Honeyguides

(Indicatoridae)

Class Aves

Order Piciformes

Family Indicatoridae

Thumbnail description
Small, generally drably colored tropical birds resembling barbets and finches

Size
4–8 in (10–20 cm)

Number of genera, species
4 genera; 17 species

Habitat
Forest, scrub

Conservation status
Near Threatened: 3 species

Distribution
Tropical and temperate Africa south of the Sahara. There are two species outside Africa, the yellow-rumped honeyguide (Indicator xanthonotus), along the southern foothills of the Himalayas, and the Malaysian honeyguide (I. archipelagicus), in Southeast Asia.

Evolution and systematics

The family Indicatoridae is within the order Piciformes, which also includes the barbets (Capitonidae), woodpeckers (Picidae), jacamars (Gabulidae), puffbirds (Bucconidae), and toucans (Ramphastidae). DNA-DNA hybridization studies seem to place honeyguides nearer the woodpeckers, but morphology and behavior strongly suggest them to be nearer the barbets.

The Indicatoridae are subdivided into four genera, Prodotiscus, with three species; Indicator, with 11 species; Melignomon, with two species; and Melichneutes, which is monotypic, with only the lyre-tailed honeyguide (M. robustus).

African honeyguides eat the wax of only one bee species, the common bee (Apis mellifera), despite the presence of other bee types throughout Africa, suggesting that their adaptations for cercophagy (wax-eating) are relatively recent, perhaps in the last one to two million years.

Physical characteristics

Body size of honeyguide species runs from 4 to 8 in (10–20 cm). The plumage is nondescript and cryptic, mostly olive-greens, grays, browns, black, and white, with occasional touches of yellow, depending on species. Only three species, including the greater (Indicator indicator) and lyre-tailed honeyguides, show sexual dichromatism in their plumage.

The bill is short and sturdy, well fitted to gouging wax and probing for insects in tree bark, and in most species the nostrils have raised rims to protect them from influxes of beeswax, honey, and other sorts of comb contents. The tail is long, often marked with white bars that the bird displays in flight, as guides for juveniles or in mating displays. The legs and toes are strong for clinging to tree bark, and the claws are long and hooked. As in all Piciformes, two toes are directed forward, the other two backward.

The wings are long, narrow, and pointed, allowing for vigorous flight, complicated maneuvering, and aerial acrobatics, which some species use to advantage in mating and territorial displays. The wings of the greater scaly-throated (I. variegatus), and lyre-tailed honeyguides make a distinctive noise in flight.

Honeyguide vision and hearing are acute. The olfactory lobe of the brain is well developed, although there are no studies showing to what extent it uses olfaction to track down bee nests. There are many accounts of the birds flying into missionary churches and attacking the beeswax candles, probably alerted by the odor, which had been intensified and spread by the candle flames.

Distribution

Honeyguides are found across nearly all Africa south of the Sahara, and there are two species in Asia. Distribution of species necessarily parallels that of their brood hosts.

Habitat

Species live variously in dense primary forest, secondary forest, gallery forest in semiarid country, and a mix of trees, shrubs, and grassland. Altitude of habitation runs from sea level to near the treeline in mountainous territory.

Behavior

The honeyguides would surely be on any list of the most interesting birds on Earth, not because of their physical appearance, which would scarcely attract notice, but because of their behavior. Two species deliberately lead animals, including humans, to honey sources. All species are cercophagous, or wax-eating, and have digestive systems able to handle the substance. All are obligate brood parasites, the females laying fertile eggs in the nests of other birds.

Honeyguides are tough, aggressive birds, whether they are harassing brood host birds, mobbing wax sources, or insistently leading humans to bee nests. Although solitary most of the time, dozens of individuals of up to four species may converge on a wax source. Scaly-throated honeyguides will shoulder aside greater and lesser (I. minor) honeyguides, while immature greater honeyguides out-bully all other species. Several African honeyguide species, notably the greater and scaly-throated honeyguides, routinely follow and watch human activities, flying about camping sites and inspecting everything, even the tents and vehicles.

All honeyguides (except the yellow-rumped [I. xanthonotus]) sing, and add to their singing a wide and various repertoire of sounds fitted to situations. Singing honeyguides add posture to their songs, as if using their entire bodies to belt out every note, arching their necks, fluffing out rump feathers, or all feathers, and quivering the tail in time with the notes. Several species enhance aggressive or mating voicings with rustling wing sounds.

