Honeyguides and humans: a wonderful mutualism between our species and a wild bird

July 22, 2016 • 12:31 pm

The story of our relationship with the Greater Honeyguide, which has the fantastic species name of Indicator indicator, is well known. The BBC had a segment on it, which is where I learned the story. And the story is this: people in Mozambique and Tanzania use honey as an important part of their diet, but the beehives, hidden in trees, are hard to find. Enter the Honeyguide, a bird that has the ability to find the nests. This has led, over God knows how many years, to a mutualism between bird and humans. The birds let humans know they’re around by chirping. The honey-hunting humans then make a special bird-summoning sound (in the case of the Yao people, the “brrr-hmm” call you can hear in the video below, but the Hadza people of Tanzania use a different “whistle” call), and that attracts the birds, which then lead the humans to a bees’ nest. As the birds fly ahead, the humans keep making that call, which keeps them aligned with the birds. Finally, the bird stops in the nest area, and, more often than not, the humans find the nest, extracting the honey and most of the honeycomb. The humans leave behind wax (and perhaps some honey) for the birds, which consume it.

So we have here a true mutualism, a wonderful alliance of bird and human that benefits each one. My question, when I first heard the tale, was also asked by a group of biologists: Is is this story true? That is, you can see humans following birds to the bees’ nests, and you can see the humans making calls, but do the human calls—the specific whistle or “brrrr-hmm” they make—really serve to attract the birds and keep them guiding? And are the birds accurate in leading humans to the nests? Finally, are the Honeyguides really leading humans, or are the humans just following a bird, parasitizing its own ability to find a nest?

The classical story does seem accurate, as without humans the birds have no way of getting either wax or honey. They can’t attack bees’ nests on their own. Further, the birds do seem to come to human calls, and no other species has been recorded following the birds. But the scientists wanted to know more; and this has produced a new paper in Science by Claire Spottiswoode, Keith Begg, and Colleen Begg (free link and reference at bottom). It turns out that the story is indeed true.

The video below, produced to accompany the paper, really gives all the salient details, but I’ll add a few more after you watch it:

The authors had two questions:

1). Does the guiding behavior give reliable information to humans about where the bees are?  The answer is yes: 75.3% of guiding events led to successful location of a bees’ nest (the bee, by the way, is almost always Apis mellifera, the common honey bee).  The average distance of a following event was 152 meters from when the bird showed up, and about 75% of nests found by humans involved following a bird.

The authors also used a GPS to track the direction of a bird’s initial travel to see how accurately it showed where the nest was. On the right part of the figure below, you can see that the birds are damn good; on average, their initial direction of flight was only 1.7° away from the true direction of the nest. Those birds know where the nests are!

Fig. 1 Greater honeyguides accurately lead humans to bees’ nests. (A) A Yao honey-hunter and a wild, free-living honeyguide. (This bird was captured using a researcher’s mist-net and is neither tame nor habitually captive.) (B) Accuracy of honeyguide initial guiding behavior in relation to direction of successfully located bees’ nests. Points represent the difference in bearing between initial guiding trajectory over the first 40 m of travel and the ultimate direction of the bees’ nest (here set at 0) and are binned into 5° intervals. Each point represents a journey (n = 58 journeys) to a separate bees’ nest that was at least 80 m away from the point where guiding began. Sometimes a honeyguide led humans to more than one nest consecutively (n = 50 guiding events). The circular distribution is unimodal (Rayleigh test, P < 0.001) with a mean of 1.7° (95% confidence interval includes zero: 352.3° to 11.1°), showing that honeyguide behavior offers reliable directional information to humans.

2). Does the specific human call really incite the birds to guide the people to bees’ nests?  Again the answer is “yes.” The researchers did an experiment in which they recorded three types of calls by the Yao. These included the normal “brrrr-hmmm” call, a control “human sound” call which was the Yao word for “honeyguide,” “honey,” or the caller’s name (alternated), and an excitement call of a ring-necked dove, serving as an animal-call control. These recordings were then played back on 72 forays into the field. The results were clear, and are shown in the figure below.

