The History and Status of Cognitive Research with Great Apes in the United States

The Japanese Journal of Animal Psychology, 68, 2, 105-119 (2018)

Lecture

The history and status of cognitive research with great apes in the United States

ROBERT W. SHUMAKER１）２）３）

Abstract Cognitive research in the United States spans approximately 100 years. Most studies have occurred in primate centers, fewer at universities, and for a brief period, in home-based projects focused on enculturation. Historically, great apes living in zoos have been under represented. A shift has occurred that affects the future of the field. Studies at primate centers have significantly decreased, all university based projects have ended, and work in zoos is increasing. The Simon Skjodt International Orangutan Center at the Indianapolis Zoo provides an example of one stable, longitudinally based project. The primary areas of study at the Center are symbolic representation, numerical competency, social learning, memory, and strategic reasoning. All data collection sessions are conducted with visitors present. Cognitive studies in a zoo environment promote great ape welfare, offer a platform for transformational public education, and provide an effective means to advance support for in situ conservation of great apes. Key words：cognition, orangutans, great apes, welfare, mental enrichment, Indianapolis Zoo

1. Introduction critically endangered in the wild (iucnredlist. Investigations into the cognitive skills of org). While readily acknowledging the many the non-human great apes (orangutans, goril- valuable contributions from colleagues inter- las, chimpanzees and bonobos) are currently nationally, the purpose of this paper is to conducted in and ex situ and involve multiple report only on the status of cognitive academic disciplines. The field is vibrant and research conducted with great apes in the productive. Results continue to document the United States. This is not intended to be an abilities of the great ape clade at a time exhaustive review of publications or topics when these species are either endangered or that have been studied. Rather, the focus is on trends associated with prevailing perspec- １）Indianapolis Zoological Society, Indianapolis, tives on research with great apes, the Indiana institutions supporting it, how that has 1200 W. Washington St., Indianapolis, Indiana 46222-0309 changed over time, and what appears likely ２）Department of Anthropology and Center for for the future. For a thorough review of all the Integrated Study of Animal Behavior, primate cognition research through 1996, see Indiana University, Bloomington, Indiana Tomasello & Call (1997). Russon’s excellent 107 S. Indiana Ave, Bloomington, Indiana (2004) review of the literature offers an evolu- 47405 ３）Krasnow Institute for Advanced Study, tionary perspective on great ape intelligence. George Mason University, Fairfax, Virginia The history of cognitive studies with great 4400 University Dr, Fairfax, Virginia 22030 apes in the United States spans slightly more Corresponding author: ROBERT W. SHUMAKER than 100 years (Parker & McKinney, 1999), E-mail: rshumaker＠indyzoo.com beginning with studies by Robert M. Yerkes, J-STAGE Advance Published Date: September 21, 2018. known as both an evolutionist and behavior- doi: 10.2502/janip.68.2.3 ist (Reed, 1987). The first report by Yerkes of

