Overview

Brief Summary

The Greater Honeyguide (Indicator indicator) is fairly common and widespread, occurring widely in the Sahel and sub-Saharan Africa, except in desert, forest, and grassland; it is found in all but the desert parts of western South Africa. The distribution extends from Senegal and southern Mali south almost to the coast, east to Eritrea and south (around the main forested belt) through east-central Africa (including eastern and southern DRC and much of East Africa), and from Angola, northeastern Namibia, and northern and eastern Botswana to Mozambique and south to the former Cape Province (South Africa).

Greater Honeyguides are found in open woods, woodland edges, bushland, streamside woods, bushes in dry areas, plantations, gardens with trees, thickets, and trees lining suburban streets; they are often seen in the vicinity of bees' nests. They may be found up to 2000 m (occasionally to 3000 m in East Africa).

These birds have an unusual diet, feeding extensively on beeswax (which they digest readily), as well as on honeybee larvae and eggs and a range of other insects (including termites, winged ants, flies, and others). The nestlings, which are raised in the nests of other species (see below), feed on food provided by their host, including fruits. Immatures generally dominate around bees' nests. In some areas, Greater Honeyguides (often immature birds) lead humans to bees' nests. After the human honey gatherers have opened and left the nest, the bird feeds on pieces of honeycomb left behind. From these, it extracts mainly the larvae and the wax to supplement its diet of insects. (For more details on the symbiotic relationship between traditional human honey gatherers and honeyguides, see Isack and Reyer 1989.)

Greater Honeyguides are brood parasites, laying their eggs in the nests of a diverse set of avian host species (mainly from the Coraciiformes and Upupiformes) at any given location. They typically deposit just a single egg per nest (sometimes more), laying up to 20 total. Females typically puncture the host's eggs when laying their own, but in many nests at least one host egg survives. The young honeyguides finish the job. Spottiswoode and Koorevaar (2012) found that hosts always hatched after honeyguide chicks (presumably in part due to an additional period of internal incubation in female honeyguides; Birkhead et al. 2011) and were killed within hours by honeyguide nestlings, which utilize a specialized sharp hook on their bills (this hook is lost after 2 weeks or more). Despite being blind and in total darkness, honeyguide chicks attack host young with sustained biting, grasping, and shaking motions, as seen in these videos. Attacks of just a few minutes in duration are sufficient to cause death, although it may sometimes be delayed for hours. Young Greater Honeyguides fledge at 35 to 40 days and are usually independent in just a few days. Greater Honeyguides are mainly resident, but may disperse 20 km or more and regularly move 8 to 10 km (juveniles disperse to 8 to 10 km in a few days). Greater Honeyguides may live to 12 years or even longer.

Spottiswoode et al. (2011) showed that Greater Honeyguides exhibit host-specific differentiation in both egg size and egg shape (mimicry of egg color is presumably of less importance in birds nesting in dark tree cavities). Genetic analysis of honeyguide eggs and chicks revealed that two highly divergent mitochondrial DNA (mtDNA) lineages are associated with ground- and tree-nesting hosts, respectively, indicating strong fidelity to two mutually exclusive sets of host species for millions of years. However, despite their age and apparent adaptive diversification, these ancient lineages do not represent cryptic species: a complete lack of differentiation in nuclear genes (which are biparentally inherited rather than maternally inherited, as is mtDNA) indicates that male and female honeyguides reared by different hosts must interbreed sufficiently often to prevent divergence at neutral nuclear loci.  Thus, ancient host-specific female lineages apparently have apparently been maintained in the absence of any detectable reproductive isolation.

Female specificity in host use is remarkably strong and maternally inherited, whether genetically (e.g. on the female-specific W chromosome) or culturally (e.g., via behavioral imprinting on young female honeyguides). Matters are complicated by the presence of phenotypic differentiation within the lineage specializing on treehole-nesting hosts.

The male Greater Honeyguide is unmistakable: brown above with black throat, white cheeks, pink bill, a yellow/golden shoulder patch, white outer tail patches, and short outer tail feathers.

(Short and Horne 2002 and references therein; Spottiswoode et al. 2011; Spottiswoode and Koorevaar 2012)

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Distribution

Indicator indicator, also known as greater honeyguides, is widely distributed throughout sub-Saharan Africa. Their range excludes a small, south-western portion of Africa consisting of Namibia, Botswana, and part of South Africa. Greater honeyguides are the most widely-distributed species of all the known honeyguides.

