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How a mutualism evolves: learning, coevolution, and their ecosystem consequences in human-honeyguide interactions

Periodic Reporting for period 3 - Honeyguides-Humans (How a mutualism evolves: learning, coevolution, and their ecosystem consequences in human-honeyguide interactions)

Reporting period: 2020-06-01 to 2021-11-30

Species interactions such as mutualism, parasitism and predation underpin much of life’s diversity. We aim to understand the role of learnt traits in the origin and maintenance of mutually beneficial interactions between species (mutualisms), and to test their evolutionary and ecological consequences. To do so, we are studying a remarkable mutualism: the foraging partnership between an African bird species, the greater honeyguide, and the human honey-hunters whom it guides to bees’ nests. Honeyguides know where bees’ nests are located and like to eat beeswax; humans have the ability to subdue the bees and open the nest, thus exposing beeswax for the honeyguides and honey for the humans. This wild system gives us a wonderful opportunity to study mutualisms, because local human and honeyguide populations vary strikingly in whether and how they interact, and because we can readily manipulate these interactions experimentally. We are doing so in close cooperation with rural honey-hunting communities, particularly in northern Mozambique. Here, and at other locations in south-eastern Africa, we are asking: is learning involved in maintaining a geographical mosaic of honeyguide adaptation to different human cultures? How does reciprocal communication between humans and honeyguides mediate their interactions? What are the effects of cultural co-extinctions on each partner and their ecosystems, and how quickly can such cultures be re-ignited following their loss? In so doing we are testing for the first time the hypothesis that reciprocal learning can give rise to matching cultural traits between interacting species. Understanding the role of such behavioural adaptations is crucial to explain how and why the outcome of species interactions varies in space and time, and to predict how they will respond to a rapidly changing world.
During the first phase of the project, our main milestones have been as follows:

First, we have established a system for the honey-hunting community we work with in northern Mozambique to collect data on their own natural interactions with honeyguides. This has been very successful, with thousands of interactions with honeyguides accurately recorded. We are now using these data to address several of our research objectives.

Second, we have established an individually-marked population of honeyguides at our field site in northern Mozambique, and carried out first field experiments to understand how the mutualism is stable against scrounging honeyguides that do not guide humans.

Finally, we have conducted reciprocal field experiments between honey-hunting communities in Tanzania and Mozambique, to test the hypothesis that honeyguides learn the communication signals of the specific local human culture with whom they cooperate.
This project is allowing us to involve rural communities in understanding a unique human-animal relationship, and in so doing to shed light on the role of learning in the evolution and maintenance of mutually beneficial relationships between species. Understanding the evolution of mutualisms is important because it sheds light on the mechanisms that can maintain cooperation among unrelated individuals. It is also important for effective conservation, because mutualisms can have wide reach in ecological communities. The honeyguide-human relationship is currently dwindling throughout Africa, and before it fades away, we need to understand this ancient part of our own species’ evolutionary history in those few places where it still thrives.