- 105 - 動物心理学研究第68巻第２号 cognitive research with a great ape (1916a) was later referred to as the Yale Laboratories describes his study of “ideational behavior” of Primate Biology (Finch, 1943). Yerkes in a young orangutan named Julius, which served as the Director until he retired in was conducted at the Franklin Field Station. 1941. The Station, renamed in honor of Yerkes noted that his results included the “first Yerkes, was moved to Atlanta in 1965. For curve of learning for an anthropoid ape”, an extensive review of the many research and when compared to other mammals, may topics that were studied at Orange Park and indicate “reasoning” on the part of the then Atlanta through the mid 1970’s, see orangutan (Dewsbury, 2006; Yerkes, 1916a). Dewsbury (2006). Coincident with this research, Yerkes also Following Yerkes, Parker and McKinney promoted the concept of establishing an (1999) note that primate studies in the United “anthropoid station” to benefit “the biological States diverged along 2 distinct paths. The and sociological sciences and for human first focused on natural-history style observa- welfare” (1916a). Yerkes envisioned that the tions of very young apes raised by humans. station would be “1) for the maintenance of The general purpose of these studies was to various types of primates in normal and document how immersion in a human cultur- healthy condition; (2) for the successful al environment, sometimes with a married breeding and rearing of the animals to many couple as “parents”, impacted the develop- generations; (3) for systematic and continuous ment of mental skills and abilities in great observation under reasonably natural condi- apes, including language comprehension and tions; (4) for experimental investigations from acquisition. Examples include the work of every significant biological point of view; (5) Luella and Winthrop Kellogg who raised a for profitable cooperation with existing bio- chimpanzee named Gua alongside their simi- logical institutes or departments of research larly aged human son Donald (Kellogg & throughout this country and the world” (Yerkes, Kellogg, 1933). Cathy and Keith Hayes home- 1916b). During the early years of his career, reared a chimpanzee named Viki with a Yerkes studied chimpanzees and what is primary focus on understanding the emer- believed to be one bonobo in both zoos and gence of vocal language (Hayes, 1951; Hayes private collections (Dewsbury, 2006). Results & Hayes, 1952). Temerlin (1975) referred to a from these studies are compiled in Chimpan- chimpanzee named Lucy as his daughter zee Intelligence and its Vocal Expressions (Yerkes during the years-long study in which she and Learned, 1925), and Almost Human (Yerkes, lived as a member of the family (Fouts & 1925). Work with Congo, a male gorilla, is Mellgren, 1976). Beatrice and Allen Gardner detailed in three separate monographs (1971) had the insight of using American published on The Mind of a Gorilla (Yerkes, Sign Language, rather than vocal language, 1927a; Yerkes 1927b; Yerkes, 1928). In 1929, in their work with a chimpanzee named The Great Apes was compiled by Robert and Washoe which began in 1966 in Nevada. Ada Yerkes. This classic volume reviewed all They were clear that this project was not existing knowledge of apes, including behav- intended to immerse their subject in a “human ior and mental abilities (Yerkes & Yerkes, family-life”. Rather, the idea was to create a 1929). Dewsbury (2006) suggests that the pub- situation with rich and interesting opportuni- lication of The Great Apes was an influential ties for signed communication but managed factor that led to financial and philosophical with the rigor of a laboratory-based investi- support for Yerkes’ proposed anthropoid gation (Gardner and Gardner, 1971). The station. In 1929, the Rockefeller Foundation project was moved to the Institute for approved funding for the station, which Primate Studies in Norman, Oklahoma in opened in 1930 as the “Anthropoid Experi- 1970, and then ultimately based at Central ment Station of Yale University” located in Washington University in Ellensburg, Wash- Orange Park, Florida (Dewsbury, 2006). It ington starting in 1980 (Fouts, 1997).

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The second path for cognitive work with allowed investigation of such topics as the great apes focused on controlled studies in organization of spatial memory (Menzel, laboratory environments, usually based in 1973). established primate research centers (Parker During the 1960s, universities began to and McKinney, 1999). The trend is illustrated take on a different role. Researchers since by examples such as Spence (1937, 1938), Yerkes had been employed by universities, Crawford (1941), Hayes et al. (1953), Ferster but their work was generally conducted at a (1964), Mason (1965) Hayes and Nissen (1971), separate primate facility. The distinction that Menzel and Davenport (1962) and Menzel (1973). emerged was important: the researchers and Spence (1937, 1938), working at Orange Park, their ape subjects came to be based at, not pioneered an understanding of learning theo- just affiliated with, a university. The first ry with chimpanzees. Crawford, working with known example of this transition was made seven chimpanzees at Orange Park, studied by David Premack who focused primarily on sequence learning, social learning, and coop- studying symbolic representation and its eration. In retrospect, it is likely that this relationship to language acquisition (Premack study also revealed abilities associated with & Premack, 1983). Starting at Orange Park in Theory of Mind, a concept that did not exist 1954, Premack moved to the University of in the great ape literature of the era. In one Missouri in 1964 with two chimpanzees, experiment during the study, the chimpanzees Gussie and Sarah, who were housed on the learned to operate electronically linked devic- campus. The project expanded over time es that delivered a food reward when with additional apes, eventually moved to the engaged in the proper sequence. Naïve University of California, Santa Barbara, and observers were housed next to an experienced finally to the University of Pennsylvania demonstrator as a means of revealing socially (Premack & Premack, 1983). cooperative behaviors. Crawford’s work (1941) During this era, a small number of is the first to employ technology-based stim- studies occurred with great apes living in uli in studies of cognition with apes (Martin, zoos. Patterned string problems were studied C. F., under review.). Hayes et al. (1953) by Riesen et al. (1953) with 3 very young studied discrimination learning set formation gorillas housed at the Lincoln Park Zoo in with 8 chimpanzees housed at Orange Park. Chicago, Illinois. Young gorillas were also Note that this group of subjects included the subjects in Fischer’s (1962) work on Viki, who was home-raised by the Cathy and learning set formation. Her work was based Keith Hayes (Hayes, 1951). Ferster performed at the Lincoln Park Zoo and utilized a “experiments in numerosity” (1964) with a standard Wisconsin General Testing Appara- pair of young chimpanzees named Dennis tus (Harlow, 1949) to present stimuli to the and Margie who were housed at the Institute apes. Fischer and Kitchener (1965) compared for Behavioral Research in Silver Spring, the intelligence of orangutans and gorillas. Maryland. Mason investigated the social be- The subjects were 2 juvenile orangutans, 2 havior of young chimpanzees at the Delta infant orangutans, and 3 juvenile gorillas, all Regional Primate Research Center, and Hayes housed at the Lincoln Park Zoo. These apes and Nissen (1971) published data from Viki were presented with patterned string prob- describing “higher mental functions” that lems, a spatial delay response task involving were collected at in Orange Park. Menzel the location of a concealed food reward, and and Davenport (1962) studied chimpanzees at a delayed match-to-sample task (Fischer and Orange Park, focusing largely on social and Kitchener, 1965). Rumbaugh followed an un- cognitive development. Menzel is likely best usual trajectory by starting at a zoo and known for his work with a group of then migrating to a primate research center. chimpanzees who lived in a 1-acre compound His early work drew heavily from data at the Delta Regional Primate Center which collected at the San Diego Zoo, but his most

