Jeffrey R. Stevens

Why be nice? Psychological constraints on the evolution of cooperation

Animals often aid others without gaining any immediate benefits. Although these acts seem to reduce the donors fitness, they are only apparently altruistic. Donors typically help because they or their kin receive future benefits or avoid costly punishment. Reciprocal altruism--alternating the roles of donor and recipient--has been a well-studied form of cooperation among non-kin because of its intuitive appeal in explaining human cooperation. Despite immense theoretical interest, little empirical evidence substantiates the biological importance of reciprocal altruism in non-human animals. We propose that this is because psychological mechanisms constrain its application in cooperative contexts. In particular, we contend that cognitive limitations such as temporal discounting, numerical discrimination and memory make reciprocity difficult for animals.

The ecology and evolution of patience in two New World monkeys

Decision making often involves choosing between small, short-term rewards and large, long-term rewards. All animals, humans included, discount future rewards—the present value of delayed rewards is viewed as less than the value of immediate rewards. Despite its ubiquity, there exists considerable but unexplained variation between species in their capacity to wait for rewards—that is, to exert patience or self-control. Using two closely related primates—common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus)—we uncover a variable that may explain differences in how species discount future rewards. Both species faced a self-control paradigm in which individuals chose between taking an immediate small reward and waiting a variable amount of time for a large reward. Under these conditions, marmosets waited significantly longer for food than tamarins. This difference cannot be explained by life history, social behaviour or brain size. It can, however, be explained by feeding ecology: marmosets rely on gum, a food product acquired by waiting for exudate to flow from trees, whereas tamarins feed on insects, a food product requiring impulsive action. Foraging ecology, therefore, may provide a selective pressure for the evolution of self-control.

A fruit in the hand or two in the bush? Divergent risk preferences in chimpanzees and bonobos

Human and non-human animals tend to avoid risky prospects. If such patterns of economic choice are adaptive, risk preferences should reflect the typical decision-making environments faced by organisms. However, this approach has not been widely used to examine the risk sensitivity in closely related species with different ecologies. Here, we experimentally examined risk-sensitive behaviour in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), closely related species whose distinct ecologies are thought to be the major selective force shaping their unique behavioural repertoires. Because chimpanzees exploit riskier food sources in the wild, we predicted that they would exhibit greater tolerance for risk in choices about food. Results confirmed this prediction: chimpanzees significantly preferred the risky option, whereas bonobos preferred the fixed option. These results provide a relatively rare example of risk-prone behaviour in the context of gains and show how ecological pressures can sculpt economic decision making.

The selfish nature of generosity: harassment and food sharing in primates

Animals may share food to gain immediate or delayed fitness benefits. Previous studies of sharing have concentrated on delayed benefits such as reciprocity, trade and punishment. This study tests an alternative model (the harassment or sharing–under–pressure hypothesis) in which a food owner immediately benefits because sharing avoids costly harassment from a beggar. I present an experiment that varies the potential ability of the beggar to harass, and of the owner to defend the food, to examine the effects of harassment on food sharing in two primate species: chimpanzees (Pan troglodytes) and squirrel monkeys (Saimiri boliviensis). For both species, high levels of harassment potential significantly increased both beggar harassment and sharing by the owner. Food defensibility did not affect harassment or sharing. Interestingly, squirrel monkeys and chimpanzees shared equally frequently with conspecifics despite a much higher natural sharing rate in chimpanzees. These results suggest that harassment can play a significant role in primate food sharing, providing a simple alternative to reciprocity. The selfish nature of harassment has implications for economic, psychological and evolutionary studies of cooperative systems.

Donor payoffs and other-regarding preferences in cotton-top tamarins (Saguinus oedipus)

Helping others at no cost to oneself is a simple way to demonstrate other-regarding preferences. Yet, primates exhibit mixed results for other-regarding preferences: chimpanzees and tamarins do not show these effects, whereas capuchin monkeys and marmosets preferentially give food to others. One factor of relevance to this no-cost food donation is the payoff to the donor. Though donors always receive the same payoffs regardless of their choice, previous work varies in whether they receive either a food reward or no food reward. Here, I tested cotton-top tamarins in a preferential giving task. Subjects could choose from two tools, one of which delivered food to a partner in an adjacent cage and the other of which delivered food to an empty cage. Thus, subjects could preferentially give or withhold food from a partner. I varied whether subjects received food payoffs, whether a partner was present or absent, and whether the partner was a non-cagemate or the subject’s mate. Results showed that the subjects’ overall motivation to pull either tool declined when they did not receive any food. Additionally, they did not preferentially donate or withhold food, regardless of their own payoff or their relationship with the partner. Thus, cotton-top tamarins do not take advantage of cost-free food giving, either when they might gain in the future (mates) or when they have no opportunity for future interactions (non-cagemates).

