A Natural History of Bat Foraging : Evolution, Physiology, Ecology, Behavior, and Conservation 9780323918206

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A Natural History of Bat Foraging

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A Natural History of Bat Foraging Evolution, Physiology, Ecology, Behavior, and Conservation Edited by Danilo Russo Animal Ecology and Evolution Laboratory (AnEcoEvo), Dipartimento di Agraria, Universita` degli Studi di Napoli Federico II, Portici, Italy

Brock Fenton Department of Biology, University of Western Ontario, London, ON, Canada

Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1650, San Diego, CA 92101, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom Copyright © 2024 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein).

Notices

Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. ISBN: 978-0-323-91820-6 For information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Nikki Levy Acquisitions Editor: Simonetta Harrison Editorial Project Manager: Lindsay Lawrence Production Project Manager: Sajana Devasi P.K Cover Designer: Greg Harris Typeset by TNQ Technologies Cover: Miniopterus natalensis emerging from Gatkop Cave in Limpopo Province of South Africa. Photo by Sherri and Brock Fenton, All Rights Reserved.

Contents Contributors.......................................................................................... xiii Author biographies ............................................................................... xvii

CHAPTER 1 Introduction ............................................................ 1 Danilo Russo and Brock Fenton References.............................................................................. 5

CHAPTER 2 Foraging in the fossil record: Diet and behavior of the earliest bats.................................................. 7 Nancy B. Simmons and Matthew F. Jones Introduction............................................................................ 7 Dental morphology and diet ...................................................... 9 Ancient bat dentitions and hypothesized diets..............................14 Fossilized stomach contents......................................................17 Postcranial clues.....................................................................18 Evolution of echolocation ........................................................20 Vision and nocturnality............................................................22 Foraging strategies in ancient bats .............................................25 Ecological and faunal diversity in the Eocene..............................28 Acknowledgments...................................................................30 References.............................................................................30

CHAPTER 3 How the moth got its ears and other just-so stories in the history of batemoth interactions........41 Jesse R. Barber and John M. Ratcliffe How the moth got its ears ........................................................42 How the moth got its voice ......................................................44 How the bat got its whisper......................................................47 How the moth got its invisibility cloak .......................................49 How the moth got its tail .........................................................50 Conclusion ............................................................................51 Acknowledgments...................................................................52 References.............................................................................52

CHAPTER 4 Sensory systems used by echolocating bats foraging in natural settings ....................................57 Clarice Anna Diebold and Cynthia F. Moss Introduction...........................................................................57 Echolocation..........................................................................58

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Sonar call structure and duty cycle ........................................58 Nonlaryngeal echolocation ...................................................60 Sonar scene analysis............................................................61 Auditory signals and ecological niche ........................................62 Aerial hawking...................................................................63 Foraging over water ............................................................64 Gleaning for prey on substrates.............................................64 Passive listening to the sounds of prey ...................................65 Insectivores and prey counter strategies ..................................65 Other bat sensory systems and specializations..............................68 Vision...............................................................................68 Olfaction...........................................................................71 Thermoreception ................................................................72 Airflow sensing for flight control...........................................73 Conclusion ............................................................................74 References.............................................................................74

CHAPTER 5 Foraging strategies of echolocating bats.................83 Hans-Ulrich Schnitzler and Annette Denzinger Introduction...........................................................................83 Commuting behavior, search behavior, and social foraging ........83 Foraging habitats ................................................................84 Habitat types......................................................................84 Foraging modes..................................................................85 Constraints that shape the foraging strategies of bats ....................85 Echolocation......................................................................85 Flight morphology ..............................................................86 Foraging strategies of bats........................................................86 Aerial hawking foraging strategy...........................................87 Trawling foraging strategy....................................................91 The passive gleaning foraging strategy of animalivorous bats .....91 The active gleaning foraging strategy in animalivorous bats.......92 Passive/active gleaning foraging strategy of phytophagous bats ..................................................................................93 Flutter detecting foraging strategy .........................................93 Species using more than one strategy .....................................94 Search and commuting behavior of foraging bats .........................95 Search behavior and social foraging in bats feeding on predictable prey..................................................................95 Search behavior and social foraging in bats feeding on ephemeral prey...................................................................99

Contents

Commuting behavior in bats............................................... 100 Outlook............................................................................... 101 References........................................................................... 101

CHAPTER 6 Foraging, movements, and diet habits of arid-zone dwelling bats........................................ 109 Irene Conenna and Carmi Korine Introduction......................................................................... 109 Nightly movements........................................................... 110 Seasonal movements ......................................................... 111 Temporal activity.............................................................. 112 Diet habits....................................................................... 114 Conclusions ......................................................................... 115 References........................................................................... 115 Further reading..................................................................... 121

CHAPTER 7 Social foraging and information transfer ............... 123 Jenna E. Kohles and Dina K.N. Dechmann History of the study of social information use in bats.................. 123 The cons of social foraging .................................................... 131 Other types of social foraging in bats....................................... 132 Conclusions ......................................................................... 133 References........................................................................... 133

CHAPTER 8 Insect migrations and the ecology, behavior, and population dynamics of bats .......................... 139 Jennifer J. Krauel, Don R. Reynolds, John K. Westbrook and Gary F. McCracken Introduction......................................................................... 139 Introduction to insect migration............................................... 141 A. Insect migration increases the resource base for insectivorous bats ............................................................. 142 B. Insect migrants may be disproportionately important to bats’ diets .................................................................... 144 C. Biomass may be more important than diversity in bat diets .......................................................................... 145 D. Insect migrations and the ecosystem services of bats are intersecting areas of study............................................. 146 E. Insect migrations are predictable and linked to major life history features of bats ................................................. 147 F. Behavior of bats changes in response to insect migrations.... 148

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G. Response to insect migrations may influence impacts of climate change on bat populations ................................... 149 Conclusions......................................................................... 149 References........................................................................... 150

CHAPTER 9 Bats as prey ........................................................ 157 Peter Mikula, Radek K. Lucan, Juan J. Pello´n, Jose W. Valdez and Brock Fenton Introduction......................................................................... 157 Bat responses to predation...................................................... 160 Bat predation and nocturnality ................................................ 161 Predators of bats................................................................... 162 Birds .............................................................................. 162 Mammals ........................................................................ 163 Reptiles........................................................................... 164 Other vertebrates .............................................................. 165 Invertebrates .................................................................... 165 Conclusions and suggestions for further research ....................... 165 Dedication and/or acknowledgments .................................... 166 References........................................................................... 166

CHAPTER 10 Energetics of foraging bats................................. 173 Liam P. McGuire and Justin G. Boyles Energy budgets and metabolism .............................................. 173 Energy balance ¼ energy in  energy out............................. 173 Metabolic rate: Basal, resting, torpid, and flight ..................... 175 Energy required to get food.................................................... 177 Flight and the power curve................................................. 177 Optimal flight speed theory and implications for foraging strategies......................................................................... 180 Variation in wing loading................................................... 182 Energetic cost of terrestrial locomotion ................................ 183 Cost of echolocation ......................................................... 183 Energy in food ..................................................................... 184 Variation in diet composition .............................................. 184 Refractory content and implications for the energetics of different diets................................................................... 184 Rapidly accessing dietary energy......................................... 187 Spatial and temporal variation in the foodscape ......................... 188 Conclusion .......................................................................... 191 Acknowledgments................................................................. 192 References........................................................................... 192

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CHAPTER 11

Bat migration and foraging: Energy-demanding journeys on tight budgets ................................... 199

Christian C. Voigt, Shannon E. Currie and Liam P. McGuire Introduction......................................................................... 199 What species of bats migrate?................................................. 200 Resource fluctuations as a driver of migration............................ 202 The energetics of migratory flights .......................................... 203 Stopover behavior and torpor-assisted migration ........................ 204 Food for migration................................................................ 206 Flight corridors .................................................................... 208 Open research questions......................................................... 208 Acknowledgments................................................................. 209 References........................................................................... 209 Further reading..................................................................... 215

CHAPTER 12

Microbiomes of bats .......................................... 217 Melissa R. Ingala Gastrointestinal structure........................................................ 217 Interactions between the gut microbiota and immune development ........................................................................ 220 Host diet influences taxonomic composition of the microbiome.... 222 Interactions between microbiome functions and diet ................... 224 Beyond bacteria: the “other” bat microbiome ............................ 226 Conclusions ......................................................................... 227 References........................................................................... 227

CHAPTER 13

The diets of bats: Think outside the guild ........... 233 Elizabeth L. Clare and Phillip J. Oelbaum Collapse of the traditional guild .............................................. 234 Are insectivores a guild?........................................................ 234 Case study 1: Antrozous pallidus, the scorpion eating bat that pollinates cacti ..................................................................... 235 Are nectarivores a guild? ....................................................... 237 Case study 2: Glossophaga - the nectar bat that sneaks an insect snack ......................................................................... 240 Are frugivores a guild? .......................................................... 241 Caste study 3: Widely distributed pteropodids ........................... 242 Are carnivores a guild?.......................................................... 244 Case study 4: Trachops the “frog eating” bat............................. 245 Assemblage-wide assessment of diet in bats.............................. 247

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A world with more omnivores? ............................................... 251 References........................................................................... 252

CHAPTER 14 Bioaccumulation and foraging behavior .............. 261 Daniel J. Becker, Natalia I. Sandoval-Herrera, Molly C. Simonis and Cecilia A. Sa´nchez Introduction......................................................................... 261 Dietary exposure to contaminants ............................................ 262 Dietary exposure to parasites .................................................. 264 Interactions between foraging, contaminants, and parasitism ........ 269 Direct health effects .......................................................... 269 Indirect health effects ........................................................ 272 Future research directions ...................................................... 273 Acknowledgments................................................................. 277 Glossary.............................................................................. 277 References........................................................................... 277

CHAPTER 15 Foraging-dependent ecosystem services ............. 287 Rieka Yu and Nathan Muchhala Introduction......................................................................... 287 Arthropod suppression........................................................... 288 Pollination and seed dispersal ................................................. 292 Ecosystem disservices ........................................................... 295 Conservation recommendations............................................... 295 References........................................................................... 296

CHAPTER 16 Conserving bats and their foraging habitats ........ 305 Winifred F. Frick, Luz A. de Wit, Ana Ibarra, Kristen Lear and M. Teague O’Mara Introduction......................................................................... 305 Threats to bat foraging .......................................................... 308 Conservation evidence........................................................... 310 The benefits to human well-being of protecting where bats eat ..... 311 Conservation initiatives targeting bat foraging ........................... 314 Restoring and conserving healthy habitat for nectarivorous bats, agaves, and people..................................................... 314 Bat Conservation International’s Agave Restoration Initiative ......................................................................... 315 Gardening for bats ................................................................ 317 Conclusion .......................................................................... 317 References........................................................................... 318

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CHAPTER 17

Bat foraging: The next steps ............................... 327 Brock Fenton and Danilo Russo

Index...................................................................................................329

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Contributors Jesse R. Barber Department of Biological Sciences, Boise State University, Boise, ID, United States Daniel J. Becker Department of Biology, University of Oklahoma, Norman, OK, United States Justin G. Boyles School of Biological Sciences, Southern Illinois University, Carbondale, IL, United States Elizabeth L. Clare Department of Biology, York University, Toronto, ON, Canada Irene Conenna Global Change and Conservation, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland Shannon E. Currie Institute for Cell and Systems Biology, University of Hamburg, Hamburg, Germany Luz A. de Wit Bat Conservation International, Austin, TX, United States Dina K.N. Dechmann Department of Migration, Max Planck Institute of Animal Behavior, Radolfzell, Germany; Centre for the Advanced Study of Collective Behaviour, University of Konstanz, Konstanz, Germany; Department of Biology, University of Konstanz, Konstanz, Germany; Smithsonian Tropical Research Institute, Balboa, Anco´n, Panama Annette Denzinger Animal Physiology, Institute for Neurobiology, University of Tu¨bingen, Tu¨bingen, Germany Clarice Anna Diebold Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, United States Brock Fenton Department of Biology, University of Western Ontario, London, ON, Canada Winifred F. Frick Bat Conservation International, Austin, TX, United States; Ecology and Evolutionary Biology, University of Santa Cruz, Santa Cruz, CA, United States Ana Ibarra Bat Conservation International, Austin, TX, United States

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Melissa R. Ingala Fairleigh Dickinson University, Madison, NJ, United States Matthew F. Jones Biodiversity Knowledge Integration Center, School of Life Sciences, Arizona State University, Tempe, AZ, United States Jenna E. Kohles Department of Migration, Max Planck Institute of Animal Behavior, Radolfzell, Germany; Centre for the Advanced Study of Collective Behaviour, University of Konstanz, Konstanz, Germany; Department of Biology, University of Konstanz, Konstanz, Germany; Smithsonian Tropical Research Institute, Balboa, Anco´n, Panama Carmi Korine Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel Jennifer J. Krauel Department of Biology and Microbiology, South Dakota State University, Brookings, SD, United States; Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TX, United States Kristen Lear Bat Conservation International, Austin, TX, United States Radek K. Lu can Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic Gary F. McCracken Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TX, United States Liam P. McGuire Department of Biology, University of Waterloo, Waterloo, ON, Canada Peter Mikula Institute of Vertebrate Biology, Czech Academy of Sciences, Brno, Czech Republic Cynthia F. Moss Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, United States; The Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD, United States; Department of Mechanical Engineering, Whiting School of Engineering, Johns Hopkins University, Baltimore, MD, United States; Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, MD, United States

Contributors

Nathan Muchhala Department of Biology, University of Missouri e St. Louis, St. Louis, MO, United States Phillip J. Oelbaum Department of Cell and Systems Biology, University of Toronto, Toronto, ON, Canada M. Teague O’Mara Bat Conservation International, Austin, TX, United States; Southeastern Louisiana University, Hammond, LA, United States; Max Planck Institute of Animal Behavior, Radolfzell, Germany; Smithsonian Tropical Research Institute, Panama City, Panama Juan J. Pello´n Laboratorio de Ecologı´a y Conservacio´n de Vertebrados Terrestres, Instituto de Ecologı´a, Universidad Nacional Auto´noma de Me´xico, Mexico City, Mexico; Departamento de Mastozoologı´a, Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Peru John M. Ratcliffe Department of Biology, University of Toronto Mississauga, Mississauga, ON, Canada Don R. Reynolds Natural Resources Institute, University of Greenwich, Chatham, United Kingdom; Rothamsted Research, Harpenden, United Kingdom Danilo Russo Animal Ecology and Evolution Laboratory (AnEcoEvo), Dipartimento di Agraria, Universita` degli Studi di Napoli Federico II, Portici, Italy Cecilia A. Sa´nchez EcoHealth Alliance, New York, NY, United States Natalia I. Sandoval-Herrera Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada Hans-Ulrich Schnitzler Animal Physiology, Institute for Neurobiology, University of Tu¨bingen, Tu¨bingen, Germany Nancy B. Simmons Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History, New York, NY, United States Molly C. Simonis Department of Biology, University of Oklahoma, Norman, OK, United States

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Jose W. Valdez German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany Christian C. Voigt Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany John K. Westbrook Retired Rieka Yu Department of Biology, University of Missouri e St. Louis, St. Louis, MO, United States

Author biographies M.B. (Brock) Fenton received his PhD in 1969 for work in the ecology and behavior of bats. Since then, he has held academic positions at Carleton University, York University, and the University of Western Ontario. He has published over 250 papers in refereed journals (most about bats), as well as numerous nontechnical contributions. He has written four books about bats intended for a general audience. He continues his research on the ecology and behavior of bats, with special emphasis on echolocation and evolution. He was inducted as a Fellow of the Royal Society of Canada (FRSC) in November 2014. In November 2018, he began a 3-year term as a Deputy Executive Editor-in-Chief, Canadian Science Publishing. In February 2020, he began a 3-year term as a member of the Board of Directors of Bat Conservation International. Dr. Fenton is a professor emeritus from the University of Western Ontario, Department of Biology, Ontario, Canada and currently serves as an academic editor for PLoS Biology and Nature Scientific Reports. Prof. Danilo Russo is a full professor of Ecology at Naples University Federico II and an honorary professor at the University of Bristol, UK. He obtained his PhD in Zoology from the University of Bristol in 2002. Currently, he serves as the head of the Animal Ecology and Evolution Laboratory in the Department of Agriculture at his university. His research interests encompass a wide range of subjects, including habitat selection, resource partitioning, sensory ecology, social behaviour, evolutionary biology, biogeography, and invasion ecology. While much of his research focuses on bats, he also investigates various other model organisms to address specific questions of interest. From 2019 to 2023, Prof. Russo chaired the Scientific Committee of the UNEP/ EUROBATS Agreement, which is responsible for the conservation of European bat populations. Additionally, he takes great pride in his role as the editor-in-chief of the highly esteemed zoological journal, Mammal Review. Furthermore, he is the main proposer and chair of the Management Committee for the EU COST Action “CLIMBATS” (CA18107), a significant initiative exploring climate change’s effects on bat populations. Prof. Russo’s contributions to the scientific community are exemplified by his publication record, which includes approximately 170 scientific articles in internationally respected journals such as Nature Communications, Current Biology, Ecology Letters, and Biological Reviews. Having conducted fieldwork in diverse regions and environments across the globe, ranging from African rainforests to the Israeli desert and European beech woodlands, Prof. Russo possesses invaluable firsthand experience in various ecosystems.

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CHAPTER

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Introduction

Danilo Russo1, Brock Fenton2 1

Animal Ecology and Evolution Laboratory (AnEcoEvo), Dipartimento di Agraria, Universita` degli Studi di Napoli Federico II, Portici, Italy; 2Department of Biology, University of Western Ontario, London, ON, Canada

Foraging is the behavior exhibited by animals searching for and acquiring food in their environment. It encompasses activities and strategies used by animals to locate, obtain, and consume food, involving a range of behaviors such as searching, capturing, handling, and eating a food item. Foraging is a vital activity for animals as it directly influences their survival, reproduction, and overall fitness (Stephens et al., 2007). The specific foraging behaviors employed by animals can vary greatly depending on their species, ecological niche, available resources, and evolutionary adaptations. The study of animal foraging behavior helps us understand how animals adapt to their environment (Dehnhard et al., 2020), make optimal foraging decisions (Trapanese et al., 2019), and allocate their energy and time to optimize food intake and ultimately fitness (Latty and Trueblood, 2020). Analyzing foraging provides invaluable insights into how animals have adapted to their environment: it offers a precious way to link individual behavior to higher organizational levels such as population dynamics, interspecific interactions, energy fluxes, and ultimately, ecosystem structure and processes (Abrams, 1984; Petchey et al., 2008; Brose, 2010; Gil et al., 2018). This book is about foraging in bats, exploring this fascinating issue from different perspectives and scales and evaluating the influence of this crucial aspect of bat behavior not only on the ecology of these outstanding mammals but also on the status and future of our planet and our own lives. Bats (order Chiroptera) are a diverse group of mammals, numbering over 1460 species (Simmons and Cirranello, 2023) and, in mammals, are second only to rodents in terms of global species richness (Fig. 1.1). This overwhelming diversity is the result of a long evolutionary history that has led to an astonishing range of foraging strategies used by bats in almost every habitat worldwide to acquire food. Nocturnality (Rydell and Speakman, 1995) and active flight (Hedenstro¨m and Johansson, 2015) add further spatial and temporal perspectives to the natural history of bat foraging, making bats an especially interesting case within mammals from the ecological but also evolutionary viewpoint. To fully understand this present-day diversity in foraging strategies, it is therefore paramount to delve into the remote past, studying ancient bats to unveil the origins of diverse diets and foraging strategies in present-day species, as Simmons and Jones discuss in Chapter 2. A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.00017-6 Copyright © 2024 Elsevier Inc. All rights reserved.

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FIGURE 1.1 A compilation of close-up images showcasing the remarkable diversity of bat species. Arranged from top to bottom and left to right: Row 1 Nycteris thebaica; Rhinolophus simulator; Hipposideros speoris; Desmodus rotundus; Row 2 Molossus nigricans; Mormoops megalophylla; Diclidurus albus; Leptonycters yerbabuenae; Row 3 Lophostoma evotis (with ears up); Lophostoma evotis (ears down); Thyroptera tricolor; Noctilio leporinus; Row 4 Pteropus poliocephalus; Epomophorus walbergi; Uroderma bilobatum; Centurio senex.

Bat predation also exerts powerful selective pressure that has elicited astonishing antipredatory adaptations in certain prey species. In response to this evolutionary challenge, bats have developed an array of behavioral and physiological countermeasures. In Chapter 3, Barber and Ratcliffe illuminate the enthralling case of tympanate moths, which stands as one of the most captivating examples of the ongoing evolutionary arms race.

Introduction

In Chapter 4, Diebold and Moss explore how foraging bats use a diverse range of sensory cues to locate food sources in various environments. Bats have evolved sophisticated systems, which are crucial to collect the sensory information needed to find food, and these solve very different tasks depending on the bat’s dietary specialization, from insects, fruit, nectar and pollen to small vertebrates, and even blood. The bats’ long evolutionary history has led to today’s surprising range of foraging strategies bats use to feed on a broad range of food items: arthropods and plants but also vertebrates such as fishes, frogs, rodents, birds, rodents, and even other bats, not to mention the three bat species that feed on blood in the Neotropics. For many of these species, echolocation plays a pivotal role in the context of their foraging strategies. The use of echolocation and the various foraging strategies used by bats are comprehensively covered in Chapter 5 by Schnitzler and Denzinger. One captivating aspect of bat foraging ecology is their remarkable ability to acquire food in seemingly inhospitable habitats, such as deserts. These arid regions are home to a variety of fascinating bat species that exhibit astonishing strategies, such as scorpion hunting, which demands the bats to be resilient to the arthropod’s venom. In Chapter 6, Conenna and Korine delve into the spatial and temporal movements of bats in the desert while also exploring their dietary preferences and adaptations to survive in these challenging environments. A further characteristic that cannot be neglected is the highly gregarious nature of bats, often forming numerous colonies made of one or more species, and the diversity of bat social systems, whose dynamics are certainly complex and still poorly understood. The use of social information to increase foraging success and how it interacts with the distribution of trophic resources is, therefore, a fascinating field of study which we have just begun to explore and is presented in Chapter 7 by Kohles and Dechmann. The spatial challenges encountered by bats become particularly intriguing when they pursue migrant insect prey. Insect migration is a captivating and still inadequately comprehended phenomenon that holds significant relevance to the investigation of bat foraging behavior. The predation of bats on these insects carries substantial ecological implications and bears crucial consequences for ecosystem services, especially considering the role of certain migratory insect species as agricultural pests, as Krauel et al. highlight in Chapter 8. In Chapter 9, Mikula et al. cover the role of bats as prey in ecosystems, illustrating the diverse range of bat predators, touching upon the behavioral responses of bats to predation and the potential evolutionary consequences of predation on bat nocturnality. The chapter remarks on the need for further research on interactions between bats and their predators, identifying important topics for future studies. Chapter 10, by McGuire and Boyles, focuses on the energetic aspects of bat foraging, highlighting the significant impact flight has on their daily energy expenditure. The review delves into the energy costs involved in obtaining food and accessing energy from their diet while also considering the consequences of changes in food availability across diverse spatial and temporal conditions. By examining

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both energy costs and gains, McGuire and Boyles provide valuable insights into the foraging ecology of bats. In Chapter 11, Voigt et al. explore the captivating realm of migratory bats, which traverse vast distances seasonally, yet encounter significant metabolic challenges along their journey. The chapter endeavors to unravel the pivotal role of foraging in aiding these bats in their arduous task while highlighting the plethora of intriguing questions that continue to captivate the scientific community in relation to this aweinspiring subject matter. The study of microbiomes in animal physiology and ecology is of ever-growing importance, as it sheds light on the intricate interactions between animals and their associated microbial communities, influencing various aspects of their health, behavior, and ecological roles. In Chapter 12, Ingala illustrates gut microbiomes in bats and how these play crucial roles in bat physiology, ranging from nutrient acquisition to immunity. Given the diverse foraging strategies and diets exhibited by bats, from insectivory to herbivory, the composition and function of these gut communities show remarkable variation. Chapter 13 challenges the classical view of bat trophic guilds, revealing that exceptions previously overlooked are increasingly evident with advanced analytical methods. In this chapter, Clare and Oelbaum stress the importance of thorough dietary analysis and caution against under-reporting or overgeneralizing bat diets to safeguard their ecological significance. In Chapter 14, Becker et al. uncover the complex interactions between bat foraging, contaminants, and infection, shedding light on the impacts on bat health, zoonotic risk, and conservation practices and showing how diverse foraging strategies shape exposure to harmful substances and parasites. Yu and Muchhala, in Chapter 15, unveil the crucial ecological services rendered by bats as they consume insects, fruits, and nectar, which, in turn, contribute to pest regulation, pollination, and seed dispersion. Delving into the varied eating habits and foraging patterns of bats, the chapter explores their far-reaching ecological and economic implications but also highlights the existing knowledge gaps on the economic benefits derived from bat-dependent ecosystem services. Bat foraging exhibits a complex web of ecological interactions, encompassing predatoreprey dynamics and mutualistic relationships like plant pollination and seed dispersal. Human activities pose threats to bats by modifying or disturbing these interactions. Therefore, safeguarding and restoring bat habitats are essential for preserving bats and promoting a One Health Strategy that addresses wildlife health, ecosystem health, and human health interconnections. In Chapter 16, Frick et al. emphasize these aspects, along with the importance of establishing and maintaining robust foraging habitats that could potentially benefit local communities. The intricate world of bat foraging offers a captivating and multifaceted lens through which we can explore the diverse strategies and adaptations these remarkable mammals employ to survive in a variety of environments. From the evolutionary origins of their diets to the astounding antipredatory adaptations they have developed, from the sophisticated sensory systems guiding their nocturnal hunts

References

to the critical ecological roles they play, bat foraging behavior unveils a rich tapestry of interconnected relationships and dependencies. As we investigate more comprehensively the complex interplay between bats and their environments, we uncover invaluable insights into population dynamics, interspecific interactions, and the intricate balance of ecosystem structure and processes. We hope that this book successfully sheds light on the fascinating world of bat foraging, sparking curiosity and inspiring further research into the extraordinary ecology, behavior and evolution of these fascinating mammals and their vital role in the broader fabric of our planet’s biodiversity and sustainability.

References Abrams, P.A., 1984. Foraging time optimization and interactions in food webs. Am. Nat. 124 (1), 80e96. Brose, U., 2010. Body-mass constraints on foraging behaviour determine population and food-web dynamics. Funct. Ecol. 24 (1), 28e34. Dehnhard, N., Achurch, H., Clarke, J., Michel, L.N., Southwell, C., Sumner, M.D., Eens, M., Emmerson, L., 2020. High inter-and intraspecific niche overlap among three sympatrically breeding, closely related seabird species: generalist foraging as an adaptation to a highly variable environment? J. Anim. Ecol. 89 (1), 104e119. Gil, M.A., Hein, A.M., Spiegel, O., Baskett, M.L., Sih, A., 2018. Social information links individual behavior to population and community dynamics. Trends Ecol. Evol. 33 (7), 535e548. Hedenstro¨m, A., Johansson, L.C., 2015. Bat flight: aerodynamics, kinematics and flight morphology. J. Exp. Biol. 218 (5), 653e663. Latty, T., Trueblood, J.S., 2020. How do insects choose flowers? A review of multi-attribute flower choice and decoy effects in flower-visiting insects. J. Anim. Ecol. 89 (12), 2750e2762. Petchey, O.L., Beckerman, A.P., Riede, J.O., Warren, P.H., 2008. Size, foraging, and food web structure. Proc. Natl. Acad. Sci. U. S. A. 105 (11), 4191e4196. Rydell, J., Speakman, J.R., 1995. Evolution of nocturnality in bats: potential competitors and predators during their early history. Biol. J. Linn. Soc. 54 (2), 183e191. Simmons, N.B., Cirranello, A.L., 2023. Bat Species of the World: A Taxonomic and Geographic Database, Version 1.4. (Accessed 22 August 2023). Stephens, D.W., Brown, J.S., Ydenberg, R.C. (Eds.), 2007. Foraging: Behavior and Ecology. University of Chicago Press. Trapanese, C., Meunier, H., Masi, S., 2019. What, where and when: spatial foraging decisions in primates. Biol. Rev. 94 (2), 483e502.

