Pretot-Et-Al-AJP-2020

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

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 constraints 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.

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 (Quiñones et al., 2020). patterned cups increased capuchins' performance (Prétôt et al., We previously tested this question with three nonhuman pri- 2016b) above that in the original study (Salwiczek et al., 2012). mates species, capuchin monkeys (Sapajus [Cebus] apella), chimpan- One key question is whether these cues are specific to ca- zees (Pan troglodytes), and orangutans (Pongo spp.), all of whom failed puchins, or generalize more broadly across the primate taxon. To to make the maximizing choice (Salwiczek et al., 2012). This was explore this, in the current study we tested three additional primate surprising given that the task is similar to other intertemporal choice species, orangutans, gorillas (Gorilla gorilla gorilla), and drill monkeys PRÉTÔT ET AL. | 3of16

(Mandrillus leucophaeus), on both of these tasks. As is often the case Note that we did not have a prediction as to how they would do with comparative research, however, there were several confounds. relative to the capuchins, but only to their own performance on the First, our subjects had different levels of experience with cognitive plate task. testing, and previous studies show a correlation between cognitive Nonetheless, these are broad brushes with which to paint very testing experience and task performance (Anderson et al., 2005; different primates, and there are reasons to predict differences Baenninger & Newcombe, 1989; Beran et al., 2016; Brosnan, Parrish, among the species. In particular, apes generally outperform monkeys et al., 2011; Klein et al., 2013; Leavens et al., 2017). For example, on cognitive tasks, including inhibitory control tasks (MacLean et al., Anderson et al. (2005) found that gorillas at Zoo Atlanta (including 2014), and while only a few studies have investigated cognition in some of our subjects), who performed more poorly than orangutans drill monkeys (Balasch et al., 1974; Maslow & Harlow, 1932), closely and chimpanzees in a numerical competence task and also had related baboons score lower than orangutans and gorillas (MacLean overall less experience with cognitive testing, improved their per- et al., 2014). Even among the apes, while gorillas and orangutans formance to the levels of the two other apes after introducing a show similar abilities at inhibiting the prepotent response in some corrective training procedure and switching to a set period of testing studies (Barth & Call, 2006; Call, 2004; Vlamings et al., 2006), others rather than a set number of trials. suggest that orangutans outperform gorillas (Amici et al., 2008; Unfortunately, this was difficult to quantify empirically, so we Amici et al., 2018; Vlamings et al., 2010). Thus, if all species perform relied on researchers' and keepers' memories of unpublished and similarly, this suggests that success at this task is supported by published past work. The orangutans had participated in numerous general intertemporal control and/or general ecological niches. If cognitive tasks, including some who participated in the earlier study none of the primates in the current study succeed, however, this (see Section 2 for additional detail), and are generally tested several might suggest that the greater experience of the capuchins swamped days a week, which gives them roughly comparable experience with any other factor. If the apes do equally well as the capuchins, but the the capuchin monkeys in the previous studies. In contrast, while the drills did not, this suggests that the absence of any experience by the gorillas in our sample had some experience with cognitive tasks, they drills negatively impacted their success. Finally, if the orangutans did not have as long or as frequent experience as the orangutans, and outperform the other two species, this could suggest either that their none had experience with our task. Finally, the drills in our sample greater level of experience or their greater success at some cognitive had, to our knowledge, never participated in a cognitive test of any tasks allowed them to succeed over the gorillas and drills, but we sort. To ensure that our subjects started with similar levels of ex- would be unable to distinguish between these possibilities. perience with the task itself, gorillas and drills received the plate task before the color and cup tasks, but this did not control for differences in the history of cognitive testing. 2 | METHODS Second, our procedures varied across species due to differences in the zoo's safety procedures for different species (see Section for 2.1 | Subjects and housing additional detail). Most importantly, the presentation of the stimuli differed between apes and monkeys, with orangutans and gorillas We tested six orangutans, nine western lowland gorillas, and six drill indicating their choice by gesturing to it while the drills, like ca- monkeys, all housed in social groups at Zoo Atlanta, Atlanta, GA, puchins, could pick the food directly from the plates. In addition, USA, between March 2015 and December 2016 (for group compo- subjects at Zoo Atlanta are typically not separated from group sitions and general information on each subject, see Table 1). While members, so many subjects were tested with other members of their all subjects received both the color task and the cup task, gorilla and social group present, which might have increased the risk of dis- drill subjects were first tested on the original plate task to have a traction while learning the task (the capuchins in the previous task similar experience with the task itself. All subjects were tested also only separate voluntarily, but more subjects choose to do so, during off exhibit. Orangutan test subjects included one Sumatran giving us a larger pool). Finally, for timing reasons orangutans were male (Dumadi), three Sumatran females (Madu, Biji, and Blaze), one not given the plate task in this study, so some orangutans never Bornean male (Satu), and one hybrid male (Chantek). Three of them received it and the others received it many years before the current (Satu, Madu, and Chantek) had been tested in Salwiczek et al. color and cup tasks (Salwiczek et al., 2012). (2012)'s original plate study and had failed. All subjects were also Our overarching hypothesis was that primates would behave tested in an unrelated computerized‐touchscreen task during the similarly to one another on these tasks and that they would do better period of our study, and some had participated in other computer- on the color and cup tasks than they did on the plate task, as the ized tasks (Diamond et al., 2016; Mallavarapu et al., 2013; Paxton capuchins did. Specifically, we predicted that they should all do Gazes et al., 2017) and manual cognitive tests (Anderson et al., 2007; better on the color task because they should focus on the foods Brosnan, Flemming, et al., 2011; Flemming et al., 2012; Mallavarapu, themselves, rather than the substrates that carried the foods, and 2009; Talbot et al., 2015) prior this one. One female, Madu, was that they should do better on the cup task because all primates are reared in a computer‐enriched environment at the Georgia State inhibited by visible food, and so covering the food should allow them University Language Research Center, where she participated in to better inhibit the prepotent response and so do better on the task. various cognitive tests (Beran, 2002; Washburn et al., 2007). In 4of16 | PRÉTÔT ET AL.

