Animals can benefit from classifying predators or other dangers into categories, tailoring their escape strategies to the type and nature of the risk. Studies of alarm vocalizations have revealed various levels of sophistication in classification []. In many taxa, reactions to danger are inflexible, but some species can learn the level of threat presented by the local population of a predator [] or by specific, recognizable individuals []. Some species distinguish several species of predator, giving differentiated warning calls and escape reactions; here, we explore an animal's classification of subgroups within a species. We show that elephants distinguish at least two Kenyan ethnic groups and can identify them by olfactory and color cues independently. In the Amboseli ecosystem, Kenya, young Maasai men demonstrate virility by spearing elephants (Loxodonta africana), but Kamba agriculturalists pose little threat. Elephants showed greater fear when they detected the scent of garments previously worn by Maasai than by Kamba men, and they reacted aggressively to the color associated with Maasai. Elephants are therefore able to classify members of a single species into subgroups that pose different degrees of danger.

Results and Discussion

2 Struhsaker T.T. Behaviour of vervet monkeys. 3 Seyfarth R.M.

Cheney D.L.

Marler P. Monkey responses to three different alarm calls: Evidence of predator classification and semantic communication. 4 Manser M.

Seyfarth R.M.

Cheney D.L. Suricate alarm calls signal predator class and urgency. 5 Kiriazis J.

Slobodchikoff C.N. Perceptual specificity in the alarm calls of Gunnison's prairie dogs. Suricates (Suricata suricatta), prairie dogs (Cynomys gunnisoni), and several species of primate are known to classify different predator species into categories depending on the type and nature of the risk posed []. Having the ability to classify all members of a single predator species into subgroups, and to thus be able to respond appropriately to each, would be of material benefit whenever a potential predator exists in subpopulations that present different degrees of risk. The predator that most obviously shows this pattern is man. In many areas of the world, human populations include ethnic groups that engage in hunting and others that, in the same areas, focus their lives on agriculture or pastoralism. It would benefit any prey species living in these areas to use ethnic subgroup classification as a basis for their antipredator response.

11 Moss C. The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya. 12 Croze H.

Sayialel S.

Sitonik D. Amboseli as a Biosphere Reserve. A Compendium of Conservation and Management Activities in the Amboseli Ecosystem. 13 Moss C. Elephant Memories. 14 Kangwana, K. (1993) Elephants and Maasai: Conflict and Conservation in Amboseli, Kenya. D.Phil thesis, University of Cambridge, Cambridge, UK. 15 McComb K.

Baker L.

Moss C. African elephants show high levels of interest in the skulls and ivory of their own species. 16 McComb K.

Moss C.

Sayialel S.

Baker L. Unusually extensive networks of vocal recognition in African elephants. 17 Wittemyer G.

Douglas-Hamilton I.

Getz W.N. The socioecology of elephants: Analysis of the processes creating multitiered social structures. African elephants offer a good opportunity to test for this kind of predator subclassification. In the Amboseli ecosystem, Kenya, elephants encounter several types of people presenting different levels of risk, including the Maasai, cattle-herding pastoralists whose young men spear elephants (although prohibited, elephant spearing is a regular, low-frequency occurrence in the area []), and the Kamba, the most numerous of the agricultural and village-living peoples, who today pose little threat to elephants. Studies aimed at understanding conflict between humans and elephants propose that elephants might respond differently to Maasai men than to other people []. Furthermore, elephants show signs of sophisticated classification in other domains, reacting to bones of dead elephants in a different way than to those of other large animals [] and showing extensive vocal recognition within their complex social hierarchies []. We experimentally presented elephants with human artifacts in order to test the hypotheses that (1) elephants classify humans into distinctive subgroups that vary in level of risk to them, in particular identifying the Maasai; (2) elephants use olfactory and visual cues independently in classifying human groups; and (3) individual or family history of spearing affects the extent and nature of the reaction toward cues signaling Maasai.

