Sensory and Cognitive Constraints and Opportunities in Bats by Jeneni Thiagavel 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 Jeneni Thiagavel, 2019 i Sensory and Cognitive Constraints and Opportunities in Bats Doctor of Philosophy, 2019 Jeneni Thiagavel, Department of Ecology and Evolutionary Biology, University of Toronto Here I report on three comparative studies and one review chapter addressing the relationships between sensory reliance, neuroanatomy, skull morphology and body size, as they relate to diet and foraging in bats. In chapter two, I use morphological and echolocation data to test whether (i) mass-signal frequency allometry or (ii) emitter-limited (maximum gape) signal directionality better explain the negative relationship between size and peak frequency in bats. The results suggest that body mass and forearm length were important predictors of open space echolocation call peak frequency in ways that (i) reflect species- specific size differences, and (ii) suggest the influence of preferred foraging habitat. In chapter three, I test the predictions that the ancestral bat had (i) an auditory brain design capable of supporting early laryngeal echolocation, but (ii) eyes of insufficient absolute size to allow insect tracking at night. The results suggest that bats’ common ancestor had eyes too small to allow for successful aerial hawking of flying insects at night, but an auditory brain design sufficient to afford echolocation. Further, we find that those with less sophisticated biosonar have relatively larger eyes than do sophisticated echolocators. ii In chapter four, I continue to explore apparent trade-offs between echolocation call design and vision in predatory bats. I also explored the effects of foraging strategy, roost preference, and migration on the brains and eyes of predatory bats. I found that external roosters had large relative eyes, as did those with conserved calls which also had larger visual regions than those with more derived calls. The results also suggest that gleaners and sedentary bats have larger brains than aerial hawking and migrating bats, respectively. In chapter five, I provide an overview of sensory and cognitive ecology as they relate to foraging ecology and diet in the Phyllostomidae. These bats have a wide spectrum of feeding ecologies and sensory system specializations. Here, I use the Phyllostomidae to illustrate the influences that foraging ecology and diet selection have on the evolution of sensory systems and relative brain and brain region volumes. iii Acknowledgments First, thank you Dr. John Ratcliffe for being the best mentor I could have ever asked for. Thank you for sculpting me into the scientist I am today and for getting me this far. Your advice and guidance has not only helped me get a doctorate degree but also helped me lay out a path for my future. I can never thank you enough for putting your faith in me when you took me on and for having brought me this far today. I am forever grateful to you and I look forward to being friends for years to come. Thank you to my committee members, Drs. Helene Wagner and Glenn Morris. You have watched me grow from the first year of my Ph.D., fresh out of undergraduate studies, to the graduate I am today. Thank you both for your insightful comments and advice for each of my projects. Helene, thank you for being such a caring mentor who has taught me how to effectively balance the various aspects of my life. Glenn, thank you for all the laughs during our meetings and for showing me that science can be quite relaxing and enjoyable to do. Thank you to my father, Sivanandam Thiagavel, who has been the biggest pillar of strength for my education. I would never have been able to get my Ph.D. without you. Thank you for making my education your life’s number one priority. Thank you to my mother, Nantha Thiagavel, for being one of my best well-wishers and for helping me become the woman I am today. I am forever grateful to you both. iv Thank you to my very best friend and fiancée, Dusan Namasivayam. You are the best thing that has ever happened to me. Thank you for being my right hand and better half during both my undergraduate and doctorate studies. I wouldn’t be where I am today or who I am today, without you. Thank you Dr. Aarthi Ashok for being my inspiration and for your constant support and advice during both my undergraduate and graduate studies. Thank you to my co-author Dr. Sharlene Santana for helping me use phylogenetic comparative methods in R, which have now become the staple of the studies I do. Thank you to my sisters, Jenodini Thiagavel and Jerubika Thiagavel, for all the laughs and for being my personal cheerleaders in life. The support I have received from you girls is a huge reason for my success. Thank you Blessing Goddey-Erikefe, for always being there for me as my longest and closest girl friend. I appreciate everything you’ve done for me. Thank you to my dear lab-mates and friends Livia Loureiro, Heather Mayberry, Cylita Guy and