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

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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Habitat and Ecology

Systems
  • Terrestrial
  • Freshwater
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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:

Mutualist Species:

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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

The IUCN Red List deems greater honeyguides of least concern due to their large range and recent population increases. This slight population increase has been attributed to an increase in man-made forests where the birds breed.

CITES: no special status

IUCN Red List of Threatened Species: least concern

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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.
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Population

Population
The global population size has not been quantified, but the species is reported to be fairly common and widespread (del Hoyo et al. 2002).

Population Trend
Increasing
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Relevance to Humans and Ecosystems

Benefits

The diet of greater honeyguides consists largely of wax and larvae of hive-dwelling insects. Greater honeyguides may lead honey-eating mammals to farmed bee hives where both species may inflict damage to the farmer's crops. There is evidence to suggest that greater honeyguides may spread a form of blight to farmed hives if they've come in contact with an infected hive.

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Greater honeyguides have played a role in folklore in the past for their habit of leading honey-eating mammals to hives. They have been depicted in many stories and works of art.

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Wikipedia

Greater honeyguide

The greater honeyguide (Indicator indicator) is a bird in the family Indicatoridae, paleotropical near passerine birds related to the woodpeckers. Its English and scientific names refer to its habit of guiding people to bee colonies.

The greater honeyguide is a resident breeder in sub-Saharan Africa. It is found in a variety of habitats that have trees, especially dry open woodland, but not in the West African jungle.

Description[edit]

The greater honeyguide is about 20 cm long and weighs about 50 g. Like all African honeyguides, it has bold white patches on the sides of the tail. The male has dark grey-brown upperparts and white underparts, with a black throat. The wings are streaked whitish, and there is a yellow shoulder patch. The bill is pink.

The female is duller and lacks the black throat. Her bill is blackish. Immature birds are very distinctive, having olive-brown upperparts with a white rump and yellow throat and upper breast.

Diet[edit]

Bee colonies[edit]

The greater honeyguide feeds primarily on the contents of bee colonies (“hives”): bee eggs, larvae and pupae; waxworms; and beeswax. (Honeyguides are among the few birds that can digest wax.) It frequently associates with other honeyguides at hives; immatures dominate adults, and immatures of this species dominate all others. Like other honeyguides, the greater honeyguide enters hives while the bees are torpid in the early morning, feeds at abandoned hives (African bees desert more often than those of the temperate zones), and scavenges at hives robbed by people or other large animals, notably the ratel or honey badger. Most remarkably, it also guides people to hives.[2]

Guiding is unpredictable and is more common among immatures and females than adult males. A guiding bird attracts a person's attention with wavering, chattering "'tya' notes compounded with peeps or pipes",[3] sounds it also gives in aggression. The guiding bird flies toward an occupied hive (greater honeyguides know the sites of many hives in their territories) and then stops and calls again. As in other situations, it spreads its tail, showing the white spots, and has a "bounding, upward flight to a perch", which make it conspicuous. If the followers are native honey-hunters, when they reach the hive they incapacitate the adult bees with smoke and open the hive with axes or pangas (machetes). After they take the honey, the honeyguide eats whatever is left.[4]

One study found that use of honeyguides by the Boran people of East Africa reduces their search time for honey by approximately two-thirds. Because of this benefit, the Boran use a specific loud whistle, known as the fuulido, when a search for honey is about to begin. The fuulido doubles the encounter rate with honeyguides.[2]

The tradition of the Bushmen and most other tribes says that the honeyguide must be thanked with a gift of honey; if not, it may lead its follower to a lion, bull elephant, or venomous snake as punishment. However, “others maintain that honeycomb spoils the bird, and leave it to find its own bits of comb”.[4]

Possible guiding of non-human animals[edit]

Many sources[5][6][7] say that this species also guides honey badgers (ratels). Friedmann (1955, quoted by Harper)[8] notes that Sparrman said in the 18th century that indigenous Africans reported this interaction, but Friedmann adds that no biologist has seen it. According to Dean and MacDonald (1981),[9] Friedmann does quote reports that greater honeyguides guide baboons and speculates that the behavior evolved in relation to these species before the appearance of humanity. However, they state,

In addition to that listed by Friedmann (1955:41-47), the only recent record is of a greater honeyguide giving its guiding call to baboons at Wankie Game Reserve, Zimbabwe (C. J. Vernon, pers. comm.). However, Vernon did not see a positive response by the baboons to the honeyguide. No additional records of honeyguides and ratels have been reported since Friedmann (1955) and the first-hand accounts given in his review in support of this association are all of incomplete guiding sequences. No biologist has ever reported this association.

