibited by the hosts and the honeyguide. For example, the young honeyguide’s failure to follow foster-parent barbets to fruiting trees, its lack of “ enthusiasm” for ground-foraging with starling fosterers, or the inability of a young honeyguide to forage in the air or to travel far to feeding sites with fostering bee-eaters must place stress on the bond between honeyguide and host.

Problems may be fewer between Prodotiscus honeyguide fledglings and foster-parent warblers or white-eyes, which do not return to the nest. Those host species glean for insects close by the nest, and perhaps roost with the youngster side-by-side in a bush or tree.

Fledged honeyguides spend either no time at all or up to seven days with their foster-parents. Many are probably independent within one or two days, as indeed are some young barbets.

Juvenile honeyguides of those species which exploit beeswax seem to tag along with other honeyguides, thus arriving at a food source at which they are apt to be dominant (see Morphological Aspects, General Habits). Furthermore, they are likely to be heavy when they leave the nest, where they have no competitors for food. This allows a period of time for them to find food before hunger becomes severe. Forthe first few months up to six months or more they enjoy a dominant status in their juvenile plumage, before acquiring a fully adult plumage.

Movements

Most male honeyguides in most areas remain more or less on, or near, their singing territory (see Breeding) throughout the year. Male Yellow-rumped Honeyguides dependent upon the colonies of giant or rock honeybees on rock faces may remain in or near the singing territory through the winter if the beeswax resource is plentiful. Immature and female Yellow-rumped Honeyguides are more mobile and move widely; even territorial males forage away from their territory, to as far as 10 km. Forest-dwelling honeyguides are less well known, although males of some species, such as the Spotted and the Lyre-tailed Honeyguides, sing or display more or less regularly all year. One problem in understanding these essentially tropical birds is that much of the information available on the Indicatoridae comes from the fringe of the subtropics in southern Africa, where the birds are strictly limited by strong summer-winter seasonality, a factor alien to most honeyguide populations, which do not reach such colder regions.

Almost all honeyguides are resident, spending their entire life in the area in which they were raised. Some undertake local movements, perhaps irregularly beyond a radius of 8-20 km of the natal site. Adverse conditions cause Lesser Honeyguides to gravitate to favourable sites in or near their place of origin. In a long-term study area in Kenya where there are few breeding Lesser Honeyguides, there is in most years a sudden deluge of young Lesser Honeyguides, many of them very young, such that more individuals of this species are ringed than of the more commonly breeding Scaly-throated and Greater Honeyguides. Within the breeding season, female honeyguides sometimes move up to 8 km or so, and, exceptionally, territorial males may do so in order to forage at a particular site.

Dispersal has led to the invasion by some species, especially the Lesser Honeyguide, of certain areas in south-western Africa. It is surely no coincidence that such movements have followed closely on the heels of the expansion into these areas of host Acacia Pied Barbets.

The Yellow-rumped Honeyguide is probably the most migratory member of the family, although it could hardly be termed a true migrant. Some birds apparently move upslope in the Himalayas after breeding. Likewise, some individuals, perhaps many, migrate to lower elevations in the autumn, although territorial males and some others remain around the cliffs where they breed, so long as they can glean beeswax from the abandoned colonies of rock honeybees that have moved downslope for the winter.

Of course, many honeyguide species are poorly known, and it is possible that some movements occur of which ornithologists are as yet unaware. Nevertheless, regional observers and authorities consider that most species are sedentary. Studies show that those honeyguides which have been investigated in some detail exhibit only local movements in search of food, except for the somewhat larger-scale dispersal by immatures.

Relationship with Man

The relationship between honeyguides and beeswax has been known to humans for a considerable time, and certainly to African honey-gathering tribesmen for millennia. Honeyguides have intrigued Western peoples and the Chinese for centuries with their wax-eating, their guiding behaviour and, more recently, their nest parasitism. The last seems to many to be cruel in the extreme, for every honeyguide is a “killer”, representing a lost brood of some host. Rather, honeyguides should be respected as highly evolved, efficient brood parasites, and unique among birds in their near dependence on beeswax.