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Foraging in the fossil record: Diet and behavior of the earliest bats

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Nancy B. Simmons1, Matthew F. Jones2 1

Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History, New York, NY, United States; 2Biodiversity Knowledge Integration Center, School of Life Sciences, Arizona State University, Tempe AZ, United States

The Eocene brought mammals mean And bats began to sing; Their food they found by ultrasound And chased it on the wing. Pye (1968: 797)

Introduction Living bats exhibit a greater range of diets and foraging strategies than any other mammalian order. Extant bat lineages include species that range from strict insectivores to carnivores, piscivores, frugivores, nectarivores, palynivores, granivores, sanguinivores, and many species have mixed diets that overlap two or more of these categories (Gardner, 1977; Freeman, 1998, 2000; Rex et al., 2010; Dumont et al., 2012; Santana et al., 2011a,b; Clare et al., 2014; Nogueira et al., 2005; Dumont, 2003). Methods of detecting and acquiring food similarly vary across chiropteran lineages. Most extant species are thought to obtain food by aerial hawking for flying insect prey, but many other species are gleaners, instead plucking food items from surfaces and branches, while yet others trawl for prey from the surface of water (Audet et al., 1991; Barclay and Brigham, 1991; Kalko et al., 1998; Kalka and Kalko, 2006; Santana et al., 2011a,b). Detection of food objects may depend on echolocation, listening for prey-generated sounds, olfaction, vision, or some combination of these senses, and getting to food once detected may involve behaviors ranging from continuous flight to perch-hunting, hovering, or even quadrupedal walking (Audet et al., 1991; Barclay and Brigham, 1991; Kalka and Kalko, 2006; Norberg and Rayner, 1987; Hessel and Schmidt, 1994; Thies et al., 1998; Riskin et al., 2006; Page and Bernal, 2020). Understanding the evolutionary history of this complex array of diets and foraging habits requires a comparative phylogenetic A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.00008-5 Copyright © 2024 Elsevier Inc. All rights reserved.

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CHAPTER 2 Foraging in the fossil record

perspective, one that includes consideration of the diets and adaptations seen in the earliest batsdthose known only from fossils. The fossil record of bats begins in the early Eocene, approximately 55 Ma (Gunnell and Simmons, 2005; Brown et al., 2019). Early Eocene (Ypresian; 56e47.6 Ma) bats are known from multiple continents including North America, South America, Europe, Africa, Australia, Asia, and the Indian subcontinent (Gunnell and Simmons, 2005; Brown et al., 2019; Hand et al., 2016; Jones et al., 2021; Simmons et al., 2016; Smith et al., 2012; Hand and Sige´, 2018; Tejedor et al., 2005). Most of these fossils consist of fragments of skulls, jaws, and teeth (Gunnell and Simmons, 2005; Brown et al., 2019; Smith et al., 2012; Tejedor et al., 2005). However, some early bat fossils are spectacularly well preserveddparticularly those from lagersta¨tten in the Green River Formation (USA: Wyoming; w52.5 Ma) and the Messel Pit (Grube Messel; Germany: Hesse; w47 Ma) (Jepsen, 1966; Richter and Storch, 1980; Habersetzer et al., 1994; Simmons and Geisler, 1998; Simmons et al., 2008; Habersetzer et al., 1992). Specimens from these localities include nearly complete articulated skeletons, some of which even contain fossilized stomach contents (Richter and Storch, 1980; Habersetzer et al., 1992, 1994). However, even fragmentary fossils may preserve important clues to foraging habits in ancient bats due to observed links between morphological and ecological traits in bats (Simmons et al., 2008, 2010, 2016; Jepsen, 1966; Simmons and Geisler, 1998; Novacek, 1985; Czaplewski and Baker, 2022). Living bats (crown clade Chiroptera) are currently classified in 21 families each containing from one to over 500 species (Simmons and Cirranello, 2022). Several of these groups have fossil records that extend back into the Eocene and/or Oligocene including Emballonuridae, Nycteridae, Hipposideridae, Rhinolophidae, Vespertilionidae, and Mormoopidae (Smith et al., 2012; Simmons and Geisler, 1998; Simmons, 2005; Ravel et al., 2014, 2016; Morgan et al., 2019). Phylogenetic relationships of extant bats are typically assessed with molecular tools that depend on tissue samples and DNA sequencing (e.g., Eick et al., 2005; Stadelmann et al., 2007; Agnarsson et al., 2011), but placing fossils into evolutionary context and dating divergence points requires analyses of phenotypic data (e.g., Simmons and Geisler, 1998; O’Leary et al., 2013; Ravel et al., 2015, Rietbergen et al., 2023). Based on morphological comparisons, 11 extinct families of bats are currently recognized (Table 2.1). While relationships of many of these taxa remain enigmatic, phylogenetic analyses of the better-known families (e.g., those known from more than just teeth) have indicated that several groups clearly fall outside the crown clade and thus may provide insights into early bat evolution that cannot be garnered from examination of only extant lineages (Gunnell and Simmons, 2005; Simmons and Geisler, 1998; O’Leary et al., 2013; Ravel et al., 2015; Rietbergen et al., 2023). Two families, Onychonycteridae and Icaronycteridae, are thought to represent the most-basal branch(es) in Chiroptera, with Archaeonycteridae, Palaeochiropterygidae, Hassianycteridae, and perhaps Tanzanycteridae, also representing stem lineages (Gunnell and Simmons, 2005; Simmons and Geisler, 1998; Simmons et al., 2008; O’Leary et al., 2013; Rietbergen et al., 2023). Among the remaining, Mixopterygidae,

Dental morphology and diet

Table 2.1 Extinct families of bats. Family

Age range

Distribution

Sources

Aegyptonycteridae Archaeonycteridae

Late Eocene Early Eocene eMiddle Eocene

Africa Europe; India

Hassianycteridae

Early Eocene eMiddle Eocene Early Eocene

Europe; India

Simmons et al. (2016) Revilliod (1917), Simmons and Geisler (1998), Smith et al. (2012), Hand and Sige´ (2018) Habersetzer and Storch (1987), Simmons and Geisler (1998), Smith et al. (2012) Jepsen (1966), Simmons and Geisler (1998), Smith et al. (2012), Rietbergen et al. (2023) Maitre et al. (2008), Smith et al. (2012)

Icaronycteridae

Mixopterygidae

Necromantidae

Onychonycteridae

Middle EoceneeLate Oligocene Early Eocene eLate Eocene Early Eocene

North America; Europe; India Europe

Africa; Europe

Sige´ (2011), Hand et al. (2012), Ravel et al. (2016)

Europe; North America

Simmons et al. (2008), Smith et al. (2012), Hand et al. (2015), Czaplewski et al. (2022) Revilliod (1917), Simmons and Geisler (1998), Smith et al. (2012), Maitre (2014), Czaplewski et al. (2022) Sige´ (1985), Smith et al. (2012), Ravel et al. (2012, 2015) Czaplewski and Morgan (2012) Gunnell et al. (2003)

Palaeochiropterygidae

Early Eocene eLate Oligocene

Asia; Europe; India; North America

Philisidae

Early Eocene eEarly Oligocene Oligocene

Africa

Speonycteridae Tanzanycteridae

Middle Eocene

North America Africa

Philisidae, and Speonycteridae are hypothesized to belong within the crown group (e.g., Ravel et al., 2015; Maitre et al., 2008; Czaplewski and Morgan, 2012), while Necromantidae and Aegyptonycteridae occupy more uncertain positions within Chiroptera (Simmons et al., 2016; Hand et al., 2012).

Dental morphology and diet The primary clues for reconstructing diets of extinct bats come from teeth, which are the most commonly fossilized part of the bat skeleton (Brown et al., 2019). Dental

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CHAPTER 2 Foraging in the fossil record

morphology is highly correlated with diet in bats as in other mammals (Freeman, 1984, 1988, 1998, 2000; Santana et al., 2011b; Lo´pez-Aguirre et al., 2022; Villalobos-Chaves and Santana, 2022) (Fig. 2.1), which allows analyses of diet in  fossil taxa (e.g., Simmons et al., 2016; Hora´cek and Spoutil, 2012; Yohe et al., 2015). Most extant bat species are thought to be either entirely or primarily insectivorous and, like other insectivorous mammals, are characterized by a tribosphenic  dentition (Santana et al., 2011b; Freeman, 1984; Hora´cek and Spoutil, 2012; Slaughter, 1970; Fenton and Simmons, 2015). This sometimes makes it difficult to distinguish isolated fossil dental remains of bats from those of other ancient mammals including Paleogene marsupials, leptictids, eulipotyphlans, adapisoricids, nyctitheres, and other dentally primitive therians (Hand et al., 1994, 2012, 2015, 2016;  Smith et al., 2012; Hand and Sige´, 2018; Hora´cek and Spoutil, 2012; Hooker, 1996; Sige´ et al., 2012). Although the majority of extant bats are primarily insectivorous, other prey is regularly taken by a few bat species including both fish and terrestrial vertebrates (Norberg and Fenton, 1988; Gual-Sua´rez and Medellı´n, 2021). However, most carnivorous and piscivorous bats also eat insects and other arthropods (Santana et al., 2011a,b; Norberg and Fenton, 1988; Gual-Sua´rez and Medellı´n, 2021). For this reason, researchers have long distinguished “animal-eating” or “animalivorous” taxa from those that feed partly or entirely on plant products (Freeman, 1984, 1988, 1998, 2000; Rex et al., 2010; Santana et al., 2011a,b; Simmons et al., 2016; Lo´pezAguirre et al., 2022; Norberg and Fenton, 1988; Gual-Sua´rez and Medellı´n, 2021). In this context, animalivory is an umbrella term that covers insectivorous, carnivorous, and piscivorous species, as well as those that have mixed diets including arthropods and other prey (Freeman, 1984, 1998, 2000; Santana et al., 2011a,b; Simmons et al., 2016; Norberg and Fenton, 1988; Gual-Sua´rez and Medellı´n, 2021). Dental morphology in plant-eating bats including frugivores, nectarivores, and granivores is often highly modified to the point that molar cusps and crests cannot be easily homologized with those of animalivorous taxa (Simmons et al., 2016; Freeman, 1988, 1995; Lo´pez-Aguirre et al., 2022; Slaughter, 1970) (Fig. 2.1). Vampire bats represent a special case with an extensively modified dentition preserving barely any trace of ancestral tribosphenic traits (Lo´pez-Aguirre et al., 2022; Slaughter, 1970). All extant animalivorous bats have a dilambdodont tribosphenic dentition including a W-shaped ectoloph on the anterior upper molars (M1 and M2) and a well-developed talonid on the lower molars (Freeman, 1984, 1998, 2000; Santana et al., 2011b; Simmons et al., 2016; Slaughter, 1970; Norberg and Fenton, 1988) (Fig. 2.1). The primitive dental formula for bats includes 3 molars, and all extant animalivorous bats retain M3 although this tooth may be reduced somewhat in size and have an incomplete N- or V-shaped ectoloph; concomitantly, the lower m3 may have a reduced talonid (Simmons et al., 2016; Freeman, 1988, 1995; Slaughter, 1970; Koopman and MacIntyre, 1980). Multivariate dental topographic analysis and phylogenetic comparative methods indicate that in at least some lineages (e.g.,

Dental morphology and diet

FIG. 2.1 Representative examples of upper premolars and molars from extant bats (not to scale) illustrating differences in tooth morphology that reflect dietary differences. A) Myotis myotis, an insectivore. B) Chrotopterus auritus, an animalivore who eats both vertebrates and insects. C) Phyllostomus hastatus, a specialized omnivore. D) Artibeus obscurus, a frugivore. E) Hylonycteris underwoodi, a nectarivore. P2-4 denotes upper premolars; M1-3 denotes upper molars.

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CHAPTER 2 Foraging in the fossil record

Noctilionoidea), animalivorous taxa tend to have larger lower molars than planteating forms (Lo´pez-Aguirre et al., 2022). In another lineage (Molossidae), smaller bats with higher molar topographic values (sharper, more complex molars) and more gracile heads mainly feed on softer insects, whereas bigger bats with lower molar topographic values (blunter, less complex molars) and more robust heads mostly feed on tougher insects (Villalobos-Chaves and Santana, 2022). Smaller-bodied animalivorous bat species tend to be mostly or entirely insectivorous, but as body size increases some species often include small vertebrates in their diet (Freeman, 1984, 1998, 2000; Santana et al., 2011a,b; Simmons et al., 2016; Norberg and Fenton, 1988). However, body size alone does not predict carnivorous or piscivorous habits. Some living bats that have medium or large body size (17 g) apparently prey only on insects (e.g., Saccolaimus peli, Hipposideros commersoni, Cheiromeles spp. (Norberg and Fenton, 1988)), while at least one tiny bat species (Micronycteris microtis, 5e7 g) occasionally eats lizards (Santana et al., 2011a). The ability to consume vertebrate prey apparently does not require large body size, although a predator must be large enough to overpower its prey and must have a sufficient gape and bite force to grasp, kill, and process it (Santana et al., 2011a,b; Simmons et al., 2016; Norberg and Fenton, 1988). Including vertebrates in the diet may actually have facilitated the evolution of larger body sizes in some lineages of animalivorous bats (e.g., by providing a selective advantage to increased body size by virtue of increasing available prey types), rather than large body size being a requirement for carnivory (Freeman, 2000; Simmons et al., 2016; Hand, 1985). Carnivorous bats lack specialized carnassial teeth, but those that regularly eat vertebrate prey do show some dental modifications (Freeman, 1984, 1998; Simmons et al., 2016). Evolution of carnivory in bats is typically associated with elongation of the metastylar shelf and relative elongation of the postmetacrista on M1 and M2 (Freeman, 1984, 1998; Simmons et al., 2016; Hand, 1985) (Fig. 2.1). In concert with elongation of the postmetacrista, the paracone and metacone are often located closer together (Freeman, 1984, 1998), thus reducing the relative length of the postparacrista and premetacrista so that the W-shaped ectoloph in these species is highly asymmetrical (Simmons et al., 2016). In contrast, insectivorous bats (and those that are more omnivorous) typically have a more symmetrical W-shaped ectoloph in which the preparacrista and postmetacrista are subequal in length, and the postparacrista and the premetacrista are subequal in length (Freeman, 1984, 1998). The “intraloph” (distance between the paracone and metacone on the same tooth) and “interloph” (distance between the metacone on one tooth and the paracone on the tooth behind it) are close to subequal in noncarnivorous bats, but the intraloph is much smaller than the interloph in carnivorous species, especially on M2-M3 (Simmons et al., 2016; Freeman, 1984) (Fig. 2.1). Although carnassial teeth are absent in Chiroptera, other shearing structures are present in some taxa. Czaplewski and Baker (2022) identified “carnassiform notches”dnamed for their resemblance to similar features on the carnassial teeth of carnivoransdon the teeth of many tribosphenic bats. A carnassiform notch

Dental morphology and diet

consists of a small cleft in the edge of a talonid shearing crest accompanied by an adjacent accessory trough on the basinward side of the notch. These notches are hypothesized to improve the functional efficiency of shearing, specifically sectioning chitin, in bats with insectivorous or insectivorouseomnivorous dietary habits (Czaplewski and Baker, 2022). Most bats have upper molars with a basal distolingual cingulum or shelf (sometimes called a hypocone basin or shelf even if no hypocone is present), and many have a hypocone (Freeman, 1998; Simmons et al., 2016; Slaughter, 1970). The hypocone, which is typically quite small, is usually formed from the crestlike edge of the distolingual cingulum (Simmons et al., 2016; Slaughter, 1970). Slaughter (1970) hypothesized that molar cingulae function to protect the gums by deflecting prey exoskeletal fragments away from the alveoli. Carnivorous bats typically have a very large hypocone shelf or basin, but the hypocone itself is poorly developed or absent (Freeman, 1998; Simmons et al., 2016). This arrangement is congruent with the observation of Hunter and Jernvall (1995) that presence of a hypocone is incompatible with carnassiform upper molars since it disrupts occlusal contact between metacrista and paracristid, which are the primary shearing blades emphasized in carnivorous mammals. Possession of a welldeveloped hypocone is therefore generally thought to be associated with herbivory (including frugivory and other forms of plant eating) in mammals (Hunter and Jernvall, 1995). Plant-eating habits in bats mostly involve consumption of fruit, nectar, and pollen although folivory and seed predation (granivory) have also been reported in some species (Gardner, 1977; Nogueira et al., 2005; Kunz and Diaz, 1995; Nogueira and Peracchi, 2003). Many specialized plant-feeding bats have highly modified teeth that at best preserve only remnants of the ancestral dilambdodont condition, and many also have a reduced number of cheek teeth (Simmons et al., 2016; Freeman, 1988, 1995; Slaughter, 1970). The teeth of nectarivores generally appear buccolingually compressed such that each molar is considerably longer than it is wide, and lower molars showed reduced molar crown height and steepness (Freeman, 1998; Lo´pez-Aguirre et al., 2022; Slaughter, 1970; Ungar, 2010) (Fig. 2.1). Pteropodids have ovoid cheek teeth with low cusps aligned along the edges of a medial basin or trough (Freeman, 1988, 2000; Slaughter, 1970; Koopman and MacIntyre, 1980). The upper molars of nectarivorous phyllostomids are dilambdodont with a narrow stylar shelf with the paracone and metacone located near the labial edge of the tooth to produce a flat, wide, W-shaped ectoloph (Freeman, 1995, 1998; Ungar, 2010; Da´valos et al., 2014, p. 891). No hypocone is present although there may be a hypocone shelf (Simmons et al., 2016; Ungar, 2010; Da´valos et al., 2014). Frugivorous phyllostomids typically have upper molars with flat, bulbous crowns and lower, blunter cusps and crests than seen in animalivorous species (Simmons et al., 2016; Lo´pez-Aguirre et al., 2022; Ungar, 2010; Da´valos et al., 2014). M1 and M2 are quadrate in occlusal outline, with greatly reduced stylar shelves and with paracones and metacones that are located near the labial edge of the tooth (Simmons et al., 2016; Freeman, 1988; Ungar, 2010; Da´valos et al., 2014). A hypocone is variously developed, ranging from well-developed to entirely absent

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CHAPTER 2 Foraging in the fossil record

(Simmons et al., 2016; Da´valos et al., 2014). Low, broad cuspsdsome that can be clearly homologized with those of dilambdodont tribosphenic molars and some that cannotdcharacterize both upper and lower molar teeth of the most specialized frugivores (Simmons et al., 2016; Freeman, 1988; Lo´pez-Aguirre et al., 2022; Da´valos et al., 2014) (Fig. 2.1). Although dietary guilds are often discussed in the literature as if they represent nonoverlapping groups, it has long been apparent that many bats utilize multiple food sources on a regular basis. Insectivorous bats may sometimes eat small vertebrates or fruit; carnivorous bats often eat insects and other arthropods; frugivorous bats sometimes eat insects; and nectarivorous bats may also eat insects and fruit (Gardner, 1977; Freeman, 2000; Rex et al., 2010; Dumont et al., 2012; Santana et al., 2011a,b; Clare et al., 2014; Simmons et al., 2016; Novaes et al., 2015; Ingala et al., 2021). Some and perhaps many species in two families (Phyllostomidae and Mystacinidae) are true omnivores that routinely consume a variety of food types including both animal and plant products (Gardner, 1977; Rex et al., 2010; Dumont et al., 2012; Clare et al., 2014; Simmons et al., 2016; Yohe et al., 2015; Ingala et al., 2021; Arkins et al., 1999; Lloyd, 2001). However, most bat species appear to have morphological specializations for fruit, nectar, or animal-based diets (Freeman, 1984, 2000; Dumont, 2003; Lo´pez-Aguirre et al., 2022; Swartz et al., 2003) and rely entirely or primarily on one type of food at least in some seasons of the year (Gardner, 1977; Freeman, 1984, 2000). Rather than exhibiting nonoverlapping cranial and dental morphologies representing discrete dietary guilds, bat species instead seem to exhibit a graded spectrum of morphologies reflecting the combinations of dietary items regularly consumed and the extent to which they focus on a particular food type (Czaplewski and Baker, 2022; Lo´pez-Aguirre et al., 2022; VillalobosChaves and Santana, 2022).

Ancient bat dentitions and hypothesized diets All known Eocene bats have a dilambdodont tribosphenic dentition with a welldeveloped W-shaped ectoloph on the anterior upper molars (Hand et al., 2016; Jones et al., 2021; Simmons et al., 2016; Smith et al., 2012; Hand and Sige´, 2018; Simmons and Geisler, 1998; Ravel et al., 2014; Gunnell et al., 2011) (Fig. 2.2). M3 is present and well-developed in all Eocene bats, with a complete W-shaped ectoloph in some taxa (e.g., Onychonycteris) and an N- or V- shaped ectoloph in others (e.g., Protorhinolophus (Simmons et al., 2016; Ravel et al., 2014; Gunnell et al., 2011)). All of these traits are consistent with an animalivorous diet. The W-shaped ectoloph of M1 and M2 in known stem bats is symmetrical without marked elongation of the postmetacrista; the postparacrista and premetacrista are roughly the same length, and the intraloph and interloph distances are subequal. A large hypocone shelf or basin is absent in most stem taxa (e.g., Icaronycteris, Onychonycteris, Archaeonycteris, and Palaeochiropteryx). These traits are indicative of a generalized arthropod diet as opposed to carnivory.

Ancient bat dentitions and hypothesized diets

FIG. 2.2 Upper molars of selected Eocene bats. (A) Icaronycteris menui right M1e3 highlighting the position of the paracone, metacone, and protocone, and the presence of a complete lingual cingulum on M2. (B) Necromantis adichaster left M2 (reflected) highlighting the position of cristae comprising the ectoloph and the presence of an expanded hypocone shelf. (C) Aegyptonycteris knightae right M2e3 illustrating the position of the W-shaped ectoloph and the presence of a metaconule and hypocone. (D) Witwatia schlosseri right M1e2 depicting the interloph (X) and intraloph (Y) distances. Images adapted from Smith, T., Habersetzer, J., Simmons, N.B., Gunnell, G.F., 2012. Systematics and paleobiogeography of early bats, In: Gunnell, G.F., Simmons, N.B. (Eds.), Evolutionary History of Bats: Fossils Molecules and Morphology. Cambridge University Press, New York, pp. 23e66, Maitre, E., 2014. Western European middle Eocene to early Oligocene Chiroptera: systematics, phylogeny and palaeoecology based on new material from the Quercy (France). Swiss J. Palaeontol. 141e242, Simmons, N.B., Seiffert, E.R., Gunnell, G.F., 2016. A new family of large omnivorous bats (Mammalia, Chiroptera) from the late Eocene of the Fayum Depression, Egypt, with comments on use of the name “Eochiroptera”. Am. Mus. Novit. 3857, 1e43, and Gunnell, G.F., Simons, E.L., Seiffert, E.R., 2008. New bats (Mammalia: Chiroptera) from the late Eocene and early Oligocene, Fayum Depression, Egypt. J. Vertebr. Paleontol. 28 (1), 1e11, respectively.

Details of molar crown morphology vary among Eocene bats and combinations of these traits are used to diagnose families (Jones et al., 2021; Simmons et al., 2016; Smith et al., 2012; Ravel et al., 2014). The upper molars of Eocene stem bats typically have sharp cusps with relatively short crests, and most lack a mesostyle, have a transversely elongate trigon, a weakly developed talon and/or lingual cingulum, and either entirely lack conules or retain small para- and/or metaconules (Jones et al.,  2021; Simmons et al., 2016; Hora´cek and Spoutil, 2012). Jones et al. (2021)

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compared morphology of stem bats with potential outgroups and concluded that the common ancestor of all bats had upper molars with a W-shaped ectoloph, transversely elongate trigon with both a paraconule and metaconule, little or no talon expansion, and lacked a lingual cingulum and/or hypocone. Lower molars of stem bats are of the typical tribosphenic pattern, lack carnassiform notches, and most are necromantodont (the hypoconulid is medially situated between the hypoconid and entoconid) rather than exhibiting twinning of talonid cusps (Smith et al., 2012; Czaplewski and Baker, 2022; Sige´ et al., 2012). The functional significance of these traits is largely unknown, although the combined presence of a W-shaped ectoloph and absence of a hypocone shelf or hypocone argues against a planteating or a specialized (as opposed to opportunistic) omnivorous diet. Several genera of Eocene bats attained moderate to unusually large sizes. Species of Witwatia (Philisidae) and Aegyptonycteris (Aegyptonycteridae) from North Africa, Cryptobune (Necromantidae) from France, and Necromantis (Necromantidae) from France and Tunisia are estimated to have weighed from w50 g to more than 100 g (Simmons et al., 2016; Hand et al., 2012; Gunnell et al., 2009) (Fig. 2.2). All are hypothesized to have at least opportunistically consumed vertebrates (Simmons et al., 2016; Hand et al., 2012; Ravel et al., 2012; Sige´, 2011). Witwatia was hypothesized by Ravel et al. (2012) to have opportunistically consumed small vertebrates based largely on the depth of the mandible and height of the lower canine. The size of the three Witwatia species, estimated to be 40e116 g (Gunnell et al., 2009), is also consistent with this hypothesis. Ravel et al. (2015) suggested Witwatia may also have opportunistically consumed fruits based on an analysis of its dental occlusion, although absence of any trace of a hypocone indicates that it was not a dedicated omnivore (Simmons et al., 2016). Morphologically, Witwatia does not differ much from its smaller relatives, such as Dizzya. Unlike living carnivorous bats, Witwatia does not possess an elongated postmetacrista or asymmetrical ectoloph; it has a relatively long intraloph distance, and it lacks the large hypocone shelf of vertebrate specialists (Freeman, 1984, 1998; Simmons et al., 2016; Ravel et al., 2012; Gunnell et al., 2008). Nonetheless, Ravel et al. (2015) suggested Witwatia may have used other structures for slicing food, including the premetacrista and elongate parastyle. The hypoconid on the lower molars of Witwatia is only slightly smaller than the protoconid, a trait shared with extant insectivorous bats (Freeman, 1984). Necromantis, known from three species from France and a fourth possible species from Tunisia, was originally described as a scavenger of carrion (Weithofer, 1887). More recent interpretations suggest Necromantis was specialized for consuming hard prey items, an activity that may have involved bone crushing (Hand et al., 2012). Dentally, Necromantis shares more features with living carnivorous bats than does Witwatia. Upper molars of Necromantis have an asymmetrical ectoloph (i.e., the preparacrista and postmetacrista are longer than the postparacrista and premetacrista) and a large hypocone shelf. Large attachment sites for the masseter muscle on the dentary and zygoma combined with relatively smaller attachments for the temporalis indicate that Necromantis was adapted for crushing and/or grinding prey (Hand et al., 2012). The skull of Necromantis is w70% as

Fossilized stomach contents

wide as it is long, a ratio Freeman (1984) determined is primarily observed in bats specializing on hard items like beetles and bone (Hand et al., 2012). Like Necromantis, Cryptobune possessed a broad and elongate mandibular symphysis, reduced lower incisors, large canines, and p4 that was narrow, but relatively tall and trenchant. Combined with somewhat bunodont molars, Sige´ (2011) concluded that Cryptobune was a carnivorous bat specialized for crushing hard itemsdlikely even more so than Necromantis. Upper molars of Cryptobune are currently unknown, and it is unclear whether they also possessed the same carnivorous adaptations as Necromantis. The only Eocene bat hypothesized to be a true omnivore is Aegyptonycteris from the late Eocene of Egypt (Simmons et al., 2016). Known only from a partial maxilla, this bat had dilambdodont molars with a well-developed symmetrical W-shaped ectoloph and a strong parastyle, uniquely combined with a large metaconule and a very large, bulbous hypocone set low on the posterolingual corner of the M2 (Simmons et al., 2016). It was also a very big batdprobably well over 125 g based on comparisons of tooth size with extant species (Simmons et al., 2016). Taken together, these traits suggest that Aegyptonycteris likely was a truly omnivorous batda “specialized generalist” (Simmons et al., 2016). It is thought to have had a diet comparable to the similarly sized extant phyllostomid Phyllostomus hastatus, probably regularly including insects, other arthropods, small vertebrates, and plant material (fruit and flowers) in its diet (Simmons et al., 2016).

Fossilized stomach contents Stomach contents are only very rarely preserved in fossil bats, but multiple exceptional specimens from Messel offer a view of the last meals of individuals of species of Palaeochiropteryx, Archaeonycteris, and Hassianycteris (Richter and Storch, 1980; Habersetzer et al., 1992, 1994). Roughly 25 specimens of Palaeochiropteryx preserve stomach contents including thick layers of insect scales thought to represent primitive Microlepidoptera (small moths), Trichoptera (caddis flies), and scale-bearing Diptera (e.g., mosquitoes (Habersetzer et al., 1994)). Thick cuticles, such as those characteristic of beetles and cockroaches, are rare in the guts of Palaeochiropteryx species (Habersetzer et al., 1994). In contrast, fossilized gut contents of Hassianycteris (eight specimens) indicate a significantly different diet emphasizing Macrolepidoptera (large moths), beetles, and cockroaches (Habersetzer et al., 1994). Less is known about the diet of Archaeonycteris, but the two known samples entirely lack fragments of scale-bearing insects like moths and caddisflies and instead indicate that these bats may have been beetle specialists (Habersetzer et al., 1994). Preserved stomach contents offer only limited snapshots of the prey of Messel bats, but the data available fit perfectly with hypotheses derived from dental morphology (see above) that have suggested that these bats were most likely insectivorous animalivores. From an ecological perspective, it is interesting to note that

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CHAPTER 2 Foraging in the fossil record

these bats are thought to have coexisted at Messel at the same time, indicating that dietary niche diversity was already present among insectivorous bats in early Eocene communities.

