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Callicebus Nigrifrons) ANTI-PREDATOR BEHAVIOUR OF BLACK-FRONTED TITI MONKEYS (CALLICEBUS NIGRIFRONS) Cristiane Cäsar A Thesis Submitted for the Degree of PhD at the University of St Andrews 2012 Full metadata for this item is available in St Andrews Research Repository at: http://research-repository.st-andrews.ac.uk/ Please use this identifier to cite or link to this item: http://hdl.handle.net/10023/2575 This item is protected by original copyright Anti-predator behaviour of black-fronted titi monkeys (Callicebus nigrifrons) Cristiane Cäsar Thesis submitted to the School of Psychology of the University of St. Andrews for the degree of Doctor of Philosophy October 2011 1. Candidate’s declarations: I, Cristiane Cäsar, hereby certify that this thesis, which is approximately 56,000 words in length, has been written by me, that it is the record of work carried out by me and that it has not been submitted in any previous application for a higher degree. I was admitted as a candidate for a degree of Doctor of Philosophy in October 2007; the higher study for which this is a record was carried out in the University of St Andrews between 2007 and 2011. Date…………………Signature of candidate………………………………………………. 2. Supervisors’ declaration: We hereby certify that the candidate has fulfilled the conditions of the Resolution and Regulations appropriated for the degree of Doctor of Philosophy in the University of St Andrews and that the candidate is qualified to submit this thesis in application for that degree. Date…………………Signature of supervisors………………………………...…………… …………………………………………….. In submitting this thesis to the University of St Andrews we understand that we are giving permission for it to be made available for use in accordance with the regulations of the University Library for the time being in force, subject to any copyright vested in the work not being affected thereby. We also understand that the title and abstract will be published, and that a copy of the work may be made and supplied to any bone fide library or research worker, that my thesis will be electronically accessible for personal or research use unless exempt by award of an embargo as requested below, and that library has the right to migrate my thesis into new electronic forms as required to ensure continued access to the thesis. We have obtained any third-party copyright permissions that may be required in order to allow such access and migration, or have requested the appropriated embargo below. The following is an agree request by candidate and supervisors regarding the electronic publication of this thesis: Access to all of printed copy, but embargo of all electronic publication of thesis for a period of 2 years on the following grounds: publication would preclude future publication. Date………………….. Signature of candidate ……………………………………………….. Signature of supervisors………………………………………………. …………………….………………………… To those who always believed me, even when I didn‘t: To my beloved husband, for all his love, support and encouragement And to the friends I found on the way. ii Acknowledgements “I may not have gone where I intended to go, but I think I have ended up where I needed to be.” (Douglas Adams, 1988). The list of people I would like to thank for their contribution (all in their own ways) to this thesis is very long and I am going to do my very best to not leave anyone out. First and foremost, I would like to thank my supervisors Dick Byrne and Klaus Zuberbühler for giving me the chance to work with them in St Andrews. Their constant guidance, support and encouragement at every step of the realization of this thesis have been extremely valuable and I feel incredibly honored to have worked with them! Whatever merits this thesis and my future as a researcher might have are undoubtedly shared with them - the imperfections remain exclusively my own. I am grateful to CAPES-Brazil (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for my PhD scholarship and FAPEMIG- Brazil for funding my field work. Thanks also to L.S.B. LEAKEY TRUST, The Experimental Psychology Society and the University of St Andrews Travel Funding. Thanks to Priests Marcos, Lauro, Wilson and Sebastião for allowing me to work in Caraça and to Aline Abreu for her support. I am thankful to IBAMA for giving me both the licence to work in Caraça and to transport biological material to the Natural Science Museum PUC Minas when needed. I am grateful to the Museum for lending me the animals I used as predator and control models, especially to directors Tudy Camara and Bonifacio for authorizing the loan, Teresa Young and Professor Castor Cartelle for their trust, Elane Simões, Marco Aurelio and Bruno Kraemer for organizing the documents and animals for me and Danilo Saraiva for taxiderming the oncilla I brought from Caraça. Thanks to my collaborator in the titi monkey project in Brazil, Robert Young. I am grateful