Introduction
Mutualistic species partnerships are not always beneficial to both partners all the time (Bronstein 2001). One partner may fail to provide the reward that the other expects (Clutton-Brock and Parker 1995), causing the costs of engaging in mutualistic behavior to outweigh its benefits (Riehl and Frederickson 2016). Across sub-Saharan Africa, greater honeyguide birds (hereafter “honeyguides”) guide humans to bees' nests, exchanging their knowledge of the locations of bees' nests for a food reward (beeswax) resulting from human honey hunters' abilities to subdue bees with smoke and open their nests using axes (Friedmann 1955; Isack and Reyer 1989). In this mutualism, one partner occasionally fails to do their part: humans may fail to harvest the nest or reward the bird, and a guiding honeyguide sometimes fails to show a human a bees' nest (Isack 1987; Spottiswoode et al. 2016; Wood et al. 2014). The latter can occur when a honeyguide prematurely stops guiding before any destination is reached. However, according to centuries of African Indigenous accounts (Figure 1), failure to find bees can also occur when a honeyguide deliberately guides humans to an animal dangerous to humans, such as a lion, buffalo, elephant, rhino, large venomous snake, or occasionally a carcass (Friedmann 1955; Isack 1987).
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The first account in scientific literature of honeyguides guiding humans to such nonbee species dates from 1776 when Khoe-Sān honey hunters in the Western Cape of South Africa recounted being occasionally guided to “dangerous animals” (Sparrman 1777). Seventy-nine years later, David Livingstone attempted to evaluate the frequency of such behavior by asking East African honey hunters whether they had been guided by a honeyguide to anything but a bees' nest and reported that “Only one out of the 114 could recall that he had had such an experience although all had been guided on a great many occasions” (Livingstone 1858). Later, in his landmark study of honeyguides in Kenya, Hussein Isack reported that “A common belief that the Boran share with several other communities in Africa is that the bird often guides man to animals such as lions, buffalos, elephants, rhinos, large poisonous snakes or to enemies or murderers from a hostile tribe… It is believed that the bird resorts to this abnormal behavior as a result of man's failure to spare some food for it after the bird had helped him discover a [bee] colony” (Isack 1987).
Unfortunately, few published accounts of guiding to nonbee animals across Africa include first-hand observations, and the ability of honeyguides to deliberately guide to nonbee species has typically been treated with skepticism by both ornithologists (Friedmann 1955; Short and Horne 2001) and by some honey hunters (Isack 1987). Such skepticism is understandable given the temptation of observers to attribute incidental encounters with such animals as deliberate on the part of the honeyguide. It is nonetheless striking that reports of this phenomenon are widespread across Africa (Figure 1) (Isack 1999).
If honeyguides deliberately guide people to nonbee animals, it is not known why such behavior would occur and whether it is adaptive. Human cultural interpretations for such a behavior vary culturally across Africa (Appendix 4), with the most influential interpretation being that honeyguides do so to punish a person for prior failure to reward them with beeswax following a honey harvest (Carr 1969; da Sorrento 1744; Friedmann 1955; Ionides 1965; Isack 1987). This has, to our knowledge, only been documented from four honey-hunting cultures (Figure 1), but strongly appeals to the human imagination and is widely repeated. Evidence for punishment between heterospecifics, where one partner sacrifices payoffs from interaction to harm a cheating partner, has rarely been observed among nonhuman animals (Jensen 2010; Raihani and Bshary 2019; Raihani et al. 2012), yet is known from client-cleaner fish mutualisms (Bshary and Grutter 2005).
In contrast, some honey-hunting cultures (including the Yao culture which is the focus of the present study) believe that when honeyguides guide a human to animals other than bees, the honeyguide is acting altruistically by warning a human of a danger nearby (Gruber 2018; D.J.L, M.M., and C.N.S unpubl. data). Meanwhile, other cultures do not provide a clear functional interpretation for this behavior and accept that “bad honeyguides” rarely yet deliberately guide people to animals other than bees (Isack 1999). Some writers dismiss the idea that honeyguides guiding to dangerous animals or other objects is intentional and instead consider these encounters to be chance events en route to a bees' nest (Friedmann 1955; Short and Horne 2001). Across a wide variety of accounts, what remains consistent is the reported infrequency of honeyguides guiding to nonbee animals, even in areas where honeyguide-human cooperation is common (e.g., Isack 1987; Livingstone 1858). Infrequent observations of an apparently rare behavior would also have likely reduced further as human-honeyguide cooperation has diminished across the African continent (Isack 1999; van der Wal et al. 2022a).
In this study, we present recent quantitative data from interactions in Mozambique between Yao honey hunters and honeyguides, which corroborate historical accounts that honeyguides deliberately guide humans to nonbee animals. We review five biological hypotheses (Table 1), some of which draw on human cultural explanations for why honeyguides may guide to nonbee animals, and generate testable predictions for each. Finally, prompted by the perspectives of Yao honey hunters and our firsthand observations, we use additional field data to retrospectively evaluate certain predictions of each hypothesis.
TABLE 1 Five hypotheses, with associated predictions, for why honeyguides guide humans to the location of nonbee animals.
| Predictions | Hypotheses | ||||
| (i) Incidental encounter | (ii) Punishment | (iii) Warning | (iv) Mobbing | (v) Spatial recall error | |
| Honeyguides stop guiding at nonbee animals, like at bees | − | + | + | + | + |
| Guiding to nonbee animals tends to occur after a nonrewarded interaction | na | + | − | na | na |
| Nonbee animal is dangerous to humans | na | + | + | na | na |
| Nonbee animal is dangerous to honeyguides | na | na | na | + | na |
| Honeyguides slow down and stop when arriving at nonbee animals, like at bees | − | + | + | + | + |
| Honeyguides make the same calls when arriving at nonbee animals, as they do at bees | − | + | + | ? | + |
| Honeyguides mob the species to which they guide humans | na | na | na | + | na |
| Nonbee animal is alive | na | + | + | + | na |
| Nonbee animal is spatially predictable (i.e., immobile, or returns to the same location at predictable times) | − | + | + | + | + |
Material and Methods
Study Site
This study was conducted in a 280 km2 area within the Niassa Special Reserve in northern Mozambique (Lloyd-Jones et al. 2022; Spottiswoode et al. 2016). This area is inhabited and utilized by honey hunters of the Yao ethnic group who live in Mbamba village (12°12’S, 38°01′ E), which has a population of ca. 2000 inhabitants, including > 20 professional honey hunters (Lloyd-Jones et al. 2022). In this miombo woodland area, honeyguide–human interactions occur daily under conditions likely comparable to those under which the mutualism evolved (see Cram et al. 2023; Lloyd-Jones et al. 2022; Spottiswoode et al. 2016 for further details of the study system). Yao honey hunters consistently reward honeyguides with beeswax of a varying amount following a harvest (Lloyd-Jones et al. 2022), although the act of harvesting a bees' nest can also enable a honeyguide to benefit from wax via access to the tree cavity containing leftover beeswax. Yao honey hunters do not reward honeyguides when they are guided to a bees' nest that they do not harvest. This rewarding behavior of Yao honey hunters is directly linked to a belief that failure to do so results in honeyguides being less cooperative in the future, both by guiding to fewer bees' nests and by guiding to other dangerous animals instead.
