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Threat-Sensitive Learning and Generalization of Predator Recognition by Aquatic Vertebrates

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Threat-Sensitive Learning and Generalization of Predator Recognition by Aquatic Vertebrates THREAT-SENSITIVE LEARNING AND GENERALIZATION OF PREDATOR RECOGNITION BY AQUATIC VERTEBRATES A Thesis Submitted to the College of Graduate Studies and Research in Partial Fulfilment of the Requirements for the Degree of Doctor of Philosophy in the Department of Biology University of Saskatchewan Saskatoon By Maud Chloé Olivia Ferrari Winter 2009 © Copyright Maud Chloé Olivia Ferrari, 2009. All rights reserved. Permission to Use In presenting this thesis in partial fulfilment of the requirements for a Postgraduate degree from the University of Saskatchewan, I agree that the Libraries of this University may make it freely available for inspection. I further agree that permission for copying of this thesis in any manner, in whole or in part, for scholarly purposes may be granted by the professor or professors who supervised my thesis work or by the Head of the Department or the Dean of the College in which my thesis work was done. It is understood that due recognition shall be given to me and to the University of Saskatchewan in any scholarly use which may be made of any material in my thesis. Requests for permission to copy or to make other use of material in this thesis in whole or part should be addressed to: Head of the Department of Biology 112 Science Place, University of Saskatchewan Saskatoon, Saskatchewan S7N 5E2, Canada i Abstract Many prey species lack innate recognition of their potential predators. Hence, learning is required for them to recognize and respond to predation threats. When wild-caught, these same species may show amazing sophistication in their responses to predator cues. They are able to adjust the intensity of their antipredator responses to a particular predator according to the degree of threat posed by that predator. This ability is therefore acquired through learning. While many studies have shown that prey can learn to respond to predator cues through different learning modes, little is known about what the prey are actually learning. The results presented in this thesis show that learned predator recognition goes beyond the simple labelling of predators as dangerous. Using fathead minnows (Pimephales promelas), woodfrog (Rana sylvatica) tadpoles and boreal chorus frog (Pseudacris maculata) tadpoles, I demonstrated that a one time learning event, either through pairing with alarm cues or through social learning, was enough for prey to learn the level of threat associated with the novel predator cues. I showed that the level of danger associated with the predator cues was determined by the concentration of alarm cues when learning through pairing of alarm cues, or by the intensity of antipredator response displayed by the tutors and by the tutor-to-observer ratio when learning occurred through cultural transmission. Moreover, when subsequently exposed to predator cues, prey adjusted their antipredator responses according to the change in concentration of predator cues between the learning event and the subsequent exposure. Prey displayed stronger antipredator responses when exposed to higher concentrations of predator cues and vice versa. When minnows were provided with conflicting information about the danger level associated with a predator, they displayed a safety strategy and used the most recent information available to respond to predation threats. On a longer time scale, the data also suggest that woodfrog tadpoles are able to learn to respond to predation threats according to the risk posed by the predator at different times of day. Finally, I showed that prey learn to recognize particular characteristics of predators and can generalize their antipredator responses to novel species sharing those characteristics. However, generalization of predator recognition is dependent on the level of risk associated with the predator. Threat-sensitive learning is an extremely complex process shaped by the millions of years of selection imposed by predators on prey. ii Acknowledgements Je dédie cette thèse à mes parents, qui ont supporté tous les choix que j’ai faits au cours de ma vie, incluant celui de déménager au bout du monde pour faire peur à des petits poissons. I dedicate this thesis to my parents, who have supported all the choices I made throughout my life, including moving halfway across the world to scare little fishes. This five-year accomplishment would not have been possible without a number of people, starting with Dr. Grant Brown, who gave me the taste of science and research and convinced me, not without great difficulty, to move to the flat, empty and cold Prairies of Saskatchewan for a Master‟s degree. I would like to thank Dr. François Messier for his help, support and guidance as a supervisor, and for the influence he had on me as a teacher. François endowed me with a deep understanding of study design and biostatistics, which doubtlessly contributed to my success as a scientist. Merci d‟avoir accepté de prendre la relève en tant que superviseur, et m‟avoir donné les moyens et la liberté de recherche dont j‟avais besoin pour réussir. I thank my committee members, Drs. Grant Brown, Cedric Gillott, Jack Gray, Dick Neal and Joe Stookey, as well as my external examiner, Dr. Dan Blumstein, for their effort on my thesis work. A special thank you goes to Joe for his amazing enthusiasm for science and his infectious optimism in life, which inspired me for the past 3 years. I would like to thank Mike and Robyn Pollock for their advice, help and support during the past 5 years. Thanks to all my lab mates, who made this a fun experience. I would also like to thank Jean and Glen Chivers for letting me invade their home and wetlands for three field seasons of fun with the frogs and the mosquitoes. Finally, I would like to thank my family. Merci papa et maman pour m‟avoir fait confiance. Merci à tous les Olivier, spécialement ma mémé Dédé, pour leur support et encouragements au cours des années, sans oublier mon pépé Maurice, qui aurait été très fier de moi. Merci à la Minette Agen de Pouzillac, Filou et Titine pour m‟avoir enseigné quelques principes importants de la vie. Last but not least, thanks to Doug, for being the only person I know, who is as excited as I am about things eating other things. Thank you for your help, patience, guidance and support, for enabling me and for teaching me an important lesson about science: shit happens. Research funding for the work presented in this thesis was provided by the Natural Sciences and Engineering Research Council of Canada Discovery Grants to D.P. Chivers and F. Messier. Additional funding was provided by the 2005 R.J.F. Smith Memorial Research Grant Award. Personal funding was provided by the University of Saskatchewan, the Malcolm A. Ramsay Memorial Award and the NSERC Discovery Grant to François Messier. All the work reported herein followed UCACS protocols no. 19920077, 20050136, 20060014, 20070083. iii Table of Contents Permission to Use ............................................................................................................................ i Abstract ........................................................................................................................................... ii Acknowledgments.......................................................................................................................... iii Table of Contents ........................................................................................................................... iv List of Tables ................................................................................................................................. vi List of Figures ............................................................................................................................... vii Chapter 1: Introduction ................................................................................................................... 1 1.1. General information ............................................................................................................. 1 1.2. Threat-sensitive predator avoidance..................................................................................... 2 1.3. Learned predator recognition ............................................................................................... 3 1.4. Study systems ....................................................................................................................... 7 1.5. Research objectives .............................................................................................................. 9 1.6. Anticipated significance ..................................................................................................... 10 Chapter 2: The development of threat-sensitive predator avoidance through pairing of predator odour and alarm cues. ................................................................................................................... 12 2.1. Introduction ........................................................................................................................ 12 2.2. Methodology ...................................................................................................................... 14 2.2.1. Prey learn to match their response intensity to a novel threat according to alarm cue concentrations ........................................................................................................................ 16 2.2.2. Prey learn to match their response intensity to a novel threat according to predator
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