to John Robinson for kindly listening to some of my recordings and giving me his impression about the similarities between the vocal repertoire of C. nigrifrons and C. cupreus. iii In St Andrews, special thanks go to Kate Arnold for all the great night-long discussions and suggestions! Thanks to Dave Perret (and Anne Perret), Andy Whiten, Tecumseh Fitch and Ines Jentsch for their encouragement and discussions. Thanks to Mike Oram, Will Hoppitt, Luke Rendell, De-Laine Cyrenne and Eric Bowman, for their support on acoustic analyses and their patience with my questions. Brian and Roy are thanked for their support whenever I encountered problems with my computer and/or technological issues. Helen, Karen, Veronica for their constant support whenever I need help with my university records. I would also like to thank all the people of the BDG and the acoustic and cognitive journal clubs to keep these initiatives alive and lively, especially to Peter Slater, Dick Byrne, Volker Deecke, Jeff Graves, and Chris Templeton. And the Burn team for their amazing scientific gathering, especially Hannah Buchanan-Smith. Without other St Andrews PhD students, the life in St Andrews would not have been as wonderful as it was. My thanks are especially going to my wonderful girlfriends including Anne, Emilie, Erica, Lynn, Marion, Elainie, Zanna, Cat, Emily and Katie, who were like a second family in different moments. Also Simon, Marietta, Sarah, Verena, Thibaud, Claudia, Marija, Bess, Jessica, Agnes, Hélène, Caroline, Sally, Lisa, Felicity, Rachel, Nuri, Kate, Guill, Katharina, Jenny, Gil, and Michelle (Stirling) for all the great moments spent together! Thanks also to Roman and Cathy for constructive comments and some stats advice. Big thanks to my first flatmates, Elena, Vaish and Raji, for their friendship during our first time living in another country and Peter for being a very trustworthy and reliable landlord. Thanks to my dearest friends from Tayport: Lynda and John Stuart, Joyce Murray, Eleanor and Anne for giving some special and reinvigorating time away from the academic world. In Caraça, Vandilso Farias for his interest, dedication and assistance in the field and data collection. Marina Bonde de Queiróz, Julianne Cosse de Azevedo, Belmiro Damas, Aryanne Clyvia Martins Moreira and Rafaela Vale dos Santos for their assistance. João Júlio for his company in the field station and his cheering, especially during difficult days. Also, Geralda for some comforting talks while waiting for, or seeing, the maned wolf feeding at the church, and all the employees of Caraça who were always helpful when needed. Furthermore, I would like to thank all past and new members of the long- iv term project who helped with habituation and demographic data collection: Guedes, D., Ferreira, S.Q.C., Nahur, A.C., Assunção, M.L, Silva, P.H.N., Sena, M.L.C., Marcolino, C.P., Franco, E.S., Soares, G.C.N., Viegas, L, R.F., Afonso, C.G., Santos, R.V, Lima, B.S.S, Santos, G.P., Morais, C.M.F., Queiróz, M.B, Moreira, A. C. M. Finally the titis, for allowing us to spend so much time walking around the forest and observing them. I must admit that I, sometimes, hated them, especially when for many and different reasons I would spend weeks trying (and failing) before successfully running one experiment with a specific group. But I think somehow they ‗perceived‘ when I was about to give up and then collaborated with me to complete my trials. I thank them for showing me a bit of their world! Back home, I would like to thank my family and a few friends in Portuguese. Muito obrigada a todos aqueles que me apoiaram e compreenderam minha ausência durante todos estes anos. Obrigada novamente ao Bel pelo companheirismo e apoio incondicional em todos os momentos –‗you are everything to me‘! Obrigada a meus pais, Diva e José, e meus irmãos, Anderson, Eduardo e Juliana por toda a torcida e apoio e por sempre tentarem me estimular a continuar – Amo vocês! Obrigada a Tia Beré, Daniela, Aline e Lilian pelo carinho e atenção durante nossa estadia com vocês, e Lilian também pela ajuda com mapas e arquivos com problema! Tia Candita e todos familiares pela torcida. Minhas queridas amigas Teresa, Juliana, Patricia, Cecilia, Fabiane e Leticia pela torcida e incentivo. v Abstract Titi monkeys have long been known for their complex vocal behaviour with numerous high- and low-pitched calls, which can be uttered singly or combined in more complex structures. However, up to date very little is known concerning the function, meaning and context-specific use of these vocal utterances, and virtually nothing is known about their vocalisations in the predation context. This thesis presents a detailed description of the form and function of the anti-predator behaviour of one species of titi monkeys, the black-fronted titi monkey (Callicebus nigrifrons), with a specific focus on their alarm call behaviour.
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