Postcranial clues Aspects of postcranial morphology are correlated with foraging strategies in extant bats, and some of these provide information useful for interpreting the capabilities and possible behavior of extinct species (Habersetzer et al., 1994; Simmons and Geisler, 1998; Norberg, 1989; Habersetzer and Storch, 1987, 1989; Gunnell et al., 2003; Amador et al., 2019; Hand et al., 2009; Lo´pez-Aguirre et al., 2021a,b; Sa´nchez and Carrizo, 2021). For fossils that preserve wing skeletons, several measures correlated with flight performance have been estimated including wing loading (body mass divided by total wing area), aspect ratio (wing length divided by width), and a variety of tip indices (relative area and shape of the wing tip (Norberg and Rayner, 1987; Habersetzer et al., 1994; Norberg, 1989; Habersetzer and Storch, 1987, 1989; Amador et al., 2019; Storch et al., 2002)). Norberg and Rayner (1987) and Norberg (1989) provided considerable discussion of how these features are best measured/calculated in extant and fossil bats. Other informative variables and morphological traits that can potentially be evaluated in fossils (e.g., humerus cross-sectional shape, features of the proximal and distal ends of the humerus, proximal end of the radius, and acromion of the scapula) have been identified in recent ecomorphological studies of extant bats (Lo´pez-Aguirre et al., 2021a,b; Sa´nchez and Carrizo, 2021), but these have yet to be systematically studied in Eocene fossil bats. Based on reconstructions of the skeleton, it appears that Icaronycteris and Archaeonycteris had relatively moderate wing loading and low aspect ratio wings resembling those of many vespertilionids characterized by relatively unspecialized flight capabilities (Habersetzer et al., 1994, 2012; Norberg, 1989; Habersetzer and Storch, 1987, 1989). Onychonycteris had even higher wing loading and lower aspect ratio wings, falling slightly outside the range of extant bats when both traits are considered simultaneously (Amador et al., 2019). Simmons et al. (2008) suggested that Onychonycteris might have had an undulating flight style involving alternating flapping and gliding, and Amador et al. (2019) additionally concluded that Onychonycteris was not capable of maneuverable flight involving sharp turns due to its uniquely primitive wing morphology. In contrast, Palaeochiropteryx species had somewhat more specialized wing morphology characterized by low aspect ratios and low wing loading similar to that seen today in rhinolophids and hipposiderids, suggesting that these bats were well adapted for maneuverable flight close to the ground and vegetation or lake surface (Habersetzer et al., 1994, 2012; Norberg, 1989; Habersetzer and Storch, 1987, 1989). A different wing morphology is seen in species of Hassianycteris, which are characterized by somewhat higher aspect ratios and high wing loading, suggesting that they were specialized for faster flight in more open spaces, probably flying well above the ground in forest clearings, above

Postcranial clues

the forest canopy, and/or over lakes or streams (Habersetzer et al., 1994, 2012; Simmons and Geisler, 1998; Norberg, 1989; Habersetzer and Storch, 1987, 1989). All of the Eocene stem bat taxa discussed above had wings with a relatively short wingtip and small hand wing (dactylopatagium), suggesting that this was the primitive condition for Chiroptera (Norberg, 1989; Amador et al., 2019). This trait, combined with the low aspect ratios seen in Icaronycteris, Archaeonycteris, and Palaeochiropteryx, led Norberg (1989), p. 205 to conclude that “ .. these ancient bats probably foraged or lived among vegetation and may have been perch hunters.” Perch hunting (including flycatching as well as some types of gleaning; sometimes called “hang and wait” hunting) is a form of foraging that involves making short flights out to capture prey detected from a fixed perch, and it is thought to be a technique that reduces the energy expenditure necessary to obtain prey (Norberg and Rayner, 1987; Fenton, 1990; Norberg, 1994). Another possible advantage of perch hunting is that it may facilitate capture and handling of larger prey, thus broadening the potential range of prey available at any given time and place (Norberg and Rayner, 1987; Fenton, 1990). Although Norberg and Rayner (1987) treated perch hunting as a foraging strategy distinct from continuous aerial hawking, many and perhaps all extant perch-hunting bats switch between perch hunting and continuous flight while foraging (Fenton, 1990). Even if many or all stem bats were perch hunters, they may also have foraged for prey from continuous flight under some circumstances (Simmons and Geisler, 1998). One Eocene bat with apparently completely modern wing proportions was Tachypteron from Messel, thought to be the oldest member of the extant family Emballonuridae (Storch et al., 2002; Habersetzer et al., 2012). These bats had very narrow, high aspect ratio wings with high wing loading, a phenotype strikingly similar to that of living Taphozous melanopogon (Storch et al., 2002; Habersetzer et al., 2012). Accordingly, it seems likely that Tachypteron similarly was a longdistance flyer that favored open spaces and employed a rapid, constant flight style (Storch et al., 2002). These bats may have hunted at a higher altitude than other Messel bats, perhaps above the tree canopy (Habersetzer et al., 2012). Most extant animalivorous bats have a long tail membrane (uropatagium) that is supported by the hind legs, tail, and calcars. When the tail is long (equal to or longer than the length of the hind legs) and calcars are present in an extant bat, the tail membrane is invariably long such that it fills the space between the legs extends posteriorly to terminate on the calcars, which may extend well beyond the feet. All known Eocene bats had a long tail, but it is possible that not all had calcars. At least some specimens of Onychonycteris, Palaeochiropteryx, Hassianycteris, and Tachypteron clearly had well-developed calcars, but a calcar is absent in all known specimens of Icaronycteris and Archaeonycteris (Rietbergen et al., 2023; Simmons and Geisler, 1998; Simmons et al., 2008; Storch et al., 2002). Simmons and Geisler (1998) suggested that the calcar in Palaeochiropteryx and Hassianycteris was cartilaginous due to its texture and appearance. In Onychonycteris, it also appears that the calcar was cartilaginous because there is no trace of this element in the paratype specimen, while the holotype clearly preserves well-developed calcars (Simmons et al.,

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2008). This leaves the status of this element in Icaronycteris and Archaeonycteris in questiondwas a calcar present but not preserved in known specimens because it was cartilaginous, or was it truly entirely absent in these forms? Simmons and Geisler (1998) suggested that Icaronycteris and Archaeonycteris entirely lacked a calcar based on absence of an obvious calcar facet on the calcaneum, but we are a bit more doubtful due to the similarities with Onychonycteris. The significance of a long uropatagium for understanding foraging habits concerns the direct use of this membrane for assisting in prey capture. Most extant animalivorous bats that forage by aerial hawking use the tail membrane to scoop their prey from the air before funneling them toward the mouth (Anderson and Racey, 1991; Kalko, 1995; Czech et al., 2008). Some bats that regularly catch fish (e.g., Myotis vivesi) use the uropatagium to scoop their prey from the water (Altenbach, 1989). Gleaning bats also use the uropatagium in prey capture, either making a tent of wings and tail over their prey on the substrate at first contact or actively using the tail membrane to scoop prey from the substrate while in flight (Czech et al., 2008; Tuttle and Ryan, 1981; Medellı´n and Arita, 1989; Swift and Racey, 2002). Evidence that most or all Eocene bats had a long uropatagium suggests that all of these behaviors may have been possible for even the earliest bats.

Evolution of echolocation Echolocation is one of the most important traits involved in foraging in bats (Fenton, 1984; Arita and Fenton, 1997). Over 85% of extant bat species belong to families known for laryngeal echolocation, and a majority of these use echolocation to detect and track prey (Simmons and Cirranello, 2022; Fenton, 1984; Arita and Fenton, 1997). Evidence for echolocation in fossil bats comes from basicranial morphology, relative cochlear dimensions, and stomach contents (Richter and Storch, 1980; Habersetzer et al., 1992, 1994; Simmons and Geisler, 1998; Simmons et al., 2008, 2010; Novacek, 1985, 1987; Hand et al., 1994; Gunnell et al., 2003; Habersetzer and Storch, 1992; Veselka et al., 2010). There is widespread agreement that many Eocene bats were capable of laryngeal echolocation including Icaronycteris, Archaeonycteris, Palaeochiropteryx, Hassianycteris, Australonycteris, Tachypteron, and Tanzanycteris (Habersetzer et al., 1992, 1994, 2012; Simmons and Geisler, 1998; Simmons et al., 2008; Novacek, 1985, 1987; Hand et al., 1994; Gunnell et al., 2003; Storch et al., 2002; Habersetzer and Storch, 1992). Relative size of the cochlea is correlated with echolocation abilities in extant bats (Simmons and Geisler, 1998; Simmons et al., 2008; Novacek, 1985, 1987; Gunnell et al., 2003; Storch et al., 2002; Habersetzer and Storch, 1992), and analyses of cochlear dimensions suggest that there was considerable variability in the echolocation abilities of various Eocene taxa. Icaronycteris and Archaeonycteris have a moderately sized cochlea comparable to that seen in some megadermatids and phyllostomids that use echolocation for orientation and obstacle detention but which forage using passive acoustic cues (e.g., prey-generated sounds) or vision to detect

Evolution of echolocation

prey which they then capture by gleaning (Simmons and Geisler, 1998; Simmons et al., 2008; Habersetzer and Storch, 1992). In contrast, Palaeochiropteryx, Hassianycteris, and Tachypteron have relatively larger cochleae that fall within the range of extant bats that use low duty-cycle echolocation and aerial hawking to detect and capture their prey (Simmons and Geisler, 1998; Simmons et al., 2008; Storch et al., 2002; Habersetzer et al., 2012; Habersetzer and Storch, 1992). Finally, Tanzanycterisdknown from only one poorly-preserved partial skeletondhad a very large cochlea comparable to those seen today in rhinolophids and hipposiderids, suggesting that it might have been capable of high duty-cycle Doppler-shift echolocation (Simmons et al., 2008; Gunnell et al., 2003). Another key osteological marker of echolocation in bats is the structure and articulation of the most distal element of the hyoid apparatus, the stylohyal. The stylohyal typically has an expanded tip that is fused or sutured to the tympanic in extant bats that use laryngeal echolocation (Simmons and Geisler, 1998; Simmons et al., 2008, 2010; Novacek, 1985, 1987; Veselka et al., 2010). This connection between the larynx and the ear is thought to play role in the process by which echolocating bats distinguish between the sounds of calls they are emitting (from the larynx) and echoes of calls they are receiving back from the environment (Simmons and Geisler, 1998; Simmons et al., 2008; Novacek, 1985, 1987; Veselka et al., 2010). In contrast, pteropodid bats, which either do not use echolocation or rely on tongue clicks or wing clapping to produce sounds for echolocation, lack both the expanded tip of the stylohyal and an articulation between this element and the tympanic (Simmons and Geisler, 1998; Simmons et al., 2008, 2010; Novacek, 1985, 1987; Veselka et al., 2010). Most other nonecholocating mammals similarly have an unmodified stylohyal that does not contact the tympanic (Simmons and Geisler, 1998; Simmons et al., 2008, 2010; Novacek, 1985, 1987; Veselka et al., 2010). Although the structure and articulations of the stylohyal cannot be determined in most fossil bats, Icaronycteris, Archaeonycteris, and Palaeochiropteryx clearly had a stylohyal with an expanded tip that articulated with the tympanic, an observation which provides additional support for the hypothesis that these taxa used laryngeal echolocation (Simmons and Geisler, 1998; Novacek, 1985, 1987). Another character once thought to be indicative of echolocation in batsdpresence of an enlarged orbicular apophysis on the malleus (Simmons and Geisler, 1998; Simmons et al., 2008)dhas been shown to vary independently of echolocation abilities in other mammalian groups (e.g., talpid moles (Mason, 2006)); hence, it is no longer considered a marker of echolocation (Simmons et al., 2010; Veselka et al., 2010). Interpretation of what appears to be the most primitive bat known, Onychonycteris finneyi, has been somewhat contentious. In the original description of this taxon, Simmons et al. (2008) noted that it has a relatively small cochlea (quite a bit smaller than the comparably sized Archaeonycteris) with proportions that fall well within the range of variation seen in extant nonecholocating pteropodids. They also noted that the stylohyal in this taxon is an unmodified rod-shaped structure lacking an expansion at the distal end. These traits were used to argue that Oncychonycteris was not an echolocating bat, and that the “flight first” hypothesis is most

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likely correct because this species, which occupies the basal branch in Chiroptera, could fly but had not yet evolved echolocation (Simmons et al., 2008). This scenario was subsequently called into question by Veselka et al. (2010) in a study focused on ear osteology in extant bats. Based on examination of the holotype, they contended that the stylohyal articulated with the tympanic in Onychonycteris, and argued that this ancient bat must have been an echolocator because a stylohyal/tympanic articulation is an unambiguous trait of laryngeal echolocation in extant bats. However, Simmons et al. (2010) subsequently provided CT scans of the holotype documenting that neither the right nor left stylohyal shows unambiguous articulation with the tympanic or any other bone, and indeed the different locations of these elements relative to the tympanics in the crushed skull argue against presence of such an articulation. Given that the only two unambiguous pieces of evidence available (cochlear size and stylohyal shape) support the hypothesis that O. finneyi did not use laryngeal echolocation comparable to that of extant bats (Simmons et al., 2008), in our view, this remains the best-supported hypothesis. However, it remains possible that this species may be representative of an earlier stage of echolocation in which sound was used for orientation and obstacle detection, but before the evolution of anatomical and neural modifications to enhance this ability. Both hypotheses are consistent with recent analyses of genetic and genomic data, neuroanatomy and cochlear morphology, and cochlear development in extant bats that suggest that sophisticated laryngeal echolocation evolved independently in yinpterochiropteran and yangochiropteran bats, and that ancestral bats were at best capable of only a primitive form of echolocation (e.g., Jebb et al., 2020; Nojiri et al., 2021; Sulser et al. 2022). This implies that stem bat lineages capable of sophisticated laryngeal echolocation (e.g., icaronycterids, archaeonycterids, palaeochiropterygids, etc.) evolved this capability independently from extant crown group bats, suggesting multiple independent origins of laryngeal echolocation early in bat evolution. Many researchers have suggested that echolocating bats probably arose from gliding, nocturnal insectivores that used a primitive form of echolocation with short, broadband (frequency modulated) calls or clicks to help in orientation (Norberg, 1989, 1994; Hill and Smith, 1984; Fenton et al., 1995). This sort of echolocation appears today among nocturnal insectivores and rodents (e.g., Thomas and Jalili, 2004; Siemers et al., 2009). Alternatively, bats may have evolved from small nocturnal insectivores that used ultrasound for intraspecific communication and which were thus preadapted for evolution of sophisticated echolocation as flight arose (Speakman and Racey, 1991; Speakman, 1993). Either way, it seems clear that laryngeal echolocation was well established in multiple bat lineages very early in the evolution of Chiroptera.

Vision and nocturnality All bats have functional eyes, and dim-light vision is thought to be present in all extant bat species (Suthers and Wallis, 1970; Eklo¨f et al., 2002b; Liu et al., 2015;

Vision and nocturnality

Sadier et al., 2018; Simo˜es et al., 2019). Many bats have UV and color vision apparently inherited from their laurasiatherian ancestors (Sadier et al., 2018; Simo˜es et al., 2019). Extant echolocating bats use vision for long-distance navigation (Griffin, 1970), homing (Griffin, 1970; Barbour et al., 1966; Williams et al., 1966), and predator surveillance (Suthers and Wallis, 1970), and vision is also thought to play an important role in obstacle avoidance (Eklo¨f et al., 2002b; Chase and Suthers, 1969; Jones and Moss, 2021) and escape responses (Chase, 1981; Mistry, 1990). Indeed, vision may be essential for normal flight performance and orientation in echolocating bats (Davis and Barbour, 1965; Ho¨ller and Schmidt, 1996). Some echolocating bats also use vision for prey detection (Bell, 1985; Eklo¨f et al., 2002a; Eklo¨f and Jones, 2003), perhaps primarily for prey that are relatively large and conspicuous (Rydell and Eklo¨f, 2003). Visual acuity in extant echolocating bats is thought to be modest but generally comparable to that of nocturnal muroid rodents and marsupials (Suthers, 1966; Suthers et al., 1969; Manske and Schmidt, 1976; Bell and Fenton, 1986; Pettigrew, 1988). Given the visual capabilities of extant bats and the likelihood that they evolved from nocturnal ancestors, it seems reasonable to expect that ancient bats had visual capabilities that were similar to those of extant echolocating bats. Based on ancestral state reconstructions of opsin genes, stem bats likely had UV and color vision in addition to low-light sensitivity (Sadier et al., 2018; Simo˜es et al., 2019). Simmons and Geisler (1998) hypothesized that adequate low-light vision may have been a necessary prerequisite for the evolution of echolocation in bats given that echolocation is essentially a short-range sensory system, whereas rapid flight may require longer-range obstacle detection. Reliance on the visual system alone for orientation probably would have precluded aerial insectivory and flight within cluttered environments like dense vegetation (Simmons and Geisler, 1998; Norberg, 1994; Thiagavel et al., 2018). However, a combination of primitive echolocation and vision may have made it possible for ancient bats to fly, forage effectively for insects, and roost in a wide variety of habitats under low-light conditions. Sensory tradeoffs between the visual and auditory systems associated body size, brain size, and eye sizedas well as trade-offs within systems (e.g., between different visual receptors)dare thought to have played a significant role in evolution of bats, particularly with respect to nocturnality and lineage-specific foraging habits (e.g., aerial hawking, frugivory, etc. (Sadier et al., 2018; Simo˜es et al., 2019; Thiagavel et al., 2018)) and roosting habits (e.g., cave roosting (Simo˜es et al., 2019)). Notably with respect to the earliest bats, small body sizes and associated small skull and orbit sizes may have precluded a visual solution to the problem of detecting and tracking night-flying insects (Thiagavel et al., 2018). The evolution and maintenance of nocturnality in bats have been discussed from the perspective of potential selective pressures that might favor nocturnal habits (Speakman, 1995; Rydell and Speakman, 1995). Several such drivers have been proposed, including temporal variation in availability of food sources (e.g., more flying insects available at night), avoidance of overheating (e.g., shedding endogenous heat generated by flight might be easier at night), predator avoidance (particularly

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avoidance of diurnal avian predators), and avoidance of competition (e.g., with aerial insectivorous birds) (Speakman, 1995; Rydell and Speakman, 1995; Thomas et al., 1991; Speakman, 1991a,b). The first of these, temporal variation in food resources, does not seem to be a valid driver for nocturnality in bats because peak flying insect activity is actually not usually at night, but rather at dawn and dusk (Rydell and Speakman, 1995). The Paleocene/Eocene Thermal Maximum (PETM) and the Early Eocene Climatic Optimum (EECO) apparently created conditions highly suitable for aerial insects, so food for aerial insectivores should have been plentiful (McInerney and Wing, 2011; Woodburne et al., 2009). Night-active noctuid moths apparently underwent rapid radiation in the Eocene, but so did other lepidopterans including butterflies as well as other insects that characteristically fly during the day (Kristensen and Skalski, 1999; Grimaldi and Engel, 2005; Toussaint et al., 2012; Kawahara et al., 2022). The other three driversdavoidance of overheating, avoidance of predators, and avoidance of resource competitiondwould be expected to affect different bat species and lineages to varying degrees depending upon body size (e.g., small versus large) and where they live (e.g., tropics versus temperate areas (Speakman, 1995; Rydell and Speakman, 1995)). Accordingly, it seems clear that there is no single functional answer to the question of why bats are all primarily nocturnal today. However, Rydell and Speakman (1995) noted that current conditions are different from past conditions, particularly with respect to biotic factors, and ancient bats might have faced different selective pressures than modern bats. There is little evidence that insectivorous birds interact antagonistically with bats today or compete with them in any meaningful way (Rydell and Speakman, 1995; Fenton and Fleming, 1976). In at least one instance where bats and birds (in this case, nighthawks) have been observed competing for a localized insect food source, the bats clearly dominated in interspecific interactions (Shields and Bildstein, 1979). In the Paleogene, potential competitors for flying insects as a food resource would have been small birds such as hirundines (swallows), caprimulgiformes (nightjars and their relatives), apodids (swifts), or extinct equivalents (Rydell and Speakman, 1995; Mayr, 2009). Although Rydell and Speakman (1995) suggested that only the extinct Aegialornithidae appear to be candidates for competition with the earliest bats, recent fossil discoveries suggest that many insectivorous birds coexisted with bats in the Eocene and hence were part of their biotic environment (Mayr, 2009). The earliest stem apodids appeared in the early and middle Eocene and some are known from Messel, although true swifts do not appear in the fossil record before the late Oligocene (Mayr, 2009). Small-bodied caprimulgids appeared in the early Eocene, and extinct relatives (fluvioviridavids) are known from the Green River Formation (Mayr, 2009). Crown passerines apparently began diversification in the Middle Eocene (Oliveros et al., 2019). Accordingly, we cannot rule out competition pressure as one factor that contributed to maintenance of nocturnality in ancient bats. Avoidance of predators seems a much more powerful driver favoring bat nocturnality than is avoidance of competition (Rydell and Speakman, 1995; Fenton

Foraging strategies in ancient bats

and Fleming, 1976). Predation risk, particularly from diurnal raptors, is thought to be a major factor currently restricting modern bats to nocturnal niches (Rydell and Speakman, 1995; Speakman, 1991b). In the Eocene, predatory birds including owls and hawks were already diverse, and stem species of roller-like birds (Coraciiformes) were also present (Rydell and Speakman, 1995; Mayr, 2009). Rydell and Speakman (1995), p. 191 concluded that “The presence of owls, small hawks, falcons and predatory roller-like birds during the early Eocene may have prevented the early bats from taking advantage of the diurnal insectivore niche. The predation hypothesis may therefore explain why bats did not evolve diurnal activity patterns.”

Foraging strategies in ancient bats All known Eocene bats were capable of powered flight, and hence, their foraging strategies would have been those of volant animals. Because bats are monophyletic, it seems clear that powered flight evolved in mammals only once, early in the chiropteran lineage (Simmons and Geisler, 1998; Simmons et al., 2008; Simmons, 1994, 1995), probably to improve mobility and reduce the amount of time and energy required for foraging (Simmons and Geisler, 1998; Norberg, 1989, 1994; Hill and Smith, 1984; Fenton et al., 1995; Speakman and Racey, 1991). Hill and Smith (1984) suggested that perch hunting may have been the primitive foraging strategy for echolocating bats, and indeed, we expect that it was the primitive strategy for the entire chiropteran clade. Perch hunting represents a reasonable intermediate between foraging strategies characteristic of arboreal mammals (e.g., scansorial foraging while clinging to surfaces) and full-time aerial hawking (Simmons and Geisler, 1998; Hill and Smith, 1984). The demands of perch hunting are probably more complex than those of scansorial foraging even when passive cues are used to locate prey because the hunter must simultaneously fly and keep track of the prey while approaching it (Simmons and Geisler, 1998; Norberg, 1994). However, perch hunting is apparently less complex (in terms of required flight maneuvers and neural processing) and probably requires lower energy expenditures than aerial hawking (Simmons and Geisler, 1998; Norberg, 1994). As described earlier, morphology of the skull, dentition, and postcranium all provide data that can be used to reconstruct the diet and habits of fossil bats. Simmons and Geisler (1998) provided an extensive review of what can be inferred about foraging habits from fossils of the better-known taxa available at that time (Icaronycteris, Archaeonycteris, Palaeochiropteryx, and Hassianycteris), and more recent work on new taxa (e.g., Onychonycteris, Tachypteron, Tanzanycteris, Aegyptonycteris) has added further to what can be inferred (Simmons et al., 2008, 2010, 2016; Gunnell et al., 2003; Amador et al., 2019; Habersetzer et al., 2012). Below we provide a summary of our current hypotheses about the capabilities and foraging strategies of various Eocene bats based on these resources. Based on these hypotheses, it seems clear that different Eocene bat lineages evolved substantial diversity in foraging strategies very early in chiropteran evolution.

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The most primitive known bat, Onychonycteris finneyi, was a volant, nocturnal insectivore that probably hunted from perches using a combination of vision and listening for prey-generated sounds to locate prey. High wing loading and low aspect ratio wings make it likely that these bats flew using an undulating flight style involving alternating flapping and gliding, and that they were capable of neither fast flight nor maneuverable flight involving sharp turns. Accordingly, they probably foraged near the ground, perhaps within forest habitats but not in dense clutter. While they may have been capable of using sound to detect obstacles, their lack of osteological traits indicative of echolocation makes it unlikely that they were capable of laryngeal echolocation comparable to modern bats. Accordingly, we expect that these bats captured their prey by gleaning it from surfaces rather than capturing it on the wing. They may have used their long, calcar-supported uropatagium to assist in prey capture, possibly tenting over the prey on the substrate as some modern gleaners do. Icaronycteris and Archaeonycteris represent another stage of chiropteran evolution in which specializations for laryngeal echolocation had begun to appear, including a modified stylohyal and moderate enlargement of the cochlea. These bats most likely used a combination of vision and laryngeal echolocation for orientation and obstacle detection, but their cochlear dimensions suggest that they did not hunt by aerial hawking but instead used passive acoustic cues (e.g., prey-generated sounds) or vision to detect prey that they then gleaned from surfaces. Dental morphology suggests an insectivorous diet for these bats, with stomach contents indicating that Archaeonycteris may have been a beetle specialist. Their moderate wing loading and low aspect ratio wings suggest that they had relatively unspecialized flight capabilities similar to those of many extant bats. Given their flight and echolocation abilities, they most likely foraged by perch hunting and probably would have avoided dense clutter. Apparent absence of a calcar argues against use of the uropatagium in prey capture, but if this structure was present (and just not preserved) in these taxa, they may have used the tail membrane in a similar fashion as Onychonycteris. Once laryngeal echolocation had evolved, enhancement and specialization of this system for detecting, tracking, and assessing airborne prey would have increased the foraging options open to ancient bats, especially given the abundant food supply offered by flying insects in the night skies (Simmons and Geisler, 1998; Norberg, 1994; Fenton, 1980, 1984). This critical step in chiropteran evolution seems to have been realized in Palaeochiropteryx, which had the basicranial traits common to extant bats that forage for insects by aerial hawking, most notably a relatively large cochlea. Stomach contents including remains of microlepidopterans (small moths), caddis flies, and scale-bearing diptera (e.g., mosquitos) are consistent with a diet obtained by aerial hawking, but Palaeochiropteryx may also have used perch hunting for both flying and nonflying prey. Their long, calcar-supported uropatagium could have been used to assist with both aerial prey capture and gleaning.

Foraging strategies in ancient bats

Palaeochiropteryx species had somewhat more specialized wing morphology than Archaeonycteris and Icaronycteris, with low aspect ratios and low wing loading similar to that seen today in rhinolophids and hipposiderids. This suggests that Palaeochiropteryx species were well adapted for maneuverable flight close to the ground and vegetation. A well-preserved skull of Stehlinia minor from the Quercy fissure fillings in France exhibits similar cochlea dimensions to Palaeochiropteryx, indicating that other members of the family Palaeochiropterygidae likely shared similar echolocation abilities although their flight capabilities remain unknown (Habersetzer et al., 2018). Hassianycteris and Tachypteron also had a cochlea well within the range of extant bats that forage by aerial hawking. With higher aspect ratios and higher wing loading than other Messel bats, these bats were probably less maneuverable but better suited for faster flight in more open spaces than other Eocene bats. Accordingly, we expect that both Hassianycteris and Tachypteron likely foraged well above the ground in forest clearings, above the forest canopy, and/or over lakes or streams. Stomach contents indicate that Hassianycteris had a diet emphasizing large moths, beetles, and cockroaches. Given their cochlear and wing morphology, it seems most likely that both Hassianycteris and Tachypteron captured their prey during fast aerial hawking. Tachypteron, with extremely long narrow wings, may have been particularly well-suited to long-distance flight and foraging above the canopy. The long, calcar-supported uropatagium would probably have been an important tool for prey capture in both taxa as it is in most extant aerial hawking bats. Tanzanycteris is known from only one incomplete specimen, but enough of the skull is preserved to show that it had an extremely enlarged cochlea like those characteristic of living bats that use high duty-cycle, Doppler shift echolocation. Modern bats sharing this trait are capable of precise navigation in forest undergrowth and can detect and localize prey even in dense clutter by using flutter detection (Gunnell et al., 2003; Fenton et al., 1995). Analysis of the cochlea and skull of Tanzanycteris suggests that this type of highly specialized foraging was already present in at least one bat by the middle Eocene. However, the lack of information on wing structure or the posterior postcranial skeleton makes it impossible to speculate further as to the abilities of Tanzanycteris. No Eocene bat described to date is thought to have been a specialized frugivore or nectarivore. Bats lineages known for those diets today (e.g., some phyllostomids and pteropodids) apparently evolved their specialized diets and phenotypes later in chiropteran evolution. We expect that facultative omnivory was a necessary intermediate step between animalivory and plant feeding in bats. Only one Eocene bat is hypothesized to have been a dedicated omnivoredAegyptonycteris. Dental traits plus large body size suggests that this taxon probably regularly included insects, other arthropods, small vertebrates, and plant material (fruit and flowers) in its diet. Flight style of Aegyptonycteris is unknown because no postcrania have been found.