- 107 - 動物心理学研究第68巻第２号 significant accomplishments were based later by university-based projects. This important at the Yerkes Regional Primate Center (Rum- work contributed substantially to the under- baugh, 1971; Rumbaugh and Gil, 1973; Rum- standing of cognitive abilities in great apes, baugh, 1977). particularly in the areas of anthropology, At this point in the history of behavioral developmental psychology, comparative psy- and cognitive research with great apes in the chology, and linguistics. However, other aca- United States, Parker and McKinney (1999) demic domains were well represented by document a notable transition. The existing, work conducted at primate centers. Examples foundational work had covered topics such include studies of social cognition with as “tool use, space, number, logic and com- chimpanzees (Tomasello et al., 1989) and munication”, among others, but there had observational learning in orangutans (Call & been little focus on development or develop- Tomasello, 1994), both at the Yerkes Regional mental psychology (Parker & McKinney, Primate Center. Various capacities associated 1999). The “third generation” of scientists in with Theory of Mind were explored by the field shifted towards an emphasis on Povinelli et al. (1998) with chimpanzees at the comparative developmental psychology (Parker New Iberia Research Center in New Iberia, & McKinney, 1999). Exemplars include Boy- Louisiana. sen, who established the Comparative Cogni- Despite the expanded focus and participation Project at The Ohio State University in tion by a larger number of academic disci- 1983. Her work, which included Premack’s plines during this era compared to earlier Sarah (Premack & Premack, 1983), largely decades (Parker and McKinney, 1999), a defined the numerical abilities of chimpan- prevailing tendency is clear. The body of zees at the time (Boysen & Berntson, 1990; work produced was consistent with previous Boysen et al., 1996). Sue Savage-Rumbaugh’s generations in that the majority relied on early career was dedicated to exploring great apes living in primate centers, and to a symbolic representation in chimpanzees lesser extent, university campuses. Great (Savage-Rumbaugh et al. 1978), with research apes living in US zoos were not excluded but based at the Yerkes Regional Primate Center. remained largely unrepresented. Exceptions Later, her focus shifted exclusively to can be found. For example, Patterson (1978) language-learning in bonobos living at the began her study of language acquisition with Language Research Center at Georgia State Koko the gorilla at the San Francisco Zoo, University (Savage-Rumbaugh, 1993). Contem- before moving to the campus of Stanford poraries devoted to the study of language University, and finally to a private site in acquisition by great apes included Fouts, as Woodside, California. Mitchell (1991) studied previously mentioned, who studied chimpan- gorillas at the Woodland Park Zoo in Seattle, zees at Central Washington University in Washington, documenting their ability to Ellensburg, Washington (Fouts, 1997) and hide, inhibit, and deceive as a means of Terrace (1979), who was based at Columbia social manipulation. However, a review of University. His project documented the fail- Zoo Biology supports the trend. Beginning ure of his chimpanzee Nim to learn Ameri- with issue 1 in 1982 through the last issue of can Sign Language (Terrace, 1979), and 1995, numerous applied studies with great Terrace ultimately became a prominent critic apes related to areas such as reproduction of ape language work in general. Working at and various aspects of husbandry were the University of Tennessee in Chattanooga, published. But, there were zero articles that Miles was the first to teach American Sign explored the cognitive abilities of great apes Language to an orangutan (Miles, 1983; Miles, in US zoos even though this subject is 1990). within the scope of the journal. The examples noted here illustrate some While there was no single event or of the major contributions that were made coordinated effort that can be identified, the