Data Collection
Given that guiding to nonbee animals appears to be rare, it was not possible to design a study specifically documenting it. Rather, we collected data opportunistically during other studies and experiments with honeyguides.
Four datasets are used here. First, four first-hand accounts of honeyguides guiding honey hunters to nonbee animals were recorded in 2018 from separate honey hunts under natural conditions and included visual, spatial, and in some cases, acoustic data. We used these data to describe our direct observations of honeyguides guiding to nonbee animals. Second, 108 records of honey hunts (defined as a single human-honeyguide interaction with a unique starting point) between January 28 and December 22, 2018. We used these data to calculate overall rates of guiding to bees' nests compared to nonbee animals. Third, we used a subset of 24 honey hunts (from the 108 honey hunts) for which we have complete GPS tracks of guiding interactions, and a further subset of 22 honey hunts with audio recordings of honeyguide vocalizations, recorded between May 18 and June 27, 2018. Twenty of these honey hunts ended with the honey hunter finding bees, and four ended with the honey hunter finding an animal other than bees. We used the 24 GPS tracks to analyze spatial movement patterns and used the 22 audio recordings to analyze honeyguide vocalizations while guiding. Some of these honey hunts were recorded on the same day (mean number of honey hunts per day ± SE = 1.71 ± 0.29, n = 24), but when this was the case, the starting points were < 1500 m apart, making it likely that different honeyguide individuals were involved. In the last dataset, we selected 28 honey hunts that occurred in close (< 1500 m) proximity to each other within a 7-day period. We used these interactions to calculate rates of honeyguide behavior in relation to prior rewarding behavior by humans (i.e., provision of beeswax) by humans.
Although we have conducted research at this site since 2013, we only analyzed data from 2018, given that all our observations of being guided to nonbee animals were made in this year, and we wanted to ensure that environmental conditions were comparable for guiding events with different outcomes.
To initially locate the bees' nests, one researcher (D.J.L or C.N.S) accompanied two Yao honey hunters (one of whom is a coauthor: M.M) on a honey hunt as they elicited guiding behavior from greater honeyguides using culturally determined, locally specialized calls, given either naturally or using controlled speaker playbacks (repeated loops of either the locally specialized call or, as a control treatment, a human calling his name) as part of behavioral experiments following methods in Spottiswoode et al. (2016). Honey hunts involving such playbacks contributed one of the four instances of guiding to dangerous animals, and six of the 28 guiding events contributed to our post hoc analyses of whether nonrewarding behavior by honey hunters is more likely to precede being guided to nonbee animals. In these seven instances, the playback was either a repeated loop of a human calling their name (n = 3), used as a control sound, or a specialized “brrr-hmm” sound (n = 4). All honey hunts began at intervals along vehicle tracks at least 500 m apart, and at least 1500 m apart when conducted on the same day, to reduce the confounding effect of prior interactions with honeyguides.
For spatial analyses of guiding behavior to bees' nests or nonbee animals, we use GPS tracks of 24 guiding events (points recorded at set 1 s intervals using Garmin eTrex 30, Garmin USA), which all involved natural honey hunter calls to honeyguides, except one guiding event to a puffadder which was accompanied by control playbacks (described above). The final destinations of all guiding events (whether bees' nests or other animals) were previously unknown to us or the honey hunters.
For audio analyses of honeyguide calls, we used stereo audio tracks recorded on 22 of these events (two of which involved guiding to nonbee animals) by D.J.L, using a unidirectional Sennheiser ME66 (Sennheiser Inc., Wennebostel, Germany) microphone recording to a Sony PCM-M10 (Sony Group Corporation, Tokyo, Japan), continuously aimed at the honeyguide. Acoustic recordings began prior to guiding and continued until the bees were located. All audio tracks were saved as Linear PCM (WAV) files at 96.00 kHz/24 bit and were reviewed, clipped to length, and normalized to −3.0 dB using Audacity version 3.0.5 (Audacity Team 2022). Raven Pro v. 1.6.1 (Center for Conservation Bioacoustics Cornell 2019) was then used to display sounds as spectrograms, from which we manually selected bounding boxes for individual syllables from within “chatter” (Audio 1) and “indication” (Audio 2) call types (Isack 1987). Following Isack (1987), we distinguished between typical “chatter” calls given by honeyguides while guiding and “indication” calls, which are also sometimes given while guiding but characteristically given as the honeyguide approaches the bees' nest, prior to going silent (Appendix 3, Figure A2).
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Data Analyses
We tested whether honeyguides were more likely to guide humans to nonbee animals after not being rewarded by humans (i.e., when a human follows a honeyguide to a bees' nest but does not harvest; Figure 4) by focusing on 11 honey hunts that had been preceded by two or more prior honey hunts within 1500 m or less, within the previous 7 days. In total, there were 28 prior honey hunts (two were counted twice, due to their proximity in different directions to two different harvests). For each of the 11 focal honey hunts, we calculated the proportion of prior honey hunts which resulted in a bees' nest harvest and consequently a wax reward versus finding a bees' nest but choosing not to harvest (Figure 4). We next compared the proportion of prior rewards for focal honey hunts that involved being guided to nonbee animals (4 of the 11 focal honey hunts), versus honey hunts that involved being guided to bees' nests (7 of the 11 focal honey hunts). We ran a generalized linear model (GLM) with a binomial logit link function to test the effect of prior reward rates on the binary outcome of being guided to a bees' nest or to nonbee animals. We visualized residuals and plotted them against fitted values to assess model assumptions, which indicated no severe deviations from linearity on the logit scale, no strong outliers, and approximate homoscedasticity.
We selected the < 1500 m and 7-day limits for the above dataset under the assumption that repeated interactions with the same individual honeyguide were possible within such limits, although it is plausible that many honeyguides could have been involved in prior interactions, given high honeyguide densities at this site (Cram et al. 2023). This represents an imperfect best attempt at detecting a relationship between past rewarding behavior and guiding to nonbees, with the parameter values supported by past work at this location showing that honeyguides can move over an area with a radius of at least 1500 m over short time periods (Spottiswoode et al. 2016).
Three measures of human movement were extracted from GPS tracks of honey hunters following honeyguides: distance guided, speed, and sinuosity. For distance guided, start points were determined from the simultaneous audio recordings as to where the honeyguide arrived and first “chattered” to the human, and stop points as to where the honeyguide reached either a bees' nest or a nonbee animal. Speed was measured from the GPS track of the honey hunter carrying a GPS. The sinuosity of human movement was the ratio of actual distance traveled to the distance of the shortest as-the-crow-flies path, measured using GPS tracks (Wood et al. 2021).