When quantity trumps number: discrimination experiments in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus)

The capacity for non-linguistic, numerical discrimination has been well characterized in non-human animals, with recent studies providing careful controls for non-numerical confounds such as continuous extent, density, and quantity. More poorly understood are the conditions under which animals use numerical versus non-numerical quantification, and the nature of the relation between these two systems. Here we test whether cotton-top tamarins and common marmosets can discriminate between two quantities on the basis of the amount of food rather than on number. In three experiments, we show that when choosing between arrays containing different numbers and sizes of food objects, both species based their decisions on the amount of food with only minor influences of numerical information. Further, we find that subjects successfully discriminated between two quantities differing by a 2:3 or greater ratio, which is consistent with the ratio limits found for numerical discrimination with this species. These studies demonstrate that non-human primates possess mechanisms that enable quantification of total amount, in addition to the numerical representations demonstrated in previous studies, with both types of quantification subject to similar processing limits.

Forgetting Constrains the Emergence of Cooperative Decision Strategies

Theoretical studies of cooperative behavior have focused on decision strategies that depend on a partners last choices. The findings from this work assume that players accurately remember past actions. The kind of memory that these strategies employ, however, does not reflect what we know about memory. Here, we show that human memory may not meet the requirements needed to use these strategies. When asked to recall the previous behavior of simulated partners in a cooperative memory task, participants performed poorly, making errors in 10-24% of the trials. Participants made more errors when required to track more partners. We conducted agent-based simulations to evaluate how well cooperative strategies cope with error. These simulations suggest that, even with few errors, cooperation could not be maintained at the error rates demonstrated by our participants. Our results indicate that the strategies typically used in the study of cooperation likely do not reflect the underlying cognitive capacities used by humans and other animals in social interactions. By including unrealistic assumptions about cognition, theoretical models may have overestimated the robustness of the existing cooperative strategies. To remedy this, future models should incorporate what we know about cognition.

The effect of handling time on temporal discounting in two New World primates

Foraging decisions in nonhuman animals often require choosing between small, immediate food rewards and larger, more delayed rewards. Faced with such choices, animals typically discount or devalue the future quite strongly. Although discounting studies often focus on delays to reward access, other temporal intervals contribute to foraging rate, and thus may potentially influence discounting levels. Here, we examine the effect of handling time, the time required to process and consume food, on discounting in cottontop tamarins, Saguinus oedipus, and common marmosets, Callithrix jacchus, two species that differ in levels of temporal discounting. We presented subjects with a discounting task under two conditions. In the first condition, we made the entire reward available after the delay expired. In the second condition, we experimentally increased the minimum length of time required to consume the reward to simulate a longer handling time. We found that tamarins and marmosets showed sensitivity to increases in the time necessary to process food rewards. Both species adjusted their preferences to account for different handling times at long delays to accessing food. Consequently, models of discounting behaviour that include handling times may better describe animal choices than models that focus exclusively on delays prior to access.

Intertemporal choice in lemurs

Different species vary in their ability to wait for delayed rewards in intertemporal choice tasks. Models of rate maximization account for part of this variation, but other factors such as social structure and feeding ecology seem to underly some species differences. Though studies have evaluated intertemporal choice in several primate species, including Old World monkeys, New World monkeys, and apes, prosimians have not been tested. This study investigated intertemporal choices in three species of lemur (black-and-white ruffed lemurs, Varecia variegata, red ruffed lemurs, Varecia rubra, and black lemurs, Eulemur macaco) to assess how they compare to other primate species and whether their choices are consistent with rate maximization. We offered lemurs a choice between two food items available immediately and six food items available after a delay. We found that by adjusting the delay to the larger reward, the lemurs were indifferent between the two options at a mean delay of 17 s, ranging from 9 to 25 s. These data are comparable to data collected from common marmosets (Callithrix jacchus). The lemur data were not consistent with models of rate maximization. The addition of lemurs to the list of species tested in these tasks will help uncover the role of life history and socio-ecological factors influencing intertemporal choices.

Evolutionary pressures on primate intertemporal choice

From finding food to choosing mates, animals must make intertemporal choices that involve fitness benefits available at different times. Species vary dramatically in their willingness to wait for delayed rewards. Why does this variation across species exist? An adaptive approach to intertemporal choice suggests that time preferences should reflect the temporal problems faced in a speciess environment. Here, I use phylogenetic regression to test whether allometric factors relating to body size, relative brain size and social group size predict how long 13 primate species will wait in laboratory intertemporal choice tasks. Controlling for phylogeny, a composite allometric factor that includes body mass, absolute brain size, lifespan and home range size predicted waiting times, but relative brain size and social group size did not. These findings support the notion that selective pressures have sculpted intertemporal choices to solve adaptive problems faced by animals. Collecting these types of data across a large number of species can provide key insights into the evolution of decision making and cognition.