- 108 - SHUMAKER：The history and status of cognitive research with great apes in the United States landscape for cognitive research with great the mental skills and abilities of these apes in the US began to shift during the animals, ranging from simple to complex (Beck mid-1990s and into the early 2000s. During et al., 1993). As part of the exhibit, a this time, the field continued to be well longitudinal study of orangutan cognitive supported by work produced at primate skills was initiated with one important dis- centers. The Living Links Center, part of the tinction: data collection was conducted in Yerkes Regional Primate Center, opened in front of zoo visitors in a demonstration 1997 with the purpose of studying “human format with live interpretation by the investi- evolution by investigating our close genetic, gator. The exhibit, named “Think Tank”, anatomical, cognitive, and behavioral similari- opened in 1994 and was supported by both ties with great apes.” (http://www.emory.edu/ visiting and resident scientists. Topic areas LIVING_LINKS/index.shtml). The contribution of study included observational learning to the field from Living Links is impressive, (Shumaker, 1997), object permanence (de Blois and results from studies into social cognition et al, 1998), mirror self-recognition (Shillito et have been exceptionally rich. Topics such as al., 1999), magnitude discrimination and ordi- visual kin recognition (Parr & deWaal, 1999), nation (Shumaker et al., 2001), theory of mind reconciliation (Preuschoft et al., 2002), facial (Shillito et al., 2005), and serial list learning perception (Plotnik et al., 2003), economic (Swartz et al., 2007). The decision to fully decision making (Brosnan et al., 2005), social embrace the process of scientific investigation diffusion of material culture (Hopper et al., as a core component for a permanent exhibit 2007), and empathy (deWaal, 2012) substan- in a zoo was unprecedented. As a result, tially expanded the understanding of chim- Think Tank changed the trajectory of cogni- panzee mental skills and abilities. tive research with great apes in the US. Through the late 1990s and into the In 2004, the Lincoln Park Zoo opened the beginning of the 21st century, universities Regenstein Center for Great Apes, which continued to be important places for the houses chimpanzees and gorillas (Ross, 2017). study of great ape mental skills. The Lan- The facility focuses on comparative cognition, guage Research Center at Georgia State routinely presents cognitive tasks via touch- University supported research on such di- sensitive computer interfaces (Ross, 2009; verse topics as chimpanzee abilities to Ross, 2017) and has explored topics including remember and communicate events to a tool use (Ross et al., 2010), the impact of a naïve human via lexigrams (Menzel, 1999), social model on ape memory (Howard et al., numerical competencies (Beran et al. 2011; 2017), social tolerance and sharing (Calcutt et Beran et al. 2013), and the expression of al. 2014), and factors that impact the success cognitive biases (Brosnan et al., 2012). of chimpanzee problem solving (Hopper et Independent of the work occurring at al., 2014). The philosophy of the Regenstein primate centers and universities, an impactful Center emphasizes welfare and structures all change was underway in the zoo community. studies so that they are voluntary for the In the early 1990s, the Smithsonian National apes and conducted in view of visitors (Ross, Zoo developed a groundbreaking, permanent 2017). Ross (2017) states that “research on new exhibit. Unlike most previous zoo exhib- display” offers the benefits of “transparency its, the core concept revolved around a in the scientific methodology and promotes biological process, “thinking”, rather than the importance of scientific research to a any specific type of animal. Conceived by wide audience”. Benjamin B. Beck, a comparative psycholo- Zoo Atlanta followed in 2007 with their gist, the plan was to design a zoo exhibit “Learning tree”, which offered orangutans that included multiple different species from the opportunity to engage in cognitive tasks a variety of taxonomic groups. Interpretation presented via a touch screen apparatus and education for visitors would focus on in front of visitors (https://zooatlanta.org/

