Profiteers of the Busy Bee

Observations on the honey guides of Africa

By James P. Chapin

Associate Curator of Birds of the
Eastern Hemisphere, American Museum

ERE a facetious journalist to attempt to endow a mythical bird with some startling but imaginary instinct, he would hardly be likely to go to the lengths to which nature has gone in the case of the common honey guide of Africa. The strange behavior of this bird has so long been known, moreover, that it surprises one to find how little has been written about it beyond simple accounts of the way the bird attracts the attention of men and reveals to them the location of beehives. Sparrman, who traveled in South Africa as long ago as 1775, gave one of the best descriptions from his personal observations, and was able to quote a still earlier account of the bird, accurate in the main, by Father Jerome Lobo, who had gone as a missionary to Abyssinia in 1625. As Sparrman concluded, the moroc, or honey bird, of the Abyssinians could be none other than the common honey guide. This testimony has been confirmed by a great number of travelers, sportsmen, and trained ornithologists who have since visited the open grassy regions of Africa, over which the bird is so widely distributed.

ONE OF THE STRANGEST CHARACTERS OF THE BIRD WORLD The common African honey guide (Indicator indicator) performs a useful but not unselfish service in conducting man to some hive it has previously located. How this bird came to know that man could be of help in obtaining the food it prefers is still a subject for conjecture, but through his willing aid the honey guide is often enabled to feast upon the bee larvae, which it probably covets more than the honey. Whether the wax that Indicator indicator so often swallows also serves as food seems very doubtful. That the substance is beeswax is apparent from the way it melts on a hot knife blade, only to congeal again as the blade cools. Birds of both sexes act as honey guides, but the female, in addition to this rather commendable habit, has the more questionable one of laying her eggs in the nests of other birds and thus of avoiding the responsibilities of motherhood. Although resembling our cowbird in this practise, Indicator indicator is a near relative not of this malefactor but of the woodpeckers. Nevertheless, it rarely if ever climbs about on the trunks of trees, preferring to perch on twigs and boughs. As in the case of the woodpeckers, only two toes of each foot are directed forward, two being pointed to the rear. The picture is that of a female and was obtained in the northeastern corner of the Belgian Congo. The female lacks the throat patch of pure black by which the male is readily distinguished. Photo by Herbert Lang

Avoiding the heavy forests of the Congo basin and other parts of western Africa, the common honey guide (Indicator indicator) ranges from Cape Colony to northeast Africa, and then across the Sudan to Senegal. It is a plain-colored, brownish-gray bird, scarcely larger than our American bluebird, but much more stockily built, with short dense plumage, and a skin so tough that it has often been considered a cuirass against the stings of bees. When fully grown, both sexes have half-concealed epaulets of yellow; and the male bird is then distinguished by a large black throat patch. The immature birds are somewhat greener and until a few years ago were regarded as a distinct species. The nearest relatives of the honey guides, in our North American fauna, are the woodpeckers; yet the honey guides have neither stiffened tail feathers nor an extensile tongue.

How well the honey guide is known and esteemed by the natives of the countries where it dwells may easily be imagined. By the Azande tribe of the northeastern Congo the bird is called turubwa, and I was told that before the arrival of Europeans an Azande chief would have cut off the ear of any man so stupid as to have killed a honey guide. Mr. Herbert Lang and I had many experiences with honey guides attracted by our caravans or hunting parties. It is the habit of the bird to locate one or more bee colonies and then wait for the passing of men, whose attention it attracts by a persistent chattering. At such times it is relatively tame and will alight in small trees only a few yards off. If a man wishes to learn where the hive is, he follows the bird, whistling occasionally to it.

Here I may quote an instance from my own notes. One afternoon in November, 1911, in a small wooded swamp near Faradje, a post in the northeastern corner of the Congo, we came upon a male bird, who at once started his chatter, and then flew off to some distance, returning shortly as though to assure himself that we were in earnest. We replied with low whistles, and following him through the tall grass and scrub, were led out on to higher ground. Now our feathered guide would fly noisily ahead about fifty yards until out of sight, perching on top of a bush and repeating the performance as soon as we came up. Presently another male bird joined him. We had gone about six hundred yards when both birds stopped in a tree too small to harbor bees in its trunk. Yet by their short aimless flights and repeated returns to the tree, the honey guides impressed upon us that this was the spot. The buzzing of passing bees now was heard and the insects were traced to a small hole in the ground close by. During these proceedings the birds allowed us to approach within ten or fifteen feet of them.