On the left side (A), you see the probability of being guided by a honeyguide when different calls were played. The “brrrr-hmmm” call, the one used in everyday life, elicited a guiding attempt 66.7% of the time, as opposed to only 25% or 33.3% of the time when human-sound or dove-sound calls were used, respectively. (The difference between the results of traditional versus other two calls was significant, as shown by the p = 0.003 notation.) When the traditional call was interrupted by playing the other two calls, the authors report that the honeybirds “ceased guiding.” They’re clearly listening to the brrr-hmmm to keep them heading toward the nest.

On the right side (B), you see the same comparison for whether the birds successfully led humans to a nest after they had been following it (the time for finding was limited to 15 minutes after arrival at the general area). And again, the recorded brrr-hmmm call led to finding a nest 54.2% of the time, as opposed to only 16.7% for each of the other two recorded calls, another highly significant difference. Clearly, the traditional call is better at inciting birds to guide.

Fig. 2 Probability of a successful mutualistic interaction, in relation to experimentally given acoustic cues. Values are predicted probabilities of (A) being guided by a honeyguide and (B) being shown a bees’ nest on a 15-min search, derived from a logistic model of data from experimental transects and accounting for time of day (minutes from sunrise to sunset). Boxes show medians and quartiles; whiskers show ranges (n = 24 trials per treatment group; P values show planned comparisons; n.s., not significant).

One potential problem: maybe the birds simply are more likely to hear the traditional call than the other two calls, but don’t recognize the traditional call as a specific call saying “please guide me.” To test this, the authors showed that the amplitude of the call—its “hearability” had no effect on either the probability of being guided or being “shown” a bees’ nest.

The mutualism between a wild animal and humans is almost unique, for the authors note only one comparable situation:

These results show that a wild animal correctly attaches meaning and responds appropriately to a human signal of recruitment toward cooperative foraging, a behavior previously associated with only domestic animals, such as dogs. Although humans use many species as foraging partners, including falcons, dogs, and cormorants, these involve trained or domesticated individuals that are specifically taught to cooperate. The honeyguide-human relationship is notable in that it involves free-living wild animals whose interactions with humans have probably evolved through natural selection. To our knowledge, the only comparable relationship involves cooperation between artisanal fishermen and free-living dolphins. Several reports exist of men “calling” dolphins to hunt, starting with Pliny the Elder around 70 CE . Whether this reflects a similarly specialized communication system to that mediating the honeyguide-human mutualism in Mozambique remains unknown.

The question that interests me now is this: How did it evolve, and is the behavior on the part of the birds genetically-hard wired, learned (from either other birds or their own experience), or a combination of both? It’s relevant here that Greater Honeyguides are nest parasites: parents lay their eggs in the nests of other species, who raise them, and so parents never interact with their young. (This is what the cuckoo does.) That means that if learning is involved, the birds can’t be learning the human call from their parents.  The authors float the idea that the recognition is innate, but then point out that in Tanzania the honeyguides respond to a different call. That’s unlikely to be a different genetic adaptation, they say, because there’s no evidence of genetic structure for other loci across the range.  They conclude that recognition of the call is learned, perhaps from other adults in the area. This would imply that they watch other birds and, seeing the reward for the behavior, copy them. This copying could include the initial call that the birds make, alerting humans to their presence.

There is, however, another possibility: the birds are hard-wired for the ability to learn a human call, but the specific call they learn is provided by the local people. This may be the case, for instance, in human language. Some think that we’re “hard wired” to acquire language (we start babbling syllables as infants, and are more attuned to speech sounds than to non-speech sounds), but the specific language we learn is determined by our local culture.  The way to determine this, in the case of the honeyguides, is to somehow hand-rear the babies and then see if, when released, they spontaneously recognize the “brrr-hmmm” or “whistle” call, or can be trained to lead when hearing either call before they’ve seen other birds. (It’s still possible that there’s genetically distinct recognition in different areas, but that other genes don’t show the same kind of geographic differentiation).

