Honeyguides, fire, and human evolution.

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Male Greater Honeyguide (Indicator Indicator).

The control and use of fire is one of the quintessential features of our species out of all the others currently existing on the planet. Exactly when our ancestors learnt to control fire is a matter of some uncertainty. Evidence in the form of hearths reaches back some 400,000 years with some scattered hints of fire being used a few hundred thousand years earlier. Proof of earlier use of fire is difficult to come by which is a problem for Richard Wrangham, primatologist and author of Catching Fire: How Cooking Made Us Human.  Wrangham expounds the theory that our ancestors mastered the use of fire much further back in the past than is currently accepted thereby shaping the evolution of our earliest hominid ancestors, as outlined in a recent interview with Scientific American (Wong 2013).

In search for evidence for early use of fire he has arrived at an unlikely clue, the Greater Honeyguide (Indicator Indicator) and our love of honey, which as can bee seen from the name on the header, happens to be a personal interest of mine. The extraordinary guiding behaviour of this small bird, which I have written about previously, in finding and leading people to wild beehives hidden in the African bush is an instinctive behaviour that must have a long evolutionary history (Isack 1989). As the Honeyguide, contrary to some claims, does not appear to guide any other species this symbiotic behaviour must have developed in the distant past in cooperation with a species now long extinct. The obvious candidate for this species is our own hominid ancestors (Dean 1990).

We humans are not the only animals that have a love for honey. As well as being a prefered food of all human foragers it is also loved by our closest relatives the African great apes. Despite their love through, our ape relatives eat very little honey. Wrangham and his colleagues have studied the honey eating habits of the chimpanzees of the Kanyawara community, Kibale National Park, Uganda finding that less than 1% of their feeding time concerned honey but probably not out of choice. The chimps failed to obtain any honey in 48% of investigations of hives and some of those where they did were old hives with few bees and little honey. Actively defended hives were another matter with the chimpanzees fleeing from the stings of the bees in at least 59% of visits to hives. These chimps would undoubtedly like to eat more honey if it weren’t for the staunch defense by the bees.

In contrast African foragers are never deterred from honey eating by the efforts of the bees. Our ape relatives the chimpanzees lack a crucial tool in the raiding of honey from wild bees that people possess, that is the control of fire. It is the smoke that calms the bees and subdues their aggressive defenses. How long could our ancestors been using smoke to avoid the stings of the bees? This is where we return to the honeyguide. If the guiding behaviour of this bird evolved along with our distant ancestors those ancestors must have had the use of fire or they would have been fleeing the bees like the chimpanzees do now. This argument points very strongly to our distant ancestors having used fire long enough for natural selection to enable this complex innate relationship to develop.

Recent research by Dr Claire Spottiswoode and her colleagues at the University of Cambridge has uncovered some fascinating details about the Honeyguide indicating the age of the species (Spottiswoode 2011). Honeyguides, like the European Cuckoo, lay their egg in the nests of other species and play no part in raising their young. A previously unexplained feature of these birds was that females lay different eggs in different species nests. Some females lay small round eggs in the underground burrows of Little Bee-eaters while others lay large tapered eggs in Green Woodhoopoes nests up in tree holes. Spottiswoode found that these two types of behavior are associat­ed with different mitochondrial DNA lineages and estimated that these diverged an astonishing three million years ago. This indicates that female Greater Honeyguides have consistently parasitised the same host nests as their mother did, without a single successful mistake, for around three million years. However, the species stays as one due to the fact that female honeyguides will mate with males from any nest, keeping the rest of their genes well mixed.

This suggests the Honeyguide has been around for at least three million year, as long as our hominid ancestors have been foraging the lands of Africa. This does not mean that the guiding behaviour is that old is does provide an long period of coexistence for this mutually beneficial relationship to develop and the evidence from chimpanzees indicates that this depended on ancient human wielding fire and smoke. For this behaviour to become so programmed into the DNA of this bird must have required untold aeons of close cooperation between the two species. During this time the Honeyguide has specialised in its joint pursuit with us for honey, being adept at digesting beeswax (Diamond 1988), the bird has access to far more honey in cooperation with humans who have the tools to break into well defended bee hives.