Map showing the distribution of two African honey guides, one (Indicator indicator) an inhabitant of the open grass country, or savanna, the other (Melichneutes robustus) restricted to the equatorial forest.

We prepared to make a fire, and our birds retired noiselessly for the time. A little later I saw them again, sitting with puffed-out breasts and open bills, tittering a low chwee-r-r, which I had not heard before. They seemed to be quarreling, and one soon chased his rival off at top speed.

With the aid of some burning grass two of my black helpers quickly had the hive unearthed, paying a penalty of only six stings. The comb contained no honey, only pollen and bee larvae. It was in a cavity previously occupied by termites. We placed some of the comb in the forks of a tree and went off to escape an impending shower. An hour or two later we found that the birds had returned to peck at the comb; and the following morning I watched them come silently, the one after the other, to seize a piece of the comb and fly off with it. Without crediting the birds with actual foresight or intelligence, I do not hesitate to say that it is for this reward that they have worked.

It is said that in sections where the negroes have artificial hives hanging in trees for the use of bees the honey guide makes no distinction and will lead to occupied hives established through man's agency as readily as to natural cavities housing wild bee colonies. This I believe, though I have not had occasion to verify it even among the Logo of the eastern Uelle District, who attract bees with hives made of reeds.

The assertion has also been made that the honey guide will sometimes lead a man up to a snake or a leopard, but this has been vigorously denied by experienced naturalists. A story far better founded is that of the honey badger (Mellivora capensis) following the honey guide. Major Stevenson-Hamilton [Animal Life in Africa, 1912; pp. 247-48] describes it as though he had often observed it himself. "You may be resting in the bush in the cool of the afternoon, or on some cloudy day, when your attention is arrested by the persistent and approaching chatter of one of these feathered spies. Presently the bird itself comes fluttering on to a branch some thirty yards distant, where it perches, flapping its wings, and displaying every sign of impatience. For a moment it is silent, and then a less familiar sound strikes the ear: a light sibilant hissing and chuckling, which at first you find yourself unable to identify. . . .

	The head of the lesser honey guide, Melignothes minor.—Note the extremely blunt beak, serviceable perhaps for tearing honeycomb apart, but of little use in pecking open the tree where it is hidden. Drawn from a specimen by W. E. Belanske.

The honey-guide understands, and having, with undulating flight, sought another tree some thirty yards further on, renews his invitation. Keeping quite still, and looking steadily, you presently spy a little gray and black form, moving along at a steady jog-trot; the tail is carried slightly above the level of the back, and the head, except when raised to glance up at the guide, is held a little low. Every time the bird utters his monotonous refrain, which, translated into feathered language, means 'Come along, come along, don't be so slow,' the follower replies, 'All right, my friend, don't be alarmed, I am coming.' And thus the strange procession passes on out of sight to the hollow log where the unlucky insects are industriously slaving, only ultimately to satisfy the appetites of bird and beast.” The favorite food of this badger is honeycomb, and it has powerful claws with which to tear open the hive.

The instinct of the honey guide is unique among birds. It is far more complex than the “guarding” of buffaloes and rhinos by the oxpeckers (Buphaga). There the birds have come to feed on the ticks that cling to the animal's hide; and they merely alarm their hosts by their cries when they take flight at the approach of an enemy. The honey guide, on the other hand, recalls the action of a dog in leading a stranger to a spot where its master lies in distress, although the motive is, of course, entirely different. It brings to mind also the story so widely circulated by the newspapers a year or two ago, of a gander on a farm in Alabama which used to lead a blind ox to the watering trough every day by its cackling. I cannot vouch for the truth of this narrative, though photographs of the strangely assorted couple appeared in a New York paper of good repute.