We used R v. 4.0.3 (R Core Team 2023) for all statistical analyses. To test whether the distance guided to nonbee animals was statistically different from that when guided to a bees' nest, we used a Mann–Whitney U test because as the data violated assumptions of normality and homogeneity of variances (tested using Shapiro–Wilk and Levene's tests). Similarly, to test whether average speed while being guided to a bees' nest differed from that while being guided to nonbee animals, we used a Wilcoxon rank-sum test because these data solely violated the assumption of normality (assessed using Shapiro–Wilk and Levene's test for homogeneity of variance). To test for differences in the sinuosity of tracks ending at nonbee animals compared to those ending at bees' nests, we used a nonparametric Mann–Whitney U test because preliminary Shapiro–Wilk and Kolmogorov–Smirnov tests indicated that these data violated the assumptions of normality and homogeneity of variance distributional assumptions.
To analyze acoustic differences between honeyguide “chatter” and “indication” calls, we used a principal components analysis (PCA) using the “stats” package in R (Bates et al. 2015), based on 20 acoustic variables for each of the “chatter” and “indication” syllables (details in Appendix 3, Table A1) extracted using the “warbleR” package (Araya-Salas and Smith-Vidaurre 2017).
Ethical Note
No animals were captured for the purposes of this study. Free-living greater honeyguides “opted in” to cooperative behavior with humans by guiding them to wild bees in a natural setting. Birds and humans were audio recorded with minimal interference. This research was approved by the University of Cape Town Faculty of Science Research Ethics Committee, Permit number FSREC 50–2018, and data were collected with permission from Administração Nacional das Áreas de Conservação (ANAC), Mozambique, Permit nos. 008/2015, 11/11/2016, 15/2019, 09/2020, and 04/08/2022.
Results
Honeyguides Only Rarely Guide to Animals Other Than Bees
At our study site in northern Mozambique, the observed rate of being guided to animals other than bees in 2018 was 3.7% (4 of 108 guiding events leading to a distinct destination). It was 0% in D.J.L and C.N.S's own personal experience of guiding events leading to a distinct destination (i.e., were “successful”) at this location during 2013–2017 and 2019–2024 (approximately N = 350), and M.M also experienced no other events during this period as an active honey hunter (approximately N = 330 honey hunts during 2017–2022).
Direct Observations of Honeyguides Guiding to Nonbee Animals
We were guided by a honeyguide to a nonbee animal on four occasions:
- On May 18, 2018, M.M, C.N.S, and one other honey hunter (Issufo Mussa) were guided by an adult female honeyguide while conducting a playback experiment (details in Methods). Guiding began at 09:05 h (all times are local time: UTC + 2) and continued until 09:26 h when the honeyguide went silent (as is typical behavior signaling arrival at bees; Isack and Reyer 1989) near an adult puffadder (Bitis arietens) in short grass. We followed the honeyguide for an 838 m walking distance (Figure 2), during which the honeyguide vocalized with “chatter” calls and at the destination flew with low swooping flight in the same way as when guiding to bees. This interaction was not audio recorded.
- On June 13, 2018, M.M, D.J.L, and one other honey hunter (Orlando Yassene), during a completely natural honey-hunt (i.e., one in which all interaction decisions and vocalizations were being made by Yao honey hunters), were guided by an adult male honeyguide to a bees' nest. On arrival at the bees' nest, the honeyguide went silent. After 65 s, the honeyguide began calling again and guided our human party onward, at 08:40:10 h, to what we presumed was another bees' nest, given that honeyguides commonly lead humans to multiple bees' nests in succession (Friedmann 1955; Isack 1987; Spottiswoode et al. 2016). The honeyguide flew ahead of the honey hunter party, chattering continuously, stopped, and then doubled back ca. 10 m, perching in a tree adjacent to a dead greater galago (
Otolemur garnettii - On June 18, 2018, while recording honey-hunting audio signals during another natural honey-hunt, D.J.L and two Yao honey hunters (Rui Francisco, Aloisi Chole Sindi) were guided by an adult female honeyguide (starting 10:53:59 h) directly to an adult black mamba (
Dendroaspis polylepis - On June 22, 2018, while recording honey-hunting audio signals during a natural honey-hunt, D.J.L and two Yao honey hunters (Carvalho Issa and Armando Pita) were guided by an adult male honeyguide to a southern African rock python (
Python natalensis
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On other occasions, we have encountered numerous snakes, and occasionally elephant (
Honeyguide Spatial Behavior When Guiding to Nonbee Animals Is Similar to When Guiding to Bees
Based on the subset of tracks with high-resolution GPS data, the distance over which honeyguides guided us to nonbee animals (range: 75–838 m, mean ± SE = 329 ± 173 m, n = 4) was not significantly different (Mann–Whitney U test; W = 36, p = 0.79, n = 24) from the distance over which honeyguides guided us to bees (range: 73–890 m, mean ± SE = 308 ± 47 m, n = 20). Walking speed when being guided to nonbee animals (range: 2.08–2.50 kph, mean ± SE = 2.3 ± 0.09 kph, n = 4, Figure 2C) was also not significantly different (Wilcoxon rank sum test; n = 4, 20, W = 35.5, p = 0.76) from walking speed when being guided to bees (range: 1.08–3.49 kph, mean ± SE = 2.5 ± 0.15 kph, n = 20). Lastly, the sinuosity of the GPS tracks recorded en route to nonbee animals (range: 1.09–1.66, mean ± SE = 1.30 ± 0.13, n = 4) was not statistically different (Mann–Whitney U test; n = 24, W = 46, p = 0.68) from track sinuosity when guided to bees (range: 0.92–6.57, mean ± SE = 1.71 ± 0.30, n = 20).
Honeyguides Emit the Same Call When Nearing Nonbee Animals as when nearing bees
To test whether honeyguides produce similar calls when guiding honey hunters to bees as to nonbees, we used audio recordings from two instances of guiding to nonbees and from 20 instances of guiding to bees' nests. On both of the former, the honeyguide altered its calls from the “chatter” call (given initially upon guiding and over much of a honey-hunt) to “indication” calls (Figure 3). This switch in call type was observed in 17 of 20 (85%) audio-recorded events of guiding to bees' nests (Figure 3A). The mean straight-line distance (from the destination) at which the “indication” calls started to be produced when being guided to bees was mean ± SE = 63 ± 15.4 m, n = 16, and when being guided to snakes was mean ± SE = 16 ± 1 m, n = 2). On all four occasions of being guided to nonbees, the honeyguide went silent upon arrival at that location, and in three of four instances perched within sight in an adjacent tree in the same way as when guiding to bees (pers. obs. all authors, also Isack 1987; Short 1988; Short and Horne 2001).