18 Poole, J.H., and Granli P.K. (2003). Visual and tactile signals of African savanna elephants http://www.elephantvoices.org/index.php?topic=what_comm&topic2=what_comm/visual_tactile_signals.html. Figure 1 Examples of Elephant Reactions to Garments Worn by Maasai Show full caption The top panel shows the high carriage of head and tail and the uplifted trunk of elephants that have just detected a cloth's scent. The lower panel shows elephants as they run downwind from the location of a cloth; note the bunching of the group and continued high head and tail. Figure 2 Reactions of Elephant Groups to Cloths Differing in Scent Show full caption Time spent stationary after first smelling the three cloth types (A), travel speed in the first minute (B), distance moved away from the cloth in the first five minutes (C), and time taken to relax (D). In each case, mean values and 95% confidence intervals are shown. Pairwise comparisons of log-transformed data (with a Bonferroni correction for multiple comparisons) were used to examine the effects. There were no differences in the time the elephants spent stationary after first smelling the cloth within the three cloth conditions ([A], mean differences: Maasai versus Kamba 0.078; Maasai versus unworn 0.100; Kamba versus unworn 0.178; for all values p > 0.98). Significant differences were found in the travel speed (B), distance moved (C), and time taken to relax (D) between the Maasai- and Kamba-worn cloths (mean differences: travel speed 0.270, p = 0.014; distance 0.656, p < 0.001; relaxation 0.389, p < 0.001), between Maasai-worn and unworn cloths (mean differences: travel speed 0.645, p < 0.001; distance 1.299, p < 0.001; relaxation 1.011, p < 0.001), and between Kamba-worn and unworn cloths (mean differences: travel speed 0.375, p = 0.001; distance 0.643, p < 0.007; relaxation 0.622, p < 0.001). To investigate use of olfaction, we used a within-subjects design to compare the reaction of 18 elephant family groups to three different types of garment: clean, unworn, red cloths; red cloths worn by adult Kamba men for a period of five days; and red cloths worn by adult Maasai men for a period of five days. The three garments were presented to each elephant group on different occasions, separated by at least a week and counterbalanced for order of presentation. Reaction was assessed by four measures: time spent stationary after first smelling the cloth, travel speed in the first minute of movement, distance moved away from the cloth in the first five minutes, and time taken to relax. Distances from the cloth were estimated in the field before and after presentation. Reaction times were measured from videotape recorded continuously during each trial. In every trial, the point when an elephant first detected the scent of a cloth was clear because it would pause with its head up and trunk curled upwards, pointed in the direction from which the scent came ( Figure 1 ). The time elapsing from this moment of detection until the group began to move was similar for the three types of cloth ( Figure 2 A), suggesting that differences in reaction were not a function simply of the strength of a scent, but rather depended on its nature. After travel ceased, individuals might still show tension by their erect head posture, sniffing, and close proximity to others; we recorded that a group had relaxed when the elephants spread out and began feeding, dust-bathing, or resting with heads lowered [].

Elephants Distinguish Maasai from Other Humans by Olfaction (8,62) = 11.786, p < 0.001, Wilks λ = 0.157; see 2 = 3.943, df = 1, p = 0.047). Travel speed, distance traveled and time taken to relax differed strikingly between the three red cloth types presented (multivariate analysis of variance [MANOVA], F= 11.786, p < 0.001, Wilks λ = 0.157; see Figure 2 for details of pairwise comparisons). Compared to the presentation of either Kamba-worn or unworn cloths, when presented with a cloth previously worn by a Maasai man, elephants traveled significantly faster in the first minute after they began to move, traveled a significantly greater distance away from the cloth in the first 5 min, and took significantly longer to relax after travel ceased ( Figures 2 B–2D). In every presentation of the Maasai cloth, the initial direction of travel was directly away from it, in the downwind direction (± 85° from the eight-point compass direction of the wind). Although reactions to a cloth worn by a Kamba man were significantly more muted than reactions to a Maasai-worn cloth, they were nevertheless significantly stronger on these measures than reactions to an unworn red cloth. When presented with an unworn red cloth, elephants moved significantly slower, for significantly shorter distances, and relaxed significantly quicker than they did to either the Maasai- or Kamba-worn cloths. When presented with the unworn cloth, groups were also less likely to travel downwind from the cloth than when presented with worn cloths (Chi square test, χ= 3.943, df = 1, p = 0.047). Because elephant groups reliably headed directly away (downwind) from worn cloths that they scented, they never came within 10 m of the experimental stimuli and gave no sign of seeing them. The results therefore imply that elephants can classify members of a potential predator species into subgroups based on olfactory stimuli alone, without prior familiarity of the specific human individuals involved. 19 McCormick J.

Elmore-Meegan M. Maasai diet. The detection of human scent, and in particular the difference between the two local peoples, might have been based on a number of olfactory cues. As well as possible differences in pheromonal profile, the diets of Maasai and Kamba peoples differ strikingly. Maasai consume substantial amounts of milk and occasionally cattle blood and meat [], whereas Kamba diet mainly comprises meat, vegetables and maize meal. These dietary differences might be reflected in the chemical composition of body odor. Furthermore, the Maasai are pastoralists, so odors of cattle permeate their villages, and they use ochre and sheep fat in body decoration, unlike the agricultural Kamba.