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Ecological and faunal diversity in the Eocene Modern bat faunas, particularly those in the tropics, include remarkably large numbers of species occupying different foraging niches. Interestingly, significant diversitydat least in terms of foraging habits of sympatric animalivorous taxadseems to have been established very early in the evolutionary history of bats. Based on our understanding of phenomic traits discussed above, the bats that co-occurred at Messel clearly occupied multiple different foraging niches by the early middle Eocene (Fig. 2.3). The Messel bat fauna (w47 Ma) included taxa ranging from relatively unspecialized gleaners that used echolocation primarily for orientation (e.g., Archaeonycteris) to aerial hawkers that foraged near vegetation (e.g., Palaeochiropteryx) and even high-flying open space specialists (e.g., Hassianycteris, Tachypteron), with each taxon apparently consuming different types of prey and likely foraging at different levels within and adjacent to the forest. More fine-grained niche variation is suggested by taxonomic diversity within several of these genera. Archaeonycteris and Palaeochiropteryx each include at least two species, and three species of Hassianycteris are currently recognized (Smith et al., 2012; Habersetzer et al., 1994; Habersetzer and Storch, 1987). Within each genus, different species had slightly different body size and wing proportions (Fig. 2.3), and/or dental traits, all features correlated with differences in diet and foraging habits in extant bats. The presence of bats belonging to Archaeonycteridae, Palaeochiropterygidae, and Hassianycteridae in the early Eocene of India led Rose (2012) to suggest the bats of Vastan Lignite Mine (w54 Ma (Clementz et al. 2010)) occupied similar niches to their Messel counterparts. While the Vastan bats are too fragmentary to determine wing morphology or cochlea size, they occur in a range of body sizes suggesting that niche partitioning similar to that seen at Messel is plausible for this fauna as well (Rose, 2012; Smith et al., 2007). The Green River Formation of Wyoming (w52.5 Ma) is older than Messel and slightly younger than the Vastan lignites, and it too has produced multiple species of bats which likely had different foraging habits (Fig. 2.3). Icaronycteris index and the more primitive Onychonycteris finneyi clearly differed in body size and wing morphology and presumably had different flight and echolocation abilities. Both were probably gleaners, but we expect that they focused on different prey. An additional species of Icaronycteris (Rietbergen et al., 2023) brings the number of known Green River bats to three species. However, each species is known from slightly different stratigraphic layers within the Sandwich Beds and 18 Inch Layer of the Fossil Butte Member (Rietbergen et al., 2023), so it is not clear to what extent they lived in sympatry. Regardless, diversity in foraging strategies was clearly established in Wyoming in the early Eocene. The presence of taxonomically and ecologically diverse bat faunas at separate sites on three continents in the early Eocene suggests that bats were already well established and speciose worldwide by this time. This conclusion is further supported by presence of many other species of Eocene bats, albeit mostly known

Ecological and faunal diversity in the Eocene

FIG. 2.3 Bat diversity at Green River (left) and Messel (right) showing reconstructed morphology and possible flight/foraging levels; the order from bottom to top reflects increasing aspect ratio and wing loading. Images adapted from Habersetzer, J., Schlosser-Sturm, E., Storch, G., Sige´, B., 2012. Shoulder joint and inner ear of Tachypteron franzeni, an emballonurid bat from the Middle Eocene of Messel. In: Gunnell, G.F., Simmons, N.B. (Eds.), Evolutionary History of Bats: Fossils, Molecules and Morphology. Cambridge University Press, Cambridge, pp. 67e104, Habersetzer, J., Rabenstein, R., Gunnell, G.F., 2018. Batsdhighly specialized nocturnal hunters with echolocation. In: Smith, K.T., Schaal, S.F.K., Habersetzer, J. (Eds.), MesseldAn Ancient Greenhouse Ecosystem. Senckenberg Gesellschaft fu¨r Naturforschung, Frankand am Main, Germany, pp. 249e261, data in Rietbergen, T.B., van den Hoek Ostende, L.W., Aase, A., Jones, M.F., Medeiros, E.D., Simmons, N.B., 2023. The oldest known bat skeletons and their implications for Eocene chiropteran diversification. PLoS One 18 (4), e0283505. https://doi.org/10.1371/ journal.pone.0283505.

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only from craniodental fragments, in North America, South America, Europe, Africa, Australia, and Asia (Gunnell and Simmons, 2005; Brown et al., 2019; Hand et al., 2016; Jones et al., 2021; Simmons et al., 2016; Smith et al., 2012; Hand and Sige´, 2018; Tejedor et al., 2005). Because fossil faunas, even seemingly quite complete ones, can be expected to only represent a percentage of the taxa alive at any given time and place, we expect that even more diversity in foraging strategies will be discovered in future years as new ancient fossil bats are discovered at sites around the world.

Acknowledgments We thank A. Aase, C. Beard, G. Gunnell, J. Habersetzer, S. Hand, M. Novacek, T. Reitbergen, K. Seymour, and T. Smith for many stimulating conversations about Eocene bats, and I. Hora´cek and one anonymous reviewer for numerous suggestions that improved this chapter.

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Oliveros, C.H., Field, D.J., Ksepka, D.T., Barker, F.K., Aleixo, A., Andersen, M.J., et al., 2019. Earth history and the passerine superradiation. Proc. Natl. Acad. Sci. USA 116 (16), 7916e7925. Page, R.A., Bernal, X.E., 2020. The challenge of detecting prey: private and social information use in predatory bats. Funct. Ecol. 34, 344e363. Pettigrew, J.D., 1988. Microbat Vision and Echolocation in an Evolutionary Context, Animal Sonar. Plenum, New York, pp. 645e650. Ravel, A., Marivaux, L., Tabuce, R., Ben Haj Ali, M., Essid, E.M., Vianey-Liaud, M., 2012. A new large philisid (Mammalia, Chiroptera, Vespertilionoidea) from the late early Eocene of Chambi, Tunisia. Palaeontology 55 (5), 1035e1041. Ravel, A., Marivaux, L., Qi, T., Wang, Y.-Q., Beard, K.C., 2014. New chiropterans from the middle Eocene of shanghuang (Jiangsu Province, Coastal China): new insight into the dawn horseshoe bats (Rhinolophidae) in Asia. Zool. Scripta 43 (1), 1e23. Ravel, A., Adaci, M., Bensalah, M., Mahboubi, M., Mebrouk, F., Essid, E.M., et al., 2015. New philisids (Mammalia, Chiroptera) from the earlyemiddle Eocene of Algeria and Tunisia: new insight into the phylogeny, palaeobiogeography and palaeoecology of the Philisidae. J. Syst. Palaeontol. 13 (8), 691e709. Ravel, A., Adaci, M., Bensalah, M., Charruault, A.-L., Essid, E.M., Ammar, H.K., et al., 2016. Origin and radiation of modern bats: new discoveries in the Eocene of North Africa. Geodiversitas 38 (3), 355e434. Revilliod, P., 1917. Flederma¨use aus der Braunkohle von Messel bei Darmstadt. Abhandlungen der Großherzoglich-Hessischen Geologischen Landesanstalt zu Darmstadt 7 (2), 157e201. Rex, K., Czaczkes, B.I., Michener, R., Kunz, T.H., Voigt, C.C., 2010. Specialization and omnivory in diverse mammalian assemblages. Ecoscience 17 (1), 37e46. Richter, G., Storch, G., 1980. Beitra¨ge zur Erna¨hrungsbiologie eoza¨ner Flederma¨use aus der Grube Messel. Nat. Museum 110, 353e367. Rietbergen, T.B., van den Hoek Ostende, L.W., Aase, A., Jones, M.F., Medeiros, E.D., Simmons, N.B., 2023. The oldest known bat skeletons and their implications for Eocene chiropteran diversification. PLoS One 18 (4), e0283505. https://doi.org/ 10.1371/journal.pone.0283505. Riskin, D.K., Parsons, S., Schutt Jr., W.A., Carter, G.G., Hermanson, J.W., 2006. Terrestrial locomotion of the New Zealand short-tailed bat Mystacina tuberculata and the common vampire bat Desmodus rotundus. J. Exp. Biol. 209 (9), 1725e1736. Rose, K.D., 2012. The importance of Messel for interpreting Eocene Holarctic mammal faunas. Palaeobiodivers. Palaeoenviron. 92, 631e647. Rydell, J., Eklo¨f, J., 2003. Vision complements echolocation in an aerial-hawking bat. Naturwissenschaften 90 (10), 481e483. Rydell, J., Speakman, J.R., 1995. Evolution of nocturnality in bats: potential competitors and predators during their early history. Biol. J. Linn. Soc. 54, 183e191. Sadier, A., Davies, K.T.J., Yohe, L.R., Yun, K., Donat, P., Hedrick, B.P., et al., 2018. Multifactorial processes underlie parallel opsin loss in neotropical bats. Elife 7, e37412. Sa´nchez, M.S., Carrizo, L.V., 2021. Forelimb bone morphology and its association with foraging ecology in four families of Neotropical bats. J. Mamm. Evol. 28, 99e110. Santana, S.E., Geipel, I., Dumont, E.R., Kalka, M.B., Kalko, E.K., 2011a. All you can eat: high performance capacity and plasticity in the common big-eared bat, Micronycteris microtis (Chiroptera: Phyllostomidae). PLoS One 6 (12), e28584.

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CHAPTER

How the moth got its ears and other just-so stories in the history of batemoth interactions

3

Jesse R. Barber1, John M. Ratcliffe2 1

Department of Biological Sciences, Boise State University, Boise, ID, United States; 2Department of Biology, University of Toronto Mississauga, Mississauga, ON, Canada

Evolutionary biology is an intrinsically story-based discipline. We develop narratives of how life unfolded and test the predictions that logically follow from these stories. Using historical narratives as a means of generating hypotheses is not without its critics. Gould and Lewontin (Gould, 1978; Gould and Lewontin, 1979) were clear that adaptive hypotheses advanced in the absence of evidence are “just-so stories” (sensu Kipling’s 1902 children’s book of origin stories), that is, intellectually weak, intrinsically untestable, and ultimately dangerous to the progress of science. The fatal flaw of adaptationist thinking, the authors argued, was to fail to test alternative hypotheses (e.g., co-option) and, most damningly, failing to test nonadaptive (e.g., byproduct) explanations for the origin of traits. Many authors (e.g., Alcock, 1998) have argued that Gould and his colleagues were wrong (even to the point of hyperbole) and that presenting adaptive stories as hypotheses for traits is indeed the way of inferential evolutionary biology. We argue thatdas much in sciencedthere is truth on both sides of this debate. Decades of modern biological research have revealed remarkable adaptations in animals (e.g., ter Hofstede and Ratcliffe, 2016) while simultaneously uncovering evidence for the structuring roles of drift, pleiotropy, gene linkage, by-product origins, and co-option of traits (e.g., Bonduriansky and Chenoweth, 2009; Picq et al., 2016). It is true, in our estimation, that biologists continue to focus on providing evidence for or against adaptive hypotheses rather than focusing on the often-harder investigation of nonadaptive mechanisms and evolutionary origins. In contrast to Gould, we see this limitation driven more by methodological constraints than a failure of scholarship. A key feature distinguishing a just-so-story from a scientific hypothesis is testability. Narrative explanations of trait origins are necessarily ultimate questions (Tinbergen, 1963), and to test historical hypotheses, we require modern phylogenetic tools. Such an evolutionary perspective gives us the ability to understand the tension between constraints and selective forces that govern the tempo and mode of evolution. As this is a book focused on bat foraging, let us turn to the fascinating A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.00001-2 Copyright © 2024 Elsevier Inc. All rights reserved.

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evolutionary arms race between bats and moths, a system brimming with narrative hypotheses of trait origins. Moths diverged from a trichopteran ancestor some 300 million years ago, and these animals were likely small, soft-bodied, weak flyers, or so one story goes (see Ratcliffe, 2009). In fact, today most of the 160,000þ species of extant moths are soft bodied (easy to chew) and slow flying (easy to catch). By flying primarily at night, the ancient moths in our narrative were safe until the appearance of echolocating bats 55e65 million years ago (Fenton and Ratcliffe, 2010). These novel predators were, so far as we know, alone in the night sky of the early Paleogene (Simmons and Geisler, 1998). Indeed, this pre-K-Pg boundary nocturnal aerial predator vacuum is historically and still often invoked as a piece of the explanation for the origination of echolocating bats themselves (Griffin, 1958; Thiagavel et al., 2018), the first and only flying predators capable of detecting (and then) capturing flying prey at night. And, then as now, moths would have been prime targets for bats: easy to detect and track and easy to catch and chew. The above scenariodthat early moths (and other night-flying insects) were safe from predation by vertebrates, yet potentially vulnerable due to their chewability and catchability and that bats evolved to exploit this heretofore unexploited foraging nichedis a great story, and one that makes some intuitive sense. But how would we test it? Well, first we would need to understand the material properties and flight biomechanics of the earliest moths. Given the availability of highly resolved lepidopteran phylogenies (e.g., Kawahara et al., 2019), we could assay dozens to hundreds of extant species for chewability and catchability to amass the data necessary to conduct robust ancestral-state reconstruction analyses. We could also assess the paleontological record, however limited it is for soft-bodied invertebrates (e.g., van Eldijk et al., 2018). Next, we would turn to bats and conduct similar analyses on flight parameters and echolocation abilities and subsequently line up these time-dated phylogenetic analyses to compare the ancestral conditions (nodes of the phylogenetic trees), over time, to test some of the assumptions of this just-so story. This (fantastical) herculean effort would indeed allow a quantitative examination of our narrative. Yet, this case study is less examined than many other stories in the batemoth arms race. Let us now turn to five well-studied examples.

How the moth got its ears Another evolutionary story, this one almost universally propagated, is that echolocating, insect-eating bats created “bat-detecting” ears in moths (a textbook example; Alcock, 2013). It is a tantalizing narrative. Moths found themselves defenseless in a night sky with squadrons of attacking bats, a scenario where selection for an earlydetection mechanism would have been intense. Indeed, hearing organs in nocturnal moths have originated multiple times (Kristensen, 2012), in diverse body regions (e.g., thorax, abdomen, mouthparts), and are found in w80% of extant moth species, giving credence to the hypothesis that bats were the singular selective force driving

How the moth got its ears

the evolution of hearing in moths (ter Hofstede and Ratcliffe, 2016). An additional line of evidence in support of bat-driven hearing in moths comes from the frequency match between bat echolocation call assemblages and the auditory sensitivity of local moth communities (the allotonic frequency hypothesis; Fullard, 1988). In fact, this pattern appears to be more than just a reflection of latitudinal drivers (i.e., greater bat species diversity nearer to the equator) as the ears of noctuid moths from the tropical islands of Hawaii (where only one species of bat exists) are among the most narrowly tuned on the planet (Fullard, 2001). Yet, despite this support for an echolocating-bat-centered origin for moth ears, what alternatives have been carefully considered? Many species of moths produce ultrasonic sounds (i.e., sounds with most frequency content >20 kHz) to transmit information to the auditory systems of conspecificsdwith males from at least six families (Crambidae, Pyralidae, Erebidae, Noctuidae, Geometridae, and Sphingidae) using this strategy to attract ultrasonically sensitive females for mating (for reviews see Conner, 1999; Nakano et al., 2015). A clear prediction from this body of work is that hearing in moths may have first evolved for listening for potential mates, not bats. Yet, this hypothesis has not been put forth (Conner and Corcoran, 2012) or tested. Of course, carefully examining this origin story would require a scale of sexual selection work rarely, if ever, conducted. Assaying, say, 100 species of moths for their use of hearing in reproductive behavior would be daunting, but the inference provided by ancestral state estimates would be worth it. Perhaps the most likely story for the evolution of moth hearing is exactly the scenario supported by evidence in orthopterans. Decades of investigation has bolstered the hypothesis that hearing in katydids, crickets and mole crickets evolved for reasons unrelated to bats (Hoy and Robert, 1996). Recent phylogenomic evidence indicates that in the Ensifera (crickets and katydids) forewing-based stridulation and tympanal ears co-evolved well before bats (Song et al., 2020). In the Caelifera (mole crickets and grasshoppers), tympanal ears likely first evolved for general auditory surveillance (again, well before the origin of echolocating bats) and were secondarily co-opted for sexual acoustic signaling (Song et al., 2020). Thus, it seems that another story might be true: perhaps moth ears evolved simply to hear the sounds of nature. If so, this would better jibe with the wealth of data supporting the notion that most sensory systems originated as general information gatherers, not as means of detecting only a single type of signal, or cue, but a multiplicity of both (Stevens, 2013). And so, it goes. Recently, a ground-breaking phylogeny from Kawahara et al. (2019) provides strong evidence (including 16 fossils for time calibration) that the overwhelming majority of eared Lepidoptera show origin ages in the Late Cretaceous (median age range of crown nodes for the specious Drepanoidea, Geometroidea, Noctuoidea, and Pyraloidea, 91.6e77.6 Ma; CI, 103.4e67 Ma), millions of years before the earliest estimated dates for the adaptive radiation of echolocating bats (Thiagavel et al., 2018). And so, it now seems clear that bats cannot be the origin story for most moth ears. In short, modern phylogenomics combined with

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dated fossils has apparently dispelled a well-worn just-so story in a single stroke, a story that has stood alone and strong since the birth of the classic neuroethological model of bats and moths (Griffin, 1958; Roeder, 1967). With the benefit of hindsight, several lines of evidence support surveillance of the auditory environment (i.e., the detection of adventitious sounds and habitat selection cues, Gomes et al., 2021) as the original selective force driving the evolution of moth ears. Vertebrate and insect movement sounds are broadband with the majority of energy generated between 3 and 30 kHz (Goerlitz et al., 2008). Behavioral and neural evidence has shown that moths respond to the low-frequency (135 dB [root mean square] @ 10 cm from their mouths (Hulgard et al., 2016). As peak-to-peak amplitude estimates are w9 dB higher than root mean square measures, this equates to w45 dB underestimation, or to put it in Pascals, more than two orders of magnitude underestimate in echolocation call pressure. From an eared moth’s perspective, this means that moths are detecting bats at distances up to 10 times further away than we had originally imagined and, thus, are even more able than we realized to avoid bats, bats which have not yet detected them. However, there are bat species that call at intensities and other species at frequencies, which may make them less detectable to these same moths than are more typical aerial hawking bats. Intriguingly, many of these bats belong to the same clade of vespertilionid bat, the tribe Plecotini, and we will focus on the two species best studied to date. While ancestral state reconstructions have not yet been reported in the literature, current phylogenetic trees suggest that the plecotine common ancestor was likely not only a hawker but also capable of gleaning. Gleaning is the act of taking prey from leaves, the ground, and other terrestrial surfaces.

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Today, at least one plecotine is now an obligate aerial hawking species (Barbastella barbastellus), while a second, Euderma maculatum, also seems to hunt primarily by catching prey in the air (see Watkins, 1977). Both species have been reported to take a preponderance of moths (Painter et al., 2009; Goerlitz et al., 2010). We will first zoom in on the spotted bat, Euderma maculatum, which produces echolocation calls of about w10 kHz while in search of flying prey. How loud these bats call is not yet known. Fullard and Dawson (1997) proposed that this species supported Fullard’s (1998) “allotonic frequency hypothesis,” that is, that 20 g Euderma, which, based on mass, should be expected to call at w30 kHz (Thiagavel et al., 2017), not 10 kHz, has evolved to call at such a low frequency to make itself less detectable to sympatric eared moths, which are most sensitive to frequencies between 20 and 50 kHz in the geographic range of Euderma (Fullard and Dawson, 1997; Fullard, 1998). However, like moth ears having evolved to detect bats, this story sounds plausible, but is it true? Beyond its unique black and white pelage and bizarrely low echolocation call frequency, Euderma is a strange bat: it has narrow wings like a molossid, that is of high aspect ratio and wing loading, making it poorly suited to gleaning prey or flying in clutter and enormous ears, an ear design most often associated with gleaning behaviors and similar to that of gleaning plecotines. Very little else suggests Euderma gleans, and its echolocation calls are certainly not optimal for the task (when gleaning, bats tend to use call of higher, not lower, frequency than aerial hawking bats of the same size; reviewed in Ratcliffe (2009)). With its wing design and reports of flight at heights above 10 m, Euderma is almost certainly an aerial hawking specialist, and as such calls of low frequency and low duration as plausibly evolved to allow long range detection of flying insects. That said, Euderma has been anecdotally reported to take insects from the ground (i.e., to glean) and to do so in a manner reminiscent of the specialized plecotine gleaner, Antrozous pallidus (see Watkins, 1977). And so, while moths, and presumably mostly eared moths, apparently make up a large portion of Euderma’s diet (Painter et al., 2009), it is not clear whether (a) if played at realistic intensities (likely >130 dB SPL [root mean square] @ 10 cm), rather than the 90 dB SPL peak-to-peak @ 10 cm used by Fullard and Dawson (1997), it is actually any less detectable by sympatric moths than sympatric hawking species and (b) even if so, whether circumventing moth ears was the primary evolutionary impetus for their low-frequency calls. Indeed, an alternative hypothesis is that instead, the major pressure came from a need to match echolocation range to fast flight in high open spaces as is known from molossids: lower frequency signals are less susceptible to atmospheric attenuation, and so Euderma may benefit from extraordinary echolocation detection range, and this, not circumventing moth hearing, may have been the original and primary advantage (Ratcliffe, 2009). The well-studied and apparently obligate aerial hawking Barbastella barbastellus, at first glance, provides a more compelling story of a bat countermeasure to moth hearing. This species (and likely other members of the genus Barbastella) has been proposed to use very low call intensity, rather than frequency, to similarly

How the moth got its invisibility cloak

make themselves less detectable to moths when hawking prey (Goerlitz et al., 2010; ter Hofstede and Ratcliffe, 2016). Here, the story seems more plausibly correct. Yet, another untested hypothesis for the origination of low-intensity sonar is that Barbestella has retained a constraint imposed by a gleaning ancestor, namely, the need to keep call intensity low to reduce echo amplitudes from highly reflective terrestrial substrates and maintain echo intensities in the “sweet spot” of their auditory system (Measor et al., 2017). Indeed, another plecotine, Corynorhinus townsendii, which does glean and has the large ears and short, broad wings characteristic of specialized gleaners, uses low-intensity echolocation when hawking and better catches eared moths as a result (Corcoran and Conner, 2017). The Plecotini are clearly a superb group to address the hunting strategy origin stories on the bat side of this arms race. Reconstructing ancient sonar characteristics on a well-resolved and clocked phylogeny would shed considerable light on whether the apparent antimoth traits in this clade of bats are (i) the result of the selective pressures and evolutionary baggage of sonar imaging or (ii) the forces imposed by the escape strategies of their eared lepidopteran prey.

How the moth got its invisibility cloak Recently, Neil and colleagues have documented that the scales on the bodies of some earless moths better absorb sound than do the scaled bodies of butterflies (Neil et al., 2020). These authors and others (Neil et al., 2022) go on to document the properties of the scales on the wings, and the organization of the scales as sheets, and demonstrate not only that the scales and scale organization absorb more sound than would a smooth surface, but these sound absorbing qualities are directional and, as such, better absorb (or scatter) sound directed at the rear of a moth, than at its head, and suggest that this reflects an adaptation for moths flying away from attacking bats (Neil et al., 2022). As compared to butterflies’ bodies and wings, Neil and colleagues measured a difference in sound absorption of w3e6 dB (Neil et al., 2020, 2022), a clear advantage against hunting bats. However, no workers have designed a study that tests ultrasound-absorbing scales against echolocating bats. Lepidoptera originated w300 million years ago (Kawahara et al., 2019) and scales predate the origin of the Order (Wang et al., 2022) and thus were clearly involved in some other function for well over 200 million years before bats came on the scene. A long-standing hypothesis for the presence of fluffy scales on moths, and the sleeker ones on butterflies, is thermoregulation (Kingsolver, 1983). While there are exceptions in both groups, most moths are nocturnal, and most butterflies are diurnal. The very same structural properties of moth scales and the way they lie in sheets may also render them insulating; insulation is needed more by night-flying moths, than diurnal butterflies. Another possible origin story for moth scales is that they render their possessors slippery and hard to grasp or stick to, something that may allow them to escape a would-be predator’s jaws,

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claws, and web (Eisner et al., 1964). Finally, some groups of moths (e.g., Megalopygidae, Lymantriidae, Dalceridae) have scales that are irritating to human respiratory systems and likely also to the vertebrate predators of moths (Scoble, 1992). Perhaps scales originated in sheets to be shed easily to clog predator airways and sensory systems. Clearly, there are more proximate investigations to be done in this system, particularly regarding how scale and scale organization influence thermoregulation. It will indeed be fascinating to see detailed trait mapping on time-dated phylogenies to ascertain if ultrasound absorption or other selective forces explain the origin of this trait and its anti-bat role as either a direct response to selection, a by-product or, more likely to our minds, a secondary co-option.

How the moth got its tail The long trailing hindwing tails of saturniid moths have been shown to divert echolocating bat attacks to these nonessential appendages, allowing tailed moths to escape more than half the time (Barber et al., 2015). High-speed video laboratory experiments of bats attacking moths with and without hindwing tails show approximately a 50% survival advantage for tails (Barber et al., 2015). In fact, some of the longest-tailed saturniids (Argema mimosa) escape bat attack in more than 75% of aerial battles (Rubin et al., 2018). Further, when Rubin et al. (2018) experimentally elongated the tails of A. luna, escape success against bats also increased. It seems clear that tails are indeed an antipredator adaptation designed to create a sensory illusion that fools bats into diverting their echolocation-guided attack. How did this remarkable adaptation originate? One option is mates. Recent sexual selection experiments have shown that female moths do not prefer a male Actias luna moth with tails over one with both tails ablated (Rubin and Kawahara, 2023). A robust test of a mating-origin story requires assaying many more species for the use of tails in sexual selection; however, this single study casts considerable doubt on this hypothesis. If we assume that bats drove the evolution of hindwing tails, another important question emerges: via what underlying proximate mechanism? During the pursuit, tails could alter a bat’s perception of the echoic target of a moth, perhaps via an illusion of larger size, due to the integration of echoes reflected across the moth’s length with an echoic center shifted backward from the moth’s vulnerable thorax (Lee and Moss, 2016). Dan Janzen (1984: 118) hypothesized, “Copiopteryx semiramis [an extremely long-tailed saturniid] flies slowly to fast in a nearly straight trajectory with a moderately rapid wing beat, and the long tails stream out behind with the tip of each tracing a 5e10 cm diameter circle in a plane at right angles to the trajectory of the moth. I suspect that the tails render this moth, the smallest (lightest) of the arsenurine saturniids at Santa Rosa, the largest saturniid in the Park in the sonar imagery of a bat.” Alternatively, bats might perceive two or more alternative targets induced by primary reflections from the forewings and the twisted and cupped tail ends

Conclusion

(Barber et al., 2015). If tails create an illusion of larger size, then we might expect bats to attack the center of the enlarged echoic target, just behind the abdomen. If tails generate an illusion of multiple targets, we would predict bat attacks would be directed at either the wings or tail ends. In fact, bats target either the forewing area or the ends of the tails in 75% of attacks (Rubin et al., 2018). These data were coded from three different high-speed camera angles, by one human observer. Future work should focus on microphone array reconstruction of sonar beams and quantification of echoic information to definitively disambiguate these hypotheses. Yet, it seems likely that both mechanisms might be at play across saturniid diversity. Tailed saturniids appear to be derived from nontailed ancestors (Rubin et al., 2018). At least four different evolutionary events spread across Asia, Africa, and Australia in different lineages (Copiopteryx (Arsenurinae), South America; Eudaemonia (Saturniinae), Africa; and Actias and Coscinocera (Saturniinae), Asia) show that long hindwing tails have originated multiple time and that in each case are derived from nontailed ancestors. It thus seems likely that illusions of larger body size preceded the illusion of multiple targets. Yet, at least one more story remains for the origin of long tails in moths. It is possible that hindwing tails increase escape success by altering flight kinematics, perhaps by increasing turning ability (e.g., angular/radial acceleration). Experiments with barn swallows (Hirundo rustica) have shown that their long tail streamer feathers increase maneuvering flight (i.e., the mean rate of change of curvature; Rowe et al., 2001). More relevantly, Corcoran and Conner (2016) showed in a study of 50 attacks by wild bats (Myotis volans) on moths, that moth radial acceleration was one of the most important predictors of escape success. The two studies that have pit bats against tailed saturniids (Barber et al., 2015; Rubin et al., 2018) used 3D high-speed video to quantify the flight kinematics of moths with and without tails and found no differences in a variety of metrics, including angular acceleration, with one exception. When Rubin and colleagues experimentally shortened A. mimosa tails, by removing part of the tail shaft and gluing the cupped and twisted end back on, angular acceleration increased. This is counter to the prediction that longer tails increase turning ability, yet it remains possible that the glueing procedure stiffened the tail shaft, and this material property change was responsible for the observed kinematic difference. To determine if increased turning ability drove the origination of hindwing tails, first more proximate work on flight kinematics during bat-moth battles needs to be done to verify the validity of this hypothesis. Next, flight kinematics need to be collected from many saturniid species, with different wing shapes, and mapped on a time-calibrated phylogeny.