It is perhaps tempting to imagine a group of our early ancestors some two million years ago or more gathered beneath a hive in a hollow tree in the African bush. One stoking a small fire to produce more smoke while others readying their stone hand axes to gather some of the delicious wild honey. On a branch nearby sits a small brown Honeyguide waiting expectantly for its reward of wax for leading its hominid friends to this hidden treasure.

References:
Wong K (2013) The first cookoutScientific American. 309:66-69.
“With our supersized brains and shrunken teeth and guts, we humans are bizarre primates.  Richard Wrangham of Harvard University has long argued that these and other peculiar traits of our kind arose as humans turned to cooking to improve food quality—making it softer and easier to digest and thus a richer source of energy. Humans, unlike any other animal, cannot survive on raw food in the wild, he observes. “We need to have our food cooked.” Based on the anatomy of our fossil forebears, Wrangham thinks that Homo erectus had mastered cooking with fire by 1.8 million years ago. Critics have countered that he lacks evidence to support the claim that cooking enhances digest­ibility and that the oldest known traces of fire are nowhere near as old as his hypothesis predicts. New findings, Wrangham says, lend support to his ideas.”
Spottiswoodea CN, Stryjewskic KF, Quadera S, Colebrook-Robjentd JFR, and Sorenson MD (2011) Ancient host specificity within a single species of brood parasitic bird. Proceedings of the National Academy of Sciences. 108(43):17738–42
“Parasites that exploit multiple hosts often experience diversifying selection for host-specific adaptations. This can result in multiple strains of host specialists coexisting within a single parasitic species. A long-standing conundrum is how such sympatric host races can be maintained within a single parasitic species in the face of interbreeding among conspecifics specializing on different hosts. Striking examples are seen in certain avian brood parasites such as cuckoos, many of which show host-specific differentiation in traits such as host egg mimicry. Exploiting a Zambian egg collection amassed over several decades and supplemented by recent fieldwork, we show that the brood parasitic Greater Honeyguide Indicator indicatorexhibits host-specific differentiation in both egg size and egg shape. Genetic analysis of honeyguide eggs and chicks show that two highly divergent mitochondrial DNA lineages are associated with ground- and tree-nesting hosts, respectively, indicating perfect fidelity to two mutually exclusive sets of host species for millions of years. Despite their age and apparent adaptive diversification, however, these ancient lineages are not cryptic species; a complete lack of differentiation in nuclear genes shows that mating between individuals reared by different hosts is sufficiently frequent to prevent speciation. These results indicate that host specificity is maternally inherited, that host-specific adaptation among conspecifics can be maintained without reproductive isolation, and that host specificity can be remarkably ancient in evolutionary terms.”
Isack H A and Reyer H U. (1989) Honeyguides and Honey Gatherers: Interspecific Communication in a Symbiotic RelationshipScience. Vol. 243, No. 4896, pp. 1343-1346.
“In many parts of Africa, people searching for honey are led to bees’ nests by the greater honeyguide (Indicator indicator Sparrman). The Boran people of Kenya claim that they can deduce the direction and the distance to the nest as well as their own arrival at the nest from the bird’s flight pattern, perching height, and calls. Analyses of the behavior of guiding birds confirmed these claims.”
Dean W R J, Siegfried W R and MacDonald I A W. (1990) The Fallacy, Fact, and Fate of Guiding Behaviour in the Greater Honeyguide. Conservation Biology. Vol. 4, No. 1, pp. 99-101.
“A conventional approach to preserving the earth’s biota involves creating nature reserves in which human activ- ities are excluded, reduced, or otherwise strictly regu- lated. In most African nature reserves, direct utilization of the biota is denied the local people. In this article, we correct a fallacy that has become entrenched in the lit- erature, and use it to propose that certain traditional subsistence activities by humans be retained in some African nature reserves.
