Chloe Aline Raderschall
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Chloe Aline Raderschall BSc, Hons I A thesis submitted for the degree of Master of Philosophy The Australian National University December 2014 VVege entstellen dadurch^ dass man sie geht. Trail of leaf-cutter ants (Atta sp.) in Tambopata National Reserve, Peru I Declaration I herewith declare that the work presented in this thesis is, to the best of my knowledge, original except where other references are cited and was undertaken during my M.Phil candidature between October 2012 and December 2014 at the Research School of Biology, The Australian National University. The corrected version of the thesis was resubmitted in September 2015 with the suggestions of two anonymous examiners. The thesis has not been submitted in parts or in full for a degree to any other University. Chloe A. Raderschall, September 2015 III IV Acknowledgements The work towards this thesis would not have been possible without the guidance, support and friendship of a number of people. First and foremost I would like to thank my supervisors Ajay Narendra and Jochen Zeil for sharing their enthusiasm to understand insect navigation and for their guidance during all aspects of my research. Ajay especially I would like to thank for initially sparking my interest in myrmecology by introducing me to the fascinating world of ants during many photo excursions around Canberra. Being able to appreciate these little critters and to learn about each of their peculiarities is a wonderful gift that I hope to be able to share with many more people in the future. W illi Ribi I would like to thank for all his technical assistance and knowledge during my histological work. Working on nocturnal ants involved spending many nights out in chilly temperatures. This fieldwork would not have been as enjoyable without the wonderful help of my field assistants and collaborators. A big thank you to Rebecca Readhead, Fiorella Ramirez Esquivel and Ajay Narendra for their enthusiastic additional (cold) hands. Besides the help in the field, 1 am also very grateful to Trish Roan, who helped me digitise footage and thereby saved me many ours of clicking! The opportunity to attend the Sensory ecology course in Lund, Sweden, the Ant course in the Peruvian Amazon, a few conferences, and a visit to the Biozentrum at the University of Würzburg allowed me to meet a bunch of people who share my interest in insect navigation and/or nocturnal vision. In particular I would like to thank Wolfgang Rössler and Franziska Schmitt for many inspiring conversations and also Eric Warrant for his supporting letter towards receiving the Fleiligenberg travel award to attend the ICN conference in Sapporo, Japan. Last but not least I would like to thank a wonderful circle of friends. First of all I would like to thank Ali Livernois, who during my last weeks of writing, in particular, was an invaluable support towards getting this thesis completed. Thank you Ali for reading my drafts, cooking me dinner (including the best Canadian V pumpkin pie) and also providing mental support. I shared a house and a garden with a lovely and diverse bunch of housemates, whose company provided a great family-substitute and simply a warm home. I would like to thank Trish Roan for her enormous patience and being a true friend, Simon Thakur for his genuine interest in my work, Dale Garner for sharing all the lovely meals with me including questionable mushrooms from the garden and for reintroducing me to the taste of home grown lamb. Frances Jacomb I would like to thank for her all-time open ear and for being an amazing housemate, friend and work companion. And finally thank you Laura Kemp for introducing me to yoga up on the hill! A special thank you also to my friend Karina Bontes Forward, who with her endless enthusiasm to learn about new things and her talent to juggle a gazillion things at once, organised for me to start giving ant walks for the public. Thank you for believing in me and giving me the confidence to do this, I greatly enjoy it. May there be many more! And lastly a big thank you to my family for their unconditional support along my path through life with its crazy decisions. Finally, just for interest's sake, the thesis corrections were written in the following places across four continents: Zanzibar, Tanzania, where I received the examiners' comments; the floor of Doha airport, Qatar; the balconies of multiple houses in Switzerland; the ICE train through Germany; the floor of Darwin airport, Australia; Hancock library back in Canberra. Needless to say, it is great to be done! Myrmecia croslandi forager at the ANU campus fieldstation. VI Abstract The ability to navigate between places of importance is fundamental for all animals and during most situations of life, be it foraging on a daily basis or migrating seasonally from and to mating or feeding grounds. Central-place foragers, such as ants, have to visually navigate between their nest and food sources every day, sometimes covering 1000 times their body length through complex terrain. Ants are known to memorise visual scenes to allow them to repeatedly navigate along familiar routes. The robustness of visual information needed to achieve this is prone to degradation by both locomotion- induced blurring but also by environmental factors such as falling light levels. By studying nocturnal bull ants that forage over a wide range of ambient light intensities I was able to show that these ants stabilise their head to varying degrees against locomotion-induced body roll movements. Their ability to do so, however, decreased as ambient light levels fall, suggesting that visual information are important in mediating this response. I discuss the consequences imperfect head roll control is likely to have for visually guided navigation, in particular for panoramic scene comparisons in the ants’ natural habitat. Ants have occupied almost every environment on earth, from barren deserts to the dense understorey of rainforests and they are active during both day and night. As a result, the navigational cues ants have available in these different environmental- and temporal niches are radically different. This makes it possible to study the mechanisms underlying navigation in closely related species by comparing (1) the reliance on different navigational cues between ants from different niches, (2) how their sensory systems have adapted to perceive and capture the information they need and (3) how their brains process the information which ultimately drives behaviour. This combination of the disciplines of ethology, evolutionary biology and neuroscience is commonly referred to as neuroethology and aims at studying the mechanisms underlying animal behaviour in the context in which they have evolved. In a second part of my thesis I describe techniques in histology, neuroanatomy and behavioural ecology that I learned to address specific questions to better understand the underlying mechanisms of navigation in nocturnal ants. VII VIII Contents Chapter I: Introduction................................................................................................1 Visual ant navigation......................................................................................... 5 Insect vision and the nocturnal light environment......................................8 The Insect pupil mechanism .......................................................................... 13 Central brain processing of visual information.......................................... 15 Head stabilisation and gaze control............................................................. 17 Thesis outline....................................................................................................23 References......................................................................................................... 25 Chapter II: Research P ro ject................................................................................... 35 Introduction.......................................................................................................39 Material and M ethods......................................................................................41 Results................................................................................................................ 44 Discussion.......................................................................................................... 54 References......................................................................................................... 58 Chapter III: Research Techniques...........................................................................63 Histology and Microscopy...............................................................................65 Neuroanatomy...................................................................................................77 Ant tracking....................................................................................................... 95 References....................................................................................................... 107 Chapter IV: Conclusions and Outlook.................................................................. 109 Conclusions..................................................................................................... 113 O utlook............................................................................................................ 115 Appendices...............................................................................................................