- 109 - 動物心理学研究第68巻第２号 orangutan-learning-tree/). An assessment of acknowledge the complex mental abilities reactions by zoo guests revealed an over- that are present for great apes. Husbandry whelmingly positive response (Perdue et al., programs emphasize “environmental enrich- 2012). Research with great apes at Zoo ment” as a means of providing cognitive Atlanta occurs on exhibit with visitors stimulation. As categorized by Bloomsmith et present as well as in off-exhibit areas al. (1991), enrichment typically falls into the without visitors (Diamond et al., 2016; Gazes categories of social, physical, nutritional, et al. 2017). sensory, and occupational. While all are Research based in primate centers contin- positive and offer species appropriate activi- ues but is less frequent than in the past. ties such as foraging or object manipulation, Examples include Hopkins (pers. comm.) who few to none of the usual forms of enrichment studies auditory learning in chimpanzees at engage the intellectual potential of great apes the Yerkes Regional Primate Center and the M. (Meehan & Mench, 2007). To do this, Meehan D. Anderson Cancer Center in Bastrop, and Mench (2007) suggest that frustration Texas. Brosnan (pers. comm) also has an and stress are important elements that ongoing research program at M. D. Anderson should be present, while Clark (2011) discuss- studying decision-making in chimpanzees es “challenge” as the essential feature for a through experimental economics tasks. The task to qualify as “cognitive enrichment”. A Living Links Center is not active, and the simpler and more useful description is that future for this site is unclear. cognitive challenges for great apes must As of early 2018, all university-based involve learning and problem solving. Addi- projects with great apes have closed. tionally, the tasks should be self-paced, The Ape Cognition and Conservation allowing the apes to continually progress Initiative (ACCI) in Des Moines, Iowa, houses based on their individual skills, abilities, and the only ongoing study of bonobos in the interests. When structured in this way, each US. The ACCI is focused on research that ape is offered opportunities that are gradual- uncovers the “evolutionary origins of human ly and perpetually challenging, resulting in language, cognition, and behavior” (http:// continuous interest and engagement. Ideally, apeinitiative.org/). This unique facility re- opportunities to participate would be ceives support from university-based investi- presented daily. Problem solving may, at gators, and researchers regularly collaborate times, include some level of healthy frustra- with zoos for data collection with their tion that focuses attention and encourages bonobos. interest. However, it is problematic and Currently, cognitive research projects with inaccurate to suggest that frustration and great apes are in residence at 4 zoos in the stress are required for a task to be mentally US. They are the Smithsonian National Zoo engaging. Further, measuring “frustration” or (Suda-King et al., 2013; Parrish et al, 2014.), “stress” can be unreliable in this context. Lincoln Park Zoo, Zoo Atlanta, and the Metrics that document learning and problem Indianapolis Zoo. The project with orang- solving are readily available through analysis utans started by Shumaker at the Smithson- of performance data on cognitive tasks. ian National Zoo’s Think Tank in 1993 (Beck These provide a useful means of assessing et al., 1993; Shumaker et al., 2001) now the value of what is being presented to the resides at the Indianapolis Zoo and will be ape. described in greater detail in the following Opportunities for great apes in US zoos section. to engage in mentally enriching tasks are becoming more common. Hopper’s (2017) 2. Factors promoting success with zoo-based review of the literature clearly illustrates that cognitive research programs. zoo-based cognitive research is increasing. Virtually all modern, accredited zoos Her analysis of publications from 15 coun-