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Guiding to Nonbee Animals Is no More Likely After Nonharvests by Humans
As an imperfect test of whether honeyguides were more likely to guide humans to nonbee animals following nonrewarding behavior by humans, we compared the proportion of honey hunts in the same area that were rewarded prior to being guided to nonbee animals versus prior to being guided to bees' nests (Figure 4). Honeyguides guided us to animals other than bees following prior reward rates of 0.5, 0, 0.75, and 0 (Figure 4), and to bees' nests following prior rewarding rates of 0.5, 1, 0.5, 0, 0, 1, 1 (Figure 4). While recognizing that the dataset is small, we found no significant effect of prior rewarding rates on the likelihood of being guided to nonbee animals compared to bees (Generalized Linear Model, Estimate = −1.69, SE = 1.71, z = −0.99, p = 0.32).
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Literature Review and Five Hypotheses for Guiding Nonbee Animals
We found 20 published references to honeyguides guiding humans to nonbee animals, originating from nine countries (original quotations and sources are given in Appendix 3, Table A1, and geographical locations, dates, and interpretations are summarized in Figure 1). Of these 20 published references, five directly state the local human cultural interpretation for why honeyguides guide to nonbee animals (four are punishment, one is an altruistic warning). We do not consider in depth here the hypothesis that honeyguides may benefit from guiding humans to dead animals or carcasses, either because they benefit from the insects on the carcass (Delegorgue 1847) or because the flies at a carcass are a bee-like stimulus (Friedmann 1955). This is because we have neither observed nor found any reports of honeyguides feeding on carcasses or flies at carcasses. In Table 1 we present five hypotheses explaining this behavior, together with their testable predictions. Hypotheses (1) to (3) have been previously proposed (da Sorrento 1744; Friedmann 1955; Isack 1987; Sparrman 1777) whereas (4) and (5) are proposed here for the first time. Briefly, these hypotheses are that guiding to animals other than bees is (1) the result of an incidental encounter occurring en route to a bees' nest, which humans mistakenly perceive to be the destination; (2) punishment of nonrewarding humans; (3) an altruistic warning to rewarding humans; (4) recruitment of mobbing partners; and (5) a cognitive recall error relating to how honeyguides store spatial information about memorable objects in the same way as they do bees' nests.
Discussion
In this study, we present first-hand data supporting centuries of assertions by a range of African honey-hunting cultures (Figure 1) that honeyguides rarely but intentionally guide honey hunters to animals other than bees. Honeyguides guided us to three snake species and a dead mammal, in each case stopping at the animal and producing “indication” calls, in the same way as when a honeyguide has arrived in the vicinity of a bees' nest. Furthermore, on three of the four observations of guiding to nonbee animals, honeyguides flew low over the snakes which, when given at bees, is a cue of arrival at a bees' nest located low down (Isack 1987 and pers. obs. all authors). The track sinuosity, distance followed, and timing of when honeyguides produced “indication” calls prior to arriving at nonbee animals were all within natural ranges observed when guided to bees (Figure 4). While the small sample size means we have to interpret these findings with caution, taken together, they are inconsistent with the first hypothesis, that encounters with these animals are incidental occurrences en route to bees (hypothesis i, Table 1).
Next, we cautiously evaluate our field data against three functional hypotheses for why honeyguides deliberately guide humans to animals other than bees: as punishment, as an altruistic warning, or to recruit mobbing partners.
First, if punishment toward humans for nonrewarding behavior is adaptive for honeyguides, then being guided to nonbee animals rather than bees should follow nonrewarding behavior by humans, and encounters with these nonbee animals should have the potential to negatively impact the human(s). Neither of these predictions was supported: the degree to which honeyguides (not necessarily the same individual) in the vicinity had previously received a beeswax reward for cooperative behavior did not predict whether we were subsequently guided to bees or nonbees, albeit in a small sample with weak statistical power (Figure 4C). In one instance, a honeyguide guided us to bees after taking us to a python, and we were guided to a dead galago immediately after being guided to and harvesting a bees' nest. Finally, the nonbee animals were largely nonthreatening to humans, since Yao honey hunters regularly encounter snakes, and even the black mamba, an agile and feared species, attempts to evade humans as a first response (Spawls et al. 2018), which is considered by Yao honey hunters to be far less threatening than an unexpected encounter with a large mammal such as buffalo, elephant, and hippopotamus.
Further to this empirical evidence, there are theoretical objections to the evolution of punishment by honeyguides. Punishment would require individual birds to: (a) recognize cheating individual honey hunters, (b) have repeat encounters with these cheating individuals, and (c) cause humans to alter their behavior to be more cooperative in future encounters (Raihani et al. 2012). These conditions are unlikely to be met, given that honey hunters interact with many different honeyguides within the large area (> 812 km2) over which each individual honey hunter ranges likely with a low re-encounter rate (unpubl. data D.J.L and C.N.S; Cram et al. 2023). Moreover, certain other honey-hunting cultures elsewhere in Africa intentionally withhold wax rewards from honeyguides, by either pretending not to spot bees' nests or choosing not to harvest so that the honeyguides “stays hungry” and shows them more bees' nests; yet there is no evidence that honeyguides are less likely to cooperate with, or more likely to “punish,” humans in these populations (e.g., Isack 1987; Laltaika 2021; van der Wal et al. 2022b; Wood et al. 2014).
Even in cultures that deliberately reward honeyguides from harvested bees' nests (such as the Yao culture in this study), honeyguides often experience unintentional nonrewarding behavior. For example, in the miombo woodland habitat of our study area, a tree containing a bees' nest can sometimes be either too big to harvest or too hard to cut into with an ax, or the bees' nest may appear to not contain enough honey to merit the effort (all authors, unpubl. data). The cost to humans of depriving honeyguide partners appears to be low, since honeyguides continue to cooperate regularly across varied cultural settings (Laltaika 2021; van der Wal et al. 2022a; Wood et al. 2014). Furthermore, unlike in other systems of punishment (Raihani et al. 2012), in the honeyguide –human system there is no scope for coercion: neither humans nor honeyguides can force their cooperative partners to cooperate. We conclude that there is neither empirical nor theoretical support for a punishment hypothesis of guiding to nonbees.
Second, in contrast to a punishment hypothesis, some cultures interpret being guided to dangerous animals as a form of altruistic warning to the humans of danger ahead (hypothesis iii, Table 1). These cultures include the Yao honey-hunting community, with whom we collaborate in this study (pers comms., all authors), and at least some other cultures (Gruber 2018). This hypothesis makes certain similar predictions to those for punishment (i.e., that honeyguides should guide deliberately to living but spatially predictable animals dangerous to humans). However, unlike the punishment hypothesis, a warning hypothesis predicts that guiding to nonbees should occur following consistent wax rewards. This was not supported, since we did not detect higher rates of guiding to nonbee animals in areas where honeyguides had been previously rewarded, albeit in a limited sample given the rarity of guiding to nonbee animals (Figure 4C).
