Proximate mechanisms underlying tactical deception and counter-deception in capuchin monkeys: stress and skepticism?

Background

The abilities to deceive and anticipate that other will attempt to deceive are argued to have been important factors favoring the evolution of large brains in primates. While many cases of apparent “tactical deception” and “counter-deception” have been observed in a range of primate taxa, the anecdotal nature of these observations has hampered research into the proximate mechanisms that underpin these behaviors. It is thus unclear if they are indeed underpinned by complex cognitive mechanisms, as would be expected if large, expensive brains are necessary to deploy them.

Experimental work with wild tufted capuchin monkeys (Cebus apella nigritus) in Iguazú National Park, Argentina has shown that individuals produce a particular type of alarm call (“hiccups”) when they detect felid predators, and listeners regularly respond to these calls with anti-predator reactions, including running up higher in the trees (Wheeler, 2010a; b). In addition, some individuals regularly produce the calls in the absence of predators but during intensely competitive feeding contexts, often causing listeners to run out of the food patch and allowing the caller to gain access to the contested food (Wheeler, 2009). Such usage of false alarms is suggestive of “tactical deception” (sensu Byrne and Whiten, 1992). However, the effectiveness of the strategy is limited by the fact that listeners are more likely to ignore hiccups given in the competitive feeding contexts than those given in noncompetitive contexts, when calls are more likely to actually indicate that a predator is present (Wheeler, 2010a). Such patterns of response suggest that listeners may be employing counter-deception, perhaps based on either the perception of subtle acoustic differences between honest and deceptive alarms, or skepticism of the reliability of calls given in certain contexts.

While the cognitive mechanisms involved in the perception of vocalizations among primates are relatively sophisticated, with listeners appearing to attach meanings to particular signals, the production of those same vocalizations seems to be based on simpler mechansisms and tightly linked with specific emotional states (Wheeler and Fischer, 2012). Thus although it is highly plausible that counter-deception by capuchins is based on skepticism of deceptive false alarms, it seems less likely that the deceptive behavior itself is underpinned by an intention to change the beliefs or even just the behavior of listeners. Instead, production of the calls may be better seen as a reflection of the caller’s internal state, perhaps driven by the stress or anxiety induced by competitive situations.

Research questions

Does an increase in the production of glucocorticoids (GCs; “stress hormones”) in some individuals during competitive feeding explain their use of deceptive false alarms? Alternatively, even if GCs are not associated with deceptive alarm calling, is it plausible that the false alarms are a reflection of the caller’s level of anxiety?

What accounts for the use of apparent counter-deception during feeding? Are listeners ignoring deceptive false alarm calls because they are don’t take those calls to mean that a predator is present? If so, is such variation in meaning attribution based on the perception of subtle acoustic differences between deceptive and honest alarms? Alternatively, do they take context into account and ignore calls given in contexts in which they are less likely to indicate that a predator has been spotted? Or is this not actually counter-deception at all, but rather a cognitively-simpler example of individuals deciding to ignore signals more generally due to their attention being focused on the feeding task at hand?

Method

This project integrates observations of behavior during three distinct types of field experiments (vocalizations playbacks, simulated predator encounters using ocelot decoys, and controlled and provisioning using wooden platforms suspended in the forest canopy and filled with banana pieces) with acoustic analysis of vocalizations and non-invasive monitoring of hormones (based on hormone metabolites extracted from fecal samples).

Findings so far and ongoing research

In terms of call production, the patterns of GC production do not match the patterns of false alarm production, and individuals do not appear to be characterized by higher GC levels on those occasions when they produce false alarms relative to when they do not give any call (Wheeler et al., 2014). As a number of studies have shown that GC output does not necessarily reflect an individual’s state of anxiety, ongoing work (with MSc student Donna Kean) is examining whether deceptive false alarms are associated with self-directed behaviors, which have been shown to be a reliable proxy for anxiety.

In terms of the perception of deceptive false alarms, variation in responses across contexts does not appear to be due to perceived acoustic differences between honest and deceptive alarms, but rather to the context in which the call is heard (Wheeler and Hammerschmidt, 2013). In remains unclear, however, if listeners use contextual cues to attribute different meanings to the calls, or if they always take the calls to mean that a felid predator is present, but that they decide to take a risk and ignore the calls when responding would result in the loss of food. Ongoing playback experiments aim to distinguish between these two possibilities. Related experiments are being conducted to test the extent to which listener responses to predator-associated vocalizations can be explained as a result of either associative or social learning.

References

Byrne R, Whiten A. 1992. Cognitive evolution in primates: evidence from tactical deception. Man 27:609–627.

Wheeler BC. 2009. Monkeys crying wolf? Tufted capuchin monkeys use anti-predator calls to usurp resources from conspecifics. Proc R Soc Lond B 276:3013–3018.

Wheeler BC. 2010a. Decrease in alarm call response among tufted capuchin monkeys in competitive feeding contexts: possible evidence for counterdeception. Int J Primatol 31:665–675.

Wheeler BC. 2010b. Production and perception of situationally variable alarm calls in wild tufted capuchin monkeys (Cebus apella nigritus). Behav Ecol Sociobiol 64:989–1000.

Wheeler BC, Fischer J. 2012. Functionally referential signals: a promising paradigm whose time has passed. Evol Anthropol 21:195–205.

Wheeler BC, Hammerschmidt K. 2013. Factors underpinning receiver responses to deceptive false alarm calls in wild tufted capuchin monkeys: is it counterdeception? Am J Primatol 75:715–725.

Wheeler BC, Tiddi B, Heistermann M. 2014. Competition-induced stress does not explain deceptive alarm calling in tufted capuchin monkeys. Anim Behav 93:49–58.