ROOTS OF PRIMATE COGNITION The Primate Cognition Test Battery applied to three species of lemurs (Varecia variegata, Lemur catta and Microcebus murinus) Dissertation for the award of the degree „Doctor rerum naturalium“ (Dr. rer. nat.) of the Georg-August-University of Göttingen within the doctoral program Biology of the Georg-August University School of Science (GAUSS) submitted by Klara Kittler from Kassel, Germany Göttingen, 2017 Thesis Committee Prof. Dr. Peter M. Kappeler Behavioural Ecology and Sociobiology Unit, German Primate Center (DPZ), Kellnerweg 4, 37077 Göttingen Prof. Dr. Eckhard Heymann Behavioural Ecology and Sociobiology Unit, German Primate Center (DPZ), Kellnerweg 4, 37077 Göttingen Members of the Examination Board Reviewer: Prof. Dr. Peter M. Kappeler Second Reviewer: Prof. Dr. Eckhard Heymann Further Members of the Examination Board: Prof. Dr. Julia Fischer Cognitive Ethology Laboratory, German Primate Center (DPZ), Kellnerweg 4, 37077 Göttingen Prof. Dr. Mark Maraun J.F. Blumenbach Institute of Zoology and Anthropology, University of Göttingen, Berliner Str. 28, 37073 Göttingen Prof. Dr. Lars Penke Biological Personality Psychology, Georg Elias Müller Institute of Psychology, University of Göttingen, Goßlerstr. 14, 37073 Göttingen Prof. Dr. Hannes Rakoczy Department of Developmental Psychology, Georg-Elias-Müller Institute of Psychology, University of Göttingen, Waldweg 26, 37073 Göttingen Date of oral examination: 16th of June 2017 Contents Summary iii Zusammenfassung v Chapter 1: General Introduction 1 1.1 Why study cognition in primates? 2 1.2 How did (primate) cognition evolve? 3 1.3 The Primate Cognition Test Battery (PCTB) 6 1.4 Why study cognition in lemurs? 8 1.5 The lemur species of my thesis 9 1.6 Objectives and structure of this thesis 11 Chapter 2: Cognition in Ring-tailed Lemurs (review) with Anna V. Schnöll and Claudia Fichtel 13 Folia Primatologica, 86(1-2):106-116, Special Issue: Ring-Tailed Lemurs: A Species Re- Imagined (2015) Chapter 3: The Lemur Baseline: How Lemurs compare to Monkeys and Apes in the Primate Cognition Test Battery with Peter M. Kappeler and Claudia Fichtel 25 Animal Cognition: submitted Chapter 4: Instrumental Problem-Solving Abilities in Three Lemur Species with Peter M. Kappeler and Claudia Fichtel 63 Journal of Comparative Psychology: in press Chapter 5: Use of gaze and pointing cues presented by a human demonstrator, modelled humans and conspecifics in Malagasy primates with Peter M. Kappeler and Claudia Fichtel 81 Animal Cognition: submitted Chapter 6: General Discussion 103 6.1 Interpreting the results of the PCTB - Lemurs vs. apes & monkeys 103 6.2 A brief comparison to gibbons 105 6.3 How did (primate) cognition evolve? 106 6.4 Comparative cognition - Problems and pitfalls 110 6.5 What to do next? - An outlook 113 6.5.1 Including more species 114 6.5.2 Adapting the PCTB 115 6.5.3 Going wild - the value of field studies 115 6.6 General conclusions 116 General Appendix 118 References 119 Acknowledgements 138 Curriculum Vitae 140 Declaration 143 General Introduction Summary In comparison to other, equally-sized mammalian species, primates have relatively large brains and outstanding cognitive skills. Since brain tissue is energetically very costly, several hypotheses on possible selection pressures that might have favoured the evolution of such large brains and increased cognitive skills have been proposed. Some hypotheses focus on ecological aspects, whereas others suggest social complexity as the main factor shaping cognitive evolution. Comparative studies on cognitive abilities of multiple species are essential for answering this evolutionary puzzle. Such studies have been conducted in various haplorhine primates (great apes, Old- & New World monkeys), but systematic studies on cognitive skills in strepsirrhine primates (lemurs & lorises) were missing until now. As strepsirrhines can serve as living models of the ancestral primate state, knowledge about their cognitive abilities could help elucidate the evolution of primate cognition. Therefore, the aim of my thesis was to first review all existing studies on cognitive skills in lemurs and then to test three species of lemurs in a systematic battery of experiments covering the physical and social cognitive domain. Subjects were black- and-white ruffed lemurs (Varecia variegata), ring-tailed lemurs (Lemur catta) and grey mouse lemurs (Microcebus murinus), chosen for differences in key socioecological traits. To facilitate comparisons to haplorhines, I used the experimental setup of the Primate Cognition Test Battery (PCTB) which has been tested with great apes (chimpanzees & orangutans; Herrmann et al., 2007) and Old World monkeys (baboons & macaques; Schmitt et al., 2012). Results showed that