Third, we propose as an alternative hypothesis that honeyguides may guide humans to recruit them as mobbing partners toward nonbee animals which they may perceive as a threat (e.g., snakes, predatory birds), much as other birds recruit other species as mobbing partners to help chase away a mutual threat (Dutour et al. 2017). The natural history of these species does not clearly support this idea, since two of the snake species guided to (python and puffadder) are terrestrial and relatively slow-moving, and small, agile, arboreal birds such as honeyguides are likely not an important part of their diet (Short 1988). In general, species in the honeyguide family (Indicatoridae) are typically cryptic and rarely mob other species (Hockey et al. 2005), and greater honeyguides only make themselves conspicuous when singing or when chattering to elicit cooperation from humans (Fry et al. 1988). Thus, a mobbing function seems unlikely.
Instead, our data were most consistent with a fifth hypothesis (hypothesis v, Table 1): that honeyguides sometimes deliberately guide humans to a location where the honeyguide has previously encountered an animal, and which it has stored in its spatial memory, but then makes a cognitive spatial recall error about which locations correspond to a food reward. In this concept, the only difference between the honeyguide's behavior when guiding to bees or nonbees is the erroneous selection of the destination. Spatial recall errors have been widely measured in scatter-hoarding bird species (Pravosudov and Roth 2013; Sonnenberg et al. 2019), and variation in spatial cognition can be influenced by environmental complexity (Branch et al. 2022; Roth et al. 2012), sleep (Rattenborg et al. 2011), and hippocampal neurogenesis (Leuner et al. 2006). It is also plausible that honeyguides may have genetic variation in their spatial cognitive ability, such as that recently demonstrated in scatter-hoarding, free-living mountain chickadees (
The honeyguide foraging system for beeswax also has intriguing parallels to systems of caching and food retrieval found in other groups of birds. Corvid species annually find, hide, and retrieve up to 100,000 food items, termed “scatter hoarding” (Clayton et al. 2007; Vander Wall 1990). For example, Western scrub-jays (
Collectively, our field data and historical accounts suggest that honeyguides guide humans to nonbee animals at a low rate which is tolerated by both partners, yet enough to culturally influence Yao honey hunters. In informal discussions with 21 Yao honey hunters, when asked “Why do you reward honeyguides after a honey-harvest?”, all 21 honey hunters consistently reported that they do so to motivate the honeyguide to (a) continue guiding to bees in the future, and also (b) altruistically guide them to nearby dangerous animals as a “warning.” A low rate of being guided to nonbee animals appears to be tolerated by Yao honey hunters since the cost is similar to that of being guiding to a bees' nest that the human cannot harvest (i.e., no honey benefits for the human, no beeswax benefits for the bird), and they perceive benefits of being warned about a potential threat.
Such human cultural interpretations of even rare experiences of encounters with dangerous animals could disproportionately influence human responses to honeyguide behavior. For example, whether people consistently reward honeyguides or not may be wholly based on a belief in punishment (or lack of altruistic warning) should they fail to do so. Rapid cultural transmission can propagate human knowledge of even rare honeyguide errors, which in turn may promote future cooperation regardless of whether the human perception of that behavior is positive (warning) or negative (punishment).
Conclusion
This study reviews and (albeit with a small sample) corroborates centuries of Indigenous African cultural knowledge asserting that honeyguides rarely but intentionally guide humans to nonbee animals. Punishment is an appealing and widely repeated explanation, but our evidence suggests that this behavior is unlikely to have evolved for this function, or as a form of altruistic warning to humans, or to recruit mobbing partners. Instead, the available evidence from our limited data best supports the hypothesis that guiding to nonbees arises from cognitive spatial recall errors that carry a low cost to individual honeyguides. Nonetheless, in some honey-hunting cultures, interpretations of this behavior as punishment or warning may reinforce cultural traditions of rewarding honeyguides with beeswax. Such cultural interpretations may benefit honeyguides at the population level by providing increased overall beeswax rewards (Lloyd-Jones et al. 2022). Such potential modest benefits may, along with low costs, reduce selection against cognitive errors.
Author Contributions
David J. Lloyd-Jones: conceptualization (equal), data curation (equal), formal analysis (equal), investigation (equal), methodology (equal), visualization (equal), writing – original draft (equal), writing – review and editing (lead). Musaji Muamedi: conceptualization (equal), data curation (equal), writing – review and editing (equal). Claire N. Spottiswoode: conceptualization (equal), data curation (supporting), formal analysis (supporting), funding acquisition (lead), investigation (equal), methodology (equal), supervision (lead), writing – original draft (supporting), writing – review and editing (equal).
Acknowledgments
We thank the honey-hunting community of Mbamba village, Niassa Special Reserve, for their insights and assistance, and particularly Rui Fransisco, Orlando Itande, Aloisi Chole Sindi, Carvalho Nanguar, and Seliano Rucunua for sharing their perspectives and knowledge of honeyguide behavior. We thank Administração Nacional das Áreas de Conservação (ANAC), Colleen and Keith Begg, Agostinho Jorge, and the Mariri Environmental Centre for their support. We thank Cameron Blair, Dominic Cram, Tanmay Dixit, Janine Dunlop, Lazaro Hamusikili, Eliupendo Laltaika, Jess Lund, David Moyer, Rob Tether, Jessica van der Wal, and Brian Wood for contributions to sourcing historical material, discussions, and/or comments on earlier drafts, and anonymous reviewers for constructive comments. Data were collected under Administração Nacional das Áreas de Conservação (ANAC) Permit nos. 008/2015, 11/11/2016, 15/2019, 09/2020, and 04/08/2022. This work was supported by funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement no. 725185), and by the Max Planck—University of Cape Town Centre for Behavior and Coevolution in collaboration with the FitzPatrick Institute of African Ornithology at the University of Cape Town and the Max Planck Society.
Conflicts of Interest
The authors declare no conflicts of interest.
Data Availability Statement
The code and data for performing the analyses are available on Github ().