TABLE 1 Summary of the experiments

Subject Group Age Gender Separated? Experience (2012–present) Order

Orangutans Satua 1 11 M Occasionally Manual/computer Plate/cup/color* Madua 2 31 F No Manual/computer Plate/color/cup Chanteka 3 37 M Occasionally Manual/computer Plate/cup/color* Dumadi 3 8 M Occasionally Manual/Computer Color*/cup* Blaze 4 19 F No Manual/computer Cup/color Biji 5 44 F Yes Manual/computer Color*/cup

Gorillas Jasiri 1 17 M Yes – Plate/cup/color Kidogo 1 17 M Yes – Plate/color/cup Kekla 2 26 M Yes Computer Plate/cup/color Stadi 2 24 M Yes Manual/computer Plate/color*/cup Charlie 2 19 M Yes Manual/computer Plate/color/cup Mbeli 3 13 M Occasionally Manual/computer Plate/cup/color* Shamba 4 56 F Yes Computer Plate/color/cup Ozzie 4 54b M Yes Computer Plate/color/cup Choomba 4 52b F Yes Computer Plate/cup/color

Drills Inge 1 29 F Yes – Plate/cup/color Bobby 1 24 M Yes – Plate/color/cup Drew 2 18 F No – Plate/cup/color Lucy 2 17 F No – Plate/color/cup Achi 2 16 F Yes – Plate/cup/color Amaka 2 14 F Yes – Plate/color/cup

Note: Subjects' social group, age, sex, whether they were separated from other group members during testing, recent experience with manual and computer tasks, and study order, is indicated. Experience data are based on experimenters' memories of unpublished and published studies since 2012. Note that experiments in which subjects reached preference criterion for the ephemeral option in the initial learning test are indicated with an asterisk (*). aSubjects previously tested in the plate task (Salwiczek et al., 2012). bSubjects' year of birth was known but not the exact date, so those numbers were an estimate. addition, one male, Chantek, had previous experience using sign time were the subjects ever food or water deprived for testing pur- language to communicate with humans (Miles, 1990). poses. Experiments involved a single subject at a time. All subjects Gorilla test subjects included six bachelor males (Jasiri, Kidogo, participated voluntarily; they were called in from their social groups and Kekla, Stadi, Charlie, and Mbeli), two older females (Shamba and tested in one of the indoor dens of their living area or any suitable Choomba) and one older male (Ozzie). Although some subjects had portion of their enclosure. When possible, subjects were tested sepa- been the focus of a large number of behavioral studies, they had rela- rately from other members of their social group, which helped limit tively less experience with cognitive testing than the orangutans (some distractions, but if they chose not to we tested them with other group did participate in Anderson et al., 2005;Draytonetal.,2013; members present (see Section 2.3 for additional detail). All experiments Mallavarapu, 2009; Paxton Gazes et al., 2017; Stoinski et al., 2001). Drill were performed at Zoo Atlanta (Atlanta, GA) and were approved by the test subjects included one male (Bobby) and five females (Inge, Drew, Scientific Review Committee of Zoo Atlanta. Zoo Atlanta is fully ac- Lucy, Achi, and Amaka). Although the drills interact daily with their credited by the Association of Zoos and Aquariums (AZA). All the human keepers in the context of feeding and training, our records in- procedures in this study adhered to the American Society of Prima- dicate that they had never participated in any cognitive test before this tologists Principles for the Ethical Treatment of Non Human Primates, study. Subjects' recent experience with manual and/or computer tasks and met the standards of the United States. is indicated in Table 1 (for further details, see Table S1). All subjects had indoor/outdoor access and extensive material enrichment (climbing structures, ropes and swings, barrels, and other 2.2 | General procedure toys), and were fed their usual diet consisting of primate chow, fruits, and vegetables before or after testing. In addition, feeding enrichment The experimental design was based on the plate task designed by was provided on a daily basis as part of the husbandry routine. At no Salwiczek et al. (2012), and the color and the cup tasks designed by PRÉTÔT ET AL. | 5of16

Prétôt et al. (2016b). Subjects had to choose between two plates, one experimenter withdrew both plates and restarted the trial. For drills, representing the permanent choice and one the ephemeral choice. like capuchin monkeys, the plates were always within reach, so they When they chose a plate, they immediately received the food reward simply picked up their choice rather than gesturing and then taking on that plate. The permanent plate was available throughout the the reward when the plate was pushed forward by the experimenter. entire trial, whereas the ephemeral plate was available only if it was As with the apes, if a subject attempted to select both options si- the first one the subjects chose. If subjects chose the permanent multaneously, the plates were quickly removed and the trial re- plate first, the ephemeral plate was withdrawn out of reach of the started. Unlike in previous work with capuchin monkeys, however, subject, which resulted in only one reward for the trial. Thus, the we were unable to use a choice apparatus that required them to optimal order was to pick the ephemeral plate first, which allowed reach through yoked doors and therefore physically limited them to the subject to then also choose the permanent plate, for a total of a single choice (Prétôt et al., 2016b; Salwiczek et al., 2012). two rewards. The side on which each plate was presented for each Second, subjects were sometimes tested in presence of other trial was pseudo‐randomized such that each option was on each side members of their social group (Table 1). This was less frequent for an equal number of times during the course of a session, but with no gorillas—for which only one male (Mbeli) was occasionally tested more than three trials in a row on the same side. The food plates with group members present (two younger males)—and more fre- were equidistant from the subject and could be moved in- quent for orangutans and drills. For the orangutans, one female (Biji) dependently by the experimenter. Before the trial started, the ex- was tested alone, one female (Madu) was tested with a 4‐year‐old perimenter placed both foods simultaneously on the plates. The trial juvenile male present, and the other female (Blaze) was tested with started when the experimenter presented the plates to the subject. her 2‐year‐old infant male and an adult male present. One male Each subject received 10 sessions of 10 trials each (unless (Satu) was occasionally tested with an adult female and her 1‐year‐ otherwise noted; see Section 2.5 below for an exception). Subjects old infant present, and the other two males (Chantek and Dumadi) that reached preference criterion in the initial learning test were were occasionally tested with the other member present. For the then tested on a reversal test. The procedure was identical to the drills, the male (Bobby) and three females (Inge, Achi, and Amaka) initial test, but the role of each stimulus was reversed (i.e., the were tested alone, and two females (Lucy and Drew) were tested ephemeral stimulus became the permanent one, and vice‐versa). with another female present (Achi and Amaka, respectively). In si- These tests are frequently used to demonstrate flexibility in cogni- tuations in which subjects of the same social group did not separate tive processing (Rumbaugh, 1971, 1997; Salwiczek et al., 2012). prior testing, we would test the dominant individual first with the However, since so few subjects even received the reversal test (most subordinate present, then shifted him/her to another enclosure and individuals failed to solve the initial learning test), we present the worked with the subordinate individual alone. data but do not comment on them further. Finally, similarly to the capuchins, our orangutans either never Subjects were tested up to four sessions a week, but never in participated in the plate task or did so 4 years before the color and more than one session per day. The intertrial interval (ITI) was 30 s, cup tasks, whereas gorillas and drills, who had not previously been chosen because it was the ITI at which apes participated and per- tested on this task, did so approximately 1 month (4 months for one formed the best in the plate task (but note that this is different from gorilla subject, Mbeli) before the color and cup tasks. the capuchins, who performed best with a 5 min ITI; Salwiczek et al., 2012). All orangutan experiments were carried out prior the gorilla and the drill experiments. 2.4 | Apparatus and foods

