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Coversheet for Thesis in Sussex Research Online A University of Sussex DPhil thesis Available online via Sussex Research Online: http://sro.sussex.ac.uk/ This thesis is protected by copyright which belongs to the author. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the Author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the Author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Please visit Sussex Research Online for more information and further details I Organisation of Foraging in Ants Tomer Joseph Czaczkes Submitted for the degree of Doctor of Philosophy Submission data: September 2012 University of Sussex i Declaration I had a large role in the planning, data collection, and discussion of the results in chapter 4. The data analysis and writing of the manuscript was carried out by Dr. Christoph Grüter. I had a large role in the planning, data collection, and discussion of the results in chapter 9. The data analysis and writing of the manuscript was carried out by Dr. Christoph Grüter, and the agent based modelling was carried out by Dr Roger Schürch. The modelling in chapter 11 was carried out by Dr Pierre Nouvellet, and appendix E, which outlines the model, was mostly written by him. I certify that, with the above qualifications, the work carried out in this thesis is entirely my own, and that any help provided by other individuals with data collection and analysis is fully acknowledged. In addition, I certify that this thesis has not been, and will not be, submitted in whole or in part to another university for the award of any other degree. I hereby declare that this thesis has not beenm, and will not be, submitted in whole or in part to another University for the award of any other degree. Signature: Tomer Joseph Czaczkes ii UNIVERSITY OF SUSSEX TOMER JOSEPH CZACZKES, DOCTOR OF PHILOSOPHY ORGANISATION OF FORAGING IN ANTS Summary In social insects, foraging is often cooperative, and so requires considerable organisation. In most ants, organisation is a bottom-up process where decisions taken by individuals result in emergent colony level patterns. Individuals base their decisions on their internal state, their past experience, and their environment. By depositing trail pheromones, for example, ants can alter the environment, and thus affect the behaviour of their nestmates. The development of emergent patterns depends on both how individuals affect the environment, and how they react to changes in the environment. Chapters 4 – 9 investigate the role of trail pheromones and route memory in the ant Lasius niger. Route memories can form rapidly and be followed accurately, and when route memories and trail pheromones contradict each other, ants overwhelmingly follow route memories (chapter 4). Route memories and trail pheromones can also interact synergistically, allowing ants to forage faster without sacrificing accuracy (chapter 5). Home range markings also interact with other information sources to affect ant behaviour (chapter 6). Trail pheromones assist experienced ants when facing complex, difficult-to-learn routes (chapter 7). When facing complicated routes, ants deposit more pheromone to assist in navigation and learning (chapter 7). Deposition of trail pheromones is suppressed by ants leaving a marked path (chapter 5), strong pheromone trails (chapter 7) and trail crowding (chapter 8). Colony level ‘decisions’ can be driven by factors other than trail pheromones, such as overcrowding at a food source (chapter 9). Chapter 10 reviews the many roles of trail pheromones in ants. Chapters 11 – 14 focus on the organisation of cooperative food retrieval. Pheidole oxyops workers arrange themselves non-randomly around items to increase transport speeds (chapter 11). Groups of ants will rotate food items to reduce drag (chapter 12). Chapters 13 and 14 encompass the ecology of cooperative transport, and how it has shaped trail pheromone recruitment in P. oxyops and Paratrechina longicornis. Lastly, chapter 15 provide a comprehensive review of cooperative transport in ants and elsewhere. iii Publications arising from this thesis Grüter C, Czaczkes TJ, Ratnieks FLW. 2011. Decision making in ant foragers (Lasius niger) facing conflicting private and social information. Behav. Ecol. Sociobiol. 