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Chemical communication in the reproductive behaviour of Neotropical poison frogs (Dendrobatidae) Vom Fachbereich VI (Raum- und Umweltwissenschaften) der Universität Trier zur Verleihung des akademischen Grades Doktor der Naturwissenschaften (Dr. rer. nat.) genehmigte Dissertation Lisa Maria Schulte Betreuender: PD Dr. Stefan Lötters Berichterstattende: PD Dr. Stefan Lötters, Prof. Dr. Michael Veith, Dr. Werner Brack Datum der wissenschaftlichen Aussprache: 18.12.2013 Trier, 2013 I dedicate my thesis to my grandparents, Maria and Josef Schulte, Agnes and Hubert Koch, as well as my grandaunt, Martha Hörster. They had a profound impact on my interest in nature, travelling, and studying, and supported me with their love and pride. Table of contents Acknowledgements ……………………………………………………………….. 1 Preliminary remarks ……………………………………………………………….. 3 Introduction ……………………………………………………………………..… 5 Chapter I A danger foreseen is a danger avoided: how chemical cues of different tadpoles influence parental decisions of a Neotropical poison frog ………………………………………………………… 34 Chapter II The chemistry of parental care: the characterization of chemical communication between poison frogs and tadpoles ………………… 54 Chapter III Avoiding predation: the importance of chemical and visual cues in poison frog reproductive behaviour ………………………… 80 Chapter IV Do poison frogs recognize chemical cues of the other sex or do they react to cues of stressed conspecifics? …………………… 98 Chapter V The power of the seasons: rainfall triggers parental care in poison frogs ……………………………………………………………….. 110 Chapter VI Feeding or avoiding? Facultative egg-feeding in a Peruvian poison frog (Ranitomeya variabilis) ………………………………………… 131 Chapter VII The response of a Neotropical poison frog (Ranitomeya variabilis) to larval chemical cues is not influenced by kinship ……………… 147 Conclusions ……………………………………………….………………………… 157 Summary/Zusammenfassung ………………………………..…………………... …. 161 Curriculum Vitae …………………………………………………………………… 167 Erklärung ………………………………………………………………………… 169 Acknowledgements The realization of this thesis would not have been possible without the help and support of many people and institutions and I am deeply grateful to all of them! First of all I want to thank my supervisor Stefan Lötters (Trier University). When I made my first scientific steps, he encouraged me to pursue research and facilitated this decision by inviting me to carry out my doctorate in the Biogeography of Trier University. He not only helped me to develop and plan my dissertation project, he also helped me to get my dissertation funded and inspired me with fruitful discussions, suggestions and advice during the last couple of years. He further always gave me the freedom and supported me to develop and realize my own ideas. Thank you for always believing in me! Likewise I am deeply grateful to Michael Veith (Trier University). He not only warmly welcomed me to his team, he also agreed to supervise my thesis until Stefan Lötters achieved his postdoctoral lecture qualification. I am thankful for his valuable contributions towards developing this dissertation project that he enriched with his ideas, as well as for providing great support writing grant proposals for my thesis. I further want to extend my gratitude to Werner Brack (UFZ Leipzig) for his agreement to help me with the chemical aspects of my work, and his enthusiasm which was especially remarkable considering that his department usually has another scientific focus. I am equally grateful to his co-workers Martin Krauss and Tobias Schulze. Together these three developed the ideas and the concept for my chemical work, and Martin helped me afterwards with the analyses of my data. For help and support in the field in Peru I want to thank Michael Mayer (Trier University), Elena Rudolf (Trier University), Denise Ellwein and Evan Twomey (East Carolina University), as well as Ysolina Mendoza Pulce, Pedro Gamonal Centurion and their little daughter Nancy Gianina Gamonal Mendoza, who helped and entertained me in San Jose. I further want to thank Rainer Schulte and the Asociación de Productores de Ranas Venenosas, Progreso (ASPRAVEP) for enabling me to use their field station and Pascual Tafur Gonzales for the use of his forest. - 1 - Acknowledgements Special thanks go to Daniela Rössler (Trier University), who enthusiastically took care of the captive poison frogs and helped wherever possible. For help in the lab I would like to thank Katharina Filz (Trier University), assisting with the genotyping, as well as the technicians in Leipzig (especially Angela Sperreuter), who supported me during the chemical analyses. I further want to thank the Soil Science department Trier, especially Sören Thiele Bruhn, for kindly allowing me to use their facilities