The orangutan and gorilla plates were approximately 60 × 12 × 2 cm, 2.3 | Procedural modifications whereas the drill plates were approximately 34 × 10 × 0.5 cm (i.e., roughly scaled for body size; Figure 1). The plates were equipped As mentioned earlier, although we strove to keep the procedures as with a handle at the bottom to make the manipulations easier for the similar as possible across species, some differences were unavoidable experimenter. We used 750 mg banana‐flavored pellets for or- due to husbandry and facility differences. First, the presentation of angutans, 1 g Piña Colada flavored pellets for gorillas (unless the choices differed between the ape and the monkey experiments, otherwise noted), and raw shelled peanuts for drills. These foods in compliance with the zoo's safety procedures. Orangutans' and could be dyed different colors, as needed for the color task. gorillas' plates were presented out of reach (the distance varied between 40 and 60 cm) and they indicated their choice by gesturing to it with their hand (or lips, for those who had been trained that 2.5 | Coding and analysis way; Brosnan, Flemming, et al., 2011; Flemming et al., 2012). The experimenter then immediately pushed the plate forward so that the Subjects' decisions to choose the ephemeral or permanent option subjects could pick up the food from the plate, underneath the front were reported for each session. Sessions were videotaped and later mesh. If they gestured at both stimuli (e.g., by stretching out both recoded for accuracy by the first author. An independent video coder hands or moving their hand from one plate to the other), the recoded approximately 20% of the videos (1220 trials total). The 6of16 | PRÉTÔT ET AL.

FIGURE 1 Pairs of stimuli (named 1 and 2) used in the plate, color, and cup tasks. Capuchins' and orangutans' plates in the plate task are from Salwiczek et al. (2012); capuchins' plates in the color task and the cup task are from Prétôt et al. (2016b)

results of the inter‐rater analysis revealed a very high agreement including a preference for the permanent option) were then tested between coders (kappa value = 0.956). Disagreements were resolved on a reversal test, using the same criterion as in the initial learning by re‐watching the video. test. Because most of the primates who failed to solve the plate task We used the same learning criterion as in earlier work (Prétôt also developed a strong side bias (Salwiczek et al., 2012), we also et al., 2016a, 2016b). Subjects were considered to have solved the reported the overall percentage of left/right choices made by each test when they met the preference criterion for choosing the reward‐ subject in each task (as a measure of side preference). Also, because maximizing ephemeral option. This criterion was based on a two‐ we were comparing these results to those of an earlier study and tailed exact binomial/sign test, thus subjects met the preference therefore needed consistency, we did not add sessions for subjects criterion when they chose the option (1) 10/10 trials on one session who did not learn within the allotted 10 sessions, with the above (but only if the subject selected each of the two stimuli on at least exception. one trial of a previous session in the initial learning test, to ensure To compare subjects' performance between tasks, we used a that they had experience with both outcomes), (2) two consecutive two‐tailed exact Fisher's test to compare the number of individuals sessions of 9/10 or 8/10 trials, or (3) three consecutive sessions of 7/ who met criterion for preferring the ephemeral option to those who 10 trials. Although we planned to limit subjects to 10 sessions, if a did not; in this way, we could include data from all subjects, even subject chose one of the options 7 or more times in the last session those who developed a preference for the permanent option. To (i.e., Session 10), it was given another session (or two, in the case of compare subjects' performance across species in each experiment, sessions with 7/10, followed by a second session with 7 or more out we conducted two analyses. First, we used a two‐tailed exact of 10) of 10 trials to maximize its chances of reaching criterion. Kruskal–Wallis test; when the test result was significant, we used Subjects were considered to have failed if they either developed a two‐tailed exact Mann–Whitney U tests for pairwise comparisons preference for the permanent option (using the same criterion as for with a Bonferroni correction, resulting in a significance level set at the ephemeral option) or did not develop any preference within 10 p < .017 (i.e., 0.05/3, because there were three possible species sessions. Subjects who developed a preference for either option (i.e., comparisons). For this comparison, we used the data from subjects PRÉTÔT ET AL. | 7of16 who either preferred the ephemeral option or did not develop any triangles and one green circle, while Plate 2 had two blue rectangles preference, but did not use the data from the subjects who sig- (one of them striped). Five of the nine gorillas and three of the six nificantly preferred the permanent stimulus (although we reported drills were tested with Plate 1 as the ephemeral choice, whereas the them), because they were difficult to interpret (i.e., they “failed”, but other four gorillas and three drills were tested with Plate 2 as the had developed a consistent preference in fewer than 100 trials; for a ephemeral choice. One male gorilla (Stadi) was tested using purple full explanation on this issue, see Prétôt et al., 2016b). Subjects that grapes rather than pellets because he would not work for pellets. failed to develop a preference for the ephemeral option within 10 Note that one drill (Amaka) mistakenly received the food from the sessions were assigned 110 trials for the purposes of this analysis, ephemeral plate after choosing the permanent plate in one trial of which was one session greater than the minimum number of trials at Session 10. Also, one gorilla (Mbeli) broke a plate in the middle of which testing ceased (for a similar approach, see Prétôt et al., 2016a). Session 3, so we stopped testing and restarted with a new session We used a within‐subjects design for the comparisons between (beginning again from Trial 1) the next testing day. tasks, and a between‐subjects design for the comparisons across species. Second, we used logistic mixed‐effects models (Bolker et al., 3.2 | Results 2009), with the proportion as the response weighed by the number of trials (see Agresti, 2003). For our entry points, we used the pro- 3.2.1 | Initial learning test portion (in percent) of ephemeral choices per session (i.e., out of 10 trials). Mixed models were run using the package “lme4” (Bates et al., At the group level, gorillas chose the ephemeral plate in 52% of the 2014). We compared our models to models excluding predictors of trials, and the right side in 68% of the trials. Drills chose the interest using likelihood ratio tests (LRTs). For the comparison, ephemeral plate in 50% of the trials, and the left side in 56% of the subject identity was fit as a random effect (intercepts) to control for trials. repeated measures. When the test result was significant, we con- At the individual level, none of the gorilla or drill subjects tested ducted post hoc analyses with multivariate t (mvt) adjustments using on the initial learning test solved the task (Ngorillas =9, Ndrills = 6). package “lsmeans.” The statistical analyses of our models were Seven out of nine gorillas and all six drills showed a significant side conducted with R statistical software (version 3.5.1, 2018‐07‐02, preference (two‐tailed exact binomial/sign test: all ps ≤ .002). Be- Feather Spray). cause no subject met criterion, no one received the reversal test. Our procedure was as follows. We first created a full model, Individual data for all subjects are in Table 2. which included our predictor variables of interest: species, task, learning phase, and session. We compared our full model to a null model, which included only our random effect terms (i.e., subject 3.2.2 | Cross‐species comparison (between‐ identity), and found that the full model was better than a null model subjects) 2 (LRT, χ 6 = 19.595, p = .003; Table S2). Second, we created separate models for each task (reduced models), which included species only. We compared the performance of gorillas and drills in the plate task Because too few subjects received the reversal test, we only used with the performance of orangutans in Salwiczek et al. (2012). There data from the initial learning test for this analysis. Note that in- was no significant difference in learning speed performance among complete sessions (13 sessions total; 7 sessions for one gorilla sub- the species (Kruskal–Wallis exact test: df =2, χ2 =0, N = 19, ject, Kekla) were not included. p = 1.000; Figure 2). The reduced model supported these results 2 (LRT, χ 2 = 0.254, p = .881; Table S2).