Biogeographic Regions: ethiopian (Native )

  • 2002. Family Indicatoridae (Honeyguides). Pp. 274-296 in J Del Hoyo, A Elliot, J Sargatal, eds. Handbook of the Birds of the World, Vol. 7, 1 Edition. Spain: Lynx Edicions.
  • Berruit, A., B. McIntosh, R. Walter. 1995. Parasitism of the blue swallow Hirundo atrocaerulea by the greater honeyguide Indicator indicator. OSTRICH, 66, 2-3: 94.
  • Johnsgard, P. 1997. Avian Brood Parasites: Deception at the Nest. Oxford: Oxford Publishing Press.
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Range

Widespread Africa south of the Sahara.
  • Clements, J. F., T. S. Schulenberg, M. J. Iliff, D. Roberson, T. A. Fredericks, B. L. Sullivan, and C. L. Wood. 2014. The eBird/Clements checklist of birds of the world: Version 6.9. Downloaded from http://www.birds.cornell.edu/clementschecklist/download/

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Physical Description

Morphology

Greater honeyguides are the largest bird of the Indicatoridae family and are usually around 20 centimeters in body length. Males are on average 48.9 grams and females average 46.8 grams. Adult males have pink bills, black throats, a pale gray ear patch, and a nearly white breast. Males have a small patch of golden feathers fringing the wing coverts which are easily visible during flight. Females are uniformly grayish brown and white underparts similar to their male counterparts, but are more brown and lacking throat and cheek patches. Juveniles have a remarkably different appearance than either parent with a distinctive yellow-gold, taupe and olive-brown plumage.

This bird is readily-distinguishable from other honeyguides by its mostly white rump and tail coverts edged with white, with brown shaft streaks. Adult plumage takes about 8 months to develop with the last adult trait to appear being the pink shading of the male’s bill. As in most honeyguides, the outer retrices of the tail are white in both sexes.

Range mass: 46.8 to 48.9 g.

Average length: 20 cm.

Other Physical Features: endothermic ; homoiothermic; bilateral symmetry

Sexual Dimorphism: sexes alike; sexes colored or patterned differently

  • Spottiswoode, C., J. Colebrook-Robjent. 2007. Egg puncturing by the brood parasitic Greater Honeyguide and potential host counteradaptations. Behavorial Ecology, 18, 4: 792-799.
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Ecology

Habitat

Habitat and Ecology

Systems
  • Terrestrial
  • Freshwater
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Greater honeyguides favor large open areas including savanna, shrubland, forest edge, riverside or orchard habitats. Greater honeyguides usually live in areas that are rich in food resources (termite, bee, and other insect nests) and avian host species whose nests they parasitize. Habitats range in elevation from sea level to nearly 3000 meters above sea level but this species is usually found under 2000 meters.

Range elevation: 3000 (high) m.

Average elevation: below 2000 m.

Habitat Regions: tropical ; terrestrial

Terrestrial Biomes: savanna or grassland ; scrub forest

Other Habitat Features: agricultural ; riparian

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Trophic Strategy

Greater honeyguides have a unique, highly wax-based diet and require enzymes in the digestive system to breakdown this normally indigestible food. They also feed on grubs and larvae found in Hymonoptera hives, and insect wings of flying swarming colonies. Greater honeyguides guide honey-gathering mammal species to hives of bees, termites, and other insects that are inaccessible to the birds alone. They occasionally will eat fruit, and will rarely consume bird eggs. Young greater honeyguides thrive predominantly on fruit that the host parents bring.

Animal Foods: eggs; insects

Primary Diet: carnivore (Insectivore )

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Associations

Greater honeyguides are closely involved with several honey-consuming mammal species, but primarily honey badgers (Mellivora capensis). Honeyguides will lead these large, clawed mammals to hidden insect hives which the mammal can break open and feed on. Honeyguides may then gain access to the previously inaccessible supply of wax and larvae.

Greater honeyguides are brood parasites and have a negative impact on the species it parasitizes. After a female lays her eggs in a host's nest, she proceeds to puncture all of the host's eggs in the nest. If she does not destroy the host's eggs, the greater honeyguide chick is equipped with a sharp, curve-tipped bill which is used to destroy any other nestlings. The productivity of the host species is greatly decreased by nest parasitism. Greater honeyguides are known brood parasites of the following species: golden-tailed woodpeckers, black-collared barbets, crested barbets, brown-hooded kingfishers, striped kingfisher, white-fronted bee-eaters, little bee-eaters, swallow-tailed bee-eaters, southern carmine bee-eaters, Cape glossy starlings, Meves's starlings, and pied starlings.

Ecosystem Impact: parasite

Species Used as Host:

  • Golden-tailed woodpeckers (Campethera abingoni)
  • Black-collared barbets (Lybius torquatus)
  • Crested barbets (Trachyphonus vaillantii)
  • Brown-hooded kingfishers (Halcyon albiventris)
  • Striped kingfishers (Halcyon chelicuti)
  • White-fronted bee-eaters (Merops bullockoides)
  • Little bee-eaters (Merops pusillus)
  • Swallow-tailed bee-eaters (Merops hirundineus)
  • Southern carmine bee-eaters (Merops nubicoides)
  • Cape glossy starlings (Lamprotornis nitens)
  • Meves's starlings (Lamprotornis mevesii)
  • Pied starlings (Spreo bicolor)

Mutualist Species:

  • Honey badgers (Mellivora capensis)

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There are no known predators of greater honeyguides.