- 110 - SHUMAKER：The history and status of cognitive research with great apes in the United States tries shows that the largest increase has and movable affordances that promote occurred in the US, and the most studied locomotion on all surfaces. Outdoor spaces species by far are gorillas, orangutans, include an unenclosed tower and cable chimpanzees, and bonobos. system reaching about 30 meters high that The Simon Skjodt International Orangutan allows for travel between the 3 buildings and Center at the Indianapolis Zoo, included in 2 outdoor yards that comprise the entire Hopper’s (2017) review, provides an example complex. The concept for this tower system of a successful cognitive research program originated with the Smithsonian National for great apes. The Center was conceptual- Zoo’s “O-Line” which opened in 1993 (Beck et ized and designed with two main objectives al., 1993), and has been successfully replicat- in mind. The first was to maximize ed at a small number of other zoos including orangutan welfare. The second was to create the Tama Zoo in Tokyo and the Guadalajara an increased “connection” for visitors with Zoo in Guadalajara. The layout of the orangutans that would result in greater buildings, yards, and tower system allows for concern for their conservation in the wild. individual choice and tremendous flexibility The physical facilities, husbandry protocols, in social groupings. The apes can choose and all programs were created to advance their location within the complex, as well as these goals. To maximize welfare, it was their social companions. Data collected over assumed that the orangutans must have the 289 days in 2015, when 7 individuals lived at ability to express a full range of physical, the Center, revealed 47 different social group- social, and mental behaviors. It was also ings overall, with an average of 3.6 different assumed that witnessing this range of behav- social combinations each day. The Center iors was the best way to maximize visitor currently houses 12 orangutans, ranging in engagement, create a “connection”, and gen- age from 2 to 40 years old. A corresponding erate concern for conservation in the wild. increase is social complexity has resulted. The dual goals of promoting ape welfare and Cognitive enrichment is structured around engaging zoo visitors converged around de- hypothesis driven research questions. A clear sign features that focus on three primary preference exists for longitudinal studies that elements for the apes. These are 1.) promot- include multiple subjects. The primary topics ing species-typical styles of locomotion, that are investigated at the Center are 2.) allowing travel for social choice, and symbolic representation, numerical competen- 3.) regularly offering cognitive tasks that cy, social learning, memory, and strategic require learning and problem solving. No reasoning. Data collection is conducted by attempt was made to address these elements staff scientists and all sessions occur in a by constructing a facility that appeared to be demonstration format that occurs with zoo an artificial forest. Rather, all efforts focused guests in attendance. Most of the work takes on creating an environment that was “func- place in the Solso Studio, which is equipped tionally naturalistic” for the apes rather than with two styles of touch-sensitive computer “aesthetically naturalistic” from a human stations utilized by the apes. The first has a perspective. single response screen that requires an ape Unlike the African great apes, orangutans to work singly. The second is a version of are physically and behaviorally adapted for the “arena system” (Martin et al., 2014) which an arboreal lifestyle. Traditional zoo architec- has two adjacent and interconnected multi- ture has emphasized terrestrial locomotion touch monitors that function together. One is for all great apes, which handicaps orang- in the ape space, and the other is in the utans and prevents the expression of many visitor area. This allows the presentation of species-typical behaviors. To maximize orang- diverse types of tasks including the ape utan movement at the Center, indoor areas working alone, in collaboration with a human reach about 18 meters high with both fixed partner, or with computer-generated respons-