3 | PLATE TASK (GORILLAS AND DRILLS) 3.3 | Discussion 3.1 | Procedure All of the primates in the current study failed to solve the plate task, Nine gorillas and six drills were tested in the plate task. Only some of consistent with our prior results showing that the plate task is par- our orangutan subjects had previous experience with the task (Satu, ticularly challenging for primates. The lack of variability across spe- Madu, and Chantek; Salwiczek et al., 2012), but because of time cies suggests that neither experience nor procedural variation constraints, we did not replicate it with the new individuals (Dumadi, influenced their decisions. One hypothesis is that their failure in the Blaze, and Biji). task is due to their inability to recognize which cue is the important In the task, subjects had a choice between two food items placed one for figuring out how to solve the task (i.e., that they should be on two plates that were similar in size and shape, but differed in distinguishing between the options based on the color/pattern of the color and pattern. In keeping with our comparative approach, the surrounding substrates). As discussed in Section 1, the substrate on design of the plates was kept similar across species (see Figure 1 for which the food is presented may not be salient to primates, who may details of plates in all studies to date). Plate 1 had two yellow pay more attention to the food itself. In the next experiment (for half 8of16 | PRÉTÔT ET AL.

TABLE 2 Number of trials needed for each subject to solve the coloring, excepting two gorillas who refused to eat some of the initial learning test in the plate task colors. One female (Shamba), who was originally presented with pink Initial learning pellets as ephemeral foods and black pellets as permanent foods, Subject Trial number Side preference Ephemeral would not eat any of the black pellets in Session 1; consequently, we tested her with new colors, blue and red, starting in Session 2. In Gorillas addition, one male refused to eat any pellets (Stadi), and was tested Kidogo >100 Right (85%)* Plate 1 using green and black grapes. Of course, our goal in using the pellets Shamba >100 Left (53%) Plate 1 was to avoid any differences in food taste between the options, but Charlie >100 Right (73%)* Plate 2 different colors of the same fruit were hopefully sufficiently similar Choomba >100 Right (95%)* Plate 2 Jasiri >100 Right (66%)* Plate 2 to avoid a preference based on food taste. Note that one drill (Lucy) Ozzie >100 Right (82%)* Plate 2 mistakenly received the ephemeral food after choosing the perma- Stadia >100 Left (78%)* Plate 1 nent food in one trial of Session 12. Kekla >97b Right (91%)* Plate 1 Mbeli >93b Left (52%) Plate 1 4.2 | Results Drills Achi >100 Right (95%)* Plate 1 4.2.1 | Initial learning test Inge >100 Left (68%)* Plate 1 Drew >100 Right (96%)* Plate 1 Amaka >100 Left (87%)* Plate 2 At the group level, orangutans chose the ephemeral food in 62% of Bobby >100 Left (79%)* Plate 2 the trials, and the left side in 76% of the trials. Gorillas chose the Lucy >100 Left (94%)* Plate 2 ephemeral food in 54% of the trials, and the right side in 63% of the trials. Drills chose the ephemeral food in 51% of the trials, and the Note that stimulus options (Plate 1 vs. Plate 2) are shown in Figure 1. Side left side in 64% of the trials. preferences with significant p values (based on a two‐tailed binomial/sign test) are indicated with an asterisk (*). At the individual level, four of the six orangutans developed a aSubject was tested with purple grapes. preference for the ephemeral food within 60 trials (range 20–60 bSubjects did not complete one session. trials, mean ± SD = 37.50 ± 17.08 trials), including two subjects who had received both the original plate task and the cup task previously of the subjects; the next two experiments were counterbalanced for (Satu and Chantek), and two subjects who had not received the plate each species), the cue was the color of the food, while the substrates task and were tested on this task first (Dumadi and Biji). One of the were identical. two orangutans that did not reach the preference criterion for either stimulus had received the plate task previously and was tested on this task prior the cup task (Madu), while the other had not received 4 | COLOR TASK the plate task and was tested on this task subsequent to the cup task (Blaze). Both individuals showed a significant side preference (two‐ 4.1 | Procedure tailed exact binomial/sign test: both ps < .001). Three of the nine gorillas reached criterion; two individuals de- Six orangutans, including three from the original plate task (Satu, veloped a preference for the ephemeral stimulus, one of whom was Madu, and Chantek), and the same nine gorillas and six drills were tested on this task subsequent to the cup task (Mbeli, within 40 tested in the color task. Five of the nine gorillas and three each of the trials), and the other was first tested on this task (Stadi, within 120 orangutans and drills were tested first in this study and subsequently trials), and one individual developed a preference for the permanent on the cup task, while the other four gorillas and three each of the stimulus (she was first tested on this task; Shamba, within 110 trials). orangutans and drills were tested first on the cup task and subse- The other six subjects did not reach criterion for either stimulus. quently on this experiment. For the orangutan who had previously Four out of six of these individuals showed a significant side pre- received the plate task (Madu), approximately 4 years passed be- ference (all ps ≤ .001). None of the drills reached criterion for either tween the plate task and the color task. For gorillas and drills, ap- stimulus (Ndrills = 6), and all six individuals showed a significant side proximately 1 month passed between the plate task and the color preference (all ps ≤ .012). Individual data for all subjects are in task. Although we did no training to reduce the side bias, we hoped Table 3. this time delay and the novel apparatus would make it clear that this was a different task. The basic procedure was the same as that in the plate task, 4.2.2 | Reversal learning phase except that the plates were identical (a solid light beige color) and the foods differed in color (Figure 1). Rewards were large pellets that Three of the four orangutans that solved the initial learning task were colored pink (Color 1) or black (Color 2) with spray food also solved the reversal task (Satu, Chantek, and Dumadi; range PRÉTÔT ET AL. | 9of16