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Life History and Behavior

Behavior

Males make vocal calls to attract mates and usually call from the same area year after year. Some females have been observed mimicking male calls from locations also used by males. Courtship behavior includes an aerial and auditory display by males, who swoop near females and create a distinct flight noise. Greater honeyguides also give distinct calls to honey-gathering mammal species to lead them to hives; by guiding stronger organisms to bee hives, the birds gain access to the stores of wax and larvae. Greater honeyguides' white tails are used to entice hosts to leave their nests, allowing the female honeyguides to lay eggs within the nest. Like all birds, greater honeyguids perceive their environment through visual, tactile, auditory and chemical stimuli.

Communication Channels: visual ; acoustic

Perception Channels: visual ; tactile ; acoustic ; chemical

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Life Expectancy

It has been noted that greater honeyguides can live up to 12 years in the wild. No information is available for lifespan in captivity.

Typical lifespan

Status: captivity:
12 (high) years.

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Reproduction

Males display for females by circling above a female while making drumming sounds with their wings. After landing near the courted female the male approaches her, spreading his white edged retrices, fluttering his wings and making a low shrill call. The mating system is not well defined, as individuals do not participate in any form of parental care and have no association after the actual mating.

Greater honeyguides breed between September and October. After mating, females lay their eggs in the nest cavities of other species. The female lays one egg per nest, and lays between 4 and 8 per breeding season. After having laid an egg in an host nest, the female will pierce the hosts’ eggs to ensure her chicks' survival. Parasitized species then incubate and raise greater honeyguide young as their own. Females time breeding so that their eggs will hatch with the brood of chicks they parasitize. The eggs take about 18 days to hatch so if she lays her eggs too late the surrogate mother will no longer incubate the greater honeyguide eggs as she knows the eggs not to be hers. When greater honeyguide young hatch, it furthermore uses its toothed, hooked bill to kill any chicks in the nest or pierce other unhatched eggs. If successful, a greater honeyguide chick will grow quickly as it is often the only chick remaining and receives all feeding attempts by the parents. Chicks fledge after 30 to 40 days, and are often fed by the parents for an additional 7 to 10 days. Juveniles reach reproductive maturity when they are 1 year old.

Breeding interval: Greater honeyguides breed once yearly.

Breeding season: Greater honeyguides breed from September to October.

Range eggs per season: 4 to 8.

Average time to hatching: 18 days.

Range fledging age: 30 to 40 days.

Range time to independence: 7 to 10 days.

Average age at sexual or reproductive maturity (female): 1 years.

Average age at sexual or reproductive maturity (male): 1 years.

Key Reproductive Features: iteroparous ; seasonal breeding ; gonochoric/gonochoristic/dioecious (sexes separate); sexual ; oviparous

Being brood parasites, the parents have little involvement with their own offspring. They may defend the broods they parasite from other predators and other brood parasites. Mothers have been known to pierce the eggs of the host's other offspring while fathers distract host birds.

Parental Investment: no parental involvement; altricial ; pre-fertilization (Provisioning, Protecting: Female); pre-hatching/birth (Protecting: Male, Female)

  • 2002. Family Indicatoridae (Honeyguides). Pp. 274-296 in J Del Hoyo, A Elliot, J Sargatal, eds. Handbook of the Birds of the World, Vol. 7, 1 Edition. Spain: Lynx Edicions.
  • Dean, W., I. MacDonald. 1981. A review of Afrian birds feeding in assocaition with mammals. Ostrich, 52: 135-155.
  • Johnsgard, P. 1997. Avian Brood Parasites: Deception at the Nest. Oxford: Oxford Publishing Press.
  • Spottiswoode, C., J. Colebrook-Robjent. 2007. Egg puncturing by the brood parasitic Greater Honeyguide and potential host counteradaptations. Behavorial Ecology, 18, 4: 792-799.
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Conservation

Conservation Status

IUCN Red List Assessment


Red List Category
LC
Least Concern

Red List Criteria

Version
3.1

Year Assessed
2012

Assessor/s
BirdLife International

Reviewer/s
Butchart, S. & Symes, A.

Contributor/s

Justification
This species has an extremely large range, and hence does not approach the thresholds for Vulnerable under the range size criterion (Extent of Occurrence <20,000 km2 combined with a declining or fluctuating range size, habitat extent/quality, or population size and a small number of locations or severe fragmentation). The population trend appears to be increasing, and hence the species does not approach the thresholds for Vulnerable under the population trend criterion (>30% decline over ten years or three generations). The population size has not been quantified, but it is not believed to approach the thresholds for Vulnerable under the population size criterion (<10,000 mature individuals with a continuing decline estimated to be >10% in ten years or three generations, or with a specified population structure). For these reasons the species is evaluated as Least Concern.

History
  • Least Concern (LC)
  • Least Concern (LC)
  • Least Concern (LC)
  • Lower Risk/least concern (LR/lc)
  • Lower Risk/least concern (LR/lc)
  • Lower Risk/least concern (LR/lc)
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