The evolution, ecology and conservation of honeyguide-human mutualism

This project focuses on a unique mutualism: the foraging partnership between Greater Honeyguides Indicator indicator and human honey-hunters whom they guide to bees’ nests. Honeyguides know where bees’ nests are located and like to eat beeswax; humans know how to subdue the bees using fire, and open nests using axes. By working together, the two species can overcome the bees’ defences, with benefits to both. Remarkably, this relationship has evolved through natural selection, and provides a wonderful opportunity to study the ecology and evolution of mutualisms in nature, because human and honeyguide populations vary strikingly in how they interact, and we can readily manipulate these interactions.

Claire Spottiswoode and her team at the Fitz and the University of Cambridge have been studying human-honeyguide interactions in the Niassa National Reserve of northern Mozambique since 2013, collaborating with the honey-hunting community of Mbamba village, and receiving crucial support from the Mariri Environmental Centre led by Dr Colleen Begg, Keith Begg and Agostinho Jorge of the Niassa Carnivore Project. One key focus has been investigating reciprocal communication between the two parties: not only do honeyguides signal to humans, but in many different cultures, humans signal back to honeyguides, giving special calls to attract honeyguides and maintain their attention while following them. The Yao honey-hunters of northern Mozambique give a loud trill followed by a grunt. A 2016 experiment showed that honeyguides were twice as likely to initiate a cooperative interaction with humans who made this sound compared to humans giving control sounds, and three times as likely to lead such humans to honey.

Supported by a Consolidator Grant from the European Research Council (as well as other grants, including the Cultural Evolution Society Transformation Fund), we now ask whether learning is involved in maintaining a geographical mosaic of honeyguide adaptation to local human cultures; how such reciprocal communication between humans and honeyguides mediates their interactions; what the effects of cultural co-extinctions may be on each partner and their ecosystems; and ultimately, how quickly such cultures can be re-ignited following their loss. In so doing we hope to test whether reciprocal learning can give rise to matching cultural traits between interacting species. Understanding the role of such phenotypic plasticity 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.

Our project, known as ‘Projecto Sego’ (‘sego’ is Greater Honeyguide in the Yao language), has the support of the community and traditional chiefs of the Mbamba and Nkuti Villages. We cooperate closely with the local community to collect data and assist with our field sampling and experiments. We also regularly carry out honeyguide fieldwork in several parts of Tanzania, again in collaboration with local honey-hunting communities, and at field sites in Zambia and South Africa. Since 2022, we have been documenting honey-hunting cultures in over ten countries as part of a Pan-African collaborative effort led by postdoctoral fellow Jessica van der Wal, funded by a Cultural Evolution Society Transformation Grant.

Activities in 2023

• David Lloyd-Jones, Jess Lund and Claire Spottiswoode carried out two successful field trips to our long-term study site at the Niassa Special Reserve in June and Nov-Dec 2023. On the latter trip, they were joined by Rion Cuthill, Lailat Guta and our close collaborator Sally Archibald from Wits
• We welcomed Lailat Guta, a Mozambican agronomist, as a researcher on the project from November 2023 who is working on the effect of honeyguide-human mutualism on pollination services. Lailat will begin her MSc dissertation at the Fitz in 2024.
• Eliupendo Alaitetei Laltaika carried out fieldwork in Tanzania for much of 2023; Claire Spottiswoode and David Lloyd-Jones visited him and his team in the field in the Rungwa region in October to assist with a new field experiment.
• Rion Cuthill (BSc Hons 2021) completed his MPhil dissertation at the University of Cambridge, entitled "The ecological impacts of honey-hunting on fire regimes in the Niassa Special Reserve, Mozambique", from work together with Claire Spottiswoode, Sally Archibald, David Lloyd-Jones, and a large team of honey-hunter collaborators in Mozambique. Rion’s studies were supported by a Skye Foundation Scholarship.
• Wiro-Bless Kamboe successfully completed his CB MSc research project documenting honey-hunting cultures via fieldwork in northern Ghana, supported by Jessica van der Wal’s Cultural Evolution Society Transformation Grant.
• BSc Hons student Daniella Mhangwana joined the project in 2023. Daniella used camera trap data to document the surprising diversity of bird species besides honeyguides that eat and apparently digest wax, and show that these are predicted by a nectarivorous diet (which might attract them to sweet-tasting food). Daniella was supervised by Claire Spottiswoode, Celiwe Ngcamphalala and Jessica van der Wal.
• Our citizen science project, Honeyguiding.me, managed by Jessica van der Wal and Cameron Blair, continues to receive records of Greater Honeyguides, which will enable us to map the changes in the extent of guiding behaviour and help to shed light on how honeyguides acquire their ability to engage with humans (see website: AfricanHoneyguides.com).
• David Lloyd-Jones gave a talk on what honeyguides and honey-hunters have taught us about Niassa’s wild honeybee ecology at the Apimondia Africa Regional Symposium held in Durban. Claire Spottiswoode shared the research team’s findings in a talk at Harvard University (online), at the Carl Friedrich von Siemens Stiftung, Munich, Germany, as well as the plenary talk at the International Bioacoustics Conference, Sapporo, Japan.
• Jessica van der Wal shared her research findings on human-honeyguide cooperation with a talk at the Netherlands Institute of Ecology as well as a guest lecture at Wageningen University.
• Jessica van der Wal launched her new project supported by a grant from the Cultural Evolution Society (CES) Transformation Fund, entitled “A pan-African collaboration to document Africa’s remaining diversity of endangered honey-hunting cultures with honeyguide birds”. This allowed her to grow a collaborative network to document Africa’s remaining diversity of endangered honey-hunting cultures with honeyguide birds. Thank you to the CES for this wonderful support.