FIGURE 2 Number of trials required for capuchins ("Caps"), drills ("Drills"), gorillas ("Gorillas"), and orangutans ("Orangs") to develop a preference for the ephemeral stimulus in the plate task (capuchins and orangutans' data based on Salwiczek et al., 2012) and to develop a preference for either stimulus in the color and cup tasks (capuchins' data based on Prétôt et al., 2016b). Each dot represents one individual; black dots indicate a preference for the ephemeral stimulus, whereas white dots indicate a preference for the permanent stimulus. For capuchins and orangutans, the gray dots designate a new subject not previously tested in the plate task; “failed” indicates subjects that did not reach the preference criterion

50–90 trials, mean ± SD = 70.33 ± 20.01 trials). The remaining 4.2.4 | Cross‐species comparison (between‐subjects) individual did not reach criterion, and showed a significant side preference (Biji; two‐tailed exact binomial/sign test: p < .001). There was a significant difference in learning speed among the None of the gorillas reached criterion in the reversal task, re- species (Kruskal–Wallis exact test: df =2, χ2 = 7.89, N = 20, p = .021; gardless of which stimulus they initially preferred. Two of these Figure 2). However, post hoc comparisons revealed that orangutans', three individuals showed a significant side preference (both gorillas', and drills' behavior were not distinguishable from one ps ≤ .035). another (two‐tailed exact Mann–Whitney U test: Norangutans =6,

Ngorillas =9, Ndrills = 6, all ps ≥ .061, Bonferroni adjusted p = .017). The reduced model revealed that preference for the ephemeral 2 4.2.3 | Plate versus color tasks (within‐subjects) food was predicted by species (LRT, χ 2 = 9.371, p = .009; Table S2). Post hoc comparisons revealed that orangutans chose the ephemeral Our sample of orangutans who participated in both tasks was too food more often than did the drills (estimate = −0.525, SE = 0.182, small for a statistically significant analysis (N = 3); however, we note p = .011, mvt adjustment) and marginally more often than did the that of the three subjects who participated in the original plate task gorillas (estimate = −0.376, SE = 0.170, p = .068, mvt adjustment). (Satu, Madu, and Chantek; Salwiczek et al., 2012), all of whom failed, There was no difference between gorillas and drills (estimate = two solved the color task (Satu and Chantek). Those two orangutans −0.149, SE = 0.139, p = .525, mvt adjustment). also participated in the cup task (which they failed), before passing the color task. Neither gorillas nor drills showed any difference in performance between the color task (two of nine gorillas succeeded, 4.3 | Discussion whereas all six drills failed in the task) and the plate task (all subjects of both species failed in the task; Fisher's exact test, gorillas: p = .471; Two‐thirds of orangutans and approximately a quarter of gorillas drills: p = 1.000; Figure 2). solved the color task, and no drills did. This does not support the 10 of 16 | PRÉTÔT ET AL.

TABLE 3 Number of trials needed for Initial learning Reversal learning each subject to reach preference criterion for the initial learning test and the reversal Trial Side Trial Side Ephemeral Initial phase in the color task Subject number preference number preference option preference Orangutans Chanteka,b 20 Right (55%) 50 Right (56%) Color 1 Ephemeral Satua,b 40 Left (73%)* 90 Left (63%)* Color 2 Ephemeral Dumadi 60 Left (52%) 71c Right (56%) Color 2 Ephemeral Biji 30 Right (70%)* >100 Right (91%)* Color 1 Ephemeral Madua >100 Left (95%)* –– Color 1 – Blazeb >100 Left (92%)* –– Color 2 –

Gorillas Mbelib 40 Right (65%) >100 Right (83%)* Color 1 Ephemeral Stadid 120 Left (68%)* >100 Right (58%) Green Ephemeral Shambae 110 Right (63%)* >100 Right (61%)* Blue Permanent Charlie >100 Right (88%)* –– Color 1 – Choombab >100 Right (53%) –– Color 1 – Jasirib >91c Right (60%) –– Color 1 – Kidogo >100 Right (68%)* –– Color 2 – Ozzie >100 Right (75%)* –– Color 2 – Keklab >99c Right (68%)* –– Color 2 –

Drills Lucy >120 Left (68%)* –– Color 2 – Ingeb >104c Left (88%)* –– Color 2 – Amaka >100 Left (97%)* –– Color 1 – Bobby >100 Left (91%)* –– Color 1 – Drewb >100 Right (63%)* –– Color 1 – Achib >100 Right (98%)* –– Color 2 –

