Active Touch Sensing in Pinnipeds Department of Natural Sciences Manchester Metropolitan University A thesis submitted in partial fulfilment of the requirements of Manchester Metropolitan University for the degree of Doctor of Philosophy Alyxandra Olivia Milne 2019 1 Alyx Milne Active Touch Sensing in Pinnipeds Abstract Active touch sensing in humans is characterised by making purposive movements with their fingertips. These movements are task-specific to maximise the relevant information gathered from an object. In whisker-touch sensing, previous research has suggested that whisker movements are purposive, but no one has ever examined task-specific whisker movements in any animal. Pinnipeds are whisker specialists, with long, mobile, sensitive whiskers and diverse whisker morphologies. The aim of this PhD is to investigate active touch sensing in Pinnipeds (seals, sea lions and walrus), by: i) describing whisker morphology; ii) comparing and quantifying whisker movements; and iii) characterising task-dependency of whisker movements during texture, size and luminance discrimination tasks. Pinnipeds with long, numerous whiskers, such as California sea lions (Zalophus californianus) and Stellar sea lions (Eumetopias jubatus) have larger infraorbital foramen (IOF) sizes and therefore, more sensitive whiskers. The IOF being a small hole in the skull, allowing the infraorbital nerve (ION) to pass through, which supplies sensation to the whiskers. Comparing whisker movements in Harbor seals (Phoca vitulina), California sea lions and Pacific walrus (Odobenidae rosmarus), showed these species all protracted their whiskers forwards and oriented their head towards a moving fish stimulus. However, California sea lions moved their whiskers more than the other species, and independently of the head. Due to the movement capabilities and sensitivity of whiskers in California sea lions, this species was used to investigate whether whiskers can be moved in a task-specific way. Results suggested that California sea lions make task-specific movements, by feeling around the edge of different-sized shapes, and focussing and spreading their whiskers on the centre of different-textured shapes. 2 Alyx Milne Active Touch Sensing in Pinnipeds Therefore, California sea lion whiskers are controlled like a true active touch sensory system, similar to human fingertips. I suggest that active touch sensing is likely to efficiently guide foraging and prey capture in dark, murky waters in these animals. Moreover, the complexity of California sea lion whisker movements and their subsequent behaviours makes them a good candidate from which to further investigate animal decision-making, perception and cognition. 3 Alyx Milne Active Touch Sensing in Pinnipeds Acknowledgements I would like to thank everyone who has encouraged and inspired me throughout my PhD. Firstly to Dr. Robyn Grant who saw some potential in a student with a passion to further her knowledge in Pinnipeds. Without this opportunity, I may not have embarked on such an exciting adventure. You have been not just a reliable supervisor, but also an honest, supportive friend. I have enjoyed every one of our journeys seeking out the next whiskered companion! My supervisory team including Matthew Sullivan and Llwyd Orton for their expertise, making sure I was headed in the right direction and to Manchester Metropolitan University for their financial support and PhD studentship. I would also like to thank undergraduate Catherine Smith for her help with whisker tracking during the fish sweeping task and Haydn Insley for designing and supporting us in making the fish model. Secondly, Blackpool Zoo, who without the zoo director Darren Webster supporting this PhD would not be possible. My fellow animal trainers: Alexandra Kidd when I first started my whisker trail; Gary Jones for his constant DIY skills and training expertise always there with another “behaviour” up his sleeve; and finally Charlie Black getting me through the final stages of my PhD; designing, making and re-making the blindfold over and over again! The PR and Marketing Department for constantly putting my ideas out to numerous TV programmes and radio stations, your media space for my videos and always making sure the cameras were ready for action. In addition, both SeaQuarium, Rhyl, UK and Dolfinarium Harderwijk, Germany for access to their Pinnipeds and the following museums Liverpool World Museum (Liverpool, UK), Manchester Museum: The 4 Alyx Milne Active Touch Sensing in Pinnipeds University of Manchester (Manchester, UK) and the National Museums of Scotland (Edinburgh, UK) for access to their specimens. Finally, I would like to thank my Mum, who has always patiently encouraged me to be whatever I want to be and tirelessly worked hard to support me, “Go confidently in the direction of your dreams…Live the life you imagined”. My sister Hannah, who always there for me when times get hard. Last but not least the three boys in my life. Firstly Billy the most, supportive person I have ever met, I cannot express how much I appreciate everything you did to help me through the highs and lows! Our Rhodesian Ridgeback who tried every trick in the book to get me to play rope by slamming it onto my laptop when I tried to study. Thirdly, the newest addition to the family, William, our son who has changed my life completely and will soon be joined by our second little one. I want to be the best for you to show you no matter what your dreams our, you can achieve them little ones just as your mum did! Finally, this thesis is dedicated to my Grandpa, Arthur Dunkerley, who passed away just one month after I began this part of my adventure. Without you and Gran, I would have never started on my “Dancing with Dolphins” career. I love you, I miss you and I will never stop trying to make you proud. Thank you for everything… 5 Alyx Milne Active Touch Sensing in Pinnipeds Contents Abstract Acknowledgements Contents 1 Chapter One: Introduction and Overview ....................... 9 1.1 Why study whiskers? ......................................................................................... 10 1.2 Active touch sensing systems ............................................................................ 12 1.3 Why study Pinniped vibrissae? .......................................................................... 17 1.4 Whisker movements .......................................................................................... 19 1.5 Conclusions ........................................................................................................ 22 1.6 Content of thesis: aims and objectives .............................................................. 23 2 Chapter Two: Literature Review ................................... 26 2.1 Aquatic mammals and the evolution of Pinnipeds ........................................... 27 2.2 Pinniped distribution and diet ........................................................................... 31 2.3 Feeding strategies and behaviour in Pinnipeds ................................................. 36 2.4 Sensory adaptations of Pinnipeds and aquatic mammals ................................ 41 2.5 Pinniped whisker anatomy and morphology ..................................................... 77 2.6 Conclusion .......................................................................................................... 82 3 Chapter Three: Pinniped Whisker & Skull Morphology... 83 3.1 Introduction ....................................................................................................... 84 3.2 Methods ............................................................................................................. 86 3.3 Results ............................................................................................................... 92 3.4 Discussion ........................................................................................................ 102 3.5 Conclusion ........................................................................................................ 107 6 Alyx Milne Active Touch Sensing in Pinnipeds 4 Chapter Four: Quantifying Whisker Movements in Pinnipeds ......................................................................... 108 4.1 Introduction ..................................................................................................... 109 4.2 Methods: Pinniped whisker control videos ...................................................... 110 4.3 Results ............................................................................................................. 116 4.4 Discussion ........................................................................................................ 122 4.5 Conclusion ........................................................................................................ 127 5 Chapter Five: Sea lion Training Programme ................ 128 5.1 Introduction ..................................................................................................... 129 5.2 Making the fish model ..................................................................................... 130 5.3 Building and designing the fish rig .................................................................. 133 5.4 Cameras ........................................................................................................... 135 5.5 Training areas .................................................................................................. 136 5.6 The Sea Lions