Feeding ecology and diet

No honeyguide species depends entirely on beeswax as a food source, but all partake of it as a major food item, while a few species, among them Zenker's honeyguide (Melignomon zenkeri) and the yellow-footed honeyguide (Melignomon eisentrauti), get some of their wax requirement by eating scale insects (Coccidae) that produce a waxy exudate that covers their dorsal surfaces. The digestive system of honeyguides produces specialized enzymes for digesting wax. Similar enzymes have been found in seabirds and other landbirds, although not in other Piciformes.

All honeyguides supplement wax with insects and spiders, including bee larvae, ants, waxworms (Galleria spp.), termites, flies, and caterpillars. Honeyguides will occasionally eat fruits and other plant matter. All honeyguides do some insect feeding by flycatching, snagging airborne insects in mid-flight.

Honeyguides feed on beeswax directly, if the nest is accessible, by flying up to a bee nest, gripping the tree's surface alongside the outer part of the comb, and biting off and swallowing pieces of wax. The birds' hides are tough and parch-mentlike, offering some but not complete protection against stings, and a ferocious onslaught of defensive bees can kill a honeyguide.

Only two species of honeyguide partake in the behavior that has made the family famous, and given it its name Indicatoridae—from the Latin for "to point toward"—deliberately alerting, then leading animals and humans to honey sources. These species are the greater, or black-throated, honeyguide and the variegated or scaly-throated honeyguide.

The greater honeyguide alerts an animal or human to a honey source by flying close to them and calling "churr-churrchurr-churr" or "tirr-tirr-tirr-tirr." Once it has attracted the attention of the partner, it flies ahead, stopping at intervals and calling. When both parties reach the nest, the bird circles near the bee nest, gives a short, toned-down "indication call," then perches silently in the vicinity of the nest and waits for the chunks of comb to fall. A honeyguide seems to know in advance where a nest is, most likely through regularly surveying its territory.

H. A. Isack of the National Museum of Kenya, and H. U. Reyer of the University of Zurich conducted a three-year study to ascertain the truth of the honeyguide-human guiding relationship. In the mid-1980s, the two ornithologists followed Boran tribesmen through dry bush country in northern Kenya, searching for honey. The Boran claimed to have worked out an elaborate communication system with the greater honeyguide, with certain signals understood by both parties. The birds would indicate direction and decreasing distance of the nest, as the parties approached it, through flight patterns and calls. Isack and Reyer confirmed all this in the field. The birds signaled by calls and movements and perchings, the tribesmen by attracting the bird with special calls, then making noise as they followed the bird to keep communication going. Nearly all the nests the Boran reached with honeyguide help were inaccessible to the honeyguide, necessitating help from other quarters. In spite of the research of Isack and Rider, and others, some researchers have disputed accounts of honeyguides leading animals, leading humans, or leading at all, asserting that such accounts are not reliable.

The favored animal accomplice is the ratel, or honey badger (Mellivora capensis), a medium-sized, powerfully built, omnivorous viverrid. The relationship between bird and follower is mutualistic; neither species needs the other to survive, but both benefit from the relationship. The honey badger, which is well equipped to deal with hive-raiding, gouges out hunks of comb, and the honeyguide helps itself to fallen pieces of comb with little risk of injury from bee stings. The ratelhoneyguide relationship has not been proven, but abundant testimony leans toward it being true.

Humans who follow the honeyguides and gorge on the honey habitually leave the birds pieces of comb, as a reward and to keep the relationship intact. Most interesting, in relation to this custom, is that in suburban areas where people prefer sugar over honey, honeyguides have been reported to have lost the ability or the desire for guiding behavior.

Reproductive biology

Honeyguides besmirch their rather charming image as guides for honey-lovers with a less charming aspect of their behavior. All honeyguide species are brood parasites. There is little or no pair bonding between sexes. Adult female honeyguides lay fertile eggs among those of other bird species, usually one egg per nest, occasionally two. A female will lay six eggs or more, but divide them up among host nests. All host nests are cavity types—in trees, in the ground, in termite mounds, or in carton ant nests.

The honeyguide female will invade a host nest when the host female is out foraging, or perhaps sit and wait if the host female is home. Although the host female must leave to feed sooner or later, the honeyguide cannot wait too long at one egg-laying spot because the host female or a bonded male and female will sometimes chase off the intruder.

When the female honeyguide does lay an egg in a host nest, she enters the cavity nest, deposits the egg and leaves in 10 to 15 seconds (perhaps in as few as three seconds). Females of some honeyguide species will puncture or remove a host's egg before replacing it with her own. Most honeyguide eggs are white, except those of the green-backed honeyguide (Prodotiscus zambesiae), which are blue, matching the color of the eggs of white-eyes, their most frequent hosts.

