Behavioral and Brain Sciences How foraging works: Uncertainty magnifies food-seeking motivation cambridge.org/bbs Patrick Anselme and Onur Güntürkün Target Article Faculty of Psychology, Department of Biopsychology, University of Bochum, D-44801 Bochum, Germany. [email protected], www.bio.psy.rub.de and Faculty of Psychology, Department of Biopsychology, University Cite this article: Anselme P, Güntürkün O. of Bochum, D-44801 Bochum, Germany. [email protected], www.bio.psy.rub.de (2019) How foraging works: Uncertainty magnifies food-seeking motivation. Behavioral Abstract and Brain Sciences 42, e35, 1–59. doi:10.1017/ S0140525X18000948 Food uncertainty has the effect of invigorating food-related responses. Psychologists have noted that mammals and birds respond more to a conditioned stimulus that unreliably pre- Target Article Accepted: 25 February 2018 dicts food delivery, and ecologists have shown that animals (especially small passerines) con- Target Article Manuscript Online: 8 March 2018 sume and/or hoard more food and can get fatter when access to that resource is unpredictable. Commentaries Accepted: 19 September 2018 Are these phenomena related? We think they are. Psychologists have proposed several mech- Keywords: anistic interpretations, while ecologists have suggested a functional interpretation: The effect animal behavior; causal model; dopamine; fat of unpredictability on fat reserves and hoarding behavior is an evolutionary strategy acting reserves; food seeking; functional model; against the risk of starvation when food is in short supply. Both perspectives are complemen- incentive motivation; reward uncertainty tary, and we argue that the psychology of incentive motivational processes can shed some light on the causal mechanisms leading animals to seek and consume more food under uncertainty What is Open Peer Commentary? What in the wild. Our theoretical approach is in agreement with neuroscientific data relating to the follows on these pages is known as a role of dopamine, a neurotransmitter strongly involved in incentive motivation, and its plau- Treatment, in which a significant and sibility has received some explanatory and predictive value with respect to Pavlovian phenom- controversial Target Article is published along with Commentaries (p. 15) and an ena. Overall, we argue that the occasional and unavoidable absence of food rewards has Authors’ Response (p. 40). See bbsonline. motivational effects (called incentive hope) that facilitate foraging effort. We show that this org for more information. hypothesis is computationally tenable, leading foragers in an unpredictable environment to consume more food items and to have higher long-term energy storage than foragers in a pre- dictable environment. 1. Introduction To explain animal behavior, functional but also causal interpretations are necessary (Tinbergen 1963). The former attempts to determine why (for which survival or reproductive purpose) specific actions are performed, while the latter tries to determine how (by which bio- logical and psychological mechanisms) those specific actions are performed. In this article, we examine the counterintuitive, though well-documented, evidence that individuals (at least in birds and mammals, including humans) exposed to unpredictable food supplies have higher fat reserves and/or cache more food items than individuals exposed to predictable food sup- plies. We show that the evolutionary origin (the why) of that phenomenon is quite well under- stood, but that the causal mechanisms (the how) contributing to increase fat reserves or to stimulate hoarding behavior remain largely unquestioned and therefore unknown (Pravosudov 2007). Here, we suggest a causal theory inspired from psychology and neurosci- ence to explain the mechanisms leading food unpredictability to enhance food seeking, a behavior that may enable animals to find more food items and hence to get fatter or to cache more items when the available amounts of food remain sufficient (e.g., Pravosudov 2003). Our causal mechanism is viewed as an adaptive consequence of the selective pressures (notably starvation and predation risks) that justify the functional interpretation put forward by behavioral ecologists. Importantly, this inquiry has the potential to also uncover processes that may underpin apparently unrelated behaviors such as drug addiction (Robinson & Berridge 1993), pathological gambling (e.g., Linnet et al. 2012), and obesity problems (Nettle et al. 2017). The words uncertainty and unpredictability are used interchangeably and simply mean that a trial (or attempt to get food) is rewarded or nonrewarded on a random basis in a specific environment, independent of the proportion of time