The Wisdom of the Acorn: Social Foraging in Temnothorax Ants by Zachary Shaffer A Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Approved April 2014 by the Graduate Supervisory Committee: Stephen Pratt, Chair Bert Hölldobler Marco Janssen Jennifer Fewell Juergen Liebig ARIZONA STATE UNIVERSITY May 2014 ABSTRACT The coordination of group behavior in the social insects is representative of a broader phenomenon in nature, emergent biological complexity. In such systems, it is believed that large- scale patterns result from the interaction of relatively simple subunits. This dissertation involved the study of one such system: the social foraging of the ant Temnothorax rugatulus. Physically tiny with small population sizes, these cavity-dwelling ants provide a good model system to explore the mechanisms and ultimate origins of collective behavior in insect societies. My studies showed that colonies robustly exploit sugar water. Given a choice between feeders unequal in quality, colonies allocate more foragers to the better feeder. If the feeders change in quality, colonies are able to reallocate their foragers to the new location of the better feeder. These qualities of flexibility and allocation could be explained by the nature of positive feedback (tandem run recruitment) that these ants use. By observing foraging colonies with paint-marked ants, I was able to determine the ‘rules’ that individuals follow: foragers recruit more and give up less when they find a better food source. By altering the nutritional condition of colonies, I found that these rules are flexible – attuned to the colony state. In starved colonies, individual ants are more likely to explore and recruit to food sources than in well-fed colonies. Similar to honeybees, Temmnothorax foragers appear to modulate their exploitation and recruitment behavior in response to environmental and social cues. Finally, I explored the influence of ecology (resource distribution) on the foraging success of colonies. Larger colonies showed increased consistency and a greater rate of harvest than smaller colonies, but this advantage was mediated by the distribution of resources. While patchy or rare food sources exaggerated the relative success of large colonies, regularly (or easily found) distributions leveled the playing field for smaller colonies. Social foraging in ant societies can best be understood when we view the colony as a single organism and the phenotype - group size, communication, and individual behavior - as integrated components of a homeostatic unit. i ACKNOWLEDGMENTS I am very grateful to my wonderful committee members – Stephen Pratt, Marco Janssen, Jennifer Fewell, Juergen Liebig, and Bert Hölldobler for their teaching, advice, and helpful criticism throughout my graduate education. In particular, I am grateful to my advisor, Stephen Pratt, who has been my intellectual ‘spirit guide’. Whatever crackpot or half-baked idea I mention to Stephen he always makes me feel valued with his respectful and thoughtful responses, and if there is any actual value in my suggestion he helps to me to ‘mine it’ - to unearth the scientific legitimacy hidden therein. In order to adequately sing Stephen’s praises, I would need another chapter, so in the interest of brevity I will simply say that I am grateful and proud to claim him as my mentor. I also thank my collaborators past, present, and future on projects that have been completed or are works in progress: Stephen Pratt, Takao Sasaki, Ted Pavlic, Aurelie Buffin, Jessie Ebie, Jennifer Fewell (co-advisor and teacher in my excursions into ant foundress research), Marco Janssen, Brian Haney, James Waters, Jon Harrison, CJ Klok, Andrew Quitmeyer, Tucker Balch, Gage Schaper, Clint Penick, Juergen Leibig, Rebecca Clark, Sara Dreyer, Yung Chang, Manfred Laubichler, Jacob Evans, Kevin Ngo, Tatsuya Kameda, Nick Poetsch, and any others I may have temporarily forgotten. Many other colleagues helped me tremendously along the way including: Adrian Smith, Dani Moore, Tate Holbrook, Josh Gibson, Kevin Haight, Bob Johnson, Adam Dolezal, Kelly Dolezal, Peter Marting, Yohan Cho, Nicola Plowes, Jon Jackson, Ioulia Bespalova, Kirsten Traynor, Athena Aktipis, Marty Anderies, Brigitte Hogan, Manuela Gonzalaz, Anna Dornhaus, Gro Amdam, Juergen Gadau, Rick Overson, Fernando Vonhoff, Arianne Cease, and John VandenBrooks. In particular, I want to thank Takao Sasaki – my friend and also teacher – who always makes me laugh. I am grateful to the excellent administrative staff of the graduate program (both faculty, managers, and supporting staff) for all of their help and support during my education: Wendi Simonson, Yvonne Delgado, Juergen Gadau, and Kenro Kusumi (when he filled in for Juergen), Elaine Finke, Juergen Liebig, Rob Page and Brian Smith. ii I thank my family and friends locally, especially the Parra family, Todd Miller and the Miller clan, and the Lindenberger/ Provost family. I am especially grateful to my parents, Pam and Warren, for their example as educated people and for their continued financial and emotional support. My parent’s financial generosity extended not only to me but also to many friends and family in my orbit, and made it possible for me to focus on my studies completely. I appreciate my talented sister Leah (Shaffer model 2.0), who even though she is 8 years younger, I consider to be the wise older sibling. I thank my kids, Ella and Phoenix (both of them smart young people – who I nonetheless managed to often dragoon into the tedious job of feeding ants). Finally, I thank my wife, Jaxinta. Thank you for listening about my scientific successes and failures and in either regard taking a walk with me and later on baking chocolate chip cookies. This research was supported by the National Science Foundation and ASU’s School of Life Sciences University Special Fellowship and doctoral completion RA. iii TABLE OF CONTENTS Page LIST OF TABLES ................................................................................................................................. vi LIST OF FIGURES .............................................................................................................................. vii CHAPTER 1 INTRODUCTION ................. .................................................................................................. 1 2 HOW ANTS ASSESS AND RESPOND TO FEEDER QUALITY .......................................... 6 Abstract ................................................................................................................ 6 Introduction .......................................................................................................... 6 Materials and Methods ...................................................................................... 10 Results ............................................................................................................... 13 Discussion ......................................................................................................... 15 3 THE INFLUENCE OF NUTRITIONAL STATE ON SOCIAL FORAGING ............................ 26 Abstract .............................................................................................................. 26 Introduction ........................................................................................................ 26 Materials and Methods ...................................................................................... 29 Results ............................................................................................................... 33 Discussion ......................................................................................................... 34 4 THE INFLUENCE OF RESOURCE DISTRIBUTION ON SOCIAL FORAGING ................. 51 Abstract .............................................................................................................. 51 Introduction ........................................................................................................ 51 Materials and Methods ...................................................................................... 54 Results ............................................................................................................... 57 Discussion ......................................................................................................... 62 5 CONCLUSION ................... ................................................................................................. 78 REFERENCES....... .......................................................................................................................... 82 iv APPENDIX……………………………………………………………………………………………………………89 A LINEAR RECRUITMENT LEADS TO ALLOCATION AND FLEXIBILITY IN FORAGING BY ANTS .............................................................................................................. 90 B NOTES ON THE NATURAL FORAGING HABITS OF TEMNOTHORAX ANTS ………99 v LIST OF TABLES Table Page 2.1 Colony-level behavior during collective choice .............................................................. 18 2.2 Individual behavior (receiver ants) ................................................................................. 19 2.3 Individual behavior (in relation to feeder quality) ............................................................ 20 vi LIST OF FIGURES Figure Page 2.1 Three hypotheses for mechanism of forager assessment (feeder quality) ........... 21 2.2 Collective