Highlights

• At the Niassa Special Reserve in Mozambique, a team of five honey-hunters successfully collected a bee genetic dataset from the bee colonies they harvested, allowing us to tackle questions on the ecology of wild honeybees and how this may be affected by honeyguide-human mutualism. The team also successfully trialled the use of GPS loggers to study honeyguide spatial ecology – a long awaited dream.
• Amana Kilawi graduated with her CB MSc, receiving a distinction for her dissertation entitled “Mutualism between honeyguides, beekeepers and honey-hunters in southern Tanzania”, which revealed some fascinating and unexpected cooperative interactions between honeyguides and beekeepers.
• Jessica van der Wal led a paper together with a large team of collaborators from the honeyguide research and honey-hunting research network, entitled “Do honey badgers and greater honeyguide birds cooperate to access bees’ nests? Ecological evidence and honey-hunteraccounts”, published in Journal of Zoology. Together they reviewed the evidence that honey badgers and honeyguides cooperate to access bees’ nests, drawing from published accounts, their own observations, and 394 interviews with honey-hunters across nine African countries. Overall, the evidence suggests that badgers and honeyguides likely do cooperate in a restricted part of Africa, but substantial uncertainty remains. Potential cooperation between honey badgers and honeyguides may have implications for the origins of our own species’ cooperation with honeyguides and for the ecology and conservation of both honey badgers and honeyguides.
• Dom Cram and other members of the honeyguide research and honey-hunter team published a paper in Proceedings of the Royal Society of London B entitled “Guides and cheats: producer-scrounger dynamics in the honeyguide-human mutualism”. The paper investigates whether cheating honeyguides jeopardise the cooperation between honey-hunters and honeyguides, by investigating which birds guide and which birds cheat, and the pay-offs of these two tactics. Overall, the details of the honeyguide producer-scrounger system we uncovered suggest that it likely strengthens rather than jeopardises honeyguide-human mutualism.
• Claire Spottiswoode, in collaboration with Brian Wood from UCLA, published a paper in Science entitled “Culturally-determined interspecies communication between humans and honeyguides”. The paper showed that Greater Honeyguides learn the distinct calls that honey-hunters in different parts of Africa use to communicate with them, facilitating cooperation between species. Human honey-hunters signal to honeyguides using specialised calls that vary culturally across Africa. Using field experiments in Mozambique and Tanzania, we showed that honeyguides prefer the specialised calls of the local human culture over those of a foreign culture. This implies that honeyguides can adjust to human cultural diversity, increasing the benefits of cooperation for both people and birds. The paper received much media attention internationally, including reports in National Geographic, New Scientist, and radio features on BBC and NPR.
• Jessica van der Wal and Dom Cram, together with Mauricio Cantor from Oregon State University, and assisted by Cameron Blair and Rion Cuthill, organised a hybrid Workshop on Interspecies Cooperation on 6 and 7 July in Cambridge (UK). The workshop was funded by an Interdisciplinary Workshop Grant from the Association for the Study of Animal Behaviour (ASAB), to whom we are most grateful. The workshop was a great success, with a collegial atmosphere, and 27 very interesting talks on different forms of animal-animal and human-animal cooperation, and enlightening round table discussions.