Note that stimulus options (Color 1 vs. Color 2) are shown in Figure 1. Subjects that did not reach preference criterion in the initial learning test were not further tested on the reversal phase. Side preferences with significant p values (based on a two‐tailed binomial/sign test) are indicated with an asterisk (*). aSubjects previously tested in the plate task (Salwiczek et al., 2012). bSubjects previously tested in the cup task. cSubjects did not complete one or more sessions. dSubject was tested with green and black grapes. eSubject was tested with blue and red pellets. hypothesis that this change should benefit all primates. Instead, apes 5 | CUP TASK outperformed monkeys, and orangutans outperformed gorillas, consistent with both some suggestions that orangutans outperform 5.1 | Procedure gorillas and apes outperform monkeys on cognitive tasks, as well as the relative level of previous cognitive testing that each subject had Half the subjects participated in this task immediately after the plate experienced (see Table S1). If the latter is the relevant factor, how- task (or first, for the orangutans), and half did it third, after com- ever, this is apparently based on general testing history, not ex- pleting the color task. For the two orangutans who had previously perience with this task, as two of the four orangutan subjects who participated in the plate task (Satu and Chantek), approximately succeeded on the color task had never experienced the task before 4 years passed between the plate task and the cup task. For gorillas in any form, while half had previously experienced both the plate and and drills, approximately 1 month (4 months for one gorilla subject, cup tasks. However, for these two orangutans, approximately 4 years Mbeli) passed between the plate task and the cup task. passed between the original plate task and the new experiments, The procedure in the cup task was the same as in previous ex- suggesting the possibility that recent previous experience with the periments, except that the two foods were identical (as in the plate original plate task was actually inhibitory of their ability to solve task and unlike in the color task) and were hidden under two dif- subsequent versions of it. We discuss this possibility in more detail in ferently patterned opaque cups (as in Prétôt et al., 2016b; Figure 1). Section 6. Cup 1 was yellow with one red dot on each side and Cup 2 was PRÉTÔT ET AL. | 11 of 16 purple with a blue triangle on each side. At the beginning of each not develop a significant side preference (two‐tailed exact binomial/ trial, the subjects saw the experimenter hiding one pellet (or purple sign test: p = .089). grape, for the gorilla Stadi) under each cup. They were then given the choice between the two options. When gorilla and orangutan subjects made a choice (by gesturing at the cup they wanted), the ex- 5.2.3 | Plate versus cup tasks (within‐subjects) perimenter lifted the cup, then pushed the plate forward so the subjects could pick up the food. If the ephemeral cup was selected Again, our sample of orangutans who participated in both tasks was first, the experimenter lifted the ephemeral cup and gave the subject too small for a statistically significant analysis (N = 3); however, we access to that food, then immediately removed the permanent cup note that all three subjects who failed in the original plate task (Satu, and gave the subject access to that food as well. If the permanent Madu, and Chantek; Salwiczek et al., 2012) also failed in the cup task. cup was chosen first, the ephemeral cup was removed with the food As in the color task, neither drills nor gorillas showed any difference still hidden. Drills could make a choice either by lifting up the cup in performance between the cup task and the plate task (all subjects themselves and taking the food, or by touching the cup, in which case of both species failed both tasks; Fisher's exact test: all ps = 1.000; the experimenter lifted the cup for them and let them take the food. Figure 2). Subjects were allowed to use whichever method they preferred. Note that one drill (Lucy) mistakenly received the food from the ephemeral cup after choosing the permanent cup in one trial of 5.2.4 | Cross‐species comparison (between‐ Session 6. subjects)

There was no significant difference in learning speed among the 5.2 | Results species (Kruskal–Wallis exact test: df =2, χ2 = 2.33, N = 20, p = .600; Figure 2). The reduced model supported these results (LRT, 2 5.2.1 | Initial learning test χ 2 = 0.912, p = .634; Table S2).

At the group level, orangutans chose the ephemeral food in 52% of the trials, and chose the left side in 52% of the trials. Gorillas chose 5.3 | Discussion the ephemeral option in 50% of the trials, and chose the right side in 67% of the trials. Drills chose the ephemeral food in 51% of the trials, Out of all the individuals tested across the three species, only one and chose the right side in 52% of the trials. orangutan learned the task. It is curious that the three species could At the individual level, one of the six orangutans reached not solve the task when the capuchins could. The fact that capuchins, preference criterion for the ephemeral stimulus within 30 trials as well as one orangutan and one gorilla (who developed a pre- (Dumadi). This subject was tested on this task subsequent to the ference for the permanent cup) reached preference criterion in- color task (which he passed), but had not previously been tested dicates that discriminating the stimuli was not the problem and may in the plate task. The other orangutans did not reach criterion for suggest that, at least for orangutans, the task is easier when the cue either stimulus. Four of these five individuals showed a sig- is the color of the food (the color task). nificant side preference (two‐tailed exact binomial/sign test: all ps ≤ .004). One of the nine gorillas reached preference criterion for the permanent stimulus within 20 trials, after having been 6 | GENERAL DISCUSSION tested on the color task (Shamba). The other gorillas did not reach criterion for either stimulus, and four of these eight in- In previous work, we found that capuchin monkeys performed better dividuals showed a significant side preference (all ps ≤ .010). on a dichotomous choice task after we changed the cues to be those None of the drills tested on the initial learning test reached cri- that we predicted would be more relevant to them (Prétôt et al., terionforeitherstimulus(Ndrills =6),andallsixsubjectsshowed 2016b). Here, we tested the extent to which these cues applied to a significant side preference (all ps ≤ .035). Individual data for all other primates by giving additional species the same tasks. As with subjects are in Table 4. capuchins, and orangutans in the original study, gorillas and drills did not solve the task in which the relevant cue was the plate on which the food was presented. However, the new cues that helped the 5.2.2 | Reversal learning phase capuchins did not benefit the other species to the same degree as they did the capuchins. Orangutans did the best, with most subjects The orangutan who solved the initial task solved the reversal task reaching criterion when the color of the food was the relevant cue. within 120 trials (Dumadi), whereas the gorilla who reached pre- However, unlike the capuchins, only one subject reached criterion ference criterion for the permanent stimulus did not reach pre- when (identical) foods were hidden under differently colored cups. ference for either stimulus in the reversal task (Shamba). She also did Although not reaching statistical significance, two gorillas found the 12 of 16 | PRÉTÔT ET AL.

