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Behavioral Responses to Mechano-Sensory Information in A BEHAVIORAL RESPONSES TO MECHANO-SENSORY INFORMATION IN A SOFT-BODIED TERRESTRIAL ANIMAL A dissertation submitted by Linnea Ingeborg Natasja Nathalie van Griethuijsen In partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology TUFTS UNIVERSITY May 2012 © 2012 Linnea I.N.N van Griethuijsen Advisor: Dr. Barry A. Trimmer Certificate of fitness II Abstract Caterpillars are the larval stage of Lepidoptera, which consists of butterflies and moths. Caterpillars were often seen as hydrostats, but recently researchers have realized that caterpillars do not function as such. Reasons are their body plan, lack of a fixed volume and the use of their substrate to transmit forces. These new insights have changed how we think about movement in caterpillars and are discussed in the first chapter of this dissertation, which aims to give an overview of the current state of knowledge on caterpillar locomotion. Chapter two discusses climbing. The movements of the caterpillar when climbing and during horizontal locomotion are indistinguishable. The similarities can be explained by 1) the caterpillar’s strong grip to the substrate, which it uses regardless of orientation, 2) the fact that it is a relatively small animal and smaller animals tend to be less influenced by gravity due to their high locomotion costs and 3) the caterpillar’s slow movement. Chapter three also looks at locomotion, but focuses on the use of sensory information to alter the normal stepping pattern. When stepping on a small obstacle, information used to adjust the movement of the leg originates from body segments anterior to that leg. In addition, information collected by the sensory hairs on the proleg is used to fine-tune the movement mid swing. Chapter four focuses on the response of the caterpillar to noxious stimuli. In this defense behavior the caterpillar rapidly moves its mandibles toward the stimulation site. The accuracy with which the caterpillar does this, is lower when responding to stimuli applied to dorsal and anterior locations on the abdomen. An explanation can be found in the caterpillar’s limited ability to move its body into a tight curve and the lack of circular muscles. III Chapter five summarizes the findings and discusses them in the light of the recent discovery of the movement of the gut during locomotion. The paper discussing this discovery can be found in the appendix as well as a short description of the change in morphology when developing from a hatchling into a fifth instar caterpillar. IV Acknowledgments The research described in this dissertation would not have been possible without the help and support of many people. I am very grateful to Dr. Barry Trimmer for giving me the opportunity to work in his lab. I was given a lot of freedom in choosing my own topics and designing my own experiments and this really helped me in becoming an independent scientist. What I am most grateful for is that Barry introduced me to the field of Neuroethology. I was already interested in questions regarding locomotion and neurobiology and I knew I Iiked questions that eventually tie back to ecology and evolution, but to find out that there is actually an entire field that focuses on these types of questions, just felt like coming home. With Barry’s support I got the chance to go to several meetings and hear about research not directly related to caterpillars. The yearly trips to East Coast Nerve Net were always fun as were the meetings of the Society of Integrative and Comparative Biology. Scientifically, I was most impressed with the talks at Adaptive Motions of Animals and Machines in 2008 and at the International Congress of Neuroethology in Salamanca in 2010. I spend most of my in the Trimmer lab at Dana with William Woods and Michael Simon. Woody’s enthusiasm for research is inspiring and I am grateful for the suggestions and feedback he has given me over the years. Mike was truly my buddy in the lab, working with him was great. I have fond memories of the Argonne adventure and the excitement around publishing the synchrotron results, and I feel honored that Michael gave the opportunity to be part of that research. I entered the Trimmer lab at the same time as Huai-Ti Lin. Although we worked in different buildings on (seemingly) very different topics, I got to know Huai-Ti well. Several of his findings have been instrumental in interpreting my own data and have enriched my research, for which I am grateful. My time at the Trimmer lab would not have been the same without the companionship and support of Meghan Kate, Cinzia Metallo, Frank Saunders, Michael Doire, John Rieffel, Ethan Golden, Amanda Baryshyan, Emily Pitcairn and Fallon Schuler. Many undergraduates did research in the Trimmer lab and there are a few I