64:141–148. (Chapter 4) Czaczkes TJ, Nouvellet P, Ratnieks FLW. 2011. Cooperative food transport in the Neotropical ant, Pheidole oxyops. Insect. Soc. 58:153–161. (Chapter 11) Czaczkes TJ, Ratnieks FLW. 2011. Simple rules result in the adaptive turning of food items to reduce drag during cooperative food transport in the ant Pheidole oxyops. Insect. Soc. 58:91– 96. (Chapter 12) Czaczkes TJ, Grüter C, Jones SM, Ratnieks FLW. 2011. Synergy between social and private information increases foraging efficiency in ants. Biol. Lett. 7:521–524. (Chapter 5) Czaczkes TJ, Grüter C, Jones SM, Ratnieks FLW. 2012. Uncovering the complexity of ant foraging trails. Commun. Integr. Biol. 5:78–80. (Chapter 6) Czaczkes TJ, Ratnieks FLW. 2012. Pheromone trails in the Brazilian ant Pheidole oxyops: extreme properties and dual recruitment action. Behav. Ecol. Sociobiol. 66:1149–1156. (Chapter 13) Czaczkes TJ, Ratnieks FLW. 2013. Cooperative Transport in Ants (Hymenoptera: Formicidae) and elsewhere. Myrmecol. News. (Chapter 15) Grüter C, Schürch Roger, Czaczkes TJ, Taylor K, Durance T, Jones SM, Ratnieks FLW. In press. Negative feedback enables fast and flexible collective decision-making in ants. PLoS ONE. 6(9): e44501. DOI: 10.1371/journal.pone.0044501 (Chapter 9) Czaczkes TJ, Grüter C, Ratnieks FLW. Accepted. Ant Foraging on Complex Trails: Route Learning and the Role of Trail Pheromones in Lasius niger. J. Exp. Biol. DOI: 10.1242/jeb.076570 (Chapter 7) iv In the course of my doctoral research, I have contributed to studies led by my colleagues in the Laboratory of Apiculturea and Social Insects, which has resulted in co-authorship on the following paper, which was not included in the thesis: Jones, S., van Zweden, J., Grüter, C., Menezes, C., Alves, D., Nunes-Silva, P., Czaczkes, T.J., Imperatriz-Fonseca, V. & Ratnieks, F.L.W. 2012. The role of wax and resin in the nestmate recognition system of a stingless bee, Tetragonisca angustula. Behav. Ecol. Sociobiol., 66, 1–12 Chapters 8 and 14 are in the process of revision and resubmission. v Acknowledgements I have been helped over the course of my PhD studies by many, many people in many ways. Whilst I cannot mention all the people with whom I have had fruitful discussions and been helped in other ways, specific acknowledgements must go to the following people. Firstly I must thank my supervisor, Prof. Francis Ratnieks. Francis was an ideal supervisor for me: always full of ideas and curiosity, and possessing a real knack for picking up on interesting patterns. His door is always open, and he always provided fantastic feedback. Critically, he gave me free rein to explore my own ideas and trusted me to get on with my work. Many, many thanks to Dr Christoph Grüter. Christoph has provided guidance and advice in all aspects of my work, from experiment planning and data collection to statistics and writing. He has a wide and insightful view of behavioural ecology, and any manuscript he comments on is dramatically improved. He has been an absolute pleasure to work with. He whistles very well, but refused to sing during data collection. Many thanks to all the other members of LASI. In no particular order, thanks to Dr Margaret Couvillion for bringing joy and life to the lab - her help with writing grammar and style are also much appreciated! Thanks to Gianluigi Bigio for many interesting conversations, both scientific and not. Thanks to Fiona Riddell Pearce for many laughs and fun times. Thanks to Sam Jones for supporting myrmecology in LASI, and stoically putting up with my occasionally bossiness. Thanks to Dr Jelle van Zweden for demonstrating that one can combine fun with being a mature, successful scientist. Thanks to Dr. Jonathan Green, Rosie Foster, Lynne Robinson, Mike Clease and the entire JMS crew, for being wonderful and friendly, for many rounds of badders, and for being a link to the world outside LASI. Dr Greens’ thesis was both inspirational and highly intimidating during my own write-up. Thanks to Prof. Tom Collett for many constructive comments about my manuscripts. He asks fantastic questions, finds unnoticed patterns, and makes great suggestions to take the work to the next level. These suggestions usually involved a lot more work. Many thanks to Dr. Paulo Nogueira-Neto for allowing us to work and stay at Fazenta Aretuzina, and making us feel so welcome. A belated, but much deserved, thanks to Dr Terry Newsome, my A-level biology teacher, who was a great inspiration to me by expecting more than just answers to the questions in the textbook. I suspect I would not have studied biology further if it were not for him. vi Thanks to the BBSRC for funding me for four years (grant reference number BB / D526888/1). I can honestly say I couldn’t do it without them, or an equivalent funding body. Also thanks to the Northwest European section of the IUSSI, and ASAB, for funding my travels to various conferences. And lastly, I would like to thank Dr. Katja Rex, for encouraging me to persevere in the search for the ideal PhD position, for reading and improving every part of this thesis, for her unceasing love and
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