Appendix - 1
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Appendix - 2
Account of a “False Positive” Report of Being Guided to a Snake
On June 11, 2023 D.J.L., C.N.S, three honey hunters and one other researcher, were guided at 0955 h by a juvenile male greater honeyguide. We followed the honeyguide, who produced stereotypical, vigorous “chatter” calls throughout for 230 m, and upon reaching a large (> 15 m high) Ficus bussei tree, lost sight of the bird but could still clearly hear it chattering in the canopy ahead of us. The habitat was riverine scrub with a nearly closed-canopy at a height of 4–5 m. Most of the group passed the large Ficus bussei (continuing to follow the honeyguide ahead) before one of the honey hunters alerted the group to a Mozambique spitting cobra (
Appendix - 3
TABLE A1 Acoustic parameters measured using the “warbleR” package in R, to compare “chatter” and “indication” calls emitted by honeyguides. Parameters in bold were not used in the principal components analysis (PCA) as they are highly correlated (R2 > 0.75) with other variables.
| Measure | Description (methods following [23]) |
| duration | Length of signal (in s) |
| meanfreq | Mean frequency (in kHz). Calculated as the weighted average of the frequency spectrum (i.e., weighted by the amplitude within the supplied band pass) |
| sd | Standard deviation of frequency (in kHz). Calculated as the weighted standard deviation of the frequency spectrum |
| freq.median | Median frequency. The frequency at which the frequency spectrum is divided in two frequency intervals of equal energy (in kHz) |
| freq.Q25 | First quartile frequency. The frequency at which the frequency spectrum is divided in two frequency intervals of 25% and 75% energy, respectively (in kHz) |
| freq.Q75 | Third quartile frequency. The frequency at which the frequency spectrum is divided in two frequency intervals of 75% and 25% energy, respectively (in kHz) |
| freq.IQR | Interquartile frequency range. Frequency range between “freq.Q25” and “freq.Q75” |
| time. median | Median time. The time at which the time envelope is divided in two time intervals of equal energy (s) |
| time.Q25 | First quartile time. The time at which the time envelope is divided in two time intervals of 25% and 75% energy, respectively (s). |
| time.Q75 | Third quartile time. The time at which the time envelope is divided in two time intervals of 75% and 25% energy, respectively (s) |
| time.IQR | Interquartile time range. Time range between “time.Q25” and “time.Q75” (s) |
| skew | Skewness. Asymmetry of the frequency spectrum |
| kurt | Kurtosis. Peakedness of the frequency spectrum |
| sp.ent | Spectral entropy. Energy distribution of the frequency spectrum. Pure tone ~0; noisy ~1. |
| time. ent | Time entropy. Energy distribution on the time envelope. ~0 means amplitude concentrated in a specific time point, 1 means amplitude equally distributed across time |
| entropy | Spectrographic entropy. Product of time and spectral entropy sp.ent * time. ent. |
| sfm | Spectral flatness. Similar to sp.ent (Pure tone ~0; noisy ~1). |
| meandom | Average of dominant frequency measured across the spectrogram |
| mindom | Minimum of dominant frequency measured across the spectrogram |
| maxdom | Maximum of dominant frequency measure across the spectrogram |
| dfrange | Range of dominant frequency measured across the spectrogram |
| modindx | Modulation index. Calculated as the cumulative absolute difference between adjacent measurements of dominant frequencies divided by the dominant frequency range (measured on the spectrogram) |
| startdom | Dominant frequency measurement at the start of the signal (measured on the spectrogram) |
| enddom | Dominant frequency measurement at the end of the signal (measured on the spectrogram) |
| dfslope | Slope of the change in dominant frequency (measured on the spectrogram) through time |
| peakf | Peak frequency. Frequency with the highest energy and is measured on the frequency spectrum. |
| meanpeakf | Mean peak frequency. Frequency with highest energy from the mean frequency spectrum |
| meanfun | Average of fundamental frequency measured across the acoustic signal |
| meanfun | Average of fundamental frequency measured across the acoustic signal |
| minfun | Minimum fundamental frequency measured across the acoustic signal |
| maxfun | Maximum fundamental frequency measured across the acoustic signal |
| hn_freq | Mean frequency of the “n” upper harmonics (kHz) (see analyze). Number of harmonics is defined with the argument “nharmonics.” Only measured if harmonicity = TRUE. |
| hn_width | Mean bandwidth of the “n” upper harmonics (kHz) |
| harmonics | The amount of energy in upper harmonics, namely the ratio of total spectral power above 1.25 x F0 to the total spectral power below 1.25 x F0 (dB) |
| HNR | Harmonics-to-noise ratio (dB). A measure of the harmonic content |
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Appendix - 4
Documented reports of honeyguides guiding to animals other than bees, and the adaptive function culturally attributed by humans to this behavior (if provided).
| Human cultural group | Location | Quote on guiding to dangerous animals or animals other than bees | Motives attributed | Animal/nonbee object guided to | Reference |
| Uncertain | Northern Ethiopia | “For there is a little Bird, by those of Tygra call'd from the noise which it makes Pipi, which, strange to tell will, lead the hunters to the places where the wild beasts lye hid: never leaving their note of Pipi, till the hunters follow them, and kill the discover'd prey. Gregory related to me, that as he was walking with one of his acquaintance, an inhabitant of Tygra; this bird cry'd Pipi over their heads; thereupon, understanding the meaning of it from his friend, he resolv'd to try the truth of the story. The bird conducted them to a shady tree, about the boughs of which, a monstrous huge snake had curl'd her self; at the sight whereof, he and his friend made more hast back again, than they did coming to satisfie their curiosity. And indeed, it is not safe to follow this bird, unless a man be provided with all his hunting instruments: nevertheless, the bird has her own ends in her double diligence too: for she is sure to have her share of the slaughtered carcase whate're it be. Nor is this bird to be found only in Habessinia, but also in Guiny in the Kingdom of Quoja, where they give it the name of Fonton, being about the bigness of a Larke, where it is reported to betray not only wild beasts, but also serpents and bees.” | Benefits from eating the carcass | Snake, wild beasts | Ludolphus 1682 |
| Uncertain | Congo Basin | “Nor is there less to be admired in another bird in these parts, and particularly the kingdom of Matamba, which as travellers are on their way, harmoniously sings, Vuichi, Vuichi, which in the language of the Blacks signifies, honey, honey; and flopping from one place to another, rest upon the tree where the honey is, that the passengers may take it, and the bird feed on what remains. But it sometimes falls out, that following the cry of the bird, the passenger falls into the clutches of some lion that lies hid, and so meets his death instead of honey; therefore when the bird cries, if he sees not the honey, they are aware of the hidden lion, and fly in time.” | Punishment | Lion | da Sorrento 1744 |
Khoe-Sān | Western Cape, South Africa | “The inhabitants in general accuse the same bird of sometimes conducting its followers where wild beasts and venomous serpents have their places of abode: this however I never had an opportunity of ascertaining myself; but am apt to believe such cases to be accidental, when dangerous animals happen to be in the neighbourhood of a bees-nest.” | Incidental | Wild beasts and venomous snakes | Sparrman 1777 |