A. Vikram Chochinov, for making this journey enjoyable for me. Thank you as well to my co-authors for their contributions to our papers. Study- specific acknowledgements to individuals and funding agencies can be found at the end of each chapter. My Ph. D. is dedicated to my father, Sivanandam Thiagavel. v Table of Contents Abstract ii Acknowledgements iv Table of Contents vi List of Tables vii List of Figures xi Chapter 1 Synopsis 1 Chapter 2 Body Size Predicts Echolocation Call Peak Frequency 19 Better than Gape Height in Vespertilionid Bats Chapter 3 Auditory Opportunity and Visual Constraint Enabled 44 the Evolution of Echolocation in Bats Chapter 4 Sensory and Cognitive Correlates of Life-history 120 Traits in Predatory Bats Chapter 5 Sensory and Cognitive Ecology of Phyllostomid Bats 159 Chapter 6 Concluding Remarks 212 vi List of Tables Chapter 2 Table 1. The fit of different evolutionary models (AICc values are shown). Supplementary Table S1. Size and call parameters for the vespertilionid species used in the study (N=86). Chapter 3 Supplementary Table 1. Post hoc comparisons of phylogenetically adjusted data (log transformed body mass, brain volume, eye mass, and brain regions) among foraging strategies (t-values and in parentheses, Holm-Bonferroni corrected p-values). Supplementary Table 2. Post hoc comparisons of phylogenetically adjusted data (mass residuals of brain volume, eye mass, and brain regions) among foraging strategies (t-values and in parentheses, Holm-Bonferroni corrected p-values). Supplementary Table 3. Post hoc comparisons of phylogenetically adjusted data (log transformed body mass, brain volume, eye mass, and brain regions) among echolocating call type (t-values and in parentheses, Holm-Bonferroni corrected p- values). vii Supplementary Table 4. Post hoc comparisons of phylogenetically adjusted data (mass residuals of total brain volume, eye mass, and brain regions) among echolocating call type (t-values and in parentheses, Holm-Bonferroni corrected p-values). Supplementary Table 5. Post hoc comparisons of phylogenetically adjusted data (log transformed body mass, brain volume, eye mass, and brain regions) among call type in predatory bats (t-values and in parentheses, Holm-Bonferroni corrected p-values). Supplementary Table 6. Post hoc comparisons of phylogenetically adjusted data (mass residuals of total brain volume, eye mass, and brain regions) among call type in predatory bats (t-values and in parentheses, Holm-Bonferroni corrected p-values). Supplementary Table 7. Specimen numbers for the skulls from Royal Ontario Museum (ROM) or Museum of Natural History in Denmark (MNHD). Supplementary Table 8. Species categorized as having either a functional (YES) or non-functional (NO) short-wave opsin (SWS) gene. Species from our dataset are shown in bold. Supplementary Table 9. Species, trait values, and categorizations by call type (MH: multiharmonic, CF: constant frequency, DH: Fundamental harmonic frequency modulated, NLE: non-laryngeal echolocator), diet (A: animal eating, P: phytophagous), echolocation ability (LE: laryngeal echolocator, NLE: nonlaryngeal echolocator) and roost type (I: roosts internally; E: roosts externally). viii Chapter 4 Table 1. Species, categorizations, trait values for predatory bats. Table 2. Post hoc comparisons of phylogenetically adjusted residuals of eye mass among call design and roost preference (t-values and in parentheses, Holm-Bonferroni corrected p-values). Table 3. Post hoc comparisons of phylogenetically adjusted residuals of hippocampus mass among migratory status and foraging strategy (t- and in parentheses, Holm- Bonferroni corrected p-values). Table 4. Post hoc comparisons of phylogenetically adjusted residuals of superior colliculus mass among migratory status and call design (t-values and in parentheses, Holm-Bonferroni corrected p-values). Table 5. Post hoc comparisons of phylogenetically adjusted residuals of neocortex mass among foraging strategy and call design (t-values and in parentheses, Holm- Bonferroni corrected p-values). Table 6. Post hoc comparisons of phylogenetically adjusted residuals of neocortex mass among migration status and call design (t-values and in parentheses, Holm- Bonferroni corrected p-values). Table 7. Post hoc comparisons of phylogenetically adjusted residuals of neocortex mass among migratory status and foraging strategy (t-values and in parentheses, Holm- Bonferroni corrected p-values). ix Table 8. Post hoc comparisons of phylogenetically adjusted residuals of brain mass among foraging strategy and call design (t-values and in parentheses, Holm-Bonferroni corrected p-values). Table 9. Post hoc comparisons of phylogenetically adjusted residuals of brain mass among migration status and call design (t-values and in parentheses, Holm-Bonferroni corrected p-values). Table 10. Post hoc comparisons of phylogenetically adjusted residuals of brain mass among migratory status and foraging strategy (t-values and in parentheses, Holm- Bonferroni corrected p-values).