Conclusion The batemoth system has generated some of the most remarkable and evocative stories in evolutionary biology. Workers in this field have primarily focused on the adaptive value of extant interactions, while often invoking origin stories to place their studies in context. Yet the data required to answer ultimate questiondto test the validity of origin storiesdare often far more numerous and complex than available.

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If we are to hazard tests of these evolutionary hypotheses, we must leverage the hyper-diverse world of insects and bats and modern phylogenetic techniques. But how do we prevent the problems with just-so-story hypothesis generation and make sure we address all possibilities, not just adaptive ones, for the origination of traits? One way is for predator-prey researchers to challenge themselves to come up with testable origin stories in each of these conceptual areas: selection, byproduct, and co-option. Clearly, other nonadaptive possibilities remain including drift, pleiotropy, and gene linkage, among others, yet, the three areas we outline above are some of the most tractable to test. To generate solid ultimate hypotheses for trait origins, we must also focus on robust proximate investigations. Gould (1991) argued, “. we must first establish ‘how’ in order to know whether or not we should be asking ‘why’ at all.” Importantly (and opposite to Tinbergen’s definitions, Tinbergen, 1963), Gould meant that we need to first answer ultimate questions before addressing proximate mechanisms. We disagree and affirm that Tinbergen remains unequivocally correct: we must simultaneously investigate proximate and ultimate questions. A refined understanding of extant anatomy, physiology, and behavior leads to well-parameterized ultimate questions and allows us to refine our storiesdour narrative hypotheses about the origin of traits.

Acknowledgments We thank Danilo Russo and Brock Fenton for the invitation to contribute this chapter and Juliette Rubin for providing constructive input on earlier drafts of it.

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Sensory systems used by echolocating bats foraging in natural settings

4

Clarice Anna Diebold1, Cynthia F. Moss1, 2, 3, 4 1

Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, United States; 2The Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD, United States; 3Department of Mechanical Engineering, Whiting School of Engineering, Johns Hopkins University, Baltimore, MD, United States; 4Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, MD, United States

Introduction Sensory systems provide animals with vital information to execute natural survival behaviors. From substrate vibrations to chemical secretions, the sensory worlds of animals are diverse and often species-specific. Through evolutionary history, animals have acquired sensory systems that are adapted to the environments they occupy, predators they avoid, food they seek, and channels they use to communicate. Indeed, habitats, diet, and social behaviors exert strong selective pressures on the morphology and function of sensory systems. Chiroptera is an order of mammals that offers many striking examples of sensory specializations (reviewed in Page and ter Hofstede (2021)). Chiroptera, from the Greek, “hand wing,” is comprised of bats that occupy diverse habitats on every continent except for the Antarctic. Over 1400 species occur in environments ranging from tropical jungles and open deserts to dense temperate forests and mountains (Simmons and Cirranello, 2022). Accordingly, these mammals exhibit a wide array of sensory specializations that support natural survival behaviors. Bats are the only mammals capable of powered flight and exhibit hearing sensitivity over a broad range of sound frequencies. Many bat species use echolocation, an active sensing system that operates largely in the ultrasound range, above 20 kHz, the upper limit of human hearing. Echolocating bats produce sonar sounds ranging from w10 kHz to over 200 kHz and use features of returning echoes to steer around obstacles, localize roosts and foraging sites, and, in some cases, track erratically moving prey. This remarkable active sensory system enables many bat species to forage in darkness (Griffin, 1958). Although bats are widely recognized for their exceptional hearing and echolocation, about 200 bat species do not echolocate and rely on vision and other senses to support navigation and foraging behaviors. Even in some echolocating bat species that eat fruit, visual and olfactory cues carry information about food location and A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.00009-7 Copyright © 2024 Elsevier Inc. All rights reserved.

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quality. Like other animals, bats are equipped with several complementary sensory systems integrate information across modalities to effectively operate in the natural environment. This chapter reviews the role of echolocation and other sensory modalities in navigation and foraging in diverse bat species.

Echolocation

Sonar call structure and duty cycle The diverse echolocation call structures of bats are adapted to the foraging and navigation tasks they face in natural habitats. Most, but not all, bats produce echolocation calls in the larynx. Laryngeal echolocation calls often consist of frequency modulated (FM) components but may also include a constant frequency (CF) component (Fig. 4.1). FM signals sweep across a broad range of frequencies, often with durations of less than 10 ms. CF signals are typically combined with FM signals and are referred to as CF-FM calls. The structure of the emitted calls determines the overall duty cycle, or the percentage time filled by acoustic signals within a given period, often one second. For example, two 250 ms calls produced within a one second window yield a duty cycle of 50%. Bats can adjust echolocation duty cycle by changing call duration and/or the number of calls per unit time. Generally, bats that emit only FM sonar signals produce calls at low duty cycle (LDC), while bats that emit CF-FM signals produce calls at relatively high duty cycle (HDC) (reviewed in Fenton et al. (2012)). The call structures and duty cycles employed by a given species are often adapted to its specific foraging niche and habitat. The short duration and broad frequency sweeps of FM calls are well suited for sonar localization: each frequency in the sweep provides a marker for computing echo arrival time, the bat’s cue for target distance (Moss and Schnitzler, 1989, 1995; Simmons, 1973), along with interaural differences for computing azimuth (Simmons et al., 1983) and spectral profile for estimating elevation (Lawrence and Simmons, 1982; Wotton et al., 1995). FM signals typically yield a shorter operating range than CF signals because energy is spread across the FM sweep, rather than concentrated in a limited frequency band. To avoid overlap between calls and echoes, bats with FM call structures often use LDC echolocation, adjusting the duration and repetition rate of calls so that echoes arrive before the production of subsequent sonar signals (Fenton et al., 2012). LDC echolocation supports high-precision localization and is prevalent in insectivorous bats that catch on the wing in low clutter conditions. CF-FM signals are often used by bat species that forage for insects in dense vegetation, as fluttering insects introduce modulations in the amplitude and frequency of echo returns (glints) that stand out amid echoes from surrounding vegetation, aiding the bat in prey detection and discrimination (Kober and Schnitzler, 1990; Schnitzler and Kalko, 2001; von der Emde and Schnitzler, 1990). Species that produce CF-FM echolocation signals often show highly specialized auditory systems that show maximum sensitivity in the spectral region of the CF component of their calls at

Echolocation

FIGURE 4.1 Spectrograms and photographs of three different species of bats illustrating example calls to highlight differences in call structure. The aerial hawking big brown bat, Eptesicus fuscus, uses short duration FM sweeps to detect small flying insects to catch on the wing. The Egyptian fruit bat Rousettus aegyptiacus make use of even shorter lingual clicks to detect objects and assist in navigation while they traverse long distances. The great roundleaf bat, Hipposideros armiger, lives primarily in dense forests in South and Southeast Asia, and emits calls with CF-FM components to detect and intercept fluttering targets within the vegetation. E. fuscus and R. aegyptiacus photos by Dr. Brock Fenton, H. armiger photo by Dr. Vu Dihn Thong.

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rest or Doppler shifted echoes in flight. These specializations can be traced in some bat species to mechanical specializations of the basilar membrane that yield an overrepresentation of neurons tuned to the frequency band around the CF call (referred to as an “acoustic fovea”) (Covey, 2005; Moss and Surlykke, 2010; Neuweiler et al., 1980; Schnitzler and Denzinger, 2011). As a result, the audiograms of bats that use CF calls often show regions of high-frequency sensitivity, flanked by regions of decreased sensitivity (Long, 1977; Long and Schnitzler, 1975). The audiograms of FM bats, by contrast, show standard U-shaped audiograms, typical of other mammals (Moss and Schnitzler, 1995). CF-FM bats have high levels of specialization to efficiently process returning echoes within a narrow frequency band, which aids them in foraging in densely cluttered environments. Many bat species that use long CF echolocation signals exhibit Doppler shift compensation (DSC), characterized by adjustments in sonar emission frequency to compensate for the Doppler Shifts introduced by their own flight velocity, thus ensuring that returning echoes return in the bat’s frequency range of maximum hearing sensitivity (Schnitzler, 1968). Bats that perform DSC separate sonar emissions and echoes into different frequency channels. Importantly, these bats are able to operate with temporal overlap between sonar emissions and returns (Schuller, 1974, 1977; Fenton et al., 2012). This is because the Doppler shift of returning echoes arrives in the spectral region of the bat’s maximum hearing sensitivity, whereas the calls they emit are outside of that range of hearing sensitivity. This separation of call and echo frequency enables the bat to effectively process sonar returns. Moreover, use of HDC calls in bats that exhibit DSC improves the detection of fluttering insects in cluttered environments (Lazure and Fenton, 2011). The bat Rhinolophus ferrumequinum can, for example, differentiate between species of insects by listening to the features of acoustic glints generated by their fluttering wings (von der Emde and Schnitzler, 1990). As stated above, bats that use CF signals also add FM components, which likely aids in sonar localization. Studies comparing FM and CF-FM bats show that they can both discriminate target range differences as small as 1e3 cm, but a species that produces a very broad bandwidth FM signal shows more accurate range discrimination than a species that produces shallow FM signals (Simmons, 1973). Thus, there appears to be a tradeoff between CF and FM signals for detecting and localizing prey in different environments. Bats that forage for fast-moving prey in open spaces weight localization more heavily, leading to very broadband FM call structure. Some CF-FM bat species that forage insects in densely cluttered environments weigh flutter detection more heavily and use FM components that cover a narrower bandwidth.

Nonlaryngeal echolocation Some species in the genus Rousettus are the only members of the family Pteropodidae that echolocate. Unlike most echolocating bats that use their larynx to produce sonar calls, Rousettus are lingual echolocators, producing broadband ultrasonic

Echolocation

clicks with the tongue (Griffin et al., 1958; Neuweiler, 2000; Yovel et al., 2010, Fig. 4.1). The emitted clicks are extremely short, approximately 50e100 ms (Holland et al., 2004). While lingual echolocation has been described as rudimentary compared to laryngeal, studies show that Rousettus perform comparable to FM laryngeal echolocators in echo detection and obstacle avoidance tasks (Raghuram et al., 2007, Yovel et al., 2010). One of the best studied species, Rousettus aegypticus, emit sonar calls in pairs (Holland, 2004) and alternate the direction of the sonar beam of each click from left to right, off-axis from their target, while placing the maximum slope of the sonar beam on the target (Yovel et al., 2010). Rousettus also supplements acoustic information with optic information (see Vision section below). This bat species uses both modalities in tandem to effectively navigate long distances and interact with their ecological niche. Remarkably, other species of bats have developed alternative forms of echolocation to navigate in darkness. The cave nectar bat, Eonycteris spelaea, is found in New Guinea, and in 1969, it was observed that these bats roost in caves, some in complete darkness. The bats flying in a dark cave produced a noticeable, raindrop-like sound that stopped once they reached a lit portion of the cave (described in Gould (1988)). E. spelaea also produce this sound when approaching fruit trees in darkness (Gould, 1978). Follow-up research in laboratory settings revealed these bats produce a sound by clapping down their wings while in darkness, but not in light, emitting an acoustic signal audible from about 30 m (Gould, 1988). These wing clapping sounds can be used for general orienting behaviors (Boonman et al., 2014), though they do not allow for highly accurate distance and localization exhibited by lingual and laryngeal echolocating bats (Boonman et al., 2014). This more rudimentary form of echolocation provides additional sensory cues, which E. spelaea can use to effectively navigate in darkness to emerge from caves, demonstrating the remarkable adaptations of Chiroptera to environmental challenges and to navigate through their habitats.

Sonar scene analysis In a complex and noisy world, animals encounter a cacophony of sounds. They must separate sounds from different auditory sources and integrate sounds from the same source that vary over time. The segregation and tracking of sound sources, commonly referred to as auditory scene analysis (Bregman, 1990), allows an organism to extract meaningful information from complex acoustic environments. For echolocating bats, objects that returns echoes are effectively sound sources, and they must track dynamic sound sources that move in space and time, integrating echoes that return from the same source and segregating echoes that return from different sources (Moss and Surlykke, 2001, 2010). Echolocating bats analyze complex auditory scenes to forage and navigate. In natural environments, each sonar call often results in a cascade of echoes, from food items, surrounding vegetation and other sound sources. The echolocating bat may encounter auditory masking, whereby sounds (call emissions or echoes) that

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precede the target echo (forward masking) or sounds that follow the target echo (backward masking) interfere with target detection and discrimination (Schnitzler et al., 2003). FM bats can detect echoes that overlap calls or other echoes to subsequently adjust signals to avoid further overlap (Surlykke et al., 2009). Bats also actively modify the directional aim and spectro-temporal content of their ultrasonic vocalizations in response to information processed from returning echoes (Moss et al., 2011; Siemers and Schnitzler, 2004) and thereby control the sound features they track over space and time (Moss and Surlykke, 2010). For example, insectivorous laryngeal echolocating bats direct the acoustic beam axis to selected prey and adjust sonar call features to maximize localization accuracy (Ghose and Moss, 2003, 2006; Warnecke et al., 2016). They also adjust their flight trajectory to prey relative to background vegetation to separate target and clutter echoes in the azimuthal plane (Taub and Yovel, 2020). These active adjustments in sonar behavior contribute directly to the analysis of echo scenes and allow bats to forage in complex acoustic environments. While clutter objects can generate acoustic interference, bats sometimes benefit from echo clutter to detect and discriminate objects. Detecting motionless prey perched on a leaf presents a perceptual challenge for bats that forage using echolocation. It is therefore noteworthy that the common big-eared bat, Micronycteris microtis, a gleaning bat, can detect and localize silent, stationary prey in cluttered environments (Geipel et al., 2013). M. microtis appears to have solved this problem by modifying its flight approach to prey, selecting oblique angles that produced echoes from the leaf on which the target rests, creating secondary reflections that enhance the acoustic profile of the prey (Geipel et al., 2019). This adaptive behavior allows this bat species to make use of clutter echoes that would otherwise obscure the prey and instead provide robust information for target detection and localization. Recently, neural recordings in the inferior colliculus (IC) in the aerial hawking insectivorous big brown bat, Eptesicus fuscus, demonstrated the benefit of clutter echoes for target discrimination (Allen et al., 2021) and reported a similar mirroring effects of background clutter to differentiate auditory objects. While clutter is typically a source of acoustic interference in bat echolocation, these studies show that bats may sometimes use the reflective properties of clutter to aid in the detection and discrimination of sonar targets.

Auditory signals and ecological niche Dynamic adjustments in the spectro-temporal features of echolocation calls, coupled with differences in call structures described above, have given rise to diverse foraging specializations in bats and allowed different species to occupy a vast array of habitats and ecological niches. The classification or grouping of bats based on different call features, from foraging behaviors to sonar call design, has been a topic of great discussion (Denzinger and Schnitzler, 2013; Fenton, 1990; Kalko et al., 1996; Neuweiler, 1989; Schnitzler et al., 2003, see other chapters in this volume).

Auditory signals and ecological niche

Here, we discuss general patterns in the foraging behaviors of bats that differ in diet and ecological niche. While this differentiation is one of many possible approaches, it provides a useful framework to consider foraging strategies employed by this vastly diverse order.

Aerial hawking Bats that specialize in catching insect prey on the wing often show dynamic echolocation strategies to effectively track and intercept prey. These aerial insectivores often emit relatively long duration search calls at relatively low rates until they detect a potential prey item (Schnitzler and Kalko, 2001). Once they have acquired a target and begin approaching their prey, bats increase their call rate and shorten the time between calls, locking their head orientation onto the selected target (Ghose and Moss, 2003). This increase in calls samples information about the location and movements of targets at high rates, providing additional information about the movement of a target over time. Bats then begin a distinctive interception phase with call rates up to 150e200 sounds per second (Griffin et al., 1960; Schnitzler and Kalko, 2001; Surlykke and Moss, 2000). While there exist widespread species differences in sonar call spectro-temporal structure, echolocating bats nonetheless show similar trends in signal adjustments during insect pursuit that likely serve common functions (Schnitzler and Kalko, 2001). When the bat prepares to intercept its target, it will enter a terminal buzz capture phase where calls typically decrease in frequency (Schnitzler and Kalko, 2001; Surlykke and Moss, 2000) and sonar beam is widened, adjustments that may support tracking errectically moving targets while monitoring background clutter (Jakobsen et al., 2015). The intensity of many aerial hawking insectivores is remarkably high, with some open-space insectivores emitting calls as high as 140 dB SPL (Holderied and von Helversen, 2003; Surlykke and Kalko, 2008). This high intensity determines the echolocation range, or the distance the reflected echoes from objects are still detectable by the bat. Thus, a small insect can still be detected at a greater range by bats that produce high intensity calls. Bats flying at high altitudes must contend with physical limitations of foraging under adverse conditions by making modifications to their echolocation signals to generate audible echoes for localizing targets. Some species of bats fly at very high altitudes, some as high as 3000 m (Davis et al., 1962; McCracken et al., 2007, 2021; Williams et al., 1973). High altitudes and reduced air pressure can dramatically attenuate ultrasound, reducing the bat’s sonar operating range. Bats flying as high as 300e800 m have been observed to track insect prey (Fenton and Griffin, 1997). Mexican free-tailed bats, Tadarida brasiliensis, forage at high altitudes, exploiting the seasonal migration patterns of some moths by foraging at higher altitudes when more migratory moths were present (Krauel et al., 2018). This bat species modifies echolocation behavior at high altitudes by lengthening calls during the search phase and lowering call frequency and bandwidth (Gillam et al., 2009; Griffin, 1971). These modifications enable bats flying at higher altitudes

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to receive relevant returning information by maximizing efficiency even with physical properties of the propagation of sound having changed with these altitudes.

Foraging over water Water in a habitat can present a foraging opportunity but also an acoustic challenge for echolocating animals. Bats that specialize in foraging over water have developed strategies to exploit this ecological niche. Some bat species forage insects or even small fish that swim close to the water surface. Large bodies of water can act like acoustic mirrors, as most of the echo energy is reflected away from the bat. Some trawling bats may use the acoustic mirror properties of water to improve detection of prey on the surface at a greater distance (Siemers et al., 2005). However, there is also evidence that many bats mistake any horizontal smooth extended surface to be a body of water, even in the presence of conflicting sensory cues, suggesting that they rely on innate representations to find drinking sources (Greif and Siemers, 2010; Russo et al., 2012). Bats that specialize in trawling or skimming insects or fish from the surface of the water detect prey that temporarily break the surface of the water. When cues are continuously available, such as an insect resting on the water surface, trawling bats, such as the greater bulldog bat, Noctilio leporinus, dynamically decrease the interval between echolocation calls with closing target distance, a relatively stereotypical echolocation behavior also observed in many aerial hawking insectivores. During the final capture phase, insectivores produce high repetition rate buzz I and buzz II call segments, with the latter marked by the highest call rates and a drop in sound frequency (Surlykke and Moss, 2000). However, when acoustic cues are transient, like a fish breaking the surface of the water and submerging, ¨ bernickel et al., 2013). In addition to modifying their N. leporinus omit buzz II (U echolocation behavior, they extend their time skimming along the surface of the water when prey appear intermittently, likely due to a reduced certainty of the target ¨ bernickel et al., 2013). These specific adaptive behaviors enable the location (U exploitation of food resources that live near large bodies of water.

Gleaning for prey on substrates Some bat species glean insects from substrates, such as leaves and branches. While some gleaning bats can detect silent, motionless prey (Geipel et al., 2013), many rely on the sounds generated by the prey themselves. Indeed, some bat species exploit passive listening, as opposed to active echolocation, to determine the location of moving or noisy prey. For example, the pallid bat, Antrozous pallidus, accurately localizes prey using passive auditory cues (Brewton et al., 2018), suggesting preyproduced sounds may be sufficient for acquiring their targets. Gleaning bats often produce echolocation signals as they forage, likely to orient through the environment and avoid obstacles (Fenton, 1990; Neuweiler, 1989; Schnitzler et al., 2003). Studies of gleaning species Myotis myotis and Myotis blythii reveal a reduction in call

Auditory signals and ecological niche

amplitude as these bats approach their prey, potentially to reduce masking of preygenerated sounds or to prevent prey with ultrasound hearing to detect their approach (Russo et al., 2007). Historically, these gleaning bats had been described as “whispering” and had been thought to have relatively low intensities (Griffin, 1958). However, more recent field recordings have revealed these bats are much louder than previously believed (Brinkløv et al., 2009, reviewed in Jakobsen et al. (2015)).

Passive listening to the sounds of prey Another bat that makes use of passive signaling is the carnivorous Trachops cirrhosus. This bat species famously listens in on the acoustic communication signals of frogs, particularly the mating calls of the tu´ngara frog Physalaemus pustulosus, to detect and localize their prey (Tuttle and Ryan, 1981). Male P. pustulosus can emit two different types of calls when advertising to female frogs, one is a simple FM sweep, or “whine,” or a more complex call that includes the whine followed by subsequent broadband “chucks” (ranging from one chuck to seven or more) (Bernal et al., 2007; Ryan, 1985). T. cirrhosus consistently prefer the more complex calls that include chucks (Ryan et al., 1982), potentially due to the broadband components aiding in effective localization in cluttered environments (Page and Ryan, 2008). Impressively, these bats can even use the incidental signals of the ripples in the water generated from a frog calling in water to further aid in localization (Halfwerk et al., 2014), using both passive and active listening to effectively capture these frogs. While T. cirrhosus feeds extensively on P. pustulosus, they are highly flexible in their foraging behavior. When presented with the calls of P. pustulosus and a second, toxic toad Bufo marinus, the bats consistently preferred the palatable frog but were able to change this preference when the palatable frog call was no longer rewarded (Page and Ryan, 2005). This suggests that these bats are able to flexibly modify their behavioral response to even these passive acoustic cues, flexibly shifting foraging strategies potentially to respond to changes in resource quality or availability of food. Echolocation and passive listening in bats enable flexible foraging for a wide variety of foods in diverse environments. Indeed, common to the success of all bat species is the use of hearing to forage at night, which is complemented by agile flight that allows them access to a broad array of food sources, including small vertebrates and insect prey. The use of echolocation by many bat species to forage insects has also driven the evolution of ears that alert prey of an impending attack.

Insectivores and prey counter strategies Echolocation allows insectivorous bats to forage at night when they have few competitors, but they must also contend with a variety of challenges, including a limited operating sonar range and interrupted sensory snapshots of moving prey (Diebold et al., 2020; Schnitzler and Kalko, 2001). Computed sonar detection distances of insect echoes are estimated to fall between 5 and 25 m for large insects and 2 and 7 m

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for small prey (Holderied and von Helversen, 2003), and the rate of echolocation call production confers the rate at which they sample information from aerial prey (Moss and Zagaeski, 1994). Some aerial insectivores optimize their flight path to intercept multiple insect targets on a single pass (Fujioka et al., 2016). There is also evidence that bats integrate echo snapshots over time to anticipate target motion, allowing for the rapid coordination of behaviors to effectively intercept targets (Diebold et al., 2020; Ghose, 2006; Salles et al., 2020, 2021). While bats have developed strategies that enable reliable foraging success, many modern insect groups possess traits helping them to avoid predation. Insectivorous bats must contend with insect prey that today are able to hear in the ultrasonic frequency range and use such acoustic information to avoid predation (Hoy et al., 1989; Miller and Surlykke, 2001; Roeder and Treat, 1965; ter Hofstede and Ratcliffe, 2016; Yager, 1999). Some insects possess specialized ears that now rapidly evoke auditory-induced behavioral changes to evade bat predation attempts (Acharya and Fenton, 1992; Miller and Surlykke, 2001). For example, praying mantids have a specialized cyclopean ear, and when stimulated with ultrasound, they initiate rapid spiral dive to avoid predation (Yager, 1999; Fig. 4.2). The echolocation calls of bats can elicit different flight behaviors from other insects, including some flying locusts, like Locusta migratoria will steer away from the ultrasonic pulses emitted from hunting bats (Robert, 1989; Fig. 4.2). The green lacewing Chrysoperla rufilabris has the smallest known tympanal hearing organ located on their wings

FIGURE 4.2 Illustration of insectivorous bat’s stereotypic echolocation capture sequence as it pursues insect prey. The bat begins in the search phase, emitting widely spaced calls to detect the presence of a potential prey. Once the bat detects its prey, it enters the approach phase, where time between calls shortens as the bat orients toward the prey. As the bat closes in on a prey item, it emits a rapid succession of calls in the terminal buzz phase. Many insects now possess counter strategies to avoid predation. Green lacewings (A) initially turn nondirectionally in response to an approaching bat, but when the bat enters the terminal buzz phase, they dive down rapidly. Preying mantids (B) respond to predatory bat calls by initiating a rapid spiral dive. Locusts (C) steer directly away from the direction of the echolocating bat to avoid capture.

Auditory signals and ecological niche

which is sensitive to the echolocation calls of bats. When this organ is stimulated with sound frequencies consistent with the approaching echolocation calls of bats, direct connections to the flexor flight muscle from this organ can trigger a rapid folding of the wings, causing the insects to stop flying and fall (Miller, 1975, 1971; Fig. 4.2). These insects will resume flight once they no longer detect the frequencies of bat echolocation calls (Roeder, 1962). Bat signals at low repetition rates and low intensities elicit a more passively turning, nondirectional response, but as the bat increases repetition rate and enters the terminal buzz phase, the insect flips open its wings and drop suddenly, reducing the success rate of predatory bats (Miller, 1982; Miller and Olesen, 1979; Miller and Surlykke, 2001). In addition to sonar-triggered flight evasion, some insects produce ultrasound clicks to undermine the success of echolocating predators. The clicks sometimes elicit startle reflexes in some naı¨ve bat species (Bates and Fenton, 1990). Some arctiid moths generate clicks in similar frequency ranges to the echolocation calls of hunting bats, suggesting the possibility that the moth clicks interfere with the bat’s ability to process returning echoes, or even misperceiving these clicks as returning echoes (Fullard et al., 1979). The tiger moth Bertholdia trigona produce clicks in response to bat echolocation calls, which seem to disrupt the big brown bat’s ability to successfully intercept prey (Corcoran et al., 2009). When bats hear tiger moth ultrasonic clicks, they increase call durations and pulse intervals, likely to contend with multiple sound streams (Corcoran et al., 2011). Click bursts from other species of tiger moth, such as Phragmatobia fuliginosa, interferes with bat performance in distance discrimination tasks when clicks arrive close in time to echoes (Miller, 1991). Some moths have evolved a vastly different strategy to combat hungry bats. The scales of a group of moths without ultrasonic hearing sensitivity can apparently function as a sound absorber (Neil et al., 2020). The thorax scales of these moths might decrease bat sonar detection range, creating a form of acoustic camouflage that can help these insects avoid predation (Neil et al., 2020). To counter predator evasion used by hearing insects, some have speculated bats have evolved a variety of behavioral strategies (Miller and Surlykke, 2001; for an alternative perspective see Barber and Ratcliffe, this volume). One possible approach may be to use sonar call frequencies to fall above or below the hearing sensitivities of prey (Fullard, 1998), though these frequency shifts come with distinct tradeoffs. For example, Tadarida teniotis forage for relatively large flying insects that hear ultrasound and make use of relatively low echolocation frequencies (11e12 kHz), suggesting they call at sound frequencies outside the auditory range of their prey (Rydell and Arlettaz, 1994). However, lower frequency calls do not reflect as well from small insect prey, rendering them undetected by bats operating with echolocation calls in the audio range. Another strategy observed in Barbastella barbastellus is “stealth echolocation,” whereby bats reduce the amplitude of echolocation calls (as much as 10e100 times lower compared to other aerial-hawking insectivores) until they are position to intercept their prey (Goerlitz et al., 2010). These bats forage almost exclusively on moths, many that have high-frequency hearing sensitivities (Vaughan et al., 1997) and by reducing the amplitude of sonar calls

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they avoid detection until they are within striking distance (Goerlitz et al., 2010). There are many examples of the possible evolutionary arms races between insects and the bats that pursue them (ter Hofstede and Ratcliffe, 2016). Bats must not only employ their own tracking strategies to capture moving targets in midair but also contend with behavioral strategies that hearing insects evolved to evade capture. For a more in-depth consideration, especially with respect to the evolutionary origins versus the current utility of such traits, see Barber and Ratcliffe (this volume).