Even if the behavior is learned, that leaves one more question: How did this system get started? Your guess is as good as mine, and the authors don’t talk about this.  Given that birds can’t acquire honey or wax on their own, it probably started when birds saw humans find a bees’ nest, and those humans left behind some edible remnants of the nest. The birds would then start following the hunters around, and could even go to the bees’ nest anticipating where the hunters were going. The hunters could then use the birds’ behavior as a way of locating the nest (birds are better at finding nests than are humans), and could start calling to the birds. That would alert the birds to the presence of humans, and thus to a treat.  That scenario implies that even if recognizing a specific human call isn’t hard-wired, perhaps the leading behavior could have evolved, for there is obvious reproductive benefit (by way of more food) to leading humans. The video above suggests that this relationship could have existed for thousands of years or more, which is ample time for some evolution to have occurred in the bird.

But however this evolved, I find it ineffably touching. Look at the picture of the Yao man and the bird above. They help each other out, and, of course, the Yao always leave some food behind for the bird. That’s not just kindness: it’s a necessity if this behavior is to remain stable. Still, it’s hard not to think that the Yao bear some sort of affection for the birds, and maybe there’s just a wee bit of bonding on the bird’s part. Ain’t nature wonderful?

But just to show this isn’t all beer and skittles, nest parasites like the Greater Honeyguide, when raised by a ‘foster species,’ will kill all the chicks of their stepparents so they get all the attention (cuckoos and other nest parasites do that, too). Here, from the Weird Birds site, is a Greater Honeyguide killing off its unrelated nestmates: Greater Honeyguide

Now, about those fishing dolphins. . .

h/t: Kevin


Spottiswoode, C. N., K. S. Begg, and C. M. Begg. 2016. Reciprocal signaling in honeyguide-human mutualism. Science 353:387-389.

50 thoughts on “Honeyguides and humans: a wonderful mutualism between our species and a wild bird

  1. Fascinating. Now, I’m wondering how far back this mutualism goes? 10,000 years – the dawn of agriculture? 100,000 years – early human ancestors? 500,000 years Homo erectus? The longer in the past, the more chance for genetic changes.

    1. The part of the video I found most amazing is where the men are opening a bee hive while shirtless! These are not just any old honey bees as Jerry’s account might suggest, but the hyper-aggressive African subspecies which when crossed with the “Italian” bee in South America gave rise to “our” killer bees. The video suggests that judicious use of smoke and other techniques have permitted efficient harvest of honey without much inconvenience even to someone wearing only shorts! The human control of fire seems to have become ubiquitous approximately 50,000 – 100,000 years ago. This could place some kind of time limit on human exploitation of bee hives and the beginning of the honey-guide X human mutualism.

      1. I think that was what I was looking for as evidence. I was not thinking of the use of smoke when I wondered about a possible age.
        Now I wonder if honey might not have led some groups of hominids to the use of fire. They would have noticed that while a forest fire was still smoldering, bees were docile. Perhaps they put two and two together.

      1. Yes, re-reading, you clearly implied it, but did not specifically spell out that we are the only ones. I was indeed ‘guided’ (:)) by these stories of honey badgers (‘ratels’ as they are called here)being ‘guided’ too.
        I don’t know which I find more fascinating, humans as the only species, or ratels and humans sharing being the servants of the honeyguides. ‘Ineffably touching’ at any rate.
        Also the fact of them being nest parasites adds -as you point out- to the fascination.

        1. The consensus seems to be that the birds do recognize the ratel as bee-nest predators, but don’t seem to have this sort of mutualistic communication. Perhaps the badgers are just dense..

  2. Especially interesting that it is nest-parasite birds involved, when you would have thought that they would be the least likely sort of bird to do this sort of thing.

  3. Wow. The nest killing is especially noteworthy. Raised as very capable orphans I suppose…like 007s, an evolutionary license to kill.

      1. Yes, creationists could use this example of a blind nestling killing other blind nestlings as an illustration how great and benevolent the Intelligent Designer is (sarcasm).

  4. “Ain’t nature wonderful?” — This line made me smile, and the post incited curiosity in me.

    I could visualize the birds anticipating that the humans wanted a nest and going to the nest in anticipation.

