Visalberghi1 Abstract Preference Transitivity and Symbolic Representation in Capuchin Monkeys (Cebus apella ) Elsa Addessi1*, Alessandra Mancini1,2, Lara Crescimbene1,2, Camillo Padoa-Schioppa3,4, Elisabetta 1 Unit of Cognitive Primatology and Primate Center, Institute of Cognitive Sciences and Technologies, Consiglio Nazionale delle Ricerche (CNR), Rome, Italy, 2 University ‘‘La Sapienza’’, Rome, Italy, 3 Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States of America, 4 Washington University School of Medicine, St Louis, Missouri, United States of America Background: Can non-human animals comprehend and employ symbols? The most convincing empirical evidence comes from language-trained apes, but little is known about this ability in monkeys. Tokens can be regarded as symbols since they are inherently non-valuable objects that acquire an arbitrarily assigned value upon exchange with an experimenter. Recent evidence suggested that capuchin monkeys, which diverged from the human lineage 35 million years ago, can estimate, represent and combine token quantities. A fundamental and open question is whether monkeys can reason about symbols in ways similar to how they reason about real objects. Methodology/Principal Findings: Here we examined this broad question in the context of economic choice behavior. Specifically, we assessed whether, in a symbolic context, capuchins’ preferences satisfy transitivity - a fundamental trait of rational decision-making. Given three options A, B and C, transitivity holds true if A$B, B$C and A$C (where $ indicates preference). In this study, we trained monkeys to exchange three types of tokens for three different foods. We then compared choices monkeys made between different types of tokens with choices monkeys made between the foods. Qualitatively, capuchins’ preferences revealed by the way of tokens were similar to those measured with the actual foods. In particular, when choosing between tokens, monkeys displayed strict economic preferences and their choices satisfied transitivity. Quantitatively, however, values measured by the way of tokens differed systematically from those measured with the actual foods. In particular, for any pair of foods, the relative value of the preferred food increased when monkeys chose between the corresponding tokens. Conclusions/Significance: These results indicate that indeed capuchins are capable of treating tokens as symbols. However, as they do so, capuchins experience the cognitive burdens imposed by symbolic representation. Citation: Addessi E, Mancini A, Crescimbene L, Padoa-Schioppa C, Visalberghi E (2008) Preference Transitivity and Symbolic Representation in Capuchin Monkeys (Cebus apella). PLoS ONE 3(6): e2414. doi:10.1371/journal.pone.0002414 Editor: Laurie Santos, Yale University, United States of America Received April 7, 2008; Accepted April 23, 2008; Published June 11, 2008 Copyright: 2008 Addessi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funded by VI Framework, NEST Pathfinder Initiative, What it means to be human, Contract nu 12984, Stages in the Evolution and Development of Sign Use - SEDSU, and Contract nu 29088, Humans: The Analogy-Making Species - ANALOGY. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: elsa.addessi@istc.cnr.it INTRODUCTION Humans have been defined ‘‘the symbolic species’’ since the use and understanding of symbols drastically transformed our hominid ancestors throughout evolution [1]. The acquisition of a complex language is unparalleled in the animal realm and probably underlies human uniqueness [2]. Besides language, humans creatively and flexibly use a huge array of symbols, thus acquiring information about the world without having direct experience of all its features. The use of symbols makes it possible to travel both in time and space and to accumulate and transmit cultural knowledge over generations [3–5]. Whether non-human animals comprehend and employ symbols is still an open question since symbolic competence is difficult to test in the absence of language. The most convincing empirical evidence of animals using symbols comes from a series of studies on language-trained apes. Two chimpanzees learned to use lexigrams to ask one another’s for the appropriate tool required to obtain food and they readily fulfill to one another’s requests [6]. Moreover, chimpanzees trained to sort out real foods from real tools and to categorize each of them by choosing the consistent lexigram out of two (generically indicating one ‘food’ and the other ‘tool’) kept categorizing using the correct lexigram also when presented with new items [7,8]. Furthermore, in a reverse-reward contingency task [9–11], where chimpanzees failed to select a smaller food array in order to receive a larger one, the use of Arabic numerals (instead of food) allowed chimpanzees to overcome their strong motivation to choose the largest between the two food arrays and to be successful. Little is known about the symbolic ability of non-apes. There is some evidence that capuchin monkeys, South-American primates that diverged from us 35 million years ago, use tokens as symbols [12,13]. Tokens are inherently non-valuable objects that acquire an associative value upon exchange with the experimenter [14]. PLoS ONE | www.plosone.org 1 June 2008 | Volume 3 | Issue 6 | e2414