Received: 13 September 2019 | Revised: 12 October 2020 | Accepted: 13 October 2020 DOI: 10.1002/ajp.23212 RESEARCH ARTICLE Comparative performance of orangutans (Pongo spp.), gorillas (Gorilla gorilla gorilla), and drills (Mandrillus leucophaeus), in an ephemeral foraging task Laurent Prétôt1 | Jennifer Mickelberg2 | Jodi Carrigan2 | Tara Stoinski2,3 | Redouan Bshary4 | Sarah F. Brosnan1,5 1Department of Psychology and Language Research Center, Georgia State University, Abstract Atlanta, Georgia, USA A goal of the comparative approach is to test a variety of species on the same 2Zoo Atlanta, Atlanta, Georgia, USA task. Here, we examined whether the factors that helped capuchin monkeys 3Dian Fossey Gorilla Fund International, Atlanta, Georgia, USA improve their performance in a dichotomous choice task would generalize to 4Department of Behavioral Ecology, three other primate species: orangutans, gorillas, and drill monkeys. In this task, University of Neuchâtel, Neuchâtel, subjects have access to two options, each resulting in an identical food, but one Switzerland (the ephemeral option) is only available if it is chosen first, whereas the other 5Department of Philosophy, Neuroscience Institute, Center for Behavioral Neuroscience, one (the permanent option) is always available. Therefore, the food‐maximizing Georgia State University, Atlanta, solution is to choose the ephemeral option first, followed by the permanent Georgia, USA option for an additional reward. On the original version (plate task), the options Correspondence were discriminated by the color and pattern of the plates holding the food, Laurent Prétôt, Department of Psychology while on two subsequent versions we used altered cues that we predicted and Counseling, Pittsburg State University, Pittsburg, KS 66762, USA. would improve performance: (1) the color of the foods themselves (color task), Email: [email protected] which we hypothesized was relevant to primates, who choose foods rather than substrates on which foods are found when foraging, and (2) patterned cups Funding information GSU Second Century Initiative in Primate covering the foods (cup task), which we hypothesized would help primates Social Cognition, Evolution & Behavior avoid the prepotent response associated with visible food. Like capuchins, all Dissertation Grant (2CI‐PSCEB); Division of Social and Economic Sciences, three species initially failed to solve the plate task. However, while orangutans Grant/Award Number: 1425216; improved their performance from the plate to the color task, they did not for Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung, the cup task, and only a few gorillas and no drills succeeded in either task. ‐ Grant/Award Number: P1SKP1 151775 Unfortunately, our ability to interpret these data was obscured by differences in the subjects' level of experience with cognitive testing and practical con- straints that precluded the use of completely identical procedures across species. Nonetheless, we consider what these results can tell us, and discuss the value of conducting studies across multiple sites despite unavoidable differences. KEYWORDS comparative research, Gorilla gorilla gorilla, Mandrillus leucophaeus, Pongo spp. Am J Primatol. 2020;e23212. wileyonlinelibrary.com/journal/ajp © 2020 Wiley Periodicals LLC | 1of16 https://doi.org/10.1002/ajp.23212 2of16 | PRÉTÔT ET AL. 1 | INTRODUCTION tasks, on which primates generally do well (Beran et al., 2014; Beran, 2002; Evans & Westergaard, 2006; Miller et al., 2019; Parrish et al., Comparative research is critical for understanding similarities and 2014; Stevens, 2017). In particular, the current task resembles delay differences in species' cognition and behavior, which can highlight of gratification procedures, in that subjects choose between two how abilities evolved and what factors may have influenced their options, but one provides an additional delayed reward (although in evolution. In particular, it is impossible to know whether factors in- this case the subjects get some reward immediately no matter what fluencing one species are due to unique aspects of that species or are they choose, whereas in at least some delay of gratification tasks more general across a taxon without testing a variety of species. This there is no immediate benefit to the delayed option). Indeed, some can be challenging for several reasons, including intrinsic differences have predicted that the capacity to first select the food‐maximizing in species (e.g., body plan, size, ecology, primary sensory system) and (ephemeral) option in this task is likely influenced by the ability to more practical ones, such as a lack of access to relevant species for inhibit the prepotent response associated with the immediacy of the