Other bat sensory systems and specializations Vision

While hearing often dominates bats’ sensory-guided behaviors, these animals also rely on other sensory modalities to negotiate natural environments and find food. The phrase “blind as a bat” is indeed misleadingdall bat species can see and many use visual cues to navigate, avoid obstacles, and forage. Bats that feed on insects tend to have smaller eyes compared to bats that primarily forage for fruit or slow-moving targets, though there are no bats that do not have at least some vision when light is available (Thiagavel et al., 2018). Larger eyes in echolocating fruit bats suggest that vision supplements sensory information gained through hearing. Species in the family Pteropodidae largely do not echolocate (except for one genus Rousettus, described above) and instead rely on vision and olfaction to find food. One study compared the spatial resolving power and features of the retinal ganglion cells (RGCs) of four different bat species, one laryngeal insectivore, and three frugivorous Pteropodidae. Of the three Pteropodidae species, two were nonecholocators and one was the lingual echolocator R. aegyptiacus. The laryngeal echolocator, Daubenton’s bat, Myotis daubentoniid, showed lower spatial resolution and fewer RGCs than the Pteropodidae species (Cechetto et al., 2020). Notably, there was some evidence to suggest that of the three Pteropodidae species, the two nonecholocators had slightly higher spatial resolving power compared to R. aegyptiacus (Cechetto et al., 2020). M. daubentonii is a trawling bat and remarkably showed evidence of dorsal specializations of the retina that may aid in effectively orienting close to the surface of water (Cechetto et al., 2020). This fascinating work reveals how much there is still to learn about the contribution of vision to the orienting and foraging behaviors of both echolocating and nonecholocating species of bats. Vision can be particularly useful for long distance navigation, due to the far greater operating range of vision than echolocation in air. Egyptian fruit bats R. aegyptiacus use vision, echolocation, and possibly olfaction to navigate and forage (Danilovich et al., 2015; Danilovich and Yovel, 2019; Sa´nchez et al., 2006). Lingual echolocating Egyptian fruit bats commute as much as over 100 km in a single day, navigating to food resources from their roosts and back home. Interestingly, when Egyptian fruit bats were displaced kilometers away from an original location, they were still able to home directly to a familiar fruit tree or their roost

Other bat sensory systems and specializations

(Tsoar et al., 2011). Further, when Egyptian fruit bats were released into a deep natural crater that disrupted access to visual cues, they initially had difficulty orienting out of the crater but eventually found their way back to their goal (Tsoar et al., 2011). These results support a compelling idea that Egyptian fruit bats use vision to selftriangulate their position relative to landmarks for large-scale navigation. The laryngeal echolocating greater spear-nosed bat, Phyllostomus hastatus, similarly migrate over long distances, and while they can effectively navigate in familiar environments with echolocation alone, blindfolded bats were unable to home effectively once they exceeded a distance of 15e20 miles (Williams et al., 1966). Because high-frequency sounds attenuate rapidly (Lawrence and Simmons, 1982), echolocation is insufficient for long-distance navigation, and visual cues are necessary to perform this task. For shorter range tasks, visual cues can complement echolocation. In the laboratory, Egyptian fruit bats increase the rate and intensity of their clicks as light level decreases (Danilovich et al., 2015). Interestingly, when Egyptian fruit bats prepared to land under high-light levels, they produced clicks at rates comparable to the dark, suggesting that even when visual information is available, distance cues gleaned from returning echoes are still important for landing (Danilovich et al., 2015). Subsequent studies of Egyptian fruit bats have further shown that vision and echolocation are weighted for performance in different tasks. In a series of experiments testing the interaction between vision and echolocation, researchers found that Egyptian fruit bats flexibly shift between these two modalities when navigating, with visual cues driving spatial navigation direction and echolocation guiding obstacle avoidance (Danilovich and Yovel, 2019). However, some tasks seem to depend largely on vision alone. When presented with three-dimensional objects, Egyptian fruit bats were able to discriminate these objects using vision, but most were unable to perform the same task using echolocation alone (Danilovich and Yovel, 2019), suggesting that for these bats, vision is a dominant sense that works in conjunction with echolocation under certain lighting conditions. For bats that are naturally active in both light and dark conditions, such as the Mexican free-tailed bat, Tadarida brasiliensis, access to visual information can affect echolocation behavior (McGowan and Kloepper, 2020). When T. brasiliensis flew into a cave or in an open field during the night compared to the day, their calls were broader in bandwidth and shorter in duration, acoustic features that would yield higher sonar localization accuracy. By contrast, during the day when visual cues were available, T. brasiliensis produced long duration, narrowband calls, suggesting a shift in the animal’s relative reliance on vision and echolocation (McGowan and Kloepper, 2020). Visual cues likely provide additional information that can aid bats in their natural behaviors and are likely to work in tandem with echolocation to guide navigation to food sources. For example, the Geoffroy’s tailless bat, Anoura geoffroyi, prefer feeding from dishes containing mealworms offered in light compared to dishes in the dark (Eklo¨f and Jones, 2003). These bats were presented with Petri dishes in four possible combinations, lit area with mealworms uncovered (providing both

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visual and sonar cues), lit area with mealworms covered by a Petri dish lid (providing visual cues only), dark area with mealworms (sonar cues only), and dark area with mealworms covered by a Petri dish lid (no cues other than from the dish itself). Results showed a higher number of attempts to feed in lit conditions, regardless of if sonar cues were available. Interestingly, these bats made more attempts at foraging when visual cues only were available compared to acoustic cues only. An additional experimental control with a Petri dish containing mealworms and one without worms in light conditions showed that the bats approached the dish with worms significantly more than the empty dish. This additional experiment confirms that the structure of the dish itself did not attract the bats in light, and they were explicitly approaching for the food reward. These results suggest that Geoffroy’s tailless bat uses echolocation for general navigation, but vision may sometimes be necessary for food detection. It is worth noting that passive listening information may have been available to the bats in all sensory conditions of this experiment, as movements by the mealworms may have generated detectible sounds, which could further aid the bats’ approach to the dishes. There is also evidence that in some instances visual input can have deleterious effects on bat navigation behaviors. The Indiana bat, Myotis sodalis, was less likely to crash into light-transmitting windows when blindfolded than when vision was available (Davis and Barbour, 1965). The authors argue that in this case, visual feedback from a clear window carried more weight than echolocation feedback, which led bats to crash into windows when visual cues were available. It is also possible that the bright light evoked general disorientation in the bats, which interfered with their ability to use echolocation. Other studies have reported increased collisions under lit conditions, suggesting that visual information may interfere with natural orienting behaviors (Orbach and Fenton, 2010). Studies in natural field conditions have also shown that light affects the behavior of echolocating bats. For example, McGuire and Fenton (2010) found that the small brown bat, Myotis lucifugus, was less likely to fly and more likely to crash in a lighted area compared to the same area in the dark. At the same time, M. lucifigus reduced the time intervals between calls when flying in lit areas, suggesting that the bats responded to echoes from the environment or the brightness of the light was disorienting. Interestingly, research also shows that visual cues can enhance bat navigation and obstacle avoidance. One such study compared two groups of M. lucifugus, one with an auditory impairment and one with normal hearing, navigating a virtual string maze. This study reported that bats were most successful in dim but not bright lighting. Further, bats in the bright light condition collided the most, even more than when the bats were in total darkness (Bradbury and Nottebohm, 1969), indicating that light levels can affect bat orientation. Specifically, deficits in behavioral performance may be due to high-light levels, and lower light levels may improve performance. There is further evidence that vision can enhance obstacle avoidance in insectivorous bats. In a laboratory study, Eptesicus fuscus trained to perform an obstacle

Other bat sensory systems and specializations

avoidance task using different sensory modalities. The obstacle was either visual (a laser beam), echoic (physical object) or visual-echoic (light surrounding an object). E. fuscus detected and avoided obstacles more frequently when both visual and acoustic cues were present, compared to single modality conditions. Interestingly, in the visual only condition, the bats did not respond to the laser as an obstacle and flew through the beam but still decreased the proportion of entrances (Jones and Moss, 2021). This, along with separate psychophysical data, demonstrates that the bats detected the laser’s presence. These studies offer evidence that visual and acoustic cues can enhance performance in obstacle avoidance tasks, though there is still much to further investigate how these modalities function together in echolocating bats.

Olfaction Foraging. Olfaction, much like echolocation, is a sensory system that is well suited to the low-light levels in which bats operate. Fruit and flowers dispersed or pollinated by bats often produce strong olfactory signals (van der Pijl, 1957), suggesting the importance of these cues for frugivorous bats to find food and determine ripeness. Frugivorous bats can discriminate between different odor sources when selecting their food, even preferentially selecting based on ripeness, indicating the importance of this modality for these bats (Korine and Kalko, 2005; Laska, 1990). One study using mist nets scented with varying levels of fruit odor reported that bats (particularly species in the genus Artibeus) were more likely to be caught in stronger scented nets compared to controls (Rieger and Jakob, 1988), indicating that these bats may be attracted to the scent cues to find their food. However, frugivores also employ echolocation for gathering fruit (Kalko and Condon, 1998), suggesting that while odor cues can be key for many species, echolocation is still a vital system for effectively navigating and foraging. Both modalities together likely enhance localization efficacy for bats foraging for odor-producing food resources. Some bat species flexibly shift between echolocation and olfactory modalities to locate and acquire fruit efficiently. Seba’s short-tailed fruit bat, Carollia perspicillata, and the chestnut short-tailed bat, C. castanea, show consistent foraging behaviors: initially orienting and detecting ripe fruit using odor cues and then shifting to echolocation for fine scale localization during the approach to fruit (Thies et al., 1998). Nectivorous bats show similar behavior, when targets with varying combinations of acoustic and olfactory cues are presented to the lesser long-nosed bat; Leptonycteris yerbabuenae most often approached targets with both cues available but showed no preference between olfaction and echolocation when cues were isolated (Gonzalez-Terrazas et al., 2016). These results suggest that when both olfactory and acoustic cues are available, the two sensory modalities enhance target detection and localization. The interaction between olfaction and echolocation can also shape the behavioral search strategies that bats employ. When the Jamaican fruit bat, Artibeus jamaicensis, performs an odor localization task, they can locate a target through olfactory cues, sample potential odor sources serially, and even continue to echolocate

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through the nostrils while using olfactory cues to orient (Brokaw et al., 2021). In this task, olfactory plumes are used to assist in locating food rewards and shapes search behaviors. Olfaction can provide supplemental information about the general location of scent producing food resources as well as information about their ripeness, which can work in conjunction with echolocation to shape foraging behaviors. Social communication. Olfactory information can also play a key role in social behaviors. Many species of bats are highly social, living in colonies ranging from dozens to thousands. Olfactory cues can carry a variety of information, from signals about mating and reproductive status to information about viable food sources. The tent-making bat, Uroderma bilobatum, can use the scents present on conspecific nest mates to acquire preferences for novel food resources (O’Mara et al., 2014). By detecting the odor cues of another bat that successfully foraged, these bats can identify the same scent in a novel food source, efficiently transferring useful information across conspecifics. One species of bat that relies extensively on scent cues for communication is the sac-winged bat, Saccopteryx bilineata. This Central and South American bat species is distinctive and named for the sacs located on the propatagium, which are filled with secretions from the genitals, urine, and saliva (Voigt and von Helversen, 1999). Saccopteryx often have harem territories with a hierarchical structure of few dominant males and a larger number of females. To attract females, dominant harem males also hover in front of females, wafting the scent from their sac in an energetically costly display, with larger harems having a higher number of these hovering displays (Voigt et al., 2001; Voigt and von Helversen, 1999). The harem males use scent cues to threaten or ward off other males, occasionally even hovering in front of other males to waft the scent from their sacs to mark their territory and prevent these males from mating with females (Bradbury and Emmons, 1974; Bradbury and Vehrencamp, 1976). Non-territorial males have even set up peripheral groups that overlap with established harem groups and cue for hierarchically established access to a harem (Voigt et al., 2001; Voigt and Streich, 2003). The behaviors that enable the maintenance of Saccopteryx harems (e.g., display behaviors, hovering, etc.) can be metabolically costly and are factored into the energetic budget of the harem males (Voigt et al., 2001). Interestingly, olfactory cues are not the only form of communication for Saccopteryx. In addition to the importance of scent, territorial songs seem to be key for the reproductive success of these bats, with males having higher reproductive success with more territorial songs performed per day (Behr et al., 2006). Male singing, in this case, appear to enhance the olfactory information for both mating and territorial displays, again showing that bats often integrate information carried by multiple sensory modalities to carry out natural behaviors. The bat’s use of olfactory communication for sharing information about food resources among conspecifics is an open area of research.

Thermoreception In addition to echolocation, passive listening, vision, and olfaction, some bats have evolved other sensory specializations that support foraging behaviors. The common

Other bat sensory systems and specializations

vampire bat Desmodus rotundus is one such notable species that consumes blood meals, primarily from ungulates. With the need to detect prey and select locations to feed from larger animals, D. rotundus have evolved temperature sensitive pits with specialized cold and heat receptors found within in the central nose leaf (Ku¨rten et al., 1984; Ku¨rten and Schmidt, 1982). Behavioral experiments reveal D. rotundus can detect the radiation of human skin up to about 13 cm (Ku¨rten and Schmidt, 1982). Remarkable work on the mechanisms that support this sensory system have revealed that vampire bats have large diameter neurons in the trigeminal ganglia, similar to those observed in pit-bearing snakes (Gracheva et al., 2011). Further, genetic specializations within a heat-sensitive channel (TRPV1) within the trigeminal ganglion enable this thermal detection in vampire bats and offer interesting comparisons across species for thermosensation (Gracheva et al., 2011). This exotic sensory mechanism is a testament to the extraordinary specializations some bat species have evolved to occupy a wide array of ecological niches.

Airflow sensing for flight control As the only mammals capable of self-powered flight, bats reveal mechanosensory specializations that enable agile maneuvers in foraging flights. Bat wings contain five digits covered with a thin, highly flexible anisotropic membrane (Swartz et al., 2007). Bats, unlike most mammals, lack glabrous skin and have hair covering their entire bodies, including the wings. On bat wing and tail membranes, there are microscopic mechanosensory hair on both the dorsal and ventral sides (Boublil et al., 2021; Kang and Reep, 2013; Maxim, 1912). These microscopic sensory hair innervate tactile receptors, including lanceolate receptors and Merkel cell neurite complexes (Marshall et al., 2015). Bat wing hair are thought to convey mechanosensory information guiding a variety of behaviors, including handling of food and cradling of young. Experimental removal of wing hair also affects flight control. In two species of echolocating bats, E. fuscus and Carollia perspicillata, bats flew at higher velocities and took wider turns to avoid obstacles after wing hair was removed (Sterbing-D’Angelo et al., 2011). Further, electrophysiological recordings in the primary somatosensory cortex reveal encoding of airflow direction, with preferential firing for reversed airflow, characteristic of vortex shedding that signals stall (Sterbing-D’Angelo et al., 2011, 2017; Sterbing-D’Angelo and Moss, 2014). These findings suggest that wing hair provides sensory feedback for airflow sensing and stall detection. Air puffs on the wing evoked sparse temporal onset responses, suggesting the importance of timing for detecting and coordinating motor responses to airflow patterns in flight (Marshall et al., 2015). Future work can shed light on mechanosensing in the context of a wide range of natural bat behaviors. A bat’s habitat and foraging niche are also tied to wing morphology, which influences maneuverability and speed. Species that hunt in open fields tend to have longer, pointed wings with high aspect ratios that support speed and agility, whereas bats that navigate dense forests show shorter and rounded wings, lower wing-

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loading, and aspect ratios to enable high maneuverability (Aldridge, 1986; Norberg and Rayner, 1987).

Conclusion Bats occupy a wide variety of habitats and ecological niches, making them powerful animal models to understand sensory system functions and specializations. Many bat species echolocate to carry out survival tasks, from navigating complex environments to localizing small moving prey. Bats exhibit a high degree of control over the spectro-temporal features of echolocation calls and directional aim of the sonar beam, which aids them in finding food in cluttered and noisy settings. In addition, passive listening complements active echolocation in some foraging tasks. Bats are equipped with other sensory systems that support diverse foraging behaviors. Many bat species are active at dusk and rely on vision for foraging. Even under low-light conditions, bats can use vision for long distance navigation. Olfactory cues play important roles in food localization and assessment, along with social communication for mating, marking territory, and sharing information about food sources. Bats exhibit agile flight to forage, and mechanosensensory wing hair carries information about airflow that enable skilled maneuvers. Some bat species have specialized sensory systems to detect heat generated by warm blooded animals to aid in locating blood food sources. Sensory systems in bats have evolved to permit access to a broad array of food resources, yielding a dazzling display of natural foraging behaviors.

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CHAPTER

Foraging strategies of echolocating bats

5

Hans-Ulrich Schnitzler, Annette Denzinger Animal Physiology, Institute for Neurobiology, University of Tu¨bingen, Tu¨bingen, Germany

Introduction Bats (Chiroptera), an order containing nearly 1400 species, represent almost a quarter of all extant mammals (Wilson and Mittermeier, 2019). Nearly 1200 of these species use laryngeal echolocation for spatial orientation and prey acquisition. Echolocation and the ability to fly are the most important driving forces for the enormous adaptive radiation of echolocating bats into a multitude of terrestrial and aquatic foraging habitats that offer a wide variety of resources. Many species are animalivorous, and their prey often take counter measures to avoid predation. Insectivorous species (about 70%) capture flying prey or prey sitting or moving on surfaces or drifting on water. Carnivorous species prey on small mammals, birds, lizards, frogs, and fish. A few sangivorous species take blood from mammals and birds. Phytophagous bats forage for stationary food like fruits and flowers with nectar, which are advertised by specific scents and reflective properties. Bats have evolved different foraging strategies to efficiently explore these habitats and exploit their highly diverse food sources (Fenton, 1990; Denzinger et al., 2018). The foraging strategies reflect species-specific constraints and depend on what bats know about their potential prey (food predictability determines commuting, search and social foraging behavior), on the site where they forage (foraging habitat), on the motor and sensory constraints set by the clutter conditions in their foraging habitat (habitat type), on how they find and acquire their food (foraging mode), and to a lesser degree, on what they eat (diet). For a better understanding of these factors, we first clarify the terms we use to describe the foraging strategies of echolocating bats.

Commuting behavior, search behavior, and social foraging Bats possess an excellent memory and can recall where and when to fly to their foraging habitats to search for a specific food type (Genzel et al., 2018; Prat and Yovel, 2020). Commuting behavior comprises the flight movements from the roost to the foraging areas and between them. Search behavior describes the search move-

A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.16003-6 Copyright © 2024 Elsevier Inc. All rights reserved.

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ments at the foraging areas, which depend on the predictability of the food resources and differ according the previous knowledge on the nature of the potential prey, on its behavior, and on its position in the foraging habitat. Social foraging describes how opportunistic or in some cases maybe even coordinated information transfer between foraging bats affects search and commuting behavior (for review see EgertBerg et al. (2018), Gager (2019), Kohles et al. (2022)).

Foraging habitats With the exception of polar and highly mountainous regions, foraging bats search for prey in many biotopes such as marshes, woodland, farmland, gardens, urban areas, parkland, ponds, and rivers. These biotopes are the living places of specific assemblages of plants and animals which offer potential food for foraging bats (Denzinger and Schnitzler, 2013). In the literature, the term “habitat” is used synonymously with the term biotope and describes the places where bats live, move, and forage. Foraging habitats offer the specific food which a species needs for survival but often do not reflect the tasks foraging bats have to perform in order to find and acquire the species-specific food. For instance, in the foraging habitat “woodland,” insect prey can fly above, within, or below the canopy of trees or can sit on leaves, trunks, or move on the ground, and the aerospace over water of the habitat “pond” offers insects drifting on the water surface as well as prey flying high up above. The exploitation of these spatially distinct resources requires different sets of motor, sensory, and cognitive adaptations, which have implications on the applied foraging strategy. Therefore, we classify the many foraging habitats of bats by considering the clutter conditions at the foraging site where bats search for food. According to the motor and sensorial task which has to be performed by a foraging bat, we discriminate three habitat types that differ in the acoustic constraints for echolocation and the motor challenges for flight.

Habitat types The habitat type classifies sites in a foraging habitat where species search for their species-specific food according to clutter conditions. Similarity in clutter conditions with respect to distance between bat, prey, and background results in shared constraints on the sensory and motor systems of a foraging bat (Aldridge and Rautenbach, 1987; Fenton, 1990; Neuweiler, 1989; Schnitzler and Kalko, 2001; Schnitzler et al., 2003). Bats are considered to be foraging in the habitat type open space if they do not react to far-off background targets in their flight and echolocation behavior. Bats are foraging in edge space when they react in their echolocation and flight behavior to background targets in order to prevent masking of potential prey echoes. Bats are considered foraging in narrow space when the echoes of food items are close to, or overlap with, background echoes, thus increasing the risk of masking. In narrow space, bats have to adjust flight behavior to the near-by clutter targets in order to avoid collisions.

Constraints that shape the foraging strategies of bats

Foraging modes The foraging mode describes how bats find (sensory and cognitive aspect) and acquire (motor aspect) their food. The aerial-hawking mode is used by insectivorous bats who search for airborne prey with echolocation and catch prey with the wing, the interfemoral pouch, or sometimes with the mouth. The trawling mode is used by bats who take prey from water surfaces also under the guidance of echolocation. The gleaning mode is used by bats who pick up food items, such as animals or plant products, from surfaces. Some species glean their food while flying (flight gleaning), while others land on the substrate to acquire it (sedentary gleaning). Active gleaning means that bats use echolocation to find their food. Passive gleaning is used by bats who use other sensory cues such as prey generated sounds or scents to identify the food item which cannot be detected by echolocation, as prey echoes are masked by background clutter. The fluttering target detection mode is used by a group of about 200 highly specialized species, which emit search signals with a long component of constant frequency at a high duty cycle to sense the amplitude und frequency modulations produced by the moving wings in echoes from fluttering flying or stationary insects. These species search for prey on the wing or while hanging on a perch and use either the aerial-hawking mode to catch flying prey or the gleaning mode to catch stationary fluttering insects (Aldridge and Rautenbach, 1987; Neuweiler, 1990; Fenton, 1995; Schnitzler et al., 2003).

Constraints that shape the foraging strategies of bats Echolocation

The foraging strategies of bats are tightly linked to the constraints set by echolocation. All echolocating bats use this sensory system when searching for food and when commuting between roost and foraging sites. They continuously emit speciesand situation-specific echolocation calls, analyze the pulse-echo trains to detect, localize, and classify echo-producing targets, and actively control and coordinate sound emission and echo reception through integrated sensory and motor mechanisms (Moss and Surlykke, 2010; Corcoran and Moss, 2017). A major constraint for the evolution of foraging strategies is the prevention of masking, which hampers the basic echolocation tasks of detection, localization, and classification of targets. The undisturbed evaluation of a prey echo is only possible if it is not masked by other signals, which can be the emitted echolocation call itself or echoes from background targets. Forward-masking is produced if the emitted signal interferes with the prey echo; backward-masking occurs if the echoes from clutter targets interfere with the prey echo. In a first approximation, this is the case if the prey echo overlaps either with the emitted signal or the background echoes. The width of the overlap zones for the emitted call (signal overlap zone) and the clutter echo (clutter overlap zone) is determined by the duration of the emitted signal. The risk of masking can be reduced by a reduction of signal duration

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which diminishes the width of the overlap zones and increases the overlap free window between them (Schnitzler and Kalko, 2001; Schnitzler et al., 2003; Denzinger et al., 2016). Bats foraging under edge space conditions therefore reduce the sound duration with closer proximity to clutter targets, which results in an opening of the overlap free window (Schaub and Schnitzler, 2007a). Another main constraint for the evolution of foraging strategies is the limited operational range of echolocation. Echolocation delivers information only over rather short distances. The maximal detection distances for large mirror like targets (buildings, water surfaces, trees) range about between 42 and 63 m in open space foragers, which use loud and low-frequency search signals, and only between 3.6 and 6.0 m in bats foraging in a tropical forest with lower source levels (SL) and signal frequencies around 80 kHz (Stilz and Schnitzler, 2012). For smaller targets like insects, the maximal detection distance ranges from 8 to 11 m in open space foragers, to only 0.6e1.1 m in edge bats foraging under tropical conditions with weaker calls of high frequency. The main factors which influence the maximal detection distance are frequency of the echolocation signals, as well as temperature and humidity of the environment (Griffin, 1971; Lawrence and Simmons, 1982). The higher these three factors, the lower the maximal detection distance.

Flight morphology Comparative eco-morphological studies revealed that wing morphology correlates with habitat use (Aldridge and Rautenbach, 1987). Morphological traits that improve the maneuverability of flight such as lower wing loading and lower aspect ratio enable bats to forage with lower flight speeds in more confined spaces, whereas high wing loading and aspect ratios improve the agility and are typical for bats that forage with higher speed in more open spaces (Norberg and Rayner, 1987; Norberg, 1994; Zou et al., 2022).

Foraging strategies of bats Constraints resulting from the echolocation and motor tasks, which have to be performed by foraging bats, have shaped their foraging strategies. According to the ability of bats to find and acquire their food in differing clutter conditions, we discriminate the following strategies: Aerial hawking, trawling, active gleaning, passive gleaning, and flutter detection in animal-eating bats, and the combination of passive/active gleaning in phytophagous foragers (Denzinger et al., 2018). All of these strategies have in common that they reflect the behavior of species groups searching for food with differing foraging modes in different habitat types. Our definitions of foraging strategies therefore overlap to a large degree with the concept of bat guilds, as both approaches consider the relevance of the habitat type and the foraging mode (Schnitzler and Kalko, 2001; Schnitzler et al., 2003;

Foraging strategies of bats

Denzinger and Schnitzler, 2013, 2016; Denzinger et al., 2018). Constraints resulting from differences in prey availability also shape the search and commuting behavior of bats.

Aerial hawking foraging strategy The aerial hawking foraging strategy is applied by species that forage for airborne prey in open and edge space and that detect and localize their prey by evaluating the pulse echo sequence formed by the emitted search signal and the returning echo train (Fig. 5.1AeC and Table 5.1). These bats are attributed to the guilds of open space and edge space aerial foragers. The acoustic scene in open space consists of the emitted signal, which is then followed by the prey echo. In edge space, the prey echo is followed by clutter echoes from the background. The clutter echoes in open space are so far behind the prey echo that they play no role in the echolocation process.

FIGURE 5.1 Search and approach signals of bats foraging in different habitat types with different foraging strategies (AeH). Bats that capture flying insects under edge and open space conditions or that take an insect from the water surface, emit a distinct terminal group with buzz II (AeD), which is not present in gleaning foragers (FeH). Flutter detecting foragers keep the CF- component of their signals throughout the whole approach (E). Modified from Denzinger, A., Schnitzler, H.-U., 2013. Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats. Front. Physiol. 4, 164, p. 7, Fig. 5.