- 111 - 動物心理学研究第68巻第２号 es that move across the screens. Additionally, elegantly when she states that “great ape multiple other units are available, including cognition requires powerful, sophisticated a token operated vending machine, a button brains.”. activated feeder, and a portable touch-panel The goal of maximizing orangutan welfare system. The feeder and portable touch-panel at the Center is being achieved. But is this system can be mounted in various locations engaging zoo visitors in a way that advances indoors and outdoors within the complex, a conservation ethic? As part of a summative and are designed to present specific tasks evaluation of the Center, a survey assessing that encompass research and enrichment, attitudes was implemented. Subjects were and also allow the apes to express preferenc- first-time visitors between the ages of 25 and es for certain tasks or desired foods and 54 with children under the age of 16. A objects. The diverse types of apparatuses, as continuous random sampling method was well as the different tasks that they can used to select potential participants at the offer, have an important effect. All of the Zoo. A total of 68 groups agreed to partici- orangutans, regardless of age, location within pate. All respondents ranked their attitudes the complex, experience level, or skill with to the following 5 questions before their visit, cognitive testing, can engage in rewarding as they exited the Center, and 6 to 8 weeks tasks that require learning and problem post visit: solving. Importantly, all cognitive work is  I am motivated to do something to voluntary for the apes, and based on positive protect wild orangutans (motivation) reinforcement. Hunger is never used as a  I feel a connection to orangutans motivator, and all apes receive the same (connection) amount of food on the same schedule every  My actions can help save wild orang- day regardless of whether they choose to utans (actions) work or not. External researchers interested  I care about the future of wild orang- in cognitive topics are also hosted by the utans (future) Zoo. Typically, this work has not been  I think orangutan conservation matters computer based and is characterized well by (conservation) a series of studies conducted by Lameira et For respondents who were exiting the al. (2013; 2016) on vocal learning in orang- Center, the results revealed statistically utans. significant attitudinal changes in all the Research with the orangutans has oc- categories as a result of visiting the curred daily since the opening of the Center orangutan exhibit (Wilcoxon Signed Rank in 2014, with rare disruptions resulting from Test, P ＜ .001). Attitudinal changes showed such things as facility maintenance, repairs, an increased “connection to orangutans” and or installation of new computer equipment. all reported greater concern for field conser- For all data collection sessions since 2014, vation. voluntary participation by the apes has oc- In the follow-up survey 6 to 8 weeks later, curred 98% of the time, averaged across all attitudinal changes of respondents remained individuals. These high rates of engagement, statistically higher than before their trip to as well as the demonstrable learning, acquisi- the Zoo (Wilcoxon Signed rank with Bonfer- tion, and expansion of skills that have onni adjustments, P ＜ .001), indicating a occurred, speak to the high levels of motiva- long-term effect of their visit to the orang- tion that exist for the apes. There should be utan Center. The “overall” category shown in little surprise that orangutans (and great Figure 2 includes the responses to all 5 apes in general) seek out opportunities for survey questions. mental exercise. Whether in the wild or a Rates of voluntary participation and docu- zoo, great apes have impressive mental skills. mented acquisition of skills demonstrate that Russon (2014) makes the point succinctly and orangutans of all ages are highly motivated

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Figure 1. Guests who visited the Simon Skjodt International Orangutan Center all reported a positive shift in their attitudes about orangutans and the importance of their conservation.

Figure 2. Attitudinal changes were statistically significant for pre, post, and follow up responses.

- 113 - 動物心理学研究第68巻第２号 to participate in cognitive tasks that require ments, and it is no coincidence that the vast learning and problem solving. These opportu- majority of research with great apes on all nities provide one important means of topics in the US has been conducted with maximizing great ape welfare in zoos. Guests chimpanzees. Research was the specific rea- that observe cognitive research have a son that labs were established, and it is the stronger connection to orangutans and care core of their institutional culture. Experimen- more about their conservation in the wild. tal work and the associated rigor was a These effects persist after the zoo visit. comfortable fit in an environment that was managed at the executive level by scientists 3. Summary with the goal of accommodating other The history of cognitive research with scientists to facilitate their research. These great apes in the United States spans slightly reasons also explain why cognitive research more than 100 years, and began with Robert W. was rare in zoos. Numbers of apes in zoos Yerkes. In his era, studies with great apes were always much lower than in labs, and were overwhelmingly based in primate that remains true today. When research did centers. After this founding generation of occur in zoos, applied studies that enhanced scholars, Parker and McKinney (1999) note husbandry and reproduction were prioritized that an important shift occurred in the field. over behavioral and cognitive investigations. Studies were largely based on two styles. Stated directly, theoretical research was The first relied on natural history style largely peripheral to the historical purpose of observations of young apes raised in human most zoos, making it a difficult cultural fit. homes, with a primary focus on language Investigators were also challenged by the acquisition. The second style involved re- nature of working in a zoo environment that search based in laboratory environments that allowed far less control compared to a was conducted under strictly controlled laboratory. Also, the presence of visitors was conditions. These studies were based in resented. Patterson (1981) summarized percep- primate centers. tions about working in a zoo perfectly by During the 1960s, universities began to stating that, “my enjoyment was tempered by host ape cognition projects on site, with the frustrations and crises of pursuing my Premack as a prime example (Premack & work in front of gawking visitors”. Premack, 1983). Apes living in zoos were not University-based projects have been highly excluded from studies, but were largely un- visible and contributed significantly to the represented in the field. literature, although the number of great apes A conceptual shift occurred when the “third housed on university campuses has always generation” of scientists to study great ape been relatively small compared to primate cognition began to focus on development and centers and zoos. The mission fit with developmental psychology (Parker and McK- universities may have been strong, but inney, 1999). As with past projects, this work concerns about expense, ape welfare, risk, was based primarily in primate centers, but and outside scrutiny have outweighed the some high-profile projects were based at benefits. Today, there are no apes living on universities. Zoo-based studies continued to university campuses, and this highly produc- be rare. What likely explanations exist for tive era has ended. these trends? Influential work continues in primate cen- Primate centers were a clear choice for ters with chimpanzees, but the number of several reasons. The ubiquity of a wide age active projects has significantly decreased. In range of potential subjects made these facili- general, these projects are short-term rather ties well-suited for cognitive work. The than longitudinal. largest number of chimpanzees in the US A significant shift occurred in the 1990s has historically been in laboratory environ- and cognitive research with zoo-living great