Thus, despite the paucity of knowledge of honeyguides, the habits of these relatively drab birds have long captured people’s interest. Third-century Chinese scribes wrote of “little birds of the wax combs”, this being based on second-hand reports referring to the Yellow-rumped Honeyguide of the Himalayas, a species which does not enter China. For many thousands of years, African tribespeople have noted and watched honeyguides, and followed them to bees' nests. Early religious missionaries in ­Africa were surprised by birds that came to altars and took pieces of wax from their beeswax candles.

Within Africa, the honeyguides have evolved investigative behaviour that involves humans, for individuals of several species of Indicator follow, watch and monitor human activities, especially chopping, hammering and fire-building. Early European explorers and ornithologists were intrigued by the honey­guides, especially when the birds’ nest parasitism and the Greater Honeyguide’s guiding behaviour came to their attention.

So far as is known, only one species, the Greater Honeyguide, has evolved the habit of leading or guiding humans to bees' nests. This behaviour allows traditional honey-hunting peoples to acquire honey more efficiently, as H. A. Isack and H. U. Reyer have shown. It has often been said that the honeyguide also guides other mammals, and particularly the ratel, or honey-badger (Mellivora capensis), to sources of food, presumably using much the same method as it does for humans. Although this remains a real possibility, there appears to be little real evidence to support such claims. Clearly, this is one aspect of the honeyguide’s behaviour that requires further research, along with investigation into whether species other than the Greater Honeyguide lead humans in a similar way.

The honeyguide’s behaviour when leading a human to a nest has already been described (see General Habits), but a further well-documented example, from Zimbabwe, is of interest. In July 1998, C. B. Cottrell encountered a female Greater Honeyguide perched 10 m away, and giving the chatter call associated with guiding. The bird, having caught the observer’s attention, then flew out of sight behind a large, extensive and densely vegetated termite mound, where it chattered again, while the observer had to take a longer route around the obstruction; the bird, although unable to see the human, must have followed an appropriate route, since it reappeared alongside the observer and chattered once more. From there it flew some 30 m and settled close to a previously invisible bees' nest, thereby placing the observer in a dilemma: the nest was a commercial one, and belonged to a colleague!

There appears to have been a substantial decline in the incidence of guiding since the middle of the twentieth century, at any rate in some of the more densely populated areas. The results of a survey, initiated in 1998 by Cottrell, may shed light on this subject.

Collection of honey from wild honeybees remains locally important to people as a source of energy in the Himalayas and in parts of Africa. Even the honeycomb pieces are utilized in Africa for the making of beverages. To the extent that the comb is collected along with the honey, the impact upon honeyguides is more or less substantial (see Status and Conservation).

Status and Conservation

Honeyguides are unique among piciform birds in that so little is known about over half of the members of the family. For these, only the most basic information is available on their distribution and a few fragments of data on their habits, two species having been discovered within the past half-century. Several seem very rare, yet this may be in part due to their inconspicuousness. Indeed, the Lyre-tailed Honeyguide is known in some areas and a few countries only from the sounds produced in its remarkable aerial display (see General Habits).

Whatever factors play roles impinging adversely on honeyguides, the greatest threat by far must be the loss of sui­table habitat associated with the increasing human populations in Africa and Asia. For the Yellow-rumped Honeyguide in the Himalayas, this means ever more frequent harvesting of honey and the attendant destruction of the nests of rock honeybees, as documented by E. Valli and D. Summers. This over-exploitation by humans interferes with the feeding and breeding activities of this honeyguide, which has certainly become much rarer throughout most of its range during the past four decades. All of the truly forest-dependent species, such as the Spotted, Lyre-tailed and Sunda Honeyguides, are experiencing fragmentation of their habitat, this sometimes resulting in their replacement by a more open-country relative. Such has been the case with the Thick-billed Honeyguide, which has lost out to the Lesser Honeyguide.

Pressure is becoming severe on woodland honeyguides, too, both directly and indirectly. The expanding human population, ever questing firewood, eliminates dead trees and stubs used by honeyguide hosts for excavating nesting cavities; fewer cavities mean fewer nesting places for honeybees, as well. Such activities have a subtle effect on the location of singing territories by male honeyguides, probably through shifts in the location of bees' nests.