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Table 5.1 Echolocation strategies used by bats. Strategy

Aerial-hawking and trawling

Flutter detecting

Active gleaning

Passive gleaning

Acoustic scene with rustling noises

Main task Trophic niche space

Detection and localization Prey found by evaluation of pulse-echo-trains with unmasked prey echoes

Pattern recognition Prey found by evaluation of flutter pattern in echoes

Pattern recognition Prey found by evaluation of spectral/ temporal patterns in prey-clutter echo complexes (e.g., insects on leaves, fruits or flowers)

Signal type

Signal parameters highly variable, adapted to detection and localization tasks

Long CF signals with high duty cycle

Short, broadband, high frequency signals

Information on nature of prey

Limited information on nature of prey in pulse echo pairs, single glints in the echoes may allow a poor prey classification

Detailed information on nature of prey, glint pattern delivers prey specific flutter information

Spectral/temporal patterns in the preyeclutter complex to find leaves with prey, or flowers or fruits. Patterns, possibly learned, may deliver detailed information on nature of prey

a

Pattern recognition Prey found by evaluation of patterns in prey generated cues (e.g., rustling noises, courtship calls, odor) Short, broadband signals used only for spatial orientation and biotope recognition Rustling noises, odor, and courtship calls deliver specific information on nature of prey

Echolocation signal and the echo returning from prey are depicted in black, echo trains from background echoes are shown in white. Reproduced with permission from Denzinger, A., Tschapka, M., Schnitzler, H.-U., 2018. The role of echolocation strategies for niche differentiation in bats. Can. J. Zool. 96 (3), 173.

CHAPTER 5 Foraging strategies of echolocating bats

Acoustic scenea

Foraging strategies of bats

The properties of the emitted signal and environmental conditions determine the chances to detect a prey item, as well as to collect information on clutter targets in the background. In general, the maximal detection range for prey insects and for clutter targets increases with lower frequency, longer signal duration, smaller bandwidth, and higher SL and is reduced with rising temperature and humidity (Stilz and Schnitzler, 2012). The extent of the search space in which bats can detect potential prey is also determined by the structure of the echolocation calls. The search space starts at the end of the signal overlap zone where the prey echo is no more masked by the emitted search signal and ends either at the maximal detection distance or near clutter targets at the begin of the clutter overlap zone where the prey echo is masked by clutter echoes. It is limited on either side by the opening angle of the search cone. The search cone depends on the directionality of the emitted signals (Jacobsen et al., 2015) and of the pinna and gets wider with lower frequencies. Additionally, the cone can be widened by scanning movements of the head, and it has been estimated that bats can reach search cone angles of up to 150 degrees (Kalko, 1995; Seibert et al., 2013). The extent of the search spaces of aerial hawking foragers differs widely depending on the area in the aerospace where a species searches for prey. Species which forage with long-range echolocation systems only in open space far off from background targets and the ground have the largest search volume, whereas species which forage with medium-range echolocation systems in open as well as in edge space habitat types have medium-sized search volumes, and species that forage with short-range echolocation systems only under pure edge space conditions have the smallest search volumes. Pure open space aerial foragers (e.g., species of the genera Tadaria, Taphozous, Rhinopoma, Eumops) are adapted for long-range detection of sparse prey and cover large search volumes. For instance, an open space forager such as Nyctalus lepidopterus, with an assumed SL of 111 dB re 1m, a frequency of 18 kHz, a sound duration of 24 ms, and a detection threshold of 20 dB could detect a large insect with a target strength of 40 dB over a distance of maximally 11.3 m at a temperature of 20 and a humidity of 60% (Stilz and Schnitzler, 2012). In this example, the extent of the search space ranges from 4.0 to 11.3 m. The low-frequency search signals (below 30 kHz) of such pure open space foragers are often shallowly modulated, have a small bandwidth, a long duration (8e26 ms), and are emitted with large pulse intervals every second or third wingbeat (Fig. 5.1A). Very high SLs (around 106e111 dB) maximize the long-range detection of prey. In species which forage in both open and edge space (e.g., pipistrelle bats), the extent of the search space is distinctly smaller. A forager like Pipistrellus kuhlii with search signals with an assumed SL of about 106 dB, a duration of 9 ms, and a frequency of 39 kHz could detect prey within a search space ranging from 1.5 to 6 m. Bats foraging in both spaces often use mixed signals consisting of a shallowly modulated narrowband QCF (quasi-constant) component, which is preceded and/or followed by a broadband steeply downward frequency-modulated component. In Myotis species, a more shallowly modulated central part is often

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preceded and followed by a steeper modulated FM component. Search signals are mostly emitted every wingbeat, with a duration of 3e10 ms and QCF frequencies between 30 and 60 kHz (Fig. 5.1B). The SL of the signals is lowerthan in pure open space foragers. Within edge space, the duration of search signals decreases and bandwidth increases with decreasing distance to the background (Schaub and Schnitzler, 2007a). Bats flying in edge space choose flight paths tangential to the clutter producing background (Hermans et al., 2023), which has the advantage that the masking effect of the clutter echoes is reduced due to spatial unmasking (Su¨mer et al., 2009). Pure edge space foragers like some of the smaller Myotis species (Siemers and Schnitzler, 2004) and species of the genera Kerivoula and Murina (Schmieder et al., 2012) forage for prey near clutter targets and most likely never in open space. They emit short, broadband, downward frequency-modulated sweeps often starting at high frequencies (Fig. 5.1C). Their performance to detect prey in front of a clutter screen depended on the bandwidth of the very short search signals (Siemers and Schnitzler, 2004). The higher the bandwidth, the closer to background bats can detect prey. This indicates that these species operate with a search space that covers the area directly adjacent to the vegetation. After prey detection, aerial hawking bats approach the prey and react to it in their echolocation behavior with an approach sequence, which is characterized by a switch to pure downward frequency-modulated signals of broad bandwidth, and with decreasing distance to the prey by a reduction of pulse interval and duration, an arrangement of signals in groups with an increasing number of calls and a lowering of the SL. The approach sequence always ends with a distinct terminal group, the buzz, consisting of two parts. In buzz I, pulse interval is further reduced, and in buzz II, it is kept constant often at a value of about 6 ms. In some species, buzz II is also characterized by a lowering of the frequency (Fig. 5.1AeC) (Schnitzler and Kalko, 2001). In aerial hawking bats, echolocation reveals the position and the movement of prey but delivers only limited information on its nature (reviewed in Jones and Rydell (2003)). Detection is facilitated if the calls hit a flying insect in the instant when the wings are perpendicular to the impinging sound waves and produce a short amplitude peak or glint in the echo. At a wingbeat rate of 40 Hz and a duty cycle of 10%, a searching bat would perceive on average approximately 4 echoes/s, which contain a glint with an up to 20e30 dB higher amplitude as compared to the body echo from the same insect prey. The flight systems of bats foraging in open and edge space are also adapted to the preferred area in aerospace where they search for food. The further away bats forage from background targets, the narrower are the wings and the higher the wing loading and aspect ratio. Pure open space bats are agile foragers that are adapted for fast aerial hawking flight in the open, whereas pure edge space bats that are adapted to hawk for prey close to vegetation, fly slower, and are more maneuverable (Norberg and Rainer, 1987; Norberg, 1994).

Foraging strategies of bats

Trawling foraging strategy The trawling foraging strategy is applied by bat species belonging to the guild of edge space trawling foragers that fly close above the water and search for insects flying above or drifting on the surface and/or for fish which break the water surface. The signals of these species hit the water surface at an oblique angle and are reflected away. Only the target echoes are reflected back to the bat. A perpendicular echo from the water surface below the bat, the belly echo, encodes the flight height. It returns rather fast and often overlaps with the emitted signal. The acoustic scenes of trawling bats resemble (with the exception of the belly echo) the scenes of aerial foraging bats and encode the distance to the prey and, when clutter targets are nearby, also to any background targets (Table 5.1 and Fig. 5.1D). The echolocation calls of the trawling foragers are similar to that of bats foraging in edge space. Most species emit downward FM signals with peak frequencies between 30 and 70 kHz and call durations between 4 and 7 ms when flying close over water (Fig. 5.1D). Species of the genus Noctilio use a combination of pure CF signals and mixed signals where the CF component is followed by an FM component. SL vary between species, from rather low observed in Macrophyllum macrophyllum, to the very loud SLs for Noctilio leporinus that search for prey further out than M. macrophyllum (Surlykke and Kalko, 2008; Brinkløv et al., 2010). Prey detection is either hampered or impossible if clutter producing items drift on the water such as leaves or debris (Boonman et al., 1998) or if the water is turbulent or covered with ripples (Frecknell and Barcley, 1987; Rydell et al., 1999; Warren et al., 2000; Siemers et al., 2001). Piscivorous species detect either fish that jump out of the water or detect the water drops that arise when the fish breaks through the water surface. At sites where N. leporinus have been successful before, they use a statistical foraging behavior where the claws are raked through the water when no fish are jumping (Schnitzler et al., 1994). The approach sequences of trawling bats are very similar to those of aerial hawking bats and also end with a long terminal group, the buzz, consisting of buzz I and II with many tightly packed short signals (Fig. 5.1D). Bats using the trawling foraging strategy show several morphological adaptations to the trawling mode. The interfemoral pouches and the hind legs are specially designed to take prey from the water surface. Long and sharp claws are adaptations for piscivory. The wings are long and have a higher average aspect ratio than that of other edge bats but with only a moderate wing loading, allowing for slow flight over water (Norberg an Rayner, 1987; Norberg, 1994).

The passive gleaning foraging strategy of animalivorous bats Bats that encounter acoustic scenes where the echo train does not deliver sufficient information to separate prey and clutter echoes rely on other modalities to find prey.

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These bats use the passive gleaning foraging strategy and are assigned to the guild of narrow space passive gleaning foragers. Animalivorous species rely on preygenerated cues and evaluate patterns of rustling noises from moving prey (Bell, 1982, 1985) or species-specific courtship calls (e.g., Tuttle and Ryan (1981), Bellwood and Morris (1987)) (Table 5.1 and Fig. 5.1F). Rustling noises contain series of broadband clicks with frequencies from 3 up to 50 kHz (Goerlitz et al., 2008). Spectral information differs between substrates (Goerlitz et al., 2008) and prey size (Goerlitz and Siemers, 2007). Prey-generated cues deliver specific information on the nature of prey. The taxonomy of prey has basically no influence on the foraging strategy. While small narrow space passive gleaning bats almost exclusively forage for arthropods, there is a gradual transition to small vertebrates in larger species. Giannini and Kalko (2005) concluded that carnivory is merely a size-dependent extreme of animalivory and that carnivorous species are basically large versions of insectivorous bats. After landing at the passively localized site with prey, these foragers use mainly olfactory and tactile cues to pinpoint the location of prey (Kolb, 1958). Narrow space passive gleaning foragers emit short broadband signals with low SL, which are mainly used for spatial orientation (Fig. 5.1F). After getting alerted to prey-generated cues, a foraging bat will approach the prey site under the guidance of echolocation. During the approach to the landing site, bats switch to shorter signals, which are emitted in groups but without a terminal buzz (e.g., in Myotis myotis, Russo et al. (2007), Budenz et al. (2018)). Wing morphology is rather similar in all gleaning bats. Their wings are broad with low wing loading and aspect ratio, which enables slow flight and high maneuverability.

The active gleaning foraging strategy in animalivorous bats Bats that find their food with the active gleaning foraging strategy evaluate spectrale temporal patterns in the pulseeecho complex consisting of the emitted signal, the food echo, and the clutter echoes around it (Table 5.1). Active gleaning foraging in animalivorous bats has so far only been described for one species, Micronycteris microtis (Denzinger and Schnitzler, 2004; Geipel et al., 2013, 2019; Denzinger et al., 2018). This species is assigned to the guild of narrow space active gleaning foragers. It forages for stationary targets sitting on leaves such as caterpillars or dragonflies and ensonifies one leaf after another with ultra-short multiharmonic FM signals of low amplitude oblique from above (Fig. 5.1G). The acoustic echo scene resembles that of a trawling bat but on a micro scale. From an empty leaf, the bat receives an echo from the frontal part of the leaf and an echo train from the back and any objects located behind the leaf. The signals hitting the surface are reflected away. If a prey item is sitting on the leaf, it will generate an additional echo between the clutter echoes. The approach sequence is characterized by groups with more signals and shorter pulse intervals and no terminal buzz (Denzinger and Schnitzler, 2004; Geipel et al., 2013).

Foraging strategies of bats

Passive/active gleaning foraging strategy of phytophagous bats Phytophagous species, which belong to the guild of narrow space passive/active foragers, use a combination of the passive and active gleaning strategy for food finding (Table 5.1). Since plants rely on bats for seed dispersal and pollination, they advertise the position of their fruits or flowers by species-specific odor bouquets, by specific echo properties of their inflorescences and/or by an exposed position in relation to the background. Odor is the primary cue to attract bats over large distances to a food site (Rieger and Jakob, 1988; Laska, 1990; Hessel and Schmidt, 1994; Thies et al., 1998; von Helversen, et al., 2000; Mikich et al., 2003; Korine and Kalko, 2005). However, odor plumes are not suited for the precise localization of a food source because they are too diffuse. Thus, bats switch to an active gleaning foraging strategy and use echolocation for precise food localization. The detection and localization of fruits or flowers are facilitated by the plants themselves, as they advertise their presence by specific echo patterns, which are produced by specific soundreflecting structures. These patterns consist of spatially invariant echoes over wide sound angles with characteristic spectral and amplitude patterns (von Helversen and von Helversen, 1999; von Helversen et al., 2003; Simon et al., 2011; Gonzalez-Terrazas et al., 2016). Another adaptation to bat pollination is cauliflory and flagelliflory, which also improves the detection of food items in the proximity of clutter (Kalko and Condon, 1998). Passive/active gleaning foragers emit short, multiharmonic broadband signals, often with the main energy in the higher harmonics (Fig. 5.1H). A low SL reduces the clutter echoes from background targets. Signals are well suited for spatial orientation and the echolocation-guided approach to a stationary food site. The sound pattern during the approach is similar to that of all other gleaners and is characterized by groups with more and shorter signals but without a buzz (e.g., Carollia perspicillata in Thies et al. (1998)).

Flutter detecting foraging strategy About 200 species of echolocating bats use the flutter detecting foraging strategy. These species have highly specialized echolocation systems to find and catch fluttering insects mainly in the highly cluttered situations of narrow space (reviewed in Schnitzler and Denzinger (2011), Fenton et al. (2012)). This strategy is used by species of the closely related rhinolophids and hipposiderids of the Old World and also by a phylogenetically very distant mormoopid bat of the new world, Pteronotus parnellii (Schnitzler, 1968, 1970; Gustafson and Schnitzler, 1979). These species all belong to the guild of narrow space flutter detecting foragers. These species emit echolocation signals at high duty cycle consisting of a long constant frequency (CF) component followed by a short downward frequencymodulated (FM) terminal part with the highest amplitude in the second harmonic (Fig. 5.1E). According to the high duty cycles of their echolocation signals, this special group of bats has also been classified as “high duty cycle bats” (Neuweiler and Fenton, 1988; Fenton, 1995).

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Echoes from fluttering insects contain modulations in the rhythm of their wingbeats such that prey echoes can be discriminated from unmodulated clutter echoes (Table 5.1). A short amplitude peak or glint (1e3 ms) with an amplitude of up to 20e30 dB above the body echo is produced at every wingbeat when the reflecting wing is perpendicular to the imping sound wave. Doppler shifts caused by the wing movement in the instant of glint production produce a corresponding spectral glint, which can reach a widening of the carrier frequency of several kHz (Schnitzler, 1987). When flying, flutter detecting foragers lower the emission CF so that the echo CF is kept constant at a reference frequency, thus compensating for Doppler shifts produced by the forward movement in the echoes from targets ahead. The auditory system of flutter detecting foragers is characterized by an auditory fovea, a highly expanded frequency representation in the cochlea at frequencies around the reference frequency. Foveal centers in the ascending auditory pathway contain many sharply tuned neurons, which are specialized to decode the glint pattern in insect echoes with CF carrier frequencies near the reference frequency. These echoes from fluttering insects contain information on wingbeat frequency, wing structure, wingbeat type, as well as wing length and size (Kober and Schnitzler, 1990). Field and psychophysical studies indicate that flutter detecting foragers use the echo information for the classification of their prey, as well as for selective foraging (Koselj et al., 2011). All flutter detecting foragers react to fluttering targets with an increase in duty cycle, which also indicates the relevance of flutter information. Search behavior differs between species, with some species searching for prey in continuous search flights, while others by scanning the environment from perches or using both behaviors. After detection, these species catch either flying insects in the aerial hawking mode or stationary fluttering insects sitting on surfaces in the active gleaning mode (for literature see Schnitzler and Denzinger (2011)). Flutter detecting foragers also reduce pulse interval and sound duration during the approach but emit their typical CF-FM signals throughout the whole approach sequence (Fig. 5.1E). The explanation for this difference may be that flutter detectors not only determine the exact target position with the FM component but also use the CF component to collect information on the relative speed between the bat and target. They may also use glints to determine the position of the prey through directional hearing (Vanderelst et al., 2015). These species generally have broad wings with low wing loading and aspect ratio that are adapted to forage under narrow space conditions (Norberg an Rayner, 1987; Norberg, 1994).

Species using more than one strategy Many species are not restricted to a single foraging strategy. A switch between foraging strategies is common in trawling foragers, which also employ the aerial hawking strategy to catch insects flying under edge space conditions, and has been reported for both Noctilio species (Brooke, 1994; Kalko et al., 1998) for Myotis daubentonii (Jones and Rayner, 1988), and for Macrophyllum macrophyllum

Search and commuting behavior of foraging bats

(Weinbeer et al., 2013). Some edge space foragers not only search for airborne prey but also glean insects from substrates in flight, for instance, Myotis evotis (Faure and Barclay, 1994), Myotis lucifugus and M. septentrionalis (Ratcliffe and Dawson, 2003), Myotis emarginatus (Krull et al., 1991), and species belonging to the genus of Murina and Kerivoula (Liao, 2013), which also catch spiders. A switch between passive gleaning and aerial hawking is described for Myotis myotis (e.g., Arlettaz (1996)), Cardioderma cor (Vaughan, 1976), and Otonycteris hemprichii (Hackett et al., 2014). Insect remains have been found in the feces of nectar- and fruiteating bats, suggesting that they are also able to use the aerial hawking strategy (Herrera et al., 2002; Clare et al., 2014).

Search and commuting behavior of foraging bats The foraging behavior of bats does not only depend on the constraints set by their echolocation and motor abilities but also on what bats know about their food. The previous knowledge on the nature of the potential prey, on its behavior, on its position in the foraging habitat, and especially on its predictability shape a forager’s search and commuting behavior. The search behavior and the movement patterns of foraging bats strongly depend on whether they forage for predictable or for ephemeral prey (Egert-Berg et al., 2018). Furthermore, bat movements also depend on whether they forage for moving or stationary food and whether they search on the wing or from a perch. When commuting to and between foraging sites and when searching for food, foragers may encounter conspecifics or members of other foraging bat species. These encounters may be accidental, or may be intentional, as a way to receive social information that can influence the pattern of movement and foraging success (Voigt et al., 2017). Kohles et al. (2022) propose a conceptual framework to describe different strategies for social information transfer that can increase the foraging success. Following behavior where food cues from successful foragers lead conspecifics to food patches results from an opportunistic use of social information in the roost. Local enhancement is another form of opportunistic information transfer where the monitoring of the feeding behavior of others helps to find previously unknown food patches. Group facilitation is described as an intentional information transfer, where a coordinated group forages using a sensory network. Recruitment is another form of coordinated information transfer where intentionally emitted social signals of successful foragers are used to attract additional foragers.

Search behavior and social foraging in bats feeding on predictable prey Sites with predictable food are spatially restricted areas, which are anchored by landmarks in the home range of bats. Bats often stay for a longer time at a site with predictable food, and they often visit more than one foraging site during their

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nightly search for food. They often return to the same foraging site in consecutive nights and forage with a similar search pattern as in previous nights. Typical examples are edge space foragers that circle around lights or exploit a gap, phytophagous species that return to fruiting or flowering trees, and perch hunters that have a set of preferred perches, which they regularly utilize. A study by EgertBerg et al. (2018) showed that M. myotis returned to the same site at consecutive nights, even flying back and forth on nearly the same flight trajectory (Fig. 5.2A), and N. leporinus and Myotis daubentonii returned with high spatial precision to feeding sites where they had been rewarded in previous nights with mealworms (unpublished own observations). The nectar-feeding bat Glossophaga commissarisi relied primarily on spatial memory to return to locations they have experienced as profitable (Thiele and Winter, 2005). Many species show stereotyped search patterns at the foraging sites. N. leporinus foraged at several consecutive nights with stereotyped search loops, which were centered at the light of a boat house attracting swarms of small fish (Fig. 5.2D) (Schnitzler et al., 1994). Stereotyped search behavior was also found in Eptesicus fuscus, which foraged in open space conditions (Hulgard et al., 2016). Perch hunting is another strategy to search for predictable prey. It is found in some species using the flutter detection foraging strategy and also in some passive gleaning foragers like Cardioderma cor (Vaughan, 1976), Megaderma lyra (Audet et al., 1991), Lophostoma silvicolum, and Trachops cirrhosus (Kalko et al., 1999) who listen from favorite perches for prey-generated sounds. Bats searching for predictable prey usually forage alone (Egert-Berg et al., 2018); however, this does not exclude that such bats might find a profitable foraging site by opportunistic use of social information. Eavesdropping, which can result in local enhancement, is a common strategy of many species. These bats monitor the behavior of other bats by overhearing both their echolocation and their social calls. These signals can be detected over far larger distances than prey echoes (Kohles et al., 2022). The switch from search to approach sequences in a bat nearby reveals the detection of prey, and especially, the terminal group of the approach, the buzz, indicates that the other bat is attempting a prey capture. Playback experiments with search, approach, and buzz sequences show an intra- and interspecific attraction to approach sequences (reviewed by Gager (2019), Kohles et al. (2022)). A special form of eavesdropping behavior has been observed in Eptesicus bottae that forage for moths, which react with evasive movements to capture attempts. Stroboscopic photos of foraging bats show that the pursuit of a moth by the first bat attracted other conspecifics, which directed their pursuits to the path of the escaping moth (unpublished data, Fig. 5.3). The eavesdropping behavior of Lasiurus borealis (Balcombe and Fenton, 1988) most probably reflects a similar strategy. When prey items are rare, eavesdropping may lead to competition and might reduce the foraging success of a resident, resulting in agonistic behavior against an intruder. Territorial behavior has been shown for P. pipistrellus foraging at

Search and commuting behavior of foraging bats

FIGURE 5.2 Commuting and search behavior in three species of bats. (A) Commuting flights between foraging sites (red dots) and the roost (black pentagon) in individual Myotis myotis and Myotis vivesi over consecutive nights. M. myotis commuted directly to a few familiar sites with predictable prey and returned to those locations, whereas M. vivesi covered large areas over the Sea of Cortes to find unfamiliar foraging sites with assumed ephemeral and clustered prey. (B) Two Myotis vivesi encountered many conspecifics (black dots) when moving between foraging sites (red dots). This may indicate that they are flying together in a group. (C) Trajectory of a foraging flight of Myotis vivesi from the roost to the foraging area and back (left side), and a close-up of the trajectories in the foraging area (right side). Despite the emission of buzzes during the flight to the foraging area, this section was classified as commuting, as turning movements and a reduction of flight speed are missing. (D) Schematic search flight loops of a Noctilio leporinus foraging for small fish, which congregated due to an attraction to the light of a boat house. The site was occasionally passed by groups of two to five individuals but was occupied by a single male. (A) Modified from Egert-Berg, K., Hurme, E.R., Greif, S., Goldstein, A., Harten, L., Herrera, M., et al., 2018. Resource ephemerality drives social foraging in bats. Curr. Biol. 28, 3670, Fig. 1A; (B) Modified from EgertBerg, K., Hurme, E.R., Greif, S., Goldstein, A., Harten, L., Herrera, M., et al., 2018. Resource ephemerality drives social foraging in bats. Curr. Biol. 28, 3671, Fig. 2A; (C) Modified from Hurme, E., Gurarie, E., Greif, S., Herrera, L.G., Flores-Martı´nez, J.J., Wilkinson, G.S. et al., 2019. Acoustic evaluation of behavioral states predicted from GPS tracking: a case study of a marine fishing bat. Mov. Ecol. 7, 11, Fig. 5A and B. (D) Modified from Schnitzler, H.-U., Kalko, E.K.V., Kaipf, I., Grinnell, A.D., 1994. Fishing and echolocation behavior of the greater bulldog bat, Noctilio leporinus, in the Field. Behav. Ecol. Sociobiol. 35, 330, Fig. 1.

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FIGURE 5.3 Opportunistic eavesdropping behavior in Eptesicus bottae foraging for an insect that escaped with evasive flight movements. The stroboscopic exposures of three bats (white, yellow, and blue paths and numbers) and an escaping insect (red locations and numbers) are produced by flashes, which were triggered every 40 ms. The 2nd, 10th, 19th, and 26th trigger pulse did not release a flash thus producing a pattern, which encodes the flight direction of the animals. Synchronized sound recordings were of low quality but still allowed a rough correlation between the flight and echolocation behavior of the bats. We interpret the scene as follows: Approach signals which were recorded about 400 ms before the first exposure indicate that Bat 1 (white) was already pursuing the insect and may have attracted Bat 2 (yellow) and Bat 3 (blue) to the foraging site. Approach and buzz signals from exposure 1 to 11 and the posture of Bat 1 at exposure 11 and 12 indicate that Bat 1 made a capture attempt but missed the escaping insect. Bat 2 reacted at exposure 9 to the approach and buzz signals of Bat 1 with a turn toward the activity area that included the escaping insect. After detection of the insect, Bat 2 pursued it and emitted, between exposure 18 and 21, both approach and buzz signals. The capture attempt at exposure 22 was unsuccessful, and the insect escaped with high speed between exposure 25 and 28. Exposure 20e27 of Bat 1 may indicate that this individual made another attempt to catch the escaping insect. Bat 3 reacted to the approach behavior of Bat 2 between exposure 18 and 21 with a distinct turn toward the action area but was too late for a capture attempt.

streetlights where a resident defended his feeding territory against an intruder with chasing flights and the emission of agonistic social calls (Go¨tze et al., 2020). Territorial behavior was also observed in N. leporinus who defended a feeding site against conspecifics (own observation). Another opportunistic social foraging strategy to find a new foraging site is the following behavior in phytophagous bats, where roost members may follow a successful forager, which signals by its odor that it has found ripe fruits (reviewed by Gager (2019), Kohles et al. (2022)).

Search and commuting behavior of foraging bats

The only coordinated foraging strategy in species that forage for predictable prey was reported for Phyllostomus hastatus, which have been observed to recruit group members with social calls to flowering balsa trees (McCracken and Bradbury, 1981; Wilkinson and Boughman, 1998).

Search behavior and social foraging in bats feeding on ephemeral prey Mainly open space foragers search for ephemeral prey, which are unpredictable in time and space. If foragers have no previous knowledge on the position of their widely distributed prey, they have to cover large search areas. The statistical chance of a single bat finding an insect swarm in a large foraging area would therefore be rather low. The observation that bats searching for ephemeral prey often accumulate at foraging sites has led to the hypothesis that some species form a flock in search of resources and that such aggregations indicate coordinated social foraging to increase the joint search volume (reviewed by Gager (2019), Kohles et al. (2022)). Group facilitation has been discussed for Noctilio albiventris and Molossus molossus after automatic radio-telemetric studies suggested bat aggregations at foraging sites (Dechmann et al., 2009, 2010). On-board recordings in Rhinopoma microphyllum (Cvikel et al., 2015) and in M. vivesi (Egert-Berg et al., 2018) (Fig. 5.2B), where echolocation signals of foraging bats were often recorded together with the search calls of conspecifics, led to the interpretation that bats may intentionally fly together in a flock to act as a sort of sensory array to increase their chances to find ephemeral prey patches. Roeleke et al. (2022) who tracked several Nyctalus noctula foraging in the same area at the same time interpreted their data “as evidence that the bats form temporary mobile sensory networks by adjusting their movements to neighboring conspecifics while probing the airspace for prey.” Theoretical models that include the estimated hearing distance of conspecifics predict an increased chance to find ephemeral prey if foragers were to search in a coordinated fashion (Cvikel et al., 2015; Roeleke et al., 2022). However, the hearing distances which were used in these models may be too large as sound emission and auditory perception of bats are highly directional and the SPL of buzzes is distinctly lower than the SL of search signals. It is questionable whether the information on position, heading, and speed of the relevant neighbors, which are necessary to establish a coordinated flock according to the forces attraction, repulsion, and alignment (Ballerini et al., 2008), is available from the overheard echolocation signals of several neighbors, which are emitted only with a rate of about 2e3 Hz. The difficulty in keeping a coordinated flock together may be further exacerbated should a single forager detect and pursue an insect, thus abandoning any group coordination. Its movements are now prey-oriented, rather than neighbor-oriented. Further studies will have to demonstrate how group cohesion rules in relation to neighbors and the prey-oriented movement patterns of foraging bats work together to form a functional sensory array. The accumulation of several bats at a foraging site may also be explained by an aggregation of bats each foraging alone, which may have independently discovered

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the same site or may have been attracted by opportunistic eavesdropping to this site. Insects are attracted to specific locations like the area above a river, the upwind zone at a cliff, the light dome of a city, or the black light of a bat scientist (Fenton and Morris, 1976). Therefore, they are often not statistically distributed as assumed for ephemeral prey but aggregate at specific sites. Bats that can recall such profitable sites could return independently from one other, thereby forming unintentionally groups allowing opportunistic social foraging by local enhancement. This, however, may not necessarily correspond to a coordinated flock forming a sensory array.