The list of host species for honeyguides is long, but all are cavity-nesters and all are mainly insectivorous. Host choices of a honeyguide species may be as specific as one or two species, or a wide selection. The most frequently chosen hosts are barbets, but honeycreepers choose hosts from among the kingfishers (Alcedinidae), bee-eaters (Meropidae), hoopoes (Upudidae), woodpeckers (Picidae), and others.

The parasitic honeyguide eggs may hatch when the host's eggs are still unhatched, or after their hatching. The young honeyguides hatch with hooked bills and formidably sharp talons, with which they puncture the eggs or savage the young of the host. Some honeyguide hatchlings heave the host hatchlings from the nest, or the host mother, following hygiene instincts, will toss out the dead chicks or punctured eggs. The host mothers, bound and trapped by their strong instincts for parental care, raise the intruders as their own.

Honeyguides are obligate brood parasites, i.e., brood parasitism is the only option open to them for raising the next generation. No honeyguide species builds nests and none are able to raise young by themselves. Of necessity, the breeding seasons of honeyguide species closely accord with those of host species.

Conservation status

No species is listed as threatened. The Malaysian honeyguide (Indicator archipelagicus), yellow-rumped honeyguide (Indicator xanthonotus), and dwarf honeyguide (Indicator pumilio) are listed as Near Threatened. In the long view, most or all honeyguide species are threatened by rampant deforestation in Africa and Asia.

Significance to humans

The species that lead people to honey sources help humans secure a treasured food. Because of that famous role, honeyguides have found their way into African folklore. A typical honeyguide tale cautions thoughtfulness and fair reciprocation, based on the human custom of leaving chunks of comb for a honeyguide as reward for its help. In such a tale, a human refuses to pay the honeyguide his fee and reaps dire consequences.

Species accounts

List of Species

Greater honeyguide

Indicator indicator

taxonomy

Indicator indicator Sparrman, 1777.

other common names

English: Black-throated honeyguide; French: Grand Indicateur; German: Schwarzkehl-Honiganzer; Spanish: Indicador de Garganta Negra.

physical characteristics

Up to 8 in (20 cm). Sexes show only minor differences; male is olive-brown on the crown, nape, wings and dorsal surface; black throat patch extends up around the eyes in a mask. Yellowish patch on cheek area, another on the wing where it meets the shoulder at rest; underparts are whitish with some grayish touches. Bill is yellow and pink. Female is more brownish and lacks throat and cheek patches. As in most honeyguides, the outer retrices of the tail are white in both sexes and are shown to advantage in flight.

distribution

Nearly all tropical and temperate Africa south of the Sahara; the most widely distributed species.

habitat

Dense bush country, grasslands with scattered trees and bushes, and dense forest, from sea level to 8,000 ft (2,438 m) above sea level. They prefer territory with large resident aardvark (Oryctoperus afer) population. Ratels shelter in aardvark

burrows, while bee-eaters (Melittophagus spp.), ant-eating chats (Myrmecochlica spp.), and swallows, all parasitized by the greater (and other) honeyguides, nest in the roofs of the burrows.

behavior

Large for a honeyguide, lively and aggressive. Individuals patrol known territories, visiting and spot-checking bee nests, and keeping their senses alert for new ones. They will also follow humans and visit human campsites, not always for beckoning and guiding. The male's most oft-heard call is "vic-tor," repeated from six to 11 times in rapid staccato, perching erect with throat feathers slightly puffed out.

feeding ecology and diet

Diet is typically wax, bee larvae, other insects, and spiders. Greater honeyguides and scaly-throated honeyguides are the only species known to guide animals, including humans, to honey sources.

reproductive biology

Males put on aerial attraction displays for females, simplified versions of the lyre-tailed honeyguide's performance. The greater honeyguide male may also put on an act wherein he circles around and above a female, making drumming sounds with his wings. The male will alight on a branch near the perching female, then slowly approach her, spreading his white-bordered tail, fluttering his wings, puffing his feathers, and making a low, "chrrr" call. Females parasitize at least 40 species, including barbets, kingfishers, bee-eaters, hoopoes, and woodpeckers.

conservation status

Not threatened.

significance to humans

Helps humans secure a treasured food and plays a significant role in folklore.