Elephants Move to Different Habitats When Presented with Different Stimuli Figure 3 Habitat Choice in Response to Experimental Trials Show full caption Bars show the number of trials that ended with the elephants resting in elephant grass after the detection of Kamba-worn, Maasai-worn, or unworn cloth. White bars indicate trials that ended in elephant grass, and shaded bars show trials that ended in any other habitat type. The association between presentation condition and final habitat was significant (Chi square test, χ2 = 33.246, df = 2, p < 0.001). Movement in response to the scent of a garment worn by a Maasai was not simply away (downwind) from the olfactory stimulus, but also toward a particular habitat, in the sense that elephants' flight tended to continue until they reached elephant grass vegetation over 1 m in height. All experimental trials with Maasai-worn garments ended in this habitat, whereas with an unworn cloth, this was rarely the case; in trials with Kamba-worn garments the tendency to seek tall grass was intermediate ( Figure 3 ). With both Kamba and Maasai garments, there was a significant increase in habitat height from where the cloth was first detected to where the elephants finally relaxed, whereas with an unworn cloth, no such difference was seen (Kamba garment, median habitat height, initial 0.20 m, final 0.55 m, Wilcoxon test, z = −2.761, p = 0.006; Maasai garment, median habitat height, initial 0.35 m, final 1.25 m, Wilcoxon test, z = −3.740, p < 0.001; unworn garment, median habitat height, initial 0.30 m, final 0.30 m, Wilcoxon test, z = −1.00, p = 0.317). Arriving in denser, taller habitat is not an inevitable result of movement: Only 7% of the Amboseli National Park, in which all trials were conducted, is covered with elephant grass [K. Lindsay, personal communication]. Rather, it seems that when alarmed by olfactory detection of humans, especially Maasai, elephants seek denser, taller habitats.

Direct Experience of Spearing Does Not Determine Reaction We predicted that individual or family history of spearing would affect the extent and nature of elephants' reaction to Maasai odor cues. However, we found no overall effects of spearing history on the strength or type of reaction. This is despite considerable variation in past aversive interactions with Maasai among the elephant groups tested. Two elephants tested were known to have been highly aggressive toward Maasai cattle, and seven of the family groups tested included individuals that had experienced multiple cases of spearing to themselves or their immediate family during the last 30 years. In contrast, three groups were composed of individuals that are not known to have experienced the spearing of any individual in their family over this period. We divided all the elephant groups we tested into three categories of different experience with spearing. Elephant group reactions, in terms of the speed of travel, distance moved, and time to relax, did not differ with their spearing history (mixed MANOVA, main effect of spearing history on elephant reactions: F (6, 26) = 0.637, p = 0.70, Wilks λ = 0.760). Elephant groups in all three categories showed a similar pattern of reaction to the three cloth types (interaction between spear history and cloth type: F (12, 20) = 0.673, p = 0.757, Wilks λ = 0.508). Reactions were strong, even in groups with the least experience of spearing, suggesting that social learning is very effective in transmitting knowledge of Maasai people and the associated emotional responses throughout the local elephant population. (2, 16) = 14.462, p < 0.001; distance moved: F (2, 16) = 6.036, p = 0.011; pairwise comparisons of travel speed: high: low experience; p < 0.001, high: medium experience; p = 0.004; pairwise comparisons of distance moved: high: low p = 0.007; Bonferroni corrections used in each case). Thus, elephant groups with personal experience of being speared did not all react in the same way to the scent of a Maasai-worn garment; some moved away very quickly, others much slower, and some moved large distances, others much shorter. This suggests that the effect of spearing incidents on subsequent reactions to Maasai encounters is modulated by individual differences among elephants [ 20 Reale D.

Reader S.M.

Sol D.

McDougall P.T.

Dingemanse N.J. Integrating animal temperament within ecology and evolution. Although there were no overall differences in reaction to the cloth types between categories of elephant groups of different spearing experience, there was variation within the category of elephant groups with personal experience of being speared (high experience). The variance in travel speed and distance moved away from the Maasai-worn cloth was large in this group and significantly greater than the variance seen in elephant groups with low or medium experience of spearing (Levene's test of homogeneity of variance on untransformed data between high-, medium-, and low-spearing-experience groups: travel speed: F= 14.462, p < 0.001; distance moved: F= 6.036, p = 0.011; pairwise comparisons of travel speed: high: low experience; p < 0.001, high: medium experience; p = 0.004; pairwise comparisons of distance moved: high: low p = 0.007; Bonferroni corrections used in each case). Thus, elephant groups with personal experience of being speared did not all react in the same way to the scent of a Maasai-worn garment; some moved away very quickly, others much slower, and some moved large distances, others much shorter. This suggests that the effect of spearing incidents on subsequent reactions to Maasai encounters is modulated by individual differences among elephants [].