No doubt the specialists in animal behavior have an explanation that does not require any reasoning on the part of the honey guide. The guiding is instinctive, for it has become hereditary with at least one species of Indicator, and is practised by old birds of both sexes, and apparently by immature birds as well. The fact that it is a characteristic form of behavior throughout the whole range of the species argues for its remote origin and leads us to believe that the instinct grew up slowly with the evolution of the family, though man is not always the beneficiary. The honey guides must have preyed on bees long before savage man reached Africa, and we may speculate, quite properly, as to the origin of the guiding instinct.

The honey guide family (Indicatoridae) is not a large one; it comprises, nevertheless, five genera [Melignothes, Melignomon, Indicator, Melichneutes, and Prodotiscus] and about twelve species, of which two are found in the Oriental region, the remainder in Africa south of the Sahara. None of them exceeds seven and a half inches in length. I myself have secured specimens of six species for the American Museum and may thus claim a speaking acquaintance with four of genera. Yet none save Indicator indicator ever offered to guide me to a beehive. A patient search of books and articles dealing with African birds reveals only one other species, Indicator variegatus of East and South Africa, which according to reliable authority [Ivy, Ibis, 1901. p. 21], renders the same service to mankind. Sir John Kirk [Ibis, 1864, pp. 327-28] seems to have used the name Indicator minor his oft-quoted account through mere accident, this being the only species in the collection upon which he was reporting. His description of the habits is quite clearly based upon I. indicator.

A young honey guide of the genus Indicator, only a few days old.—This drawing was made by W. E. Belanske from a photograph by Dr. Alwin Haagner, director of the Pretoria Zoological Garden. The young bird, the feathers of which are beginning to sprout, was found in the nest hole of a diamond sparrow, Petronia superciliaris; and from the fact that an adult of the scaly-throated honey guide (Indicator variegatus) had previously been seen in the tree, it was inferred that the young bird was also of that species. The extraordinary hooks at the tips of both mandibles may be homologous with the extensive calcareous cap which at first covers the entire tip of the upper mandible of young woodpeckers, although the latter have nothing of the sort on the end of the lower mandible. Doctor Haagner later received a live nestling of the common honey guide (Indicator indicator) almost fully fledged, which still retained both hooks on its beak. After a few days that on the tip of the lower mandible was shed, and the upper one would doubtless soon have followed suit, had the bird survived. The foot was not shown in the photograph, but has been introduced in the drawing from a somewhat older nestling of Indicator in the American Museum collection. Note the roughened heel-pad, which recalls those of young barbets and toucans—neither of them very distant relatives.

It is entirely safe to say that the majority of honey guides do not guide, or at least do not guide men. Nevertheless, I have noted in examining their stomachs in the Congo, as has Mr. G. L. Bates in the Cameroon, that more often than not these other species have swallowed beeswax, just as does the common honey guide, which has hives opened for it by men. Other insects, such as winged termites and perhaps adult bees in the open, are also preyed upon occasionally, but bee comb and bee larvae seem to be preferred. The stomach contents not infrequently smell of honey, and we may suppose that the wax is swallowed incidentally—not by preference.

The one evident exception to these tastes is seen in the genus Prodotiscus, which differs in many respects—the bill and plumage especially—from all the other genera of the family. It does not eat bee larvae, and one of the species frequents, it is said, trees of the genus Sterculia when they are in flower.

How then do the normal honey guides procure their favorite food? The only bees in Africa from which the wax could come are the common honeybee, Apis mellifera (represented by a somewhat smaller African race), and the much smaller species of Trigona, which are stingless. The honeybees, we know, nearly always store their sweets in a secure place,—a cavity in a tree, among rocks, or in the ground, where the birds unaided have little chance of stealing them. The nests of Trigona are usually in hollow trees, and are if anything harder to get at. Had the honey guides the strong chisel-shaped beak of their allies, the woodpeckers, they might hew their way through the wood; but, as it is, they are without any tools for use in such a direct attack. Birds of the genus Melignothes, for example, have an exceptionally blunt beak.

Thus all the typical honey guides eat honeycomb and yet are apparently unable to secure it without help. What else can we conclude save that they adopt some method similar to that reported from South Africa, of enlisting the aid of the honey badger? In the forests of western equatorial Africa this mammal is extremely rare or wanting, and therefore we may only guess that squirrels, small carnivores, lemurs, or monkeys, are the creatures with which the honey guides carry on this commensal existence. This seems a bold assumption, but it is the best explanation I can offer of what we know to be their food habits. An alternative would be to suppose that the honey guides simply happen upon the hives after they have been robbed by some other animal. I doubt if they would get as much plunder in this manner as we know they secure.