Malaysian honeyguide

Indicator archipelagicus

taxonomy

Indicator archipelagicus Temminck, 1832.

other common names

English: Sunda honeyguide; French: Indicateur archipélagique; German: Malaien-Honiganzeiger; Spanish: Indicador Malayo.

physical characteristics

2.5 in (16 cm). Plumage brownish gray with small, bright yellow shoulder patch, underparts are white, and breast light gray. Eyes and bill are brown, legs and feet black. Female lacks yellow shoulder patch.

distribution

Malaysian Peninsula, Sumatra, and Borneo.

habitat

Tropical rainforest from sea level to 3,280 ft (1,000 m) above sea level.

behavior

Calls with harsh, catlike "miaow," followed by a churring "miaow-krrruuu" or "miao-miao-krruuu," rising in pitch.

feeding ecology and diet

Often seen near nests of Asian honeybees (Apis dorsata and A. florea). Eats beeswax, bee larvae, and adults of those species and other insects. Some individuals sing in presence of humans, but none exhibits guiding behavior.

reproductive biology

Little is known other than the voice of the singing male, although presumed to be brood parasites like other honeyguide species. Breeding seasons thought to be February into May in Malaya, during August in Thailand, May into June in Sumatra, and from January into March in Borneo.

conservation status

Listed as Near Threatened due to deforestation.

significance to humans

None known.

Lyre-tailed honeyguide

Melichneutes robustus

taxonomy

Melichneutes robustus Bates, 1909.

other common names

French: Indicateur à queue-en-lyre; German: Leierschwanz-Honiganzeiger; Spanish: Indicador Cola de Lira.

physical characteristics

6 in (17 cm). Long, lyre-shaped tail is most distinctive feature; two median pairs of retrices are curved outward at distal ends, outermost retrices are narrow and short.

Undersurface of tail is white; bird shows the white part conspicuously in flight. Both sexes uniformly olive-green above and whitish below; female shows some gray streaks on rear underbelly, and tail is not as large or exaggerated, but has similar shape.

distribution

Two separate areas of distribution in western Africa, one including Sierra Leone, Liberia, and the Ivory Coast, the other, larger area centering around Cameroon.

habitat

Lowland tropical rainforest.

behavior

Only incomplete information on behavior, since species is rare and individuals are difficult to spot. The spectacular aerial displays are described below. Individuals have been seen perched in trees near bees' nests, and associated with barbets and tinkerbirds, presumably as preferred brood hosts.

feeding ecology and diet

Includes beeswax, bee larvae, and other arthropods.

reproductive biology

Most spectacular mating display of all honeyguides. The male, airborne, voices several "peee" notes, then executes rapid, steep dive with tail feathers spread. Those feathers produce a signatory "kwa-ba kwa-ba" series of sounds. Male may also ascend and descend in spirals.

conservation status

Not threatened.

significance to humans

None known.

Scaly-throated honeyguide

Indicator variegatus

taxonomy

Indicator variegatus Lesson, 1830.

other common names

French: Indicateur écaillé; German: Strichelstirn-Honiganzeiger; Spanish: Indicador de Garganta Escamosa.

physical characteristics

Source of common name "scaly-throated" is network of small, alternating light and dark spots (not of scales, but feathers) adorning the throat and extending down onto the breast like a long bib. Otherwise, colored as most honeyguides, gray-olive on upperparts, off-white along breast and belly (except for spots).

distribution

Eastern South Africa to southern Sudan, Ethiopia, and Somalia; also in west Africa from coastal Angola to Zambia.

habitat

Forest patches and wooded and dense vegetation along rivers in dry areas.

behavior

Show wide range of vocalizations fitted to situations. Males assert or threaten with a high-pitched whistling. Females in similar mode make loud chatterings. Both sexes accompany aggressive voice with rustling wing sounds.

feeding ecology and diet

An aggressive species, individuals generally dominate a beeswax source as a feeding post, but will make off with small chunks of comb and eat them elsewhere. Also eats bee larvae and adults,

waxmoth larvae, beetles, and other insects, including termites, on which they gorge on the wing when the insects emerge in hordes. Occasionally takes fruits and seeds. Small groups sometimes join mixed-species flocks of foraging birds.

reproductive biology

Male displays for female similarly to greater honeyguide.

conservation status

Not threatened.

significance to humans

Alleged to lead humans to honey sources.

Spotted honeyguide

Indicator maculatus

taxonomy

Indicator maculatus G. R. Gray, 1847.

other common names

French: Indicateur tacheté German: Tropfenbrust-Honiganzeiger; Spanish: Indicador Moteado.

physical characteristics

6.75 in (16.5 cm). Olive-brown with some green tinges above, brownish underparts with parallel rows of yellow-white spots running from the throat to tail. Crown has array of small spots that echo rows on the underside. No appreciable sexual dichromatism. Bill is short, stout, and conical.

distribution

Equatorial Africa from Senegambia to eastern Zaire.

habitat

Dense, lowland forest along rivers.