Honey-hunting research network

• George Malembo completed his MSc at Mzuzu University in Malawi, supported by the Nyika Vwaza (UK) Trust research grant and a Society for Conservation Biology Student Research Award, on honey-hunting culture in northern Malawi. He was supervised by Jessica van der Wal, Dr Lusayo Mwabumba and Dr Tiwonge Mzumara-Gawa.
• David Garakva completed his MSc at the University of Ngaoundere in Cameroon, on honey-hunting culture in the Adamawa Region in Cameroon. David’s fieldwork was in part supported by the Cultural Evolution Society Transformation grant, and he was supervised by Jessica van der Wal and Dr Mazi Sanda.
• Wiro-Bless Kamboe successfully passed the coursework for his CB MSc and completed fieldwork for his thesis on human-honeyguide interactions in northern Ghana. His fieldwork was supported by the Cultural Evolution Society Transformation grant. Wiro is supervised by Jessica van der Wal, Claire Spottiswoode and Timothy Aikins Khan.
• Six research assistants (all MSc graduates) joined the Honey-hunting research network to document remaining honey-hunting cultures in their home countries: Rochelle Mphetlhe in Botswana, Faroukou Wabi in Benin, Sanele Nhlabatsi in Eswatini, Samson Zelleke in Ethiopia and Ali Langa in Chad. This is funded by the Cultural Evolution Society Transformation Grant.
• Farisayi Dakwa, Data and Analytics Coordinator of the honey-hunting research network, developed a very useful interactive Excel template and an R Shiny App to aid data entry and visualisation, respectively, for all researchers in the network.

Impact of the project

This project involves rural communities in understanding a unique human-animal relationship. We hope to further our understanding of how mutualisms evolve, and specifically how learnt traits mediating mutualisms may coevolve. Understanding the evolution of mutualisms sheds light on the mechanisms that can maintain cooperation among unrelated individuals. It is also important for effective conservation because mutualisms can have a wide reach in ecological communities. The honeyguide-human mutualism has disappeared from large parts of Africa, as the continent develops. It would be a tragedy if it vanished altogether before we fully understood this part of our own evolutionary history.

Key co-supporters
European Research Council; Cultural Evolution Society; National Geographic Society; Max Planck Institute for Evolutionary Anthropology; DSI-NRF CoE grant; British Ecological Society; Association for the Study of Animal Behaviour; American Ornithological Society.

Research team 2023
Prof. Claire Spottiswoode (FIAO, UCT / U. Cambridge)
Dr Jessica van der Wal (FIAO, UCT)
Dr Susan Miller (FIAO, UCT)
Farisayi Dakwa (FIAO, UCT)
Dr Dominic Cram (U. Cambridge)
Assoc. Prof. Brian Wood (U. California, Los Angeles)
Prof. Sally Archibald (Wits University) Prof. Timm Hoffman (Biological Sciences, UCT)
Dr Colleen Begg (Niassa Carnivore Project)
Keith Begg (Niassa Carnivore Project)
Celestino Dauda (Niassa Carnivore Project)
Dr Yusuf Abdullahi Ahmed (U. Pretoria)
Prof. Robin Crewe (U. Pretoria)
Prof. Christian Pirk (U. Pretoria)
Prof. Robert Fleischer (Smithsonian Institution)
Dr Anne Kandler (Max Planck Institute for Anthropology, Leipzig, Germany)
Dr Laurel Fogarty (Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany)
Dr Mazi Sanda (U. Ngaoundéré, Cameroon)
Dr Celiwe Ngcamphalala (Biological Sciences, UCT)
Dr Timothy Aikins Khan (University for Development Studies, Ghana)
Dr Rodrigue Idohou (Université Nationale d'Agriculture, Benin)
 

Honey-hunting research network: Anap Afan (APLORI, Nigeria); George Malembo (Mzuzu University, Malawi); Sanele Nhlabatsi (Eswatini); Wiro-Bless Kamboe (UCT); Faroukou Wabi (Benin); David Garakva (U. Ngaoundéré, Cameroon); Rochelle Mphetlhe (UCT); Ali Langa (Chad); Samson Zelleke (Ethiopia).

Students: Eliupendo Alaitetei Laltaika (PhD, UCT); David Lloyd-Jones (PhD, UCT); Jess Lund (PhD, U. Cambridge); Rion Cuthill (MPhil, U. Cambridge); Amana Kilawi (CB MSc, UCT); Wiro-Bless Kamboe (CB MSc, UCT); Daniella Mhangwana (BSc Hons, UCT)

Project Sego data collection team: Fatima Balasani, Iahaia Buanachique, Musaji Muamedi, Carvalho Issa Nanguar, Seliano Alberto Rucunua, with data collection by many others.