One of the most frequently cited examples of so- called coevolved mutualistic behavior between birds and mammals is the association between the Greater Honeyguide, Indicator indicator, and the Honey Badger or Ratel, Mellivora capensis. In this mutualistic associ- ation, the Honeyguide is reputed to guide or lead the Honey Badger to a honey bee nest, where the bird shares the spoils after the mammal has broken open the hive. The description of this association has become firmly entrenched in standard texts on animal behavior, in popular articles, and in many scientific works on birds and mammals, such as the most recent authoritative work on African birds (Fry et al. 1988:502).
Naturalists and biologists have been active in Africa for more than 200 years. During this period, to the best of our knowledge, no biologist or naturalist, amateur or professional, has observed a Greater Honeyguide lead- ing a Honey Badger to a beehive. The primary source of the many published accounts of the association between Greater Honeyguides and Honey Badgers is Sparrman (1785-1786:141-152), who did not personally observe the behavior, but received information on it from local people.”
Diamond AW and A. R. Place AR (1988) Wax digestion by Black-throated Honey-guides Indicator indicator. The International Journal of Avian Science. 130(6):558–61
“The honey-guides (Indicatoridae) are brood parasites and specialist feeders on wax; the larger species obtain wax from bees’ nests and the smaller ones from scale-insects or fruit (Friedmann 1955, Diamond 1985). The ability to digest beeswax has been demonstrated experimentally in only one bird species, the Lesser Honey-guide Indicator minor (Friedmann & Kern 1956a). Here we describe an experiment confirming the same ability in the Black-throated or Greater Honey-guide, 1.indicator, and discuss reasons for questioning Friedmann and Kern’s claim that wax digestion in honey-guides need be accomplished hy symbiotic microorganisms.”
Wrangham RW and Machanda Z (2013) Honey exploitation by chimpanzees and hunter-gatherers indicates an ancient use of fire by humans. The 82nd Annual Meeting of the American Association of Physical Anthropologists.
“Honey is a ubiquitous and preferred food for all African apes and human foragers, often occurring at high density and providing much more food for foragers than for apes. Here we investigate the factors constraining the frequency of honey-eating by chimpanzees Pan troglodytes foraging on honey of stinging bees Apis mellifera. We studied Apis honey-eating over 19 years by chimpanzees of the Kanyawara community, Kibale National Park, Uganda. Honey-eating occurred in a strongly seasonal pattern and occupied less than 1% of feeding time. In 48% of their investigations of hives, chimpanzees obtained no honey. Some visits were to old hives with few bees and little honey, but active hives were strongly defended by bees, responsible for chimpanzees fleeing the hive in at least 59% of visits. We conclude that defense by bees prevented chimpanzees from eating honey at higher rates. By contrast African foragers are never deterred from honey-eating by the activity of Apis defenders, thanks to their use of smoke to control bee aggression. A review of the mutualistic interaction of foragers with greater honeyguides Indicator indicator indicates that honeyguides have an innate propensity to lead humans to honey, that hominids are the most likely species responsible for the evolution of this habit, and that the habit depended on ancient human control of fire.”
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2 Responses to Honeyguides, fire, and human evolution.

  1. John Smith says:

    What conclusions do you reach about the digestibility of beeswax, especially by humans?

    If in fact, the wax is completely indigestible by humans, what other impact might it have on human health: ‘polishing’ the digestive tract, protecting the stomach lining, lubricating the colon, etc.?

    It occurs to me that if beeswax is not supportive of human health, it is the only product of the beehive that is not, which seems to be self contradictory. Certainly as a topical dressing we use it often, but what about when we ingest the wax?

  2. Juan Fontecilla says:

    What about early humans developing some resistance to bee stings? I remember seeing a documentary about Africa where a local human smoked a hive but got stung by several bees without seeming to care much about it.

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