the question at hand and, because most facilities only house one or a rewards (Zentall, 2019; Zentall et al., 2018), although the evidence few species, the challenges of using identical protocols across dif- from intertemporal choice tasks suggests that most primates possess ferent species and facilities (Leavens et al., 2017; Rowe & Healy, sufficient inhibitory ability for the short time intervals required for 2014; Smith et al., 2018). As a result, we have a priori introduced the current procedure (Stevens, 2014, 2017). variables other than intrinsic species differences into our compar- One hypothesis for the primates' failure was that the cues used isons, such as enclosure size, husbandry habits, constraints on foods in the experiment were not obviously relevant to the primates, that can be given or procedures that can be run, and subjects' pre- meaning that they had to first learn the appropriate cue and then the vious experiences. Unfortunately, many of these may influence re- contingencies of the task (following Lotem & Halpern, 2012). In the sults; for instance, apes respond differently to perspective‐taking task, the cue was the color of the substrate on which the food was tasks depending on the spatial arrangement of the experimental placed (i.e., the color and pattern of the tray) rather than the foods, setup (Bräuer et al., 2007; Mulcahy & Call, 2009). When such see- which were identical in the different options. This is typically re- mingly superficial details can affect research, it may seem that levant to cleaner fish, who choose clients and then eat the nearly comparative research is tilting at windmills. Nonetheless, even when invisible parasites (though some cleaners may choose based on size we must make educated guesses at what is the cause of the differ- rather than color‐pattern, which negatively affects their perfor- ences the data are valuable, and as they accumulate across multiple mance; Wismer et al., 2019), but not to primates, who choose foods studies, we eventually have enough for more certainty in our directly (i.e., the fruit or insect rather than the tree itself, which will interpretations. not tell you if the fruit is ripe or if there is an insect present). Thus, In the current study, we explored whether factors that helped we tested capuchins' performance when the cue was the color of the capuchin monkeys to solve a dichotomous choice task would also food rather than the plate, which increased performance to the level help other primates to see whether these factors were specific to of the fish, including for monkeys who had not participated in the capuchins or more broadly beneficial across primates. The task was a original task, suggesting that this cue was important for the monkeys dichotomous choice in which subjects were given two options, one of (Prétôt et al., 2016b). which was always available (the permanent option) and one of which A second hypothesis was that the visibility of the food might was only available if it was chosen first (the ephemeral option). The have impacted the primates' performance. Primates' performance in maximizing solution is to choose the ephemeral option first, then the some choice tasks is negatively impacted by the presence of visible permanent one. This task was originally developed for use with rewards, presumably because they cannot inhibit their impulse to cleaner fish, a species that forages by consuming microscopic para- grab the food (Boysen & Berntson, 1995; Murray et al., 2005), thus sites off of other fish species, called clients. Cleaners' skill at the task we predicted that if the foods were hidden, subjects might do better. varies with the complexity of their natural ecology: cleaners from a For this task, the cue was the cover that needed to be lifted off to see complex ecology in which clients have multiple options solve the task and obtain the food. A second potential benefit to this procedure was easily (Bshary & Grutter, 2002), whereas those from less complex that when food is hidden, it cannot be used as the cue, which might environments, in which client fish have fewer cleaning options, fail to encourage them to use an alternate cue. Although we could not solve the task (Triki et al., 2018, 2019; Wismer et al., 2014). This distinguish among these possibilities (which are also not mutually suggests that there may have been environmental influences on how exclusive), our goal was to determine if there were procedural different species deal with the task. Indeed, a learning model pro- changes that would impact the monkeys' performance. As with poses that client fish density in combination with client behavior changing the cue to the color of the food, hiding the food under causes the variation in cleaner performance