Khoe-Sān | KwaZulu-Natal, North West Province, South Africa | “A number of travelers have described the characteristics of the honey-guide and maintain that it is spared by the hunter because of its usefulness to man. Somebody has said, and Buffon has repeated it, that there is danger in following this bird as it will often lead the hunter into the clutches of wild animals, such as lions and leopards. At first, when I has studied the honey-guide only in the Amazoulou [Zulu] country, I was tempted to reject this theory as a fable for in those parts the bird appeared to have no instinct other than the one to which it owes its name; it led us to the hives and only to the hives; and so we had to reason to mistrust it. But later, beyond Malalis-Berg [Magaliesberg], I watched my men set out on numerous fruitless searches in answer to the bird's call; after ten or fifteen vain attempts, I heard them cursing the om-schlanvo; one of them had twice been led to a rhinoceros skeleton, another to a dead buffalo and a third to the bones of a canna. Henning himself, who loved honey, had been deceived on four occasions; each time he had been led to a skeleton and twice the hyaenas had fled at his approach. One must not conclude from these facts that the cuckoo [honeyguide] has an understanding with the great carnivores to bring them men to eat, by rather that, feeding on insects, this fragile bird has the need of the assistance of man to move the bones beneath which swarm beetles and other insects, and which the cuckoo [honeyguide] is unable to reach while they are hidden. It is only just and fair that, when he cannot himself obtain the food which is necessary for his existence, this bird will ask assistance of man who he has already helped to procure the sweets contained by nature.” | To gain access to insects upon which to feed | Lions, leopards, rhino skeleton, dead buffalo | Delegorgue 1847 |
| Uncertain | Limpopo, South Africa | “Interesting as the honey-bird is, and though sweet be the stores to which it leads, I have often had cause to wish it far enough, as, when following the warm ‘spoor’ or track of elephants, I have often seen my [trackers] at moments of the utmost importance, resign the spoor of the beasts to attend to the summons of the bird. Sometimes, however, they are ‘sold’, it being a well-known fact, both among the Hottentots and tribes of the interior, that they often lead the unwary pursuer to danger, sometimes guiding him to the mid-day retreat of a grizzly lion, or bringing him suddenly upon the den of the crouching panther. I remember on one occasion, about three years later, when weary with warring against the mighty elephants and hippopotami which roam the vast forests and sport in the floods of the fair Limpopo, having mounted a pair of unwonted shot-barrels, I sought recreation in the humbler pursuit of quail-shooting. While thus employed, my attention was suddenly invited by a garrulous honeybird, which pertinaciously adhered to me for a considerable time, heedless of the reports made by my gun. Having bagged as many quails and partridges as I cared about shooting, I whistled lustily to the honeybird, and gave him chase; after following him to a distance of upward of a mile, through the open glades adjoining the Limpopo, he led me to an unusually vast crocodile, who was lying with his entire body concealed, nothing but his horrid head being visible above the surface of the water, his eyes anxiously watching the movements of eight or ten large bull buffaloes, which, in seeking to quench their thirst in the waters of the river, were crackling through the dry reeds as they cautiously waded in the deep mud that a recent flood had deposited along the edge. Fortunately for the buffaloes, the depth of the mud prevented their reaching the stream, and thus the scaly monster of the river was disappointed of his prey.” | Unattributed | Lion, “panther” [leopard] Crocodile | Cumming 1856 |
| Uncertain | Northern modern day Zambia | “DECEMBER 2, 1855. We remained near a small hill, called Maundo, where we began to be frequently invited by the honey-guide (‘Cuculus indicator’). Wishing to ascertain the truth of the native assertion that this bird is a deceiver, and by its call sometimes leads to a wild beast and not to honey, I inquired if any of my men had ever been led by this friendly little bird to any thing else than what its name implies. Only one of the 114 could say he had been led to an elephant instead of a hive, like myself with the black rhinoceros mentioned before. I am quite convinced that the majority of people who commit themselves to its guidance are led to honey, and to it alone.” | Unattributed | Elephant | Livingstone 1858 |
| Wakamba | East Africa | “East African natives, so far as I am aware, have no stories of guides wreaking their vengeance on the man who omits to leave some honey for them by leading him up to dangerous animals, as have the natives of South Africa… I have been told of cases in which men have been led to snakes and dangerous beasts, but these must be discounted by the obvious chances of the bush. When men take a ‘beeline’ through the bush, whether following a honey-guide or not, there is always the chance of happening on dangerous animals or the reverse. My own boys have followed for honey hundreds, perhaps one thousand times; once they returned to say that the bird led them up to buffalo. I have very often followed myself, and was once thus brought to a wounded lion. I was as firmly persuaded then that the thing was intentional as I am now that it was not.” | Incidental | Snakes, dangerous animals, buffalo, wounded lion | Percival 1924 |
| Uncertain | East Africa | “In East Africa… there is a chance of being led by the honey-guide to a lion or leopard. This would seem to be mere accident, but Blayney Percival [12; A Game Ranger's Notebook] vouches for one case in his own experience.” | Unattributed | Lion, Leopard | Chapin 1939 |
| Uncertain | Northern Zimbabwe | “Natives often make use of the fact that very occasionally a honeyguide may appear to lead to a dangerous animal instead of a bees' nest, to impute a revenge motive to the bird. This has given rise to a variety of proverbs, such as: If you do not leave anything for the guide, it will lead you to a dangerous animal the next time. If you do not leave anything for the guide, it will not lead you at all in the future. If you do not leave anything for the guide, it will come to you and chatter when you are stalking game, and thus reveal our presence to the intended quarry. “Still another bit of evidence as to the nature of the performance is the fact that on occasions the bird will lead not to a bees' nest but to a dead animal or to a live snake, leopard, rhinoceros, etc. I doubt that these are in any sense the “purposive” goals behind the species habit of guiding, and that in most cases they may be dismissed quite easily as distracting incidents on the guiding trip that cause the guide and, more certainly, the follower to “forget” the original “goal.” “Major Haydock, in Northern Rhodesia, was told by his native collectors that when a honey-guide led them to a leopard or a lion it was always a sleeping beast, and that the bird seemed to mistake the flies hovering about it for bees (this is the natives' own, unaided conclusion). It seems very probable that the real explanation is that the flies hovering about may have a similar effect on the honey-guide as would a flight of bees. In some of these instances the observers made particular search to see if there might have been a bees' nest near the animal; if so, the animal's presence could not be looked upon as more than a coincidence, but in a number of cases there was no sign of a hive. It might be mentioned, parenthetically, that there are some who think that the actions of the bird may be slightly different when coming to a large animal than when arriving at a bees' nest.” | Revenge motive (punishment), distraction while guiding, punishment | Live snake, leopard, rhinocerous | Friedmann 1955 1955 |
| Uncertain | Eastern Cape Province, South Africa | “The natives on the farm, when asked, repeated the story of birds guiding people to snakes but in the absence of actual instances this seems illusory. In addition they referred to people being led to dead animals, but this I believe to be apocryphal…” | Unattributed | Snakes, dead animals | Skead 1951 |
