When wax wanes: competitors for beeswax stabilize rather than jeopardize the honeyguide–human mutualism

Abstract

Many mutualisms are exploited by third-party species, which benefit without providing anything in return. Exploitation can either destabilize or promote mutualisms, via mechanisms that are highly dependent on the ecological context. Here we study a remarkable bird–human mutualism, in which wax-eating greater honeyguides ( Indicator indicator ) guide humans ( Homo sapiens ) to wild bees' nests, in an exchange of knowledge about the location of nests for access to the wax combs inside. We test whether the depletion of wax by mammalian and avian exploiter species either threatens or stabilizes the mutualism. Using camera traps, we monitored feeding visits to wax comb made available following honey harvests. We found that greater honeyguides face competition for wax from conspecifics and nine exploiter species, five of which were not previously known to consume wax. Our results support the hypothesis that heterospecific exploiters stabilize the mutualism, because wax depletion by these competitors probably limits feeding opportunities for conspecific exploiters, favouring the early-arriving individual that guided humans to the bees’ nest. These findings highlight the importance of the ecological context of species interactions and provide further evidence for how mutualisms can persist because of, and not in spite of, exploitation by third-party species.

Guides and cheats: producer–scrounger dynamics in the human–honeyguide mutualism

“…The guiding bird is therefore more likely to have the opportunity to feed on this preferred white wax comb. Furthermore, previous work has shown that the initially abundant beeswax reward can be rapidly depleted by an ecological guild of wax-scavengers including honey badgers ( Mellivora capensis ) and African civets ( Civettictis civetta ) [32]. As a result, scroungers have limited access to the best elements of the food source and risk being deprived altogether, while the producer is typically guaranteed a feeding opportunity (and often on the highest value parts of the resource).…”

“…Consequently, scrounging honeyguides arrive after the human has left and scavenge on beeswax without having invested in locating the bees’ nest and guiding the human [32]. The productivity of the human–honeyguide mutualism, which has significant ecological, economic and cultural importance [29,30,32–34] is therefore strongly influenced by the outcome of the producer–scrounger game among honeyguides. It is not known whether aspects of this game are likely to strengthen the mutualism, or make it vulnerable to human cultural change or prevalent ‘cheating’ by scroungers.…”

Do honey badgers and greater honeyguide birds cooperate to access bees' nests? Ecological evidence and honey‐hunter accounts

“…data), which is supported by research elsewhere (Allen et al., 2018; Begg et al., 2016; Gil‐Sánchez et al., 2020; Skinner & Chimimba, 2005; Wood et al., 2021) and is more common where badgers are not persecuted by humans (Begg & Begg, 2002). Therefore, badgers could encounter diurnal honeyguides during the period that they are most active in guiding humans and eating beeswax (early morning and evening, Lloyd‐Jones et al., 2022; Spottiswoode et al., 2016). Badgers also occur in places where honeyguides commonly guide humans, meaning that where badgers and honeyguides are sympatric, honeyguides know how to guide and could feasibly cooperate with badgers as they do with humans (Fig.…”

“…Honeyguides frequently scavenge on wax made accessible by a human honey‐harvest even if they did not guide a human partner to that bees' nest themselves (Lloyd‐Jones et al., 2022), suggesting that they likely do so at nests opened by badgers. Although honeyguides are very likely to have increased access to wax after a badger opens a bees' nest, the scavenging opportunities might vary depending on how much wax the badger consumes (scavenging badgers frequently consume all the wax revealed by human honey‐harvests; Lloyd‐Jones et al., 2022) and the aggression of the bees (Isack & Reyer, 1989; Short & Horne, 2001).…”

“…Honeyguides frequently scavenge on wax made accessible by a human honey‐harvest even if they did not guide a human partner to that bees' nest themselves (Lloyd‐Jones et al., 2022), suggesting that they likely do so at nests opened by badgers. Although honeyguides are very likely to have increased access to wax after a badger opens a bees' nest, the scavenging opportunities might vary depending on how much wax the badger consumes (scavenging badgers frequently consume all the wax revealed by human honey‐harvests; Lloyd‐Jones et al., 2022) and the aggression of the bees (Isack & Reyer, 1989; Short & Horne, 2001). Although we did not directly ask whether interviewees thought honeyguides benefited from the interaction they saw, 15 honey‐hunters noted that they had seen honeyguides eating beeswax leftovers after a badger had opened a bees' nest, whilst 13 Emaswati interviewees said badgers deplete the entire bees' nest leaving nothing for honeyguides, and 1 Ju/’Hoansi interviewee noted that honeyguides guide badgers without any reward.…”