Anim Cogn (2012) 15:15–25 DOI 10.1007/s10071-011-0425-2 ORIGINAL PAPER Variance-sensitive choice in lemurs: constancy trumps quantity Evan L. MacLean • Tara M. Mandalaywala • Elizabeth M. Brannon Received: 28 March 2011 / Revised: 23 May 2011 / Accepted: 26 May 2011 / Published online: 14 June 2011 Ó Springer-Verlag 2011 Abstract Numerous studies have demonstrated that ani- island of Madagascar. Lemurs have evolved diverse ana- mals’ tolerance for risk when foraging can be affected by tomical and behavioral traits for survival in a harsh and changes in metabolic state. Specifically, animals on a unpredictable ecology, and these traits have been explained negative energy budget increase their preferences for risk, as forms of anatomical and behavioral risk reduction. We while animals on a positive energy budget are typically therefore predicted that lemurs would also be risk-averse in risk-averse. The malleability of these preferences may be a behavioral task that offered subjects a choice between a evolutionarily advantageous, and important for maximizing small certain reward, and an uncertain but potentially large chances of survival during brief periods of energetic stress. reward. In Experiment 1, the average rewards associated However, animals adapted to living in unpredictable con- with the constant and variable options were equal and ditions are unlikely to benefit from risk-seeking strategies, lemurs exhibited high levels of risk-aversion, replicating a and instead are expected to reduce energetic demands phenomenon that has been demonstrated in dozens of taxa. while maintaining risk-aversion. We measured risk pref- In Experiment 2, we gradually increased the average value erences in lemurs, a group of primates restricted to the of the variable option relative to the constant option. Lemurs’ preferences tracked these changes and subjects became more risk-seeking as the risk premium increased. Electronic supplementary material The online version of this However, many subjects maintained high levels of risk- article (doi:10.1007/s10071-011-0425-2) contains supplementary aversion even when the average payout of the variable material, which is available to authorized users. option yielded double that of the constant option. These E. L. MacLean (&) results are consistent with the notion that lemur cognition Department of Evolutionary Anthropology, Duke University, has evolved to minimize risk in an unpredictable island Box 90383, Biological Sciences Building, environment. Durham, NC 27708, USA e-mail: [email protected] Keywords Risk Á Variance-sensitivity Á Cognition Á T. M. Mandalaywala Lemur Á Primate Á Evolution Institute for Mind and Biology, The University of Chicago, Chicago, IL, USA T. M. Mandalaywala Introduction Department of Comparative Human Development, The University of Chicago, Chicago, IL, USA Risk is implicit in nearly all decisions an animal makes. E. M. Brannon Whether deciding between foraging patches, potential Center for Cognitive Neuroscience, mates, or sleeping sites, animals are routinely faced with Duke University, Durham, NC, USA decisions between options that differ in the variance of their potential outcomes. How animals navigate these E. M. Brannon Department of Psychology and Neuroscience, decisions, and the factors that influence the decision- Duke University, Durham, NC, USA making process has generated much theoretical and 123 16 Anim Cogn (2012) 15:15–25 empirical work in disciplines ranging from behavioral should prefer this option to other food sources with greater ecology (Stephens 2008) to neuroeconomics (Platt and variance in energetic yield (Stephens 1981). Thus, the Huettel 2008). Several recent articles have addressed majority of species living in stable, energetically produc- whether stable preferences for risk can be understood as tive environments are predicted to be risk-averse. How- adaptations to particular problems that species face in their ever, if faced with a scenario in which the less variant food natural environments (Watson and Platt 2008; Heilbronner supply will not meet an animal’s expected energetic needs et al. 2008; Gilby and Wrangham 2007; Rode and Wang for survival, the animal should switch to a higher risk food 2000). For example, Heilbronner et al. (2008) recently source that affords a greater chance of survival (Stephens compared the risk preferences of chimpanzees and bono- 1981; Caraco et al. 1980; Caraco 1981). In other words, if bos, two closely related species that may have evolved the rate of energy gain associated with the less variant, behavioral and cognitive differences as a result of selective ‘‘safe’’ food supply falls short of that needed for survival, pressures relevant to foraging. Compared to bonobos, adopting a risk-seeking strategy