and Bernd Fontaine (Trier University) whose craftsmanship was multiple times a valuable help. For proofreading parts of the thesis I am thankful to Evan Twomey (East Carolina University), Tony Dunnell, Daniela Rössler, Daniela Matenaar (Trier University) and Andrew Holmes (University of Liverpool). Moreover I am grateful to Ortwin Elle (Trier University) for repeatedly helping me with statistical problems. I am indebted to the Studienstiftung des deutschen Volkes for funding me through their doctoral scholarship. Travel grants and conference fees were paid by the Forschungsfonds of Trier University and the Deutsche Forschungsgesellschaft (DFG). Furthermore I owe thanks to the Dirección General Forestal y de Fauna Silvestre (DGFFS), Peru for the permits of my field work and especially to Elisa Ruiz Ramos (DGFFS), Oscar Portocarrero Alcedo (DGFFS), Pablo J. Venegas (Centro de Ornitología y Biodiversidad, Peru, CORBIDI), Pedro G. Vásquez Ruesta (Universidad Nacional Agraria La Molina, UNALM), Kyle Summers (East Carolina University) and Sofía Rubio Chávez (Servicio Nacional de Áreas Naturales Protegidas, SERNANP) for their help obtaining those permits. I also would like to express my gratitude to all members of the Department of Biogeography of Trier University, not only for providing the research facilities, but especially for the friendly and vivid atmosphere (particularly during the very amusing coffee breaks). Special thanks go to my office mates Katharina Filz, Philine Werner, Kerstin Bidinger and Joscha Beninde. And last but not least I would like to thank all my friends in Germany and Peru for encouragement and distraction. I sincerely thank my parents Petra and Burkhard Schulte for their love and moral support as well as Evan Twomey who came in my life at the beginning of my doctorate and made this time (and especially my field seasons) so very special. Thank you! - 2 - Preliminary remarks This thesis was carried out at the Department of Biogeography, Faculty of Regional and Environmental Sciences, Trier University, in cooperation with the Department of Effect- Directed Analysis, Helmholtz Centre for Environmental Research (UFZ), Leipzig. Field work for the project was done under permission of the Dirección General Forestal y de Fauna Silvestre (DGFFS), Peru. Financial support was provided through a scholarship by the Studienstiftung des deutschen Volkes and field and lab work was funded by the Forschungsfonds of Trier University and the Deutsche Forschungsgemeinschaft (DFG). The work was performed under the supervision of PD Dr. Stefan Lötters and Prof. Dr. Michael Veith (both from Trier University), who were involved in all aspects of the thesis, i.e. planning of the studies, data analysis and writing of the manuscripts, and Dr. Werner Brack (UFZ Leipzig), who was substantially involved in the chemical aspects of the study. The thesis consists of a general introduction including a summarized overview about the scientific background and the aims of the thesis, a general conclusion as well as seven chapters written as scientific papers. Six of the latter are listed below as published or accepted for publication in peer-reviewed scientific journals or represented as unpublished manuscripts, one is published as a chapter of a peer-reviewed book. The authors and their specific contributions to the collection and analysis of data, along with the preparation of the manuscripts are represented in the following list, as well. Schulte, L.M. & Lötters, S. A danger foreseen is a danger avoided: how chemical cues of different tadpoles influence parental decisions of a Neotropical poison frog. Animal Cognition, doi 10.1007/s10071-013-0659-2 (online first) – published Concept and design of the experiments: LMS and SL Performance of the experiments: LMS Analysis of the data: LMS Writing of the paper: LMS and SL Schulte, L.M., Krauss, M., Lötters, S., Schulz, T. & Brack, W. The chemistry of parental care: the characterization of chemical communication between poison frogs and tadpoles – unpublished Concept and design of the experiments: LMS, WB, MK and TS Performance of the experiments: LMS Analysis of the data: LMS, MK and TS Writing of the paper: LMS and MS, with significant contributions of SL - 3 - Prelimimary remarks Schulte, L.M., Schulte, R. & Lötters, S. Avoiding predation: the importance of chemical and visual cues in poison frog reproductive behaviour. In Chemical Signals in Vertebrates 12, 309-321. East, M.L. & Dehnhard, M. (eds), Springer (2013). – published Concept and design of the experiments: LMS and LS Performance of the experiments: LMS Analysis of the data: LMS Writing of the paper: LMS and SL , with significant contributions of RS Schulte, L.M. & Rössler, D.C. Do poison frogs recognize chemical cues of
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