| Uncertain | Southern Tanzania | “By constantly twittering and nagging till you follow, a honey guide will lead you to a beehive. It wants you to get rid of the bees and open the hive, being interested in the grubs and honey. It is usual to leave some honey for the bird, and there is a belief among Africans that if this is not done it will lead the next man it sees to a lion or snake. There is evidence of the truth of this behaviour - though not the bird's motives - because I have on three occasions been led by it to things other than honey, and this was one of them. It would fly around us twittering insistently, then go over to the man-eater: it was fairly open country and we could follow the passage of our quarry by the birds suddenly getting up from bushes as it passed under. We came upon several places where the lion had tried to lie down and rest, but had got up and moved on because of the racket this infernal bird was making. This performance went on quite a long time, till the lion suddenly bolted away, probably in an attempt to shake off the pest.” | Punishment | Lion or Snake | Ionides 1965 |
| Senga | Chikwa, Northern Zambia | “Because of this Nsulu [greater honeyguide] commands a great respect among the tribes and much of their folklore and legends centre round the birds, as around any creature which touches the economy of their lives. There are certain rites, too, which must be followed when honey is taken from the hive. It is important for instance to leave a fair portion of the comb for the honey-guide in payment for services rendered. This act must be performed with deference and the appropriate obeisance's. And woe betide anyone who neglects this little courtesy. There is no doubt in the minds of these people that such an offender against the properties will be adequately punished; the next time he follows Nsulu he will certainly be led into the clutches of a waiting lion, or toward any of the other fates that await evil-doers.” | Punishment | Lion | Carr 1969 |
| Boran | Northern Kenya | “A common belief that the Boran share with several other communities in Africa is that the bird often guides man to animals such as lions, buffalos, elephants, rhinos, large poisonous snakes or to enemies or murderers from a hostile tribe. They are also said to lead someone to old weapons (bows, arrows, spears) and hidden trophies such as elephant tusks and rhino horns. It is believed that the bird resorts to this abnormal result of man's failure to spare some food for it after the bird had helped him discover a colony. Some people claim that as soon as a bird arrives and start guiding, they can tell whether it has such a motive or not. This, they say, can be established by observing the guiding behavior of the bird during the trip. Others claim that there are two types of honeyguides: the good ones which guide to bee colonies, and the rogue ones who specialize in guiding to dangerous destinations.” | Punishment | Lions, buffalos, elephants, rhinos, large poisonous snakes, old weapons (bows, arrows, spears), hidden trophies such as elephant tusks and rhino horns | Isack 1987 |
Wataa | Tsavo, southern Kenya | “It was a woman's task to hunt for the nests of wild bees found in trees or in the ground, sometimes with the help of the greater honeyguide ( | Unattributed | Rhino, Snake | Ville 1995 |
| Boran | Northern Kenya | “Does the bird guide man to dangerous animals? Contrary to the traditional belief that the honeyguide often leads people to dangerous objects, I have never witnessed such an event, except on coincidental situations. However this belief is so widespread across the whole continent of Africa that a study of it may be warranted.” | Incidental | Dangerous (to human) animals | Isack 1999 |
| Uncertain | Kenya | “There is a considerable literature (Friedmann 1955) on Greater Honeyguides ‘guiding’ humans to lions, or poisonous snakes, or the presence of elephants. Persons with sufficient field experience will be aware that such animals are of much greater consequence to humans than to the guiding Greater Honeyguide in a tree above. We have been ‘guided’ to an abrupt precipice and to a bull elephant by Greater Honeyguides. In these cases there were bee-hives below the cliff (in a valley) and beyond the elephant. Concern for the welfare of the guided person is beyond any reasonable expectation of a honeyguide, yet it is easy to appreciate how an untrained or unobservant individual could interpret such ‘evil’ guiding wrongly.” | Incidental en route to bees | Lions, snakes, elephants | Short and Horne 2001 |
| Batonga | Southern Zambia | “ ‘One honeyguide’, Lazaro [Hamusikili] said, ‘showed me four hives; one hive then another then another; and sometimes, because it is interested, it showed us other things as well, a snake or dead animal in the bush’.” | Out of interest | Snake, dead animal | Dee 2013 |
| Fulani, Mbum, Baya | Central Cameroon | “We tried to locate the bird and climbed down a steep slope toward a small riverbed, but the vegetation was too dense to even see it. After a few minutes, as we were unable to follow the bird, the chattering slowly moved further away and eventually vanished in the distance. When the bird was gone, our guide immediately pointed to a hole in the ground—a snake's hole he said—and explained that the honeyguide probably wanted to warn us of a snake (See Figure 2). In that moment, it sounded to me like an excuse for the ethnographers' benefit. However, the bird is frequently and widely reported to indicate the presence of dangerous animals. Friedmann dismisses such reports as ‘native legends’ or as coincidental (1955: 57). Our interlocutors told us that when this happens, the bird wants to warn them. For hunters of game this may have negative effects as the honeyguides' calls may also warn and chase away their prey. Unfortunately, the phenomenon has not been followed up and further research is necessary…” | Warning | Dangerous (to human) animals, Snake | Gruber 2018 |
| Maasai | Northern Tanzania | “For example, Maasai respondents reported using simple words (“enjarwatai”, meaning “sheep”) mixed with trill-grunts when attracting honeyguides. But when a honeyguide starts to guide them, they then switch to more complex messages interspersed among trill-grunts (transcribed here as “Prrr, Hii”) as guiding calls… which approximately means “Please my dear sheep, please show me the location of the honey, I can harvest it while I am kneeling or standing from the tree or from the termite mound, but please don't lead me to a dangerous animal.” | Unattributed | Dangerous (to human) animals | Laltaika 2021 |
| Awer | Northern Kenya | “All interviewees also reported that they have sometimes been guided to animals other than bees, namely snakes (n = 4 interviewees), lions (n = 5 interviewees) and other animals (n = 6 interviewees). These events were not interpreted in any particular way, and one interviewee explicitly attributed this to chance.” | Unattributed, Incidental (when attributed) | Snakes, lions, other animals | van der Wal et al. 2022 |
Araya‐Salas, M., and G. Smith‐Vidaurre. 2017. “warbleR: An R Package to Streamline Analysis of Animal Acoustic Signals.” Methods in Ecology and Evolution 8: 184–191. [DOI: https://dx.doi.org/10.1111/2041-210X.12624].
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Abstract
ABSTRACT
Greater honeyguides (
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; Muamedi, Musaji 2 ; Spottiswoode, Claire N. 3
1 FitzPatrick Institute of African Ornithology, Department of Biological Sciences, University of Cape Town, South Africa
2 Mbamba Village, Niassa Special Reserve, Niassa Province, Mozambique
3 FitzPatrick Institute of African Ornithology, Department of Biological Sciences, University of Cape Town, South Africa, Department of Zoology, University of Cambridge, Cambridge, UK