offers the only chance of chimpanzees face more variability in the distribution and survival and should become the favored strategy. availability of their food sources, rendering foraging a Importantly, these shifts in risk preference that are asso- relatively less predictable activity. When tested in a task ciated with changes in metabolic state are thought to rep- that allowed subjects to choose either a certain intermediate resent only short-term adaptations to an organism’s amount of food or a gamble with a 50% chance of changing environment (Caraco 1981). Thus, a small bird obtaining a larger or smaller reward, chimpanzees chose living in a generally stable energetic environment may sur- the risky option more frequently than bonobos. These vive one or two extremely cold nights by switching to a results were interpreted as reflecting different species-typ- riskier food source. However, long-term dependence on ical foraging preferences that affected subjects’ choices in such a highly variable food source is sure to produce as many the experimental task (Heilbronner et al. 2008). Here, we shortcomings as it is windfalls. Therefore, the preference for applied a similar rationale in exploring the preferences of risk is not thought to be a viable long-term adaptation for lemurs, a group of primates adapted to living in the harsh species living in energy-poor environments (McNamara and unpredictable environment of Madagascar (Wright 1996). Rather, ‘‘survivorship might be better enhanced by 1999). reducing energetic requirements (if possible) and main- In a typical risky choice task, an animal is given a taining risk-aversion, rather than adopting a long-term risk- choice between two options, one of which yields a reward prone strategy in a poor environment’’ (Caraco 1981). that is constant in amount, the other of which varies, but Lemurs provide an interesting case for evaluating the has the same average value across trials. Animals’ attitudes predictions of this hypothesis because they possess many toward risk are inferred based on their preference for the anatomical and behavioral traits thought to have evolved constant or variable options. Throughout this article, we for exactly this purpose: energy conservation and risk use the terms ‘‘risk-seeking’’ and ‘‘risk-averse’’ to describe minimization (Wright 1999; Jolly 1966). Lemurs are pri- these preferences (Kacelnik and Bateson 1997; Bateson mates who last share a common ancestor with monkeys and and Kacelnik 1998). However, it should be noted that the apes approximately 75 million years ago (Horvath et al. economic definition of risk implies certainty of the prob- 2008), and who have been geographically restricted to the abilities associated with each option (Knight 1921; Luce island of Madagascar for over 50 million years (Yoder and Raiffa 1957), a criterion that is not likely met in many et al. 1996). Compared to other primate habitats, Mada- animal studies of variance-sensitive choice. When faced gascar is unusually susceptible to droughts, cyclones, with a risky choice, the majority of species that have been periods of frost and cold, and a highly seasonal fruit supply studied prefer the option that yields a constant amount of (Wright 1999). As a consequence, most lemur habitats are food (Kacelnik and Bateson 1996). That is, most species considered to be relatively unpredictable and energetically are risk-averse when the average gains between the safe stressful (Jolly 1966). Compared to monkeys and apes, and risky options are equal. lemurs have many unusual anatomical and behavioral However, these baseline levels of risk-aversion fre- traits, all of which are thought to be adaptations for sur- quently shift in response to changes in an animal’s meta- vival in an energetically scarce and frequently unpredict- bolic state. Specifically, animals tend to become more risk able ecology. Among these traits are strict seasonal prone when making choices on a negative energy budget, breeding, cathemerality (equal activity during both day and but more risk averse when on a positive energy budget night), low basal metabolic rates, a low degree of frugivory (reviewed in Kacelnik and Bateson 1996). This phenome- (a highly variable food source) for primates of their body non has been explained by risk-sensitive foraging theory size, female dominance, and a lack of sexual dimorphism which proposes that animals with access to a consistent (reviewed in Wright 1999). Given the costs of pregnancy food source that meets the energetic demands of survival and lactation in lemurs, females of many lemur species are 123 Anim Cogn (2012) 15:15–25 17 dominant to males in feeding contexts, an adaptation reward delivery was housed in a custom-built, stainless believed to ensure sufficient