would like to mention by name as they directly contributed to my research: Faith Hester, Songjun Li and Kelly Banks. V My committee, Dr. Barry Trimmer, Dr. Michael Romero, Dr. David Cochrane, Dr. Harry Bernheim and Dr. Jason Rife offered valuable feedback and perspectives at our biyearly meetings. I particularly would like to thank Michael Romero, for the great time I had rotating in his lab in the fall of 2006, for his career advice and for being my nr 2 go-to person for recommendation letters. I would also like to express my gratitude to Dr. Stacey Combes from Harvard University for being my outside committee member. One of the goals I had for graduate school was to learn more statistics. Sara Lewis’ excellent Biostatistics course and the Advanced Statistics Seminar helped me reach that goal. As the designs of my experiments got quite complex, I was fortunate to get great help from Michael Reed and Durwood Marshall. The Biology Department at Tufts is a great place and it’s the people that make it great. I would like to thank the faculty, staff, students and postdocs for making this such a supportive environment. Michael Grossi, Eileen Magnant, Liz Palmer, Karin Murphy and Tony Keevan have been such a great help with the logistics of teaching, travel and organizing invited speaker events. Tufts Graduate School of Arts and Sciences has co-sponsored several of my trips to conferences. I am grateful for these contributions. Some of my best memories of my time at Tufts are those of the birding trips to (mostly) Plum Island, with Michael Reed, David Desrochers, Nicole Cyr, Brian Tavernia, Sasha Keyel, Christine Lattin, Jenn Mortensen, Carolyn Bauer and Chuong Le. The group changed over the years and this list is probably not complete, but birding was always a great excuse to get out of the city and I even learned to recognize some species! In the last year of my graduate career, the Trimmer lab moved from Dana Laboratories to 200 Boston Avenue. Until then I had a desk in Barnum 110 and over the years I shared my office with a group of great people: Colleen Butler, Sasha Keyel, Jocelyn Mueller, Natasha Tigreros, Dan Kane and Adam South. I want to thank Jocelyn for our many conversations on cultural differences, Natasha for dragging me to the gym and sharing the tasks of the grad student invited speaker committee with me and Dan for his humor and support. I would like to thank the Boston Chapter of the Graduate Women in Science (GWIS). After winning their travel grant in 2008 I actively joined this group. Their meetings, book discussions and outreach activities have enriched my experience as a graduate student. VI I would like to thank ‘the Ladies’, a group of dear friends from my biology studies at Wageningen University. Gabry, Tessa, Lieke, Annemarie, Margot and Jolanda, thank you for the many supportive emails, fun outings during my visits to the Netherlands and the superfun visit to Boston and New York! Many thanks too to my friends Linda Felen, Maartje Steegmans, and Katie and Eric Matzen for their support. I would like to thank my extended family: uncles, aunts and cousins and my fiancé’s parents, Luut and Jetty Zandbergen, for their continued interest in my scientific career. I am very grateful to my late father, Erik, for introducing me to the beauty of nature and the wonderful world of biology. I thank my mother Heleen for her continuing support during my seemingly endless educational endeavors, and for the many Skype calls and wise words. I thank my brother Ralf and his partner Leonard for their support and our many discussions about science and academia. I thank my brother Nils for reminding me that there is more to life than research. Lastly, I would like to thank my fiancé Fokko Zandbergen. Science brought us both to the Boston area, Fokko for a postdoc position at Harvard, and me for graduate school at Tufts. Having been through grad school himself, Fokko gave me perspective, understanding and encouragement. Our many talks about science, initially after work and later, when Fokko moved to Cape Cod for a second postdoc, via Skype and while preparing dinner in the weekends, were very helpful in keeping me going when experiments did not work. I can’t wait to see where we go next! VII Table of contents Certificate of fitness ................................................................... II Abstract ................................................................................... III Acknowledgments ....................................................................... V Table of contents ..................................................................... VIII Table of figures.......................................................................... X Chapter One – Locomotion in caterpillars .........................................
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