the three lemur species did not differ significantly in performance and in general had a better understanding of the physical than the social domain. Surprisingly, an overall comparison with the four haplorhine species revealed that although lemurs performed slightly inferior in the physical domain, they were at level with haplorhines in the social domain. Specifically, lemurs were outperformed by haplorhines particularly on the scale on spatial understanding and in the active tool use task. All other scales revealed comparable results for all seven species and in the scale theory of mind lemurs even outperformed great apes. However, in several of the experimental setups results might have been influenced by confounding factors such as lemurs’ limited dexterity, local enhancement or the heterospecific human demonstrator in the social tasks, and thus results have to be discussed carefully. iii General Introduction To investigate some of the possible influences on the performance of individuals within cognitive tasks, I incorporated two additional studies on selected tasks of the PCTB. First, I explored whether the reason for the lemurs’ poor performance in the tool use task was caused by their limited dexterity. I increased the number of trials by retrieving the stick if it was lost by the subject. In contrast to the original setup in which only one ring-tailed lemur solved the task, in total 13 individuals from all three species managed to obtain the reward. In addition, lemurs performed at the same level as haplorhines in a task testing the understanding of tool properties. Thus, my results revealed that lemurs may lack the necessary fine motor skills to actively use more difficult tools, but they nevertheless appear to have an understanding of tool functionality comparable to naturally tool-using species. The second additional study concerned the influence that different kinds of demonstrators may have on performance in gaze following tasks and in object-choice tasks using pointing cues. In the original PCTB results may have been biased by only using a human as demonstrator and thus, I additionally presented subjects with photos and videos of conspecifics. Only ring-tailed lemurs followed human gaze. Photos did not have an influence on general performance of lemurs, but videos increased performance in the gaze following task. Comparing two differently handled populations revealed that in the object-choice tasks performance was positively influenced by a high level of socialisation with humans. Thus, performance of individuals in social cognitive tasks can be influenced by the exact nature of the stimulus as well as the level of human socialisation. The overall results of my thesis suggest that in many aspects of the physical and social domain, haplorhines and strepsirrhines do not differ substantially from each other, at least in the experiments of the PCTB. Since they differ strongly in their absolute brain sizes, my results question the notion of a clear-cut correlation between brain size and cognitive abilities, as well as assumptions of domain-general cognitive skills in primates. My thesis represents the first systematic comparative investigation of the cognitive skills of lemurs and thus provides important insights into the cognitive evolution of primates. However, further comparative studies on a wide range of species using tasks from both cognitive domains are essential to fully understand the evolutionary puzzle of cognition. iv General Introduction Zusammenfassung Im Vergleich zu anderen Säugetieren haben Primaten in Bezug auf ihre Körpermasse relativ große Gehirne und herausragende kognitive Fähigkeiten. Da das Gehirn energetisch gesehen äußerst kostspielig ist, wurden bereits diverse Hypothesen zu möglichen Selektionsdrücken aufgestellt, welche die Evolution von größeren Gehirnen und erhöhter kognitiver Kompetenz beeinflusst haben könnten. Einige Hypothesen erwägen ökologische Aspekte, während andere die Komplexität des Sozialgefüges als Haupteinfluss für die kognitive Evolution vorschlagen. Um Antworten auf dieses evolutionäre Rätsel zu erlangen, sind vergleichende Analysen der kognitiven Fähigkeiten unterschiedlicher Arten unerlässlich. Diverse Haplorhini-Arten (Menschenaffen, Alt- & Neuweltaffen) wurden diesbezüglich bereits erforscht, aber systematische Untersuchungen der kognitiven Fähigkeiten von Strepsirrhini (Lemuren & Loris) fehlen bislang gänzlich. Dabei sind gerade die Strepsirrhini für die Erforschung der kognitiven Evolution von Primaten besonders geeignet, da sie zu den phylogenetisch basalsten Primaten gehören und als lebendes Modell ursprünglicher kognitiver Fähigkeiten dienen können. Aus diesem Grund waren die Ziele meiner Doktorarbeit zunächst alle bisherigen Studien zur Kognition