Dean and MacDonald go on to express doubt that honeyguides guide other animals and suggest that the behavior may have evolved with "early man". It has also been acknowledged[10] that bee colonies are seasonally very common in Africa and ratels probably have no trouble finding them.

Another argument against guiding of non-human animals is that near cities, where Africans increasingly buy sugar rather than hunting for wild honey, guiding behavior is disappearing. Ultimately it may disappear everywhere.[4]

Other food[edit]

The greater honeyguide also catches some flying insects, especially swarming termites. It sometimes follows mammals or birds to catch the insects they flush, and joins mixed-species flocks in ones and twos. It has been known to eat the eggs of small birds.

Reproduction[edit]

In addition to being a predator of insects and a mutualist with its follower species, the greater honeyguide is a brood parasite. It lays white eggs in series of 3 to 7, for a total of 10 to 20 in a year. Each egg is laid in a different nest of a bird of another species, including some woodpeckers, barbets, kingfishers, bee-eaters, woodhoopoes, starlings, and large swallows. All the species parasitized nest in holes, covered nests, or deep cup nests. The chick has a membranous hook on the bill that it uses, while still blind and featherless, to kill the host's young outright or by repeated wounds.

References[edit]

  1. ^ BirdLife International (2012). "Indicator indicator". IUCN Red List of Threatened Species. Version 2013.2. International Union for Conservation of Nature. Retrieved 26 November 2013. 
  2. ^ a b Isack, H. A. and H.-U. Reyer (1989). "Honeyguides and honey gatherers: interspecific communication in a symbiotic relationship". Science 243 (4896): 1343–1346. doi:10.1126/science.243.4896.1343. PMID 17808267. 
  3. ^ Short, Lester, and Jennifer Horne (2002a). "Family INDICATORIDAE (HONEYGUIDES)". In Josep Del Hoyo, Andrew Elliott, and Jordi Sargatal (Eds.). Handbook of the Birds of the World: Jacamars to Woodpeckers, Vol. 7. Lynx Edicions. ISBN 84-87334-37-7. 
  4. ^ a b c Short, Lester, Jennifer Horne, and A. W. Diamond (2003). "honeyguides". In Christopher Perrins (Ed.). Firefly Encyclopedia of Birds. Firefly Books. pp. 396–397. ISBN 1-55297-777-3. 
  5. ^ Attenborough, David (1998). The Life of Birds. Princeton University Press. ISBN 0-691-01633-X. 
  6. ^ Estes, Richard D. (1999). The Safari Companion: A Guide to Watching African Mammals. Chelsea Green. pp. 361–362. ISBN 1-890132-44-6. 
  7. ^ Zimmerman, Dale A., Donald A. Turner, and David J. Pearson (1999). Birds of Kenya and Northern Tanzania. Princeton University Press. p. 406. ISBN 0-691-01022-6. 
  8. ^ Harper, W. Ed (2003). "honeyguides". Bird Families of the World. Don Roberson. Retrieved 2006-03-22. 
  9. ^ Dean, W.R.J, and I.A.W. MacDonald (1981). "A review of African birds feeding in association with mammals". Ostrich 52 (3): 135–155. doi:10.1080/00306525.1981.9633599. 
  10. ^ Short, Lester, and Jennifer Horne (2002b). Toucans, Barbets and Honeyguides. Oxford University Press. pp. 473–480. ISBN 0-19-854666-1. 

Further reading[edit]

  • Friedmann, Herbert (1955). The Honeyguides. U.S. National Museum (Bulletin 208). 
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