TABLE 4 Number of trials needed for Initial learning Reversal learning each subject to reach preference criterion for the initial learning test and the reversal Trial Side Trial Side Ephemeral Initial phase in the cup task Subject number preference number preference option preference Orangutans Dumadia 30 Right (60%) 111b Right (65%)* Cup 2 Ephemeral Blaze >100 Left (76%)* –– Cup 1 – Madua,c >100 Left (100%)* –– Cup 1 – Satuc >95b Left (54%) –– Cup 1 – Chantekc >100 Right (65%)* –– Cup 2 – Bijia >100 Right (99%)* –– Cup 2 –

Gorillas Shambaa 20 Right (65%) >100 Left (59%) Cup 1 Permanent Choomba >110 Right (51%) –– Cup 2 – Stadia,d >110 Right (63%)* –– Cup 2 – Jasiri >100 Right (52%) –– Cup 1 – Kidogoa >100 Right (59%) –– Cup 1 – Ozziea >100 Right (83%)* –– Cup 1 – Charliea >100 Right (74%)* –– Cup 2 – Mbeli >100 Right (97%)* –– Cup 2 – Kekla >98b Right (57%) –– Cup 2 –

Drills Inge >100 Left (61%)* –– Cup 1 – Amakaa >100 Left (98%)* –– Cup 1 – Bobbya >100 Left (96%)* –– Cup 1 – Achi >100 Right (69%)* –– Cup 2 – Drew >100 Right (98%)* –– Cup 2 – Lucya >100 Right (100%)* –– Cup 2 –