It seems credible that the partnership began in such a way, but that sooner or later the birds took to accompanying bee-hunting mammals until finally the bird became the leader. The theoretic bearing of observations on the honey badger and its bird guide is now evident. Once the method had been well worked out with certain lower mammals, man would have been admitted into the association as a matter of course.

The breeding habits of the Indicatoridai are bizarre, and similar to those of the parasitic cuckoos of the Old World or of our North American cowbird. Each white egg is deposited in the nest of some other bird, preferably that of a barbet, which is hewn out like a woodpecker's hole. Where possible, the adult honey guide breaks the legitimate eggs, it is said, and when the young is found, it is always the sole occupant of the nest. In the two species which lead men to hives, Indicator indicator and Indicator variegatus, Dr. Alwin Haagner [Journ. S. Afr. Orn. Union, Vol. III, 1907, p. 3, Pl. 1] has found that the nestling has both upper and lower mandibles armed with a sharp, curved hook, as though for seizing any competitors and ejecting them from the nest it has usurped. It is said that these hooks are shed at about the time of leaving the nest. In two other members of the family, Melignothes conirostris and Melichneutes robustus, I have examined skins of nestlings partly fledged, but found only the usual egg-tooth on the upper mandible.

Adult male of the lyre-tailed honey guide, Melichneutes robustus, drawn by W. E. Belanske from the single individual secured by the American Museum Congo Expedition.—Only three adult specimens and two young are preserved thus far in museums. There is very little difference between the sexes, even in respect to the curious modifications of the tail feathers; and the tail of the young foreshadows clearly that of the adult, though the young in first plumage differs in having the head and breast blackish instead of olive and gray. The feathers here seen extending out beneath the middle of the tail are merely coverts, the true middle tail feathers are somewhat lyrate. If, as the writer suggests, the tail serves as an aeolian sound-producer, the "strings" are placed outside instead of between the arms of the lyre, in the form of narrow, relatively stiff feathers on each side. This specimen was shot by the writer from its perch in the top of a tall tree in the Ituri forest, after he had scrutinized the extraordinary tail through a binocular.

Among the honey guides of the West African forests, from the Cameroon to the upper Congo, there is one with a most unusual development of the tail, Melichneutes robustus. The four middle tail feathers are curved outward at the tip, and the three outermost on each side are greatly narrowed and shortened, reminding one of the outer rectrices of some snipe. This lyrate tail of Melichneutes has been compared to that of the black cock of Europe, but it is the small snipelike feathers that prove most interesting.

In this forest region of the upper Congo one may hear throughout a large portion of the year a reiterated note of tin-horn quality, the double syllables rising slowly in pitch, then dropping off, and repeated from twelve to thirty times. It may be heard afar, certainly at a quarter of a mile, and seems to come from above the forest canopy. The natives I consulted were all ignorant of the common honey guides of the grasslands and could not tell me what kind of bird we were listening to. Some ventured the opinion that it might be a woodpecker; but all were familiar with the sound and had a name for its author, the Azande of the southern border of the Uelle District calling it nyeté in imitation of its voice. From 1910 to 1914 I wondered what the bird could be; and then, on the occasion when I secured my only specimen of Melichneutes, I heard the strange noise given after a second bird of the species had flown off from the same high tree in the forest. It is almost certain that the nyeté is none other than our lyre-tailed honey guide. The “bleating” of certain species of snipe, it has been shown, is produced by their narrowed outer tail feathers during flight, by vibration of the webs as the air passes between them [Bahr, Proc. Zool. Soc. London, 1907, pp- 12-35]. Is it not likely, too, that the nasal, tooting call of Melichneutes is made by the air rushing past the edges of the same feathers? We know that Melichneutes, while perching, emits a hoarse chattering vocal note, which is entirely different. For future field naturalists in equatorial Africa I would suggest a. thorough investigation, though it will be anything but easy. For I suspect that when the life history of this most remarkable of honey guides is more fully known, it will be found that it summons by its curious note some mammalian accomplice to aid it in robbing the hoard of an industrious colony of bees.

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