Although no species of the Indicatoridae is currently considered threatened by BirdLife International, the Yellow-footed Honeyguide is officially classified as Data-deficient. In addition, three species are classified as Near-threatened: the Dwarf Honeyguide, and the two Asian species, the Sunda and Yellow-rumped Honeyguides.

The forest-inhabiting Yellow-footed Honeyguide quite probably is threatened, but assessment of its true status is difficult since its range is incompletely known, this at a time when forest is being cleared at a staggering rate in West and Central Africa. The Lyre-tailed Honeyguide, conspicuous through its aerial di­splays, may possibly be threatened, or may become so shortly. So long as huge areas of lowland forest remained intact, man could arguably afford to be complacent in his lack of knowledge of such species, but this situation no longer applies. Both of these forest honeyguides, and others, urgently require study in order to acquire data on which to base methods of monitoring such species, and then measures for safeguarding them.

A further human activity having a major impact upon honeyguides is the greatly expanded practice of apiculture. As honeybees become “domesticated”, and as they increasingly occupy artificial hives, the beeswax resource becomes unavailable to honeyguides. This is particularly true of suburban and near-suburban areas surrounding major and even minor cities in Africa. Nowadays, households in rural areas frequently have several or more bee hives that they control. Honeyguides that are, naturally, attracted to artificial hives are driven away by some honey-culturers. In any event, since the surrounding areas are largely cleared, and remaining patches of natural vegetation are manicured through firewood-gathering, the effects on the structure and size of honeyguide populations are likely to be severe, although, essentially, they are unknown.

To the extent that habitat and hosts remain, it is likely that some benefits accrue to the Prodotiscus species through the planting of flowerbeds and the presence of some natural herbs and bushes that support scale insects, the wax covering of which is a major food resource for these honeyguides (see Food and Feeding). For the Greater Honeyguide, the most open-country member of the family, it is possible that the loss of wax that results from modern methods of apiculture is partly or even mainly offset by the widespread opening-up of formerly forested areas, which thus become accessible to this honeyguide.

So long as some honey-gathering persists in remaining natural habitat, and pastoral herd-tenders still locate and open up bees' nests, the guiding behaviour of Greater Honeyguides may survive. Perhaps it is only in very large reserves, where honey-hunting humans can co-exist with wildlife in reasonably natural situations, that we can be assured of the continuance of this unique symbiotic association.

General Bibliography

Avise & Aquadro (1987), Barnard (1998), Bennett et al. (1986), Bock (1994), Bowden et al. (1995), Brosset (1981), Burton (1984), Chapin (1958, 1962), Colston (1981), Cottrell (1998), Cracraft (1981), Cronin & Sherman (1977), Diamond (1985), Diamond & Place (1988), Forbes-Watson (1977), Friedmann (1954a, 1954b, 1955, 1958a, 1970, 1971, 1976, 1978b), Friedmann & Kern (1956), Fry (1977a), Gyldenstolpe (1917), Hoesch (1957), Hussain (1978, 1988), Hussain & Ali (1983), Isack & Reyer (1989), Johnsgard (1997), Lanyon & Zink (1987), Louette (1981a), Lowe (1946), Maclean (1990), Miller (1915), Olson (1983, 1985), Payne (1984, 1989, 1992), Peters (1948), Place et al. (1991), Raikow & Cracraft (1983), Ranger (1955), Rothstein & Robinson (1998), Short (1985b), Short & Horne (1979, 1983a, 1985b, 1988b, 1990a, 1992a, 1992b, 1992c, 2001), Sibley (1996), Sibley & Ahlquist (1985, 1990), Sibley & Monroe (1990, 1993), Sibley et al. (1988), Simpson & Cracraft (1981), Skead (1950), Stager (1967), Stuart & Stuart (1999), Swierczewski (1977), Swierczewski & Raikow (1981), Valli & Summers (1988), Verheyen (1955a, 1955b), Vernon (1987a, 1987b), Wong (1984).