Note that stimulus options (Cup 1 vs. Cup 2) are shown in Figure 1. Subjects that did not reach preference criterion in the initial learning test were not further tested on the reversal phase. Side preferences with significant p values (based on a two‐tailed binomial/sign test) are indicated with an asterisk (*). aSubjects previously tested in the color task. bSubjects did not complete one session. cSubjects previously tested in the plate task (Salwiczek et al., 2012). dSubject was tested with purple grapes. solution in the color task, and another one developed a stable pre- Second, our pattern of results is suggestive that subjects who ference (for the permanent option) in both the color and cup tasks. had previous experience with cognitive testing were more likely to Finally, drills were the least successful, with none of the subjects find the solution in the tasks than those who had little to no ex- succeeding on any task. While this pattern does not perfectly match perience. Orangutan subjects, who had the most experience with any of those discussed in Section 1, it is consistent in two ways. cognitive testing, performed better than the gorillas, who had some First, this task has been hypothesized to be grounded in in- previous experience with cognitive tasks, but not nearly the same in hibitory control (Zentall et al., 2018; Zentall, 2019), and these results frequency or variety as the orangutans. Drill monkeys, who had no are consistent with earlier work showing that orangutans outper- previous experience with cognitive testing, performed the worst. form gorillas and baboons (a species, i.e., closely related to drills) on Intriguingly, despite a sample so small that these results are at best inhibitory control tasks, suggesting that this is an important factor in anecdotal, our pattern also suggests that experience with this par- the current task. However, capuchin monkeys are not particularly ticular task is irrelevant; subjects did not do any better on sub- successful at the same inhibitory control tasks (Amici et al., 2008, sequent versions once they had experienced the task. Instead, it 2018), yet they are extremely successful in these tasks, suggesting seemed that the critical feature was familiarity with cognitive testing, that inhibitory control is not the only factor at play. Moreover, while suggesting that perhaps these more experienced subjects under- it is true that on this particular inhibitory control task, orangutans stood that there were ways to maximize food intake. Although there outperformed gorillas, other studies have found them to be equally is no evidence that cleaner wrasse show an experience effect in the successful (Barth & Call, 2006; Call, 2004; Vlamings et al., 2006). lab, their ability to solve it does depend on the complexity of their PRÉTÔT ET AL. | 13 of 16 environment, with those from more complex environments solving to learn the task than it was for the orangutans. Again, this also the task more readily than those from less complex ones (Triki et al., suggests that while additional experience on cognitive tasks, in 2018, 2019; Wismer et al., 2014). Although a different context, this general, improves performance, it is either a general phenomenon or may suggest that animals first need to learn to be good at solving an effect of being more cognizant of the goal of these studies, not an experimental tasks, before they can learn the task itself (Lotem & effect of greater experience with the specific task at hand. Halpern, 2012). One major limitation of our study is that we did not do numerosity Unfortunately from our results, we cannot distinguish between pre‐testing, so it is also possible that gorillas and drills had more diffi- these possibilities, and in addition, there were other factors that may culty distinguishing the reward payoffs between the two options (i.e., have influenced performance in the task. For instance, due to differ- 1 vs. 2) than did the orangutans. However, we think this is unlikely for ences in zoo protocols and the primates' preferences and habits, the the gorillas, who have previously demonstrated that they are perfectly presentation of the plates and the choices differed between apes and capable of quantity judgments, including some of the specific subjects in monkeys: the apes were presented the two plates at distance and in- our current study, who were previously tested for quantity dis- dicated their choice by gesturing to the plate (after which the experi- crimination at Zoo Atlanta (Anderson et al., 2005; Hanus & Call, 2007; menter handed them the plate upon which the food rested), whereas for similar results using nonfood stimuli, see Paxton Gazes et al., 2017; drills (like capuchins) were able to pick up their own foods directly from Vonk et al., 2014). We know of no similar task in drills, although ba- the plate. This difference could be particularly salient in the cup task, in boons, a closely related species, also discriminate quantities success- which it was the experimenter who removed the cup and handed the fully, especially when the options are presented simultaneously plate to the apes, whereas the monkeys removed their own cup and (compared to sequentially), as was done in the current study (Barnard took the food. However, while we would have predicted that being able et al., 2013; Schmitt & Fischer, 2011;Smithetal.,2003). to directly access the food would have improved success, the two Interestingly, a majority of subjects who did not find the solution species that were able to directly access their food were the least reverted to a side bias (this was particularly striking in drill monkeys), (drills) and most (capuchins) successful at the task. Nonetheless, it is suggesting they became frustrated and may not have properly re‐ possible that the apes were generally more successful in the task than evaluated the task when the new version was presented. Such side the drills because learning was facilitated by the salience of the cues biases have previously been reported in the study by Salwiczek et al. that were inadvertently given by the experimenter. (2012), and in a variety of species across a variety of cognitive tests One advantage to our comparison was that both our zoo pri- (Gácsi et al., 2009; Genty et al., 2004; Ventricelli et al., 2013). There mates and the capuchins live in overall similar environments—both is debate about whether side biases occur because animals do not live in stable mixed‐sex social groups in large indoor/outdoor en- know how to solve the task (i.e., they do not understand the con- closures with extensive environmental and daily food enrichment, tingencies) or because they are indifferent between the available neither are ever food or water deprived, and both facilities only options. It has been suggested that if it was the former, side bias allow noninvasive cognitive and behavioral studies in which partici- should show early in the test, while if it was the latter, it should pation by the primate is voluntary (i.e., subjects are never restricted appear later (Ventricelli et al., 2013). Although most subjects in our from anything to encourage participation, including food, water, study picked both sides within the first few trials, suggesting they did treats, their social group or outdoor access). However, one key dif- know food was available on both sides, side biases generally ap- ference is that capuchins always voluntarily separated from other peared early in the sessions, supporting the hypothesis that our side group members for testing (or chose not to test), whereas some zoo bias resulted from a lack of understanding of our task. In addition, primates were tested with other group members present. Never- our subjects were always rewarded no matter which side they picked theless, subjects who were separated during testing did not perform first, which would have removed a key penalty from the wrong better than those who were tested in presence of other group choice. Indeed, this high frequency of reward may also have de- members, suggesting that this was not a major distractor or key creased their motivation to pay attention and make careful decisions factor in shaping their choice. (c.f., Schubiger et al., 2016). It is notable that other species that have Intriguingly, the pattern also suggests that subjects who had no struggled with this task have either chosen randomly (rats; Zentall experience with the original—and apparently very challenging—plate et al., 2017) or tended to preferentially choose the permanent option task, or had their experience years prior, did better. The more suc- (pigeons; Zentall et al., 2016), rather than showing a side bias, sug- cessful orangutans either never underwent the plate task or did so gesting that this is not a universal response. long before the color and the cup tasks (this was also the case with Thus, we find it premature to conclude that our cues were the capuchins), while the gorillas and drills received all three tasks in specific to the capuchins and did not help the other species. Indeed, a shorter period of time. The plate task was the only one of these the most likely possible explanation seems to be the potential impact three tasks that no primate of any species ever passed on the first of subjects' previous experience with cognitive tasks (and not this set of sessions, suggesting that it is extremely difficult for them. This task specifically). While this is frustrating from the perspective of experience may have affected future studies by increasing frustra- answering our original question, it does suggest an interesting future tion with the procedure and/or reducing interest in paying attention direction comparing the impact of general experience versus ex- in later manifestations, making it more difficult for gorillas and drills perience with a specific task per se on subjects' performance in 14 of 16 | PRÉTÔT ET AL. cognitive tasks. In addition, we will continue to pursue our original ORCID question, exploring the role of ecology in shaping different species' Laurent Prétôt http://orcid.org/0000-0002-9936-5506 responses to cues, albeit hopefully in a more controlled set of circumstances. REFERENCES One of the challenges of comparative work is finding sufficient Agresti, A. (2003). Categorical data analysis (Vol. 482). 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Maintenance of self‐imposed delay of gratification by re‐think our comparative approach and ensure that we give full four chimpanzees (Pan troglodytes) and an orangutan (Pongo pygmaeus). The Journal of General Psychology, 129,49–66. credit to less experimentally savvy populations of subjects so that we Beran, M. J., Evans, T. A., Paglieri, F., McIntyre, J. M., Addessi, E., & do not underestimate their abilities. Hopkins, W. D. (2014). Chimpanzees (Pan troglodytes) can wait, when they choose to: A study with the hybrid delay task. Animal ACKNOWLEDGMENTS Cognition, 17, 197–205. Beran, M. J., Perdue, B. M., Rossettie, M. S., James, B. T., Whitham, W., We thank the Zoo Atlanta primate staff for their support in making Walker, B., Futch, S., & Parrish, A. E. (2016). Self‐control this study possible. We also thank Benjamin Grantier for his help assessments of capuchin monkeys with the rotating tray task and with video coding, the Research Services of Boston College for their the accumulation task. Behavioural Processes, 129,68–79. assistance with statistical analysis and advice, and two anonymous Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., ‐ reviewers for their helpful comments on an earlier version of this Stevens, M. H. H., & White, J. S. S. (2009). Generalized linear mixed models: A practical guide for ecology and evolution. Trends in manuscript. This study was supported by Zoo Atlanta. Laurent Prétôt Ecology & Evolution, 24, 127–135. was funded by the Swiss Science Foundation (Doc.Mobility, Boysen, S. T., & Berntson, G. G. (1995). Responses to quantity: Perceptual P1SKP1_151775) and a GSU Second Century Initiative in Primate versus cognitive mechanisms in chimpanzees (Pan troglodytes). Social Cognition, Evolution & Behavior Dissertation Grant Journal of Experimental Psychology: Animal Behavior Processes, 21, 82–86. (2CI‐PSCEB). Redouan Bshary was funded by the Swiss Science Bräuer, J., Call, J., & Tomasello, M. (2007). Chimpanzees really know what Foundation. Sarah F. Brosnan was funded in part during writing by others can see in a competitive situation. Animal Cognition, 10, National Science Foundation grant SES 1425216. 439–448. Brosnan, S. F., Flemming, T., Talbot, C. F., Mayo, L., & Stoinski, T. S. (2011). Orangutans (Pongo pygmaeus) do not form expectations based on DATA AVAILABILITY STATEMENT their partner's outcomes. Folia Primatologica, 82,56–70. The data and code that support the findings of this study are openly Brosnan, S. F., Parrish, A., Beran, M. J., Flemming, T., Heimbauer, L., available at the following link: https://osf.io/xe836/?view_only= Talbot, C. F., Lambeth, S. P., Schapiro, S. J., & Wilson, B. J. (2011). d6c9d685b9e843529804591c638afe0e. 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