behavior

Similar to that of its close relative, the scaly-throated honeyguide. Individuals are solitary, roaming about the forest canopy most of the time, but regularly foraging at lower levels. Most prominent vocalization is trill like that of the scalythroated honeyguide's, described as low "brrrr" or "prrrr." Other voicings include a loud "woe-woe-woe" similar to calls of falcons or eagles, with tail fanned and body feathers puffed.

feeding ecology and diet

Forages throughout all forest levels, but prefers the canopy. Regularly search out beeswax sites, and vary that diet with caterpillars, beetles, other insects, and spiders.

reproductive biology

Preferred host species is buff-spotted woodpecker (Campethera nivosa). Plumage approximates that of woodpecker, so they enhance their brood parasitism by imitating the woodpecker's voice.

conservation status

Not threatened.

significance to humans

None known.

Yellow-rumped honeyguide

Indicator xanthonotus

taxonomy

Blyth 1842

other common names

English: Indian honeyguide, orange-rumped honeyguide; French: Indicateur à dos jaune; German: Gelbbürzel-Honiganzeiger; Spanish: Indicador Hindú.

physical characteristics

5 in (15 cm). Most brightly colored honeyguides. Both sexes adorned with golden caps and more gold on the throat and lower back; female's gold patches not as extensive as male's. Remainder of livery for both sexes is gray and olive-green.

distribution

Foothills of the southern Himalayas, from Afghanistan to Burma.

habitat

Forests up to 7,000 ft (2,134 m) above sea level, in coniferous, dry deciduous, and lowland tropical rainforests.

behavior

No song has been noted. Instead, males stake out territory in forests near rock cliffs where the preferred honey producers, rock bees (Apis dorsata), build their nests in fissures well off the ground. Males feed off wax of chosen nest, while guarding and defending the valuable food source against rival males, and enticing females with the promise of food.

feeding ecology and diet

Wax and other comb ingredients in rock bee nests; also flycatch winged insects. Males perch alone in a tree near a honeycomb, erect or hunched, for hours.

reproductive biology

Females parasitize local species of woodpeckers and barbets.

conservation status

Listed as Near Threatened. Threats include deforestation and increased human consumption of rock bee honey.

significance to humans

None known.

Resources

Books

Ali, Salim, Dillon Ripley, and John Henry Dick. A Pictorial Guide to the Birds of the Indian Subcontinent. Oxford: Oxford University Press, 1996.

Barlow, Clive, Tim Wacher, and Tony Disley. A Field Guide to the Birds of the Gambia and Senegal. New Haven: Yale University Press, 1998.

Bernard, Robin, and Nneka Bennett. Juma and the Honey Guide: An African Story. Parsippany, NJ: Silver Press, 1996.

Friedmann, Herbert. The Honey-Guides. United States National Museum Bulletin 208. Washington, DC: Smithsonian Institution, 1955.

Keith, Stuart, Emil Urban, C. Hilary Fry, eds. Birds of Africa.

London: Academic Press, 1997.

Short, Lester, and Jennifer Horne. Toucans, Barbets and Honeyguides: Rhamphastidae, Capitonidae and Indicatoridae Oxford: Oxford University Press, 2001.

Species Survival Commission (SSC) Red List Programme. 2000 Red List of Threatened Species. Cambridge: IUCN Publications Unit, 2000.

Strange, Morten. A Photographic Guide to the Birds of Southeast Asia, Including the Philippines and Borneo. Boston: Charles E. Tuttle Co., 2001.

Periodicals

Isack, H. A., and H. U. Reyer. "Honeyguides and Honey Gatherers: Interspecific Communication in a Symbiotic Relationship." Science 243, (1989): 1343–1346.

May, Robert M. "Honeyguides and Humans." Nature 338, (1989): 707–709.

Organizations

African Bird Club, c/o Birdlife International. Wellbrook Court, Girton Road, Cambridge, Cambridgeshire CB3 0NA United Kingdom. Phone: +44 1 223 277 318. Fax: +44-1-223-277-200. E-mail: [email protected] Web site: <http://www.africanbirdclub.org>

BirdLife International. Wellbrook Court, Girton Road, Cambridge, Cambridgeshire CB3 0NA United Kingdom. Phone: +44 1 223 277 318. Fax: +44-1-223-277-200. E-mail: [email protected] Web site: <http://www.birdlife.net>

IUCN Species Survival Commission. 219c Huntingdon Road, Cambridge, Cambridgeshire CB3 0DL United Kingdom. E-mail: [email protected] Web site: <http://www.iucn.org/themes/ssc>

Other

The IUCN Species Survival Commission. "2000 IUCN Red List of Threatened Species" <http://www.redlist.org/> (1 April 2002).

Kevin F. Fitzgerald, BS