- 114 - SHUMAKER：The history and status of cognitive research with great apes in the United States apes began to accelerate. A likely contribut- tion, and provide an effective means to ing factor included scientific interest in advance support for in situ conservation of studying all species of great ape in response great apes. to a strong chimpanzee bias in the literature. More recently, the number of available great Acknowledgements apes in laboratory environments declined as chimpanzees were retired and moved into The author is grateful to Drs. Chris sanctuaries (Kaiser, 2015), none of which Martin, Steve Ross, Lydia Hopper, Ben Beck, host cognitive research. Modern zoos house Sarah Brosnan, and Bill Hopkins for their species-typical social groupings for apes in expert assistance and insightful comments. enriched and behaviorally naturalistic environments, which is highly compatible with References longitudinal studies. For studies of social cognition, these factors are particularly ap- Baker, K. C., Aureli, F., 1997 Behavioural propriate and desirable (de Waal, 1991). indicators of anxiety: an empirical test in Perhaps most influentially, a culture shift chimpanzees. Behaviour, 134, 1031-1050. occurred in the zoo community with the Beck, B. B., Dolnick, L., Jenkins, D., Keane- realization that cognitive challenges for great Timberlake, S., Shumaker, R. W., & apes are valuable, enriching and in perfect Stevens, L. 1993 Mind matters at the zoo. alignment with husbandry goals. In contrast Zoogoer, 22-25. to primate centers and universities, zoos are Beran, M. J., Evans, T. A., & Hoyle, D. 2011 the only sites where research focused on the Numerical judgments by chimpanzees (Pan mental abilities of the great apes is increas- troglodytes) in a token economy. Journal ing. of Experimental Psychology: Animal Zoos offer a tremendous potential resource Behavior Processes, 37, 165-174. for investigators who are interested in great Beran, M. J., McIntyre, J. M., Garland, A., & ape mental abilities. In fact, modern zoos Evans, T. A. 2013 What counts for meet all the criteria for an optimal research “counting”? Chimpanzees (Pan troglodytes) setting as envisioned by Yerkes (1916b). respond appropriately to relevant and Several factors have proven to be highly irrelevant information in a quantity beneficial for promoting the success of a zoo- judgment task. Animal Behaviour, 85, based cognitive research program. Of primary 987-993. importance are staff scientists and the de Blois, S. T., Novak, M. A., & Bond, M. institutional commitment to authentic mental 1998 Object permanence in orangutans enrichment as an essential element of care. (Pongo pygmaeus) and squirrel monkeys Hypothesis based research involving learning (Saimiri sciureus). Journal of Comparative and problem solving is the best way to Psychology, 112 , 137-152. provide the cognitive stimulation that great Bloomsmith, M. A., Brent, L. Y., Schapiro, S. apes in zoos require and deserve. J., 1991 Guidelines for developing and Current trends suggest that zoos are managing an environmental enrichment essential for the future of cognitive research program for nonhuman primates. Lab. with great apes in the US. As described by Anim. Sci, 41, 372-377. de Waal (1991), the opportunity to compare Boysen, S. T., & Bernston, G. G. 1990 The results from zoos with data collected in other development of numerical skills in the settings will provide converging evidence that chimpanzee (Pan troglodytes). In S. T. advances that science of understanding great Parker & K. Gibson (Eds.). “Language” ape mental abilities. In addition, cognitive and intelligence in monkeys and apes: studies promote great ape welfare, offer a Comparative developmental perspectives platform for transformational public educa- (pp.435-450). New York, NY, US:

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