    (Incidentally, the cat that has adopted me has similar behaviors. He’s started to anticipate when I’ll awake. I leave my door open at night so that he can come and go. He used to arrive in the middle of the night. Now he comes at 6 am, when I’ll actually get up. I can’t prove it, but I think he’s learned that he can anticipate food near that time but not earlier. This morning he jumped on my back, and when I wasn’t detoured from bed he pilfered my garbage. I got up due to the ruckus. So, he’s training me.)

    1. I always think it’s funny when dog people say dogs are smarter because they’re so easy to train. I always answer that cats are smarter because they train us.

  5. This is a very interesting subject that I had heard about from time to time, but did not know if it were likely true.

  6. I too saw it on The BBC or some show like that. Fascinating. Animals are so wonderful. I don’t remember for sure, but I think it might have been ‎David Attenbrough.

  7. See The Genius of Birds by Jennifer Ackerman. Many kinds of birds are far smarter than most people realize.

  8. Great post. I wonder how much the successful nest-guiding can vary from person to person within the group. Clearly some people are better hunters, fishers, farmers, so perhaps there are people who are better at calling the birds. and if so, what do they do differently. Overall, though, it’s not thaw surprising really. If humans refrain from slaughtering every living thing around them, there’s certainly more of a chance for these types of interactions. Crows and Ravens for example (I’m sure Berndt Heinrich has discussed something like this but can’t recall exactly). And why not? If a variety of oceanic fishes, shrimps, and turtles can establish cleaning stations, or crocodilians and bird… and it just occurred to me, how does this fit, if at all, into the theory of mind?

    and you gotta love that scientific name: Indicator indicator

    1. oops, I mean Bernd Heinrich! i’ve read all his books, I should be able to spell his name by now.

  9. “This would imply that they watch other birds and, seeing the reward for the behavior, copy them. This copying could include the initial call that the birds make, alerting humans to their presence.”

    I think this is it. The Cardinals that visit my window each morning now give a very loud chirp (contact call) if there is no seed. Loud enough for me to get out of bed to put some seed out (they always come at daybreak). I believe I have habituated them to this behavior. Now, some House Finches have caught on and come when they hear the Cardinals chirp. Birds are remarkably observant animals.

  10. I too have had cardinals that requested food. This spring wrens built a nest in my pot of flowers. They would squawk loudly when my neighbor’s cat came around and wouldn’t stop till I opened the door and sent the cat home. Both of these birds had me well trained.

      1. In the short term it makes sense for the Hadza to keep the honeyguide hungry. A sated honeyguide is expected to be unresponsive to the call to work.

        In the long term it seems that consistently depriving the honeyguide would surely lead to eventual extinction of the guiding behavior.

  11. I was using a device without a proper keyboard when commenting with the hadza-and-honeyguide link and so was terse.

    The article writes that the hadza make a point of not sharing with the the bird to the point of destroying any comb they do not themselves use. So why does the bird bother?

    Perhaps it developed the behavior with more generous partners like the Yao?

    1. The article you posted was most informative. I especially liked the 1907 comments on “Nature Faking” by Theodore Roosevelt and the practice setting up false narratives in nature films, in particular the lemming suicide fakery in Walt Disney’s 1958 “White Wilderness”.
      Reading this made me remember a copy of Roosevelt’s (1909)”African Game Trails” (vol. 2, only)at hand, where I found a long paragraph on “honey birds”,
      Before leaving for Africa, Roosevelt writes, a friend “had especially charged me to look personally into this extraordinary habit of the honey bird; a habit so extraordinary that he was inclined to disbelieve the reality of its existence. But it unquestionably does exist. Every experienced hunter and every native who lives in the wilderness has again and again been an eyewitness of it. Kermit [Roosevelt’s son] . . . had been led by a honey bird to honey in a rock, near Lake Hannington. . . . On the morning of the day we reached the ‘Nzoi, a honey bird appeared beside the safari, behaving in the same manner [i.e., the bird ‘made his appearance, chattering loudly and flying beside us’]. Some of the men begged to be allowed to follow it; while they were talking to me the honey bird flew to a big tree fifty yards off, and called loudly as it flitted to and fro in the branches; and sure enough there was honey in the tree. I let some of the men stay to get the honey; but they found little except comb filled with grubs. Some of this was put aside for the bird, which ate the grubs. The natives believe that misfortune will follow any failure on their part to leave the honey bird its share of the booty. They also insist [and is it true?] that sometimes the honey bird will lead a man to a serpent or wild beast; and sure enough Dr. Mearns was once thus led up to a rhinoceros. While camped on the “Nzoi the honey birds were almost a nuisance . . . Several times we followed birds, which in each case led us to bee trees, and then perched quietly by until the gun-beares and porters . . . got out the honey — we found excellent eating by the way.”