spent in that environment relative to another environment. An animal may experience uncertainty over repeated sessions in a Skinner box, a situation in which the exact same number of rewarded and nonrewarded trials © Cambridge University Press 2019 occurs on each session. In nature, not all foraging bouts (or sessions) are likely to be similarly rewarded, especially when food is scarce. Some foraging bouts may be unsuccessful because of unfavorable meteorological conditions, whereas others are more profitable. But overall, the animal also experiences uncertainty over repeated foraging bouts in the environment in which it is used to seeking food. In all cases, uncertainty or unpredictability results in this Downloaded from https://www.cambridge.org/core. Institut d'Architecture, on 28 Apr 2019 at 10:30:50, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0140525X18000948 2 Anselme and Güntürkün: How foraging works: Uncertainty magnifies food-seeking motivation simple – but crucial – effect: the individual’s inability to predict mechanisms have been proposed to explain this effect at a causal whether the next foraging trial in a given environment will be level (Anselme 2015a; Hug & Amsel 1969; Pearce & Hall 1980), rewarded or not. The goal of this article is to describe how organ- and there is strong evidence that food uncertainty recruits the isms psychologically deal with such an absence of predictive con- brain reward system, in particular, the release of dopamine from trol at the trial level, in a way that fits the functional perspective the midbrain (de Lafuente & Romo 2011; Dreher et al. 2006; on behavior. Fiorillo et al. 2003; Hart et al. 2015; Preuschoff et al. 2006;Tan In behavioral ecology, hundreds of publications report that & Bullock 2008). Accordingly, higher dopamine levels in the animals, like small passerines and rodents, as well as humans, brain enhance the inclination to gamble both in animals and in accumulate more fat reserves and/or hoard more food items humans (e.g., Dodd et al. 2005; Johnson et al. 2011; Joutsa when their food sources are unpredictable, that is, hard to obtain et al. 2012; Tremblay et al. 2017). However, no functional perspec- and sometimes unavailable (e.g., Bauer et al. 2011; Brodin 2007; tive on this process has ever been discussed (e.g., Domjan 2005; Cresswell 2003; Cuthill et al. 1997; Ekman & Hake 1990; Foster Hollis 1997). In summary, two distinct research areas describe a et al. 2006; Gosler 1996; Hurly 1992; Lilliendahl 1998; similar phenomenon (enhanced responding to signals that food Lundberg 1985; MacLeod et al. 2007; Nettle et al. 2017; Polo & is uncertain), but one (ecology) approaches it from a functional Bautista 2006; Pravosudov 2003; Pravosudov & Grubb 1997; perspective only, whereas the other (psychology) approaches it Pravosudov & Lucas 2000; Ratikainen & Wright 2013; Rogers solely from a causal perspective. 1987; Witter & Swaddle 1995). Functionally, this phenomenon Could the increase in fat reserves or in hoarding behavior acts as insurance against starvation, because temporarily inacces- observed under harsh environmental conditions (ecology) and sible food items prevent animals from meeting their daily budget the increase in responding to a CS in a Skinner box (psychology) requirements. For example, Hake (1996) found that greenfinches be the consequences of a common underpinning mechanism? We (Carduelis chloris) with low social status carried larger body mas- think the answer to this question is yes. In this article, we provide ses than higher-ranked individuals. This occurred because domi- a comprehensive review of the literature on the stimulating effects nant individuals prevented them from accessing the most of food unpredictability, both in behavioral ecology and in behav- predictable food sites, increasing the risk of famine among subor- ioral psychology. We also discuss some neuroscientific data, dinate individuals. If bad weather conditions increased that risk because identifying brain correlates may help disentangle distinct for dominants as well, they could temporarily put on more fat mechanistic interpretations. On this basis, we suggest an integra- than subordinates. Extra fat plays a crucial role for survival. tive idea: Psychology and ecology describe the two faces (causal Fatter great tits (Parus major), for example, have a better survival and functional) of the same coin. In other words, enhanced rate than leaner individuals in the absence of beech mast during responding to unpredictable CSs in Pavlovian conditioning and winter (Gosler 1996). Hoarding behavior also provides insurance the increased fat reserves or increased hoarding in response to against starvation, with the advantage