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Vibratory Communication in the Black Widow Spider, Latrodectus Hesperus (Araneae: Theridiidae)

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Vibratory Communication in the Black Widow Spider, Latrodectus Hesperus (Araneae: Theridiidae) Vibratory Communication in the Black Widow Spider, Latrodectus hesperus (Araneae: Theridiidae) by Senthurran Sivalinghem A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Senthurran Sivalinghem 2020 Vibratory Communication in the Black Widow Spider, Latrodectus hesperus (Araneae: Theridiidae) Senthurran Sivalinghem Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto 2020 Abstract Several studies have described vibration producing behaviours across many web-building spiders, and vibratory communication is thought to play an integral role during male-female interactions. Despite the presumed ubiquity of vibratory communication in this group of spiders, very little is known about the characteristics and functions of the signals involved, how signals are produced and transmitted through webs, or how vibrations are perceived. In this thesis, I used the western black widow spider, Latrodectus hesperus, as my focal organism, to investigate the details of vibratory communication from sender to the receiver. My results show that male L. hesperus courtship vibration signals comprise three distinct components (abdominal tremulation, bounce and web plucks), each produced using different signal production mechanism. Larger males produced bounce and web pluck signals with high power, which suggests that these signals may carry information about male traits. I found that during the early phase of courtship, males produced these different signal components haphazardly, with little temporal organization among the individual components (unstructured signaling). However, during the later phase of courtship, as males approach females, males intermittently organized signal components into a stereotyped temporal sequence (structured signaling). I tested the importance of these composite multicomponent signals, and found that males that displayed these structured signals more often ii were more likely to successfully copulate and copulate sooner. Vibrations arriving at the females are transmitted through the legs. My results show that the more distal joints of the legs (i.e. tarsus-metatarsus joint) move more to higher frequencies, and more proximal joints are tuned to lower frequencies. This suggests that female leg-joints play an important role in segregating vibration frequencies, and this may have important implications for prey/mate discrimination, as well as vibration source localization. These results show that L. hesperus males employ multiple signal components during courtship, and provide novel insights into emergent signal complexities in a web-building spider, previously thought to be ‘simple’ signalers. Additionally, the spider body mechanics can play a key role in influence vibration perception. iii En Kudumbathirkaaha & In Memory Of Thaveswaran Kandavanam (Thavam Sithappa) iv Acknowledgments This thesis would not have been possible without the support and input from numerous people. First, and foremost, I am forever grateful to my mentor Andrew Mason for introducing me to research in invertebrate sounds and vibrations, and in particular vibratory communication in spiders. It felt like kismet. I thank Andrew for being a supportive advisor and an inspiring mentor to me during my scientific and personal development. His endless support and guidance gave me the confidence I needed to explore my own research interests independently and complete research projects. It is not possible for me to put in words how much I value Andrew’s mentorship, and what it has meant to me. Andrew was always available to hear my doubts and questions and provide input and feedback to help me find clarity, both in life and research. It was an honour and a privilege to be his student. I am also thankful to my thesis committee members, Maydianne Andrade and Ken Welch, for their insights, guidance, and perspectives on my research projects, and for giving me feedback, comments and suggestions on my manuscripts. I thank Maydianne for allowing me to use her lab resources, when needed, to keep my spider populations alive and to conduct mating experiments. Maydianne has also provided me numerous opportunities to communicate my science to elementary school children and to the public, to help me grow as a science educator and communicator. As a dazed and confused freshman many years ago, not knowing what I wanted to do, meeting Maydianne was one of the most significant moments in my life. I am always inspired by her intelligence, integrity, and passion and enthusiasm for science. My PhD experience was greatly enhanced by all my colleagues and peers in the Mason lab. I thank my current lab-mates Terrence Chang and Andrew Masson (AJ) for the many interesting and thoughtful conversations, which were much needed from time to time. Working with Natasha Mhatre was truly an amazing learning experience, which helped me grow as a researcher. Natasha was always generous with her time and provided great support in training me on the scanning laser vibrometer and explaining many concepts related to biomechanics. I am also grateful for the support and genuine sense of bonhomie I received from Norman Lee, Dean Koucoulas, and Jenn van Eindhoven during my early years. My research would also not be possible without the tireless help of many undergraduate research assistants and work-study students who fed my spiders and helped with experiments. v Outside of the Mason lab, I was also fortunate enough to have received support and friendship from colleagues in the Andrade lab, as well as the department of biological sciences at UTSC: Emily MacLeod, Luciana Baruffaldi, Sheena Fry, Allan Edelsparre, Anders Vesterberg, Charmaine Condy, Monica Mowery, Malcolm Rosenthal, Catherine Scott, and Nishant Singh. I’m especially grateful for Emily, Luciana, and Sheena, who were always willing to spare me black widow males and females. My research would not have been possible without the initial population of black widows I inherited from them. I would also like to thank Damian Elias at UC Berkley for providing comments and suggestions on my manuscripts. Damian’s research on jumping spiders and his writing style has been a source of influence and inspiration to me, and has guided me on many aspects of the research conducted in my dissertation. I am very blessed to have continuous, never-ending love and support from my family and friends. They never stopped believing in me, and have always encouraged me to keep moving forward. I owe them a debt of gratitude for always being there for me. I would like to thank my father and mother, Sivalinghem and Selvakumary, who have always given me everything they can. I would not be where I am today without their love and effort. I thank Priya and Mayurran for their love and admiration, and for giving me strength and courage when needed. My family has grown since I started my PhD, and the love and encouragement I have received from my wife Vinusha, and my in-laws have given me additional motivation to keep moving forward. Vinusha has selflessly supported me throughout my writing process and has helped me stay focused and ambitious. I hope I keep making you all proud. Lastly, I would like to acknowledge the financial support provided by graduate fellowships from the University of Toronto, Natural Science and Engineering Research Council (NSERC) of Canada, and the Ontario Graduate Scholarship; as well as support provided to my advisor Andrew Mason: NSERC Discovery Grant. vi Table of Contents Contents Abstract ........................................................................................................................................... ii Acknowledgments............................................................................................................................v Table of Contents .......................................................................................................................... vii List of Tables ................................................................................................................................. ix List of Figures ..................................................................................................................................x Chapter 1 Vibratory Communication in Spiders: An Integrative Approach to Understanding Signal Complexity .......................................................... 1 1.1 Introduction ...............................................................................................................1 1.1.1 Vibratory Communication in Spiders ............................................................3 1.1.2 Vibratory Communication in Web-Building Spiders ..................................10 1.2 Western Black Widow Spider (Latrodectus hesperus) .........................................12 1.2.1 General Natural History and Mating Behaviour ..........................................12 1.2.2 Vibration Signals of L. hesperus ..................................................................22 1.3 Thesis Outline ..........................................................................................................24 1.4 References ................................................................................................................26 Chapter 2 Vibratory Communication in a Black Widow Spider (Latrodectus hesperus): Signal Structure and Signaling Mechanisms....................... 40 2.1
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