  12. One more remarkable thing about the honey guides is that the entire family [20 or so species] seems metabolically adapted to feeding on waxes.

    I had always assumed that “they eat the honeycombs” meant “they eat honey — and bee larvae”. No — they can digest the long aliphatic chains of beeswax, though they must consume larvae as a nitrogen source.

    And to deepity the evolution, it appears the whole family Indicatoridae feed on insect waxes. Not just honeybees but also wax-producing moth larvae, and homoptera of the scale/mealybug/lac group. I’d guess that the waxy homoptera were the entry point for the indicators moving from insectivory to a preference for waxes.

    1. Very good point! Or it could be that feeding on honey assured that some wax was always ingested. In bad times, with little honey or few grubs in the combs, being able to digest the incidentally ingested wax could be decisive.

  13. After learning of the parasitic behaviour, that is, the use of an unrelated species for rearing of young, it occurred that perhaps the Honeyguide has a ‘natural’ incline given the opportunity, to ‘use’ other species for a food source as well. A genetic predisposition for learning the behaviour.
    Bit of a stretch but it has a intuitive feel about it.

  14. I have been ‘guided’ by a Honeyguide in Botswana and it did lead us to a bees nest although we didn’t call it or uphold our side of the bargain by opening up the nest. It was an amazing experience.
    ‘The Birds of Africa’ (Fry et al, 1988. vol III, Academic Press) states that the Greater Honeyguide Indicator indicator “guides humans and ratel (possibly baboons, genets, mongooses)”. It also comments that the congeneric Scaly-throated Honeyguide, Indicator variegatus “…reportedly guides humans and ratels to [bee hives]” but goes on to suggest that the species’ otherwise secretive habits make this unlikely or rare.
    As Loren Russell comments above, all the honeyguide species feed on comb and so all likely benefit from other species, including humans, breaking open hives (much like gulls and other birds profit from the exposure of soil invertbrates by the plough). The Greater Honeyguide has taken the next step of pointing out the location of hives to the other species.

    Nick Davies’ wonderful book “Cuckoo – Cheating by Nature” gives an account of Claire Spottiswoode’s work on the nest parasitic behaviour of Lesser Honeyguides Indicator minor.

  15. Let’s face it. We have no idea how animals inherit their infinitely complex behaviours. Although there are constant references to this or that behaviour being “hard wired” genetically, there is hardly any proof of it. We simply assume that because we know that physical characteristics are heritable by genetics, everything else must be as well. It seems to me possible in this instance that the honey guides are simply born with this knowledge in the same way that it has been shown that newly hatched goslings can tell the difference between a bird which is a threat (such as a hawk) and one that isn’t (such as a pigeon).

    1. “It seems to me possible in this instance that the honey guides are simply born with this knowledge in the same way that it has been shown that newly hatched goslings can tell the difference between a bird which is a threat (such as a hawk) and one that isn’t (such as a pigeon).”

      Isn’t that just another way of saying they inherited it?

      1. That is what I am saying. The point is that nobody seems to know how but simply assumes that it is genetically, for which there is no evidence.

  16. Very interesting!

    Did I miss it – what is the mechanism for the bird to learn the honey location?

    1. Just guessing, but the birds can presumably follow the bees in flight over longer distances than humans can.

  17. Ravens are said to lead wolves to suitable prey, then make off with big chunks of the kill. It appears similar on the surface, though the wolves in the video seem resentful.

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