Lessons from vervets and macaques

1. Lessons from vervets and macaques MSc ACSB module 2006/07 AC Session 3

2. Vervet monkey alarm calls • Cheney & Seyfarth: "How monkeys see the world“ Vervet monkeys (tree + ground living monkey, Africa) • Predators = Leopard, Monkey-eating Eagle, Python, + baboons, etc, and 3 calls • Eagle gets a Cough, • Snake gets a Chutter • Leopard gets a Bark

3. Vervet alarm-call responses • Behave appropriately when they hear one of these calls (run down from treetops / walk carefully / run up into trees) • Do they know what messages the calls carry? (e.g “There is an Eagle, / a Snake, / a Leopard”) • Film response to plausible taped call; no real caller whose behaviour might give hearers a clue to the right response • 3 responses are given in appropriate contexts using just the information in the call itself, showing the monkeys are responding to the acoustic signals, not just to caller’s concurrent behaviour

4. Vervet calls on www • http://www.wjh.harvard.edu/~mnkylab/media/vervetcalls.html

5. Vervet alarm calls provide information… • … about environment, not about signaller’s motivational state (e.g. different levels of fear) – equivalent of words for the 3 predators? • Nearer to language than the displays considered last time – is call-use learned c.f. word-use? • Are monkey vocalisations acquired/learned? • Not in squirrel monkey - innate. • Perhaps in X-fostered Japanese & rhesus macaque food-coos • Learning probably contributes in vervets

6. Ontogeny of vervet predator calls • Vervet infants give alarms to appropriate class of stimuli, but too wide a spread of targets within each class • “Leopard” to many large ground animals • “Eagle” to birds of all sorts • “Snake” to sticks and other long thin objects • As grow up, they focus alarms down on the real predators, the class-members that spell danger

7. Vervet call development (2)

8. Vervet call development (3) Probability of adult alarm call after infant has given eagle alarm call – high only to Martial eagle + 1 other sp. Infants give fewer wrong and more adult-like responses to alarm call playback as they grow older

9. Vervet call development (4) • Narrowing down of call-triggers may depend on response from adults: take up and repeat alarm to real hazards, ignore it to a harmless stimulus • Responses to alarm calls not fully adult • Initially respond after looking at an adult which has started to respond • More often show adult-like response when near mother than when mother has wandered away • Vervets use wrrr-call to indicate threat from another group; experience shapes its correct use over 1st two years of life (earlier if more frequently in contact with other groups)

10. Involuntary or voluntary? • High ranking vervets call more often, and are more often the first to call; but don’t scan for predators more often. So subordinates must also scan and detect predators, but omit call • Females call more readily if kin present • Captive males call more when female companion(s) than when companion is male • Never call “eagle” when should say “leopard”

11. Is this alarm call system unique? • Calls provide info about dangers, not level of fear • Vervet monkey grunts (Cheney & Seyfarth) • Can't be distinguished by ear by humans • 4 types: Dom>Sub, Sub>Dom, Move Into Open, see Another Group • Difference in response to taped grunts indicates monkeys can separate them, appropriate information conveyed, e.g. • MIO : listener looks towards loudspeaker • AG: looks away towards where loudspeaker points

12. Vervet grunts 16 acoustic parameters from one female: 82% correct classification of her calls and others' calls Spectrographically distinct but cannot be distinguished by ear by humans

13. Rhesus macaque screams • Rhesus & pigtail macaque screams studied by Gouzoules • Rhesus has 5 types of scream – code for • Rank of the opponent • Whether a relative (safer) or non-kin (risky) • Whether or not any physical contact • Pigtail has 4 types of scream

14. Rhesus screams (2) • High rank, contact • Low rank, no contact • Relative, or • High rank, no contact • Relative • High rank, no contact

15. Interim conclusions • In Vervet alarm call system, information is encoded in specific calls; coding is partly pre-wired but is refined by experience • Several other call systems which communicate environmental information • Kitui used the leopard call (sans leopard) to halt a fight that his troop were losing – but then walked across ground repeating the call, which made it plain to humans that there was no real danger

16. What information is in a call? • Do primates lump-together different calls that refer to the same thing? • Habituation • Do primates learn to ignore specific calls, or to distrust a mental state (eg fear) in the caller? • Are changes in risk tied to a particular threat? • Do callers aim to inform, or to trigger a specific response?

17. Rhesus food calls • 4 food calls • Warble, Harmonic Arch (Good food) • Coos, Grunts (low-quality food) • S1 and S2 initially elicit orientation • Habituate S1, then test S2, where S2 may be a different signal for same quality of food, or a different signal for different-quality food

18. Hauser’s results • Hauser, 1998, Anim Behav 55, 1647-1658 • Habituate response to one HQ food call: • Eliminates response to other HQ call • Leaves intact response to LQ calls • Habituate response to one LQ food call: • Leaves intact responses to HQ food calls

19. Cheney & Seyfarth - Vervet • Inter-group calls: • Wrr (low arousal – just spotted) & Chutter (high arousal – scrap going on or likely) • Habituation paradigm: • Test Chutter; habituate Wrr (same #); re-test Chutter • Decreased response if all 3 stimuli for same hazard, from same #, not if different monkeys’ calls used • Implications: • know that A and B represent the same threat, conclude that this # has become unreliable about other groups • No decrement if calls represent different threats

20. Superb staring alarms • Aerial and ground predator alarms • Test starling alarms: habituate vervet eagle alarm; test starling alarms again • Decreased response to starling eagle alarm • No decrement for starling ground predator call • Have learned to be sceptical about (any) warnings about aerial predators, not just habituated to vervet coughs specifically

21. What does caller aim to achieve? • In Cameroon, vervets attacked by feral dogs • Dogs trigger ‘leopard’ alarm, troop runs into trees • Elsewhere, hunted by men with dogs + guns • Leopard alarm would attract attention and a shot • So dogs trigger a quiet call that allows troop to flee silently • Monkey link signals to the action that the signal needs to achieve

22. Limits on understanding • Kitui used a leopard-call to stop a fight (deception?), but then walked across ground showing that there was probably no leopard – none of the hearers noticed the incongruity • Vervets also can’t recognise other indirect cues to danger – e.g., snake track on ground, or antelope carcass stored in tree (which signals that a leopard is nearby)

23. References – session 6 • Cheney & Seyfarth (1992) Behavioral and Brain Sciences, 15, 135-147 (commentary 147-182) • Cheney & Seyfarth (1990) How monkeys see the world, Ch. 3-6. • Seyfarth & Cheney (2003) Meaning and emotion in animal vocalizations. Annals of the New York Academy of Sciences, 1000, 32-55. • Hauser (1997) The evolution of communication. Ch. 5, 7