Commuting behavior in bats The commuting behavior of bats describes their flight movements to the foraging sites, between them, and back to the roost. Commuting to a specific foraging area requires the ability of bats to remember the quality and geographical position of promising foraging sites, the decision as to which site will be visited, and the ability to handle the sensory, motor, and cognitive tasks when navigating to or between them (Ulanovsky and Moss, 2008; Genzel et al., 2018; Prat and Yovel, 2020). After arrival at a promising foraging site, bats switch to their species-specific search behavior. Commuting flights of bats are goal-oriented and involve memory-based information together with a variety of sensory inputs from echolocation, vision, magnetic sense, and possibly olfaction (Prat and Yovel, 2020). On-board recordings from Rhinopoma hardwicki showed that bats continuously emit echolocation signals during commuting even when they fly high enough above the ground that they can no longer detect it. Their echolocation behavior differed between commuting and search flight, with lower sound pressure level and lower emission rates in commuting signals. Pulse intervals in search flights were mostly below 500 ms, whereas in commuting flights, they were often above (Krause, 2021). A difference in the echolocation behavior has also been observed in the narrow space passive gleaning forager Myotis myotis (Stidtsholt et al., 2021), where search signals during ground foraging had a lower SL than the calls emitted during commuting. Bats searching for predictable prey commute alone (Egert-Berg et al., 2018). When commuting with echolocation contact to the environment, they pursue distinct routes along linear landscape structures, which are characterized by the spatial configuration of specific landmarks. Often, different individuals follow similar routes (Fig. 5.2A). These flyways have a high spatial constancy (Limpens and Kapteyn, 1991; Schaub and Schnitzler, 2007b). In bats that search for ephemeral food, it is more difficult to discriminate between foraging and commuting flights. In these cases, the evaluation of the echolocation behavior and of the movement pattern may help to distinguish the different behavioral states. In the fishing bat M. vivesi, area-restricted searches with many turns at patchy resource sites were discriminated from commuting flights with fast straight movements in one direction (Hurme et al., 2019, Fig. 5.2C). Buzzes, however, which indicate prey capture, were also found in segments which were classified as commuting flight. Such prey encounters during commuting flights may help to direct an individual to promising new foraging sites.

References

In contrast to bats which forage alone for predictable prey, species that forage for ephemeral prey have been observed to commute together with conspecifics. N. leporinus and N.albiventris have been observed to fly in small groups over water (Dechmann, 2009; Schnitzler et al., 1994), and M. vivesi commute together (EgertBerg et al., 2018) (Fig. 5.2B). Strong evidence for a coordinated group flight comes from personal observations of R. hardwickii. At dawn, separate groups of at least 20 individuals left the roost, circled upward, and changed to horizontal flight. Each group stayed together and flew in a different direction (unpublished observation). This raises the question on the possible mechanisms to coordinate the group. We assume that the bats were so close together that they could determine the position of their neighbors by echolocation so that the group coordination results from active echolocation rather than from eavesdropping. Such a mechanism was proposed for chase flights of pairs of Myotis daubentonii (Giuggioli et al., 2015). Commuting flights in a group would have the advantage that the bat density is increased after arrival at the search area, which may further increase the chances for opportunistic eavesdropping.

Outlook For a comprehensive understanding of the foraging strategies of bats, information is needed on forager movements and echolocation patterns while searching and acquiring prey, on the nature and behavior of the available prey and its position in relation to clutter targets, on the synchronized motor and sensory behavior of the bats while commuting, and on the previous knowledge of the bats concerning the visited foraging sites. Due to methodological limitations, it had been historically difficult to compare the echolocation behavior of bats with their movement patterns. Modern advances in methods, like recordings with synchronized sound and 3D video systems, 3D flight path reconstructions with microphone arrays, on-board tags with storage for sound, GPS and other sensor data, reverse on-board GPS tracking systems, and methods for prey identification with barcoding, are now able to deliver comprehensive data for the understanding of foraging strategies and movement patterns of bats and their ecological relevance. With imminent future studies and advances in the field, further knowledge of these complex patterns may allow us to better understand the behavior of foraging bats and their role as essential contributors to ecosystem function.

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Stidsholt, L., Johnson, M., Goerlitz, H.R., Madsen, P.T., 2021. Wild bats briefly decouple sound production from wingbeats to increase sensory flow during prey captures. iScience 24, 102896. https://doi.org/10.1016/j.isci.2021.102896. Stilz, W.-P., Schnitzler, H.-U., 2012. Estimation of the acoustic range of bat echolocation for extended targets. J. Acoust. Soc. Am. 132, 1765e1775. Su¨mer, S., Schnitzler, H.U., Denzinger, A., 2009. Spatial unmasking in the echolocating big Brown bat, Eptesicus fuscus. J. Comp. Physiol. 195, 463e472. https://doi.org/10.1007/ s00359-009-0424-9. Surlykke, A., Kalko, E.K.V., 2008. Echolocating bats cry out loud to detect their prey. PLoS One 4, e2036. https://doi.org/10.1371/journal.pone.0002036. Thiele, J., Winter, Y., 2005. Hierarchical strategy for relocating food targets in flower bats: spatial memory versus cue-directed search. Anim. Behav. 65, 315e327. Thies, W., Kalko, E.K.V., Schnitzler, H.-U., 1998. The roles of echolocation and olfaction in two neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behav. Ecol. Sociobiol. 42, 397e409. Tuttle, M.D., Ryan, M.J., 1981. Bat predation and the evolution of frog vocalizations in the Neotropics. Science 314 (4521), 677e678. Ulanovsky, N., Moss, C.F., 2008. What the bat’s voice tells the bat’s brain. Proc. Natl. Acad. Sci. USA 105 (25), 8491e8498. Vanderelst, D., Reijniers, J., Firzlaff, U., Peremans, H., 2015. Dominant glint based prey localization in horseshoe bats: a possible strategy for noise rejection. PLoS Comput. Biol. 7 (12), e1002268. https://doi.org/10.1371/journal.pcbi.1002268. Vaughan, T.A., 1976. Nocturnal behavior of the African false vampire bat (Cardioderma cor). J. Mammal. 57 (2), 227e248. von Helversen, D., von Helversen, O., 1999. Acoustic guide in bat-pollinated flower. Nature 398, 259e260. von Helversen, O., Winkler, L., Bestmann, H.J., 2000. Sulphur-containing “perfumes” attract flower-visiting bats. J. Comp. Physiol. 186, 143e153. von Helversen, D., Holderied, M.W., von Helversen, O., 2003. Echoes of bat-pollinated bellshaped flowers: conspicuous for nectar-feeding bats? J. Exp. Biol. 206, 1025e1034. Voigt, C.C., Frick, W.F., Holderied, M.W., Holland, R., Kert, G., Mello, M.R., et al., 2017. Principles and patterns of bat movements: from aerodynamics to ecology. Q. Rev. Biol. 92 (3), 267e287. Warren, R.D., Waters, D.A., Altringham, J.D., Bullock, D.J., 2000. The distribution of Daubenton’s bats (Myotis daubentonii) and pipistrelle bats (Pipistrellus pipistrellus) (Vespertilionidae) in relation to small-scale variation in riverine habitat. Biol. Conserv. 92, 85e91. Weinbeer, M., Kalko, E.K.V., Jung, K., 2013. Behavioral flexibility of the trawling longlegged bat, Macrophyllum macrophyllum. Front. Physiol. 4, 342. https://doi.org/ 10.3389/fphys.2013.00342. Wilkinson, G.S., Boughman, J.W., 1998. Social calls coordinate foraging in greater spearnosed bats. Anim. Behav. 55, 337e350. Wilson, D.E., Mittermeier, R.A. (Eds.), 2019. Handbook of the Mammals of the Worde Volume 9: Bats. Lynx Edicions in association with Conservation International and IUCN, Barcelona. Zou, W., Liang, H., Wu, P., Luo, B., Zhou, D., Liu, W., et al., 2022. Correlated evolution of wing morphology and echolocation calls in bats. Front. Ecol. Evol. 10, 1031548. https:// doi.org/10.3389/fevo.2022.1031548.

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CHAPTER

Foraging, movements, and diet habits of arid-zone dwelling bats

6

Irene Conenna1, Carmi Korine2 1

Global Change and Conservation, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland; 2Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel

Introduction Foraging activity and movements of bats as well as their diets vary in response to different exogenous and endogenous factors (Hayes, 1997). Foraging activity in insectivorous bats is affected by the stochasticity of the availability of their prey, which may vary daily or seasonally as a function of environmental factors such as temperature, wind, light (Altringham, 2011), predictability (Egert-Berg et al., 2018), or seasonality (Fleming et al., 1993; Levin et al., 2009). The abundance of insects is of primary importance because food variety and availability can affect the choice of foraging site (Rydell and Racey, 1995), the length of foraging bouts (Swift, 1980), and potentially even the reproductive cycle by influencing the time of parturition (Arlettaz et al., 2001). In arid environments, the climatic extremes and unpredictability of precipitation determine the sparsity and ephemerality of food sources, negatively affecting foraging success and imposing additional constraints on the way arid zone bats balance energy and water fluxes (Noy-Meir, 1973). These constraints reflect on bat movements and foraging habits (Adams and Hayes, 2008, 2021; Korine et al., 2016; Razgour et al., 2018), which are modulated to offset local environmental conditions and play a fundamental role in ensuring viability of populations. In addition to these factors, bat movements and overall foraging behaviors must account for the spatial distribution of other fundamental resources, such as roosting sites and the location of bodies of water, as well as their species-specific social structure and interspecific interactions (Lewis, 1995; Korine et al., 2016; Egert-Berg et al., 2018). Arid zone bats are found in some of the most extreme desert habitats and are diverse in terms of their taxonomy, ecological diversity, and diet habits (Liso´n et al., 2020). Of the over 1400 described species of bats (Simmons and Cirranello, 2020), over one-third (n ¼ 536, range >5% in arid zone) is distributed in arid environments (Fig. 6.1), with a total representation of 140 genera within 16 families, where Vespertilionidae, Molossidae, and Rhinolophidae are the most abundant (Conenna, 2021). In this chapter, we review behavioral strategies, and in particular A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.16001-2 Copyright © 2024 Elsevier Inc. All rights reserved.

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FIGURE 6.1 Map of arid environments based on the aridity index provided by Zomer et al. (2022).

changes in movements, temporal activity and diet, employed by bats to offset the increased water stress and the reduced foraging success brought by arid conditions. Additionally, we relate these behaviors to the context of climatic conditions and landscape structures in which they are exhibited, for example, varying levels of aridity, seasonality patterns, and distribution and availability of water and roosting sites.

Nightly movements Several tracking studies of insectivorous and nectarivorous species from arid environments have shown that bats cover long distances during their nightly activity time. Some species show relatively high fidelity to favorable foraging grounds and commute along predictable routes to reach them (Daniel et al., 2008; Rainho and Palmereim, 2011; Korine et al., 2013; Rodhouse and Hyde, 2014; Goldshtein et al., 2020). Nectarivorous bats can undertake nightly round trips of up to 104 km to reach areas of flowering cacti (Medellin et al., 2018). Insectivorous bats, for which water sources are fundamental for their water balance, commute over a range of distances (1-tens of kilometers to locate their foraging sites near water (Korine et al., 2013; Rodhouse and Hyde, 2014; Goldshtein et al., 2020). Nevertheless, several species rely on short-distance movements (Monadjem et al., 2009; Smarsh and Smotherman, 2015; Conenna et al., 2019, 2021), and for these bats, local roost availability might be particularly crucial. Female and male bats differ in their ability to cross-geographical barriers due to differential energetic demands during pregnancy and lactation, which confine females to more profitable foraging

Introduction

habitats (Barclay, 1991; Senior et al., 2005; Daniel et al., 2010). Therefore, arid-zone female bats may depend more on water sources for drinking and foraging than males (Barclay, 1991; Entwistle et al., 1997; Davidson-Watts and Jones, 2005) and thus may be confined to water sites during this period or face trade-offs between commuting distance and roost suitability (Kunz, 1982; Rainho and Palmereim, 2011). For example, in a study on nursing females of Otonycteris hemprichii foraging in the proximity of a lake in the Negev Desert, Daniel et al. (2008) identified two groups of females according to the commuting distances from their roosting site (0.5e2 versus 9 km). The authors hypothesized that there might be a trade-off between increased costs of long commutes (e.g., lower nursing frequency) and roost site safety. On the other hand, other species of bats do not show foraging site fidelity and rely on ephemeral food sources; in these cases, movement patterns are erratic. Egert-Berg et al. (2018) showed how Rhinopoma microphyllum, a desert-dwelling species relying on insect swarms, visited many sites each night and often changed locations across nights. Nightly movements can be also affected by differences in movement and dispersal patterns between males and females; however, these types of movements were hardly explored in arid-dwelling bats. Direct links between aridity and nightly movements have not yet been explored. However, Conenna et al. (2019) observed that the foliage-roosting Lavia frons, a low-mobility bat with small home ranges, enlarged their foraging areas during the dry season in a semi-desert, presumably to ensure access to sufficient resources in a time of low food abundance. Similarly, Best and Geluso (2003) suggested that nightly foraging ranges of Tadarida brasiliensis in New Mexico might be larger during years of drought because bats will need to cover longer distances to find insects (see also Sosa and Soriano, 1996). In summary, it seems that the fluctuation in water and food availability could be one of the main determinants of the observed patterns of mobility and foraging in bats from arid environments. Modulation of night movements is an important behavior for bats from arid areas to ensure foraging and drinking access. These movements in turn depend on a number of intrinsic and extrinsic factors, such as the large variability in species’ flight ability, roosting habits, and local roost availability. Environmental variables such as ambient humidity and temperatures are likely to interact, producing different kinds of trade-offs and responses in aridzone species than in species inhabiting temperature environments. More studies on the movement responses and profitable foraging habitats of bats living in arid environments are needed.

Seasonal movements While some species of bats are permanent residents in arid environments and respond to seasonal fluctuations with changes in nightly movement patterns, other species use seasonal short-distance and regional displacements as well as longdistance migrations from arid to more mesic areas (Fleming, 2019). Some species

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can survive in arid lands only when resources are abundant and foraging success is adequate. Species of subtropical and tropical nectar-feeding bats, namely, Leptonycteris yerbabuenae (formerly L. curasoae yerbabuenae), L. nivalis, and Choeronycteris mexicana, migrate to the Sonoran and Chihuahuan Deserts of the southwestern United States and northern Mexico during summer (Rojas-Martinez et al., 1999; Bogan et al., 2017; Fleming and Holland, 2018; Fleming, 2019). Here, they exploit the seasonally abundant nectar and fruit resources provided by columnar cacti and Agave species and establish maternity colonies, only to return to the dry forests of central Mexico where resources are available throughout winter (Rojas-Martinez et al., 1999; Bogan et al., 2017; Fleming and Holland, 2018). Populations of the insectivorous bat T. brasiliensis located in the southwestern United States display a similar migration pattern, migrating in late autumn to reside in winter and early spring in central Mexico (Villa and Cockrum, 1962; McCracken and Gassel, 1997; Krutzsch et al., 2002). In continental Australia, Tadarida australis shows a seasonal range contraction and expansion, with northernmost populations migrating south during summer and southernmost ones migrating north during winter (Bullen and McKenzie, 2005). These seasonal continental-scale movements seem to be driven by a combination of temperature and humidity conditions: T. australis selects regions with a monthly rainfall of 10e50 mm per month and average temperatures of 5e20 C; this species avoids the seasonally dry and hot environments in the north while timing the reproductive cycle with rainfall patterns in the southern part of its range (Bullen and McKenzie, 2005). Short-distance migrations have been documented for species of rhinolophids and hipposiderids in East Africa, where bats migrate from inland sites to avoid the long dry season, likely to reach coastal habitats presenting complementary rainfall patterns (O’Shea and Vaughan, 1980). Finally, bats might move to alternative roosting sites to have access to fluctuating resources in arid habitats (Sosa and Soriano, 1996; Geluso and Geluso, 2012; Conenna, personal observation). For example, during dry seasons and especially in drought years, bats concentrate around permanent water sources for drinking and foraging (Korine and Pinshow, 2004; Razgour et al., 2010; Geluso and Geluso, 2012; Korine et al., 2015). However, data on these movements are scarce, and it is not entirely clear why bats would seasonally change roosting locations or rather display longer commutes. Among possible factors that can explain these behaviors, we have remoteness and rarity of water, water quality, roost availability, the harshness of environmental conditions, species’ drinking requirements, and flight ability.

Temporal activity Insectivorous bats often follow a pattern of nightly activity presenting two peaks, one right after sunset and another one before returning to the roost in the morning (e.g., Hayes, 1997; Conenna et al., 2019). However, these patterns can vary in response to aridity and the challenges that come along with it. As a response to seasonally drier conditions and to low prey abundance, bats can increase the time spent foraging, sometimes shifting from a two-peak activity pattern to being active

Introduction

throughout the night (Vaughan, 1976; Cvikel et al., 2015; Egert-Berg et al., 2018; Conenna et al., 2019). Similarly, roost emergence of T. brasiliensis in a semi-arid region of Texas occurred as early as 1.5 h before sunset in drought years, about 2 h earlier compared with the time of emergence in moister years (Frick et al., 2012). This difference was attributed either to the bats responding to stressful conditions during day-roosting (e.g., high water stress) or as a compensatory behavior that would allow bats to increase foraging time and therefore cope with lower insect abundance in drier conditions (Frick et al., 2012). It should be noted that these behaviors also occur in temperate bats. Changes in temporal activity patterns can also constitute a behavioral strategy to be able to access resources that in arid environments are not only critical but also highly contested. Temporal partitioning can happen at water sources due to competitive interactions among bat species (Adams and Thibault, 2006; Razgour et al., 2011), particularly during dry seasons, when activity over permanent water sources increases (Lo´pez-Gonza´lez et al., 2015). Razgour et al. (2011) observed how partitioning in the use of water sources changes across seasons in a community of bats in the Negev desert, with species segregating spatially during the rainy season, and shifting to temporal partitioning during the dry season when temporary water sources are no longer available. The reproductive season can greatly influence the activity patterns of females, both in terms of time spent foraging and the number and duration of foraging bouts, reflecting the greater demands for energy and water (Kuenzi and Morrison, 2003; Daniel et al., 2008, 2010; Korine et al., 2013; Loumassine et al., 2020), but little information is available on how aridity and reproductive stage interact to modify temporal patterns of foraging in female bats.

Approaches to the study of movement in arid-zone bats Movement of bats in arid environments has been investigated employing a variety of approaches, including trapping (Harrison and Bates, 1991) and direct observations (O’Neill and Taylor (1986), but also see Vaughan and Vaughan (1986)), tracking with radiotelemetry (Corbett et al., 2008; Daniel et al., 2008), and in the last years tracking with GPS units (Egert-Berg et al., 2018; Conenna et al., 2019). In the past, trapping and direct observations aided in revealing general broad-scale patterns such as seasonal migrations (O’shea and Vaughan, 1980). The introduction of radiotracking made it possible to increasingly investigate and quantify finer patterns of space use in different environments. GPS tracking has surpassed radio-tracking and revolutionized the quality, quantity, and scale of tracking data of animals in the wild (Recio et al., 2011). By allowing the collection of spatially and temporally unbiased locations and the simultaneous tracking of multiple individuals, GPS technology opened the doors to the understanding of movement patterns previously out of reach, both on a local and global scales (e.g., habitat use, migration, etc.), as well as of interactions among individuals by understanding partitioning over space and time during foraging (Bo¨rger et al., 2008; Hebblewhite and Haydon, 2010). GPS tracking of arid-zone bats has additionally been employed to study, for example, social foraging (Cvikel et al., 2015; Egert-Berg et al., 2018; Goldshtein et al., 2020), effects of urbanization on habitat and resource use (CentenoCuadros et al., 2017; Egert-Berg et al., 2021), habitat-use (Ryszard et al., 2015), and long-range navigation mechanisms (Tsoar et al., 2011). However, studies of movement in bats using GPS have predominantly focused on frugivorous and partly nectarivorous bats, while insectivorous bats have yet marginally taken advantage of these advancements due to their body sizes, which are often too Continued

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Approaches to the study of movement in arid-zone batsdcont’d light to allow for the relative device mass to remain within the maximum recommended 10% of the bat weight (O’Mara et al., 2014). This has hindered the study of bat movement ecology in arid environments, where insectivorous species make up the largest share of bat biodiversity and often restricted the focus to a limited number of species (e.g., the well-studied lesser long-nosed bat Leptonycteris yerbabuenae, and the large-bodied Egyptian fruit bat Rousettus aegyptiacus). The w1e1.5 g weight threshold for GPS tags has represented a limit for some time, but efforts to reduce this value and address these challenges are continuously underway (Conenna, 2021; Wild et al., 2022). An example of these efforts is the ATLAS system (Advanced Tracking and Localisation of Animals in real-life Systems; Toledo et al., 2020). This system is based on the use of tags transmitting radio signals, which are detected by a network of receivers located in a study area or a regional level (Toledo et al., 2020) and therefore allowing the employment of tags of weight potentially 1400 living species), generally displaying a slow pace-of-life (including high survival, increased longevity, slow reproduction, and delayed senescence), crepuscular and nocturnal activity, and agile and fast flight (Kunz and Fenton, 2003). Yet, the study of interactions between bats and their predators has been neglected with an assumption that bats rarely experience mortality due to predation and have few natural enemies. However, the high diversity of bats and the propensity of some species to live in large groups (Wilson and Mittermeier, 2019) provides many predators with excellent feeding opportunity (Lee and Kuo, 2001; Haarsma and Kaal, 2016; Dinets, 2017; Cichocki et al., 2021). Predation on bats ranges from opportunism to regular exploitation, but we still largely lack comprehensive data on the impact of predation on bat populations. The potential of bats as prey is reflected by the situation they present when it comes to understanding optimal foraging behavior of predator. Just as bats exploit insects, high densities of bats and their generally small body size translate into high encounter rates with predators and short handling times (e.g., Stephens and Krebs, 1986; see also Fenton et al., 1994). For example, many species of bats form large groups, up to several million individuals (Fenton and Simmons, 2015), attracting many predators (Mikula et al., 2016). Some studies have found considerable predation of bats from locations where large numbers of individuals predictably emerge at the same times from day roosts, such as caves, mines, and bridges (Fenton et al., 1994; Esbe´rard and Vrcibradic, 2007; Mikula et al., 2016; Tanalgo et al., 2020; Brighton et al., 2021). Bats are particularly vulnerable to predation when emerging from their roosts and during hibernation when they are less active and mobile (Esto´k et al., 2010; Haarsma and Kaal, 2016; Mikula et al., 2016; Cichocki et al., 2021). Bat A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.00003-6 Copyright © 2024 Elsevier Inc. All rights reserved.

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predators may gather near roost entrances and exploit emerging animals and enter roosts and hibernacula to prey on bats (Esbe´rard and Vrcibradic, 2007; Spitzenberger et al., 2014; Mikula et al., 2016; Tanalgo et al., 2020; Cichocki et al., 2021). The generally small size of bats exposes them to a large range of predators, more so than larger prey (Cohen et al., 1993; Sinclair et al., 2003). The diversity and distribution of bats also make them widespread prey and expose them to a considerable diversity of predators (Alves et al., 2018) (Fig. 9.1). Predatoreprey interactions between bats and their enemies may be more important in tropical regions, where both these communities are more diverse and abundant. Moreover, the year-round presence of huge bat groups makes them a predictable source of prey in tropical environment (Furey et al., 2016). Roosting and foraging patterns of some bats make them more vulnerable to predators. In Nietoperek nature reserve (Poland), one of the largest bat hibernation sites in Central Europe, mainly stone martens (Martes foina) (Lesinski and Romanowski, 1988) and likely a single individual of invasive raccoon (Procyon lotor) (Cichocki et al., 2021) consumed mainly bat species hibernating close to the ground. Indirect evidence suggests that endangered ground-foraging New Zealand lesser short-tailed bats (Mystacina tuberculata) may be particularly vulnerable to predation by rats and cats (Welch and Leppanen, 2017). The vulnerability of bats to predation can be linked to age, roost emergence patterns, and flight performance of bats. Peregrine falcons (Falco peregrinus) and redtailed hawks (Buteo jamaicensis) significantly improved their hunting success during periods when young Brazilian free-tailed bats (Tadarida brasiliensis) became volant and started to forage (Lee and Kuo, 2001). In Culebrones cave (Puerto Rico), cats consumed nectar-feeding species of bats, which often flutter when leaving a cave, more often than expected based on their abundance (Rodrı´guez-Dura´n et al., 2010). Larger and faster flying insectivorous bat species emerge from roosts earlier than smaller and slower flying species, which may reduce their vulnerability to bird predation (Thomas and Jacobs, 2013). Moreover, Barti et al. (2019) have suggested that bat species with less predictable flying paths are more difficult for snakes to catch. Success in catching bats is highly variable among predators and likely reflects some combination of hunting behavior of predators and evasive behavior of bats. For example, bat hunting success varied from 41% in reptile-feeding Wahlberg’s eagles (Hieraaetus wahlbergi) to 75% in bird-feeding African goshawks (Accipiter tachiro) (Fenton et al., 1994). Hunting success of bat hawks (Macheiramphus alcinus), a sole vertebrate predator which consistently relies on bat prey (Fenton et al., 1977; Black et al., 1979), was typically higher (reaching w50%) than that of most nonspecialized raptors (Brighton et al., 2021). The hunting success of Swainson’s hawks (B. swainsoni) preying upon swarming bats depended on hunting technique, being most successful if attacks involved a high-speed stoop or rolling grab (Brighton et al., 2021). Finally, communal hunting can increase the hunting success of the predators like in some nonraptorial bird groups such as corvids (Lefevre, 2005; Tanalgo et al., 2020). However, the hunting success of predators was typically estimated from nonstandardized and very limited number of observations.

Introduction

FIGURE 9.1 Bats caught by predators. (A) Gray-headed flying fox (Pteropus poliocephalus) kept by human in a cage in a wildmeat market. (B) Domestic cat (Felis catus) caught and killed parti-colored bat (Vespertilio murinus) which fell on the ground. (C) The big-eared woolly bat (Chrotopterus auritus) consuming smaller Carollia bat taken in a flight cage. (D) Tropical screech owl (Megaschops choliba) caught a tent-making bat (Uroderma sp.) in the backyard of a house. (E) Swainson’s hawks (Buteo swainsoni) attacking swarming Brazilian free-tailed bats (Tadarida brasiliensis) on emergence from cave. (F) European bee-eater (Merops apiaster) trying to swallow Kuhl’s pipistrelle (Pipistrellus kuhlii). (G) African rock python (Python sebae) captured Egyptian fruit bat (Rousettus aegyptiacus) as it flied out of the cave. (H) The juvenile rock monitor (Varanus albigularis) has grabbed the molossid bat and pulled it down toward the ground. (I) Australian green tree frog (Litorea cerulea) swallowing a little bent-wing bat (Miniopterus australis). (J) Centipede (Scolopendra viridicornis) was found feeding upon Argentine brown bat (Eptesicus furinalis) on the floor of the house porch. (K) An adult proboscis bat (Rhynchonycteris naso) was found entangled in a web of spider (Argiope savignyi) located near bat colony.


´, 2015, Indonesia (A); Photo: Peter Mikula, 2016, Slovakia (B); Photo: Marco Photo: Tereza Svejcarova

Tschapka, 2016, Peru (C); Photo: Guilherme Colugnatti, 2009, Brazil (D); Photo: Caroline H. Brighton, 2018, USA (E); Photo: Shuki Cheled, 2015, Israel (F); Photo: Low de Vries, 2018, South Africa (G); Photo: Nicolette Josling, 2016, South Africa (H); Photo: Bruce Means, 2001, Australia (I); Photo: Ana Carolina Srbek-Araujo, 2008, Brazil (J); Photo: Mirjam Kno¨rnschild, 2005, Costa Rica (K).

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Bat responses to predation While bats can detect predators and may estimate acute predation risk by auditory, olfactory, and visual cues, and echolocation, there are few reports on the antipredator behavior of bats (Lima and Dill, 1990). Empirical studies provide mixed evidence for the role of these senses in avoiding predation (Petr
zelkova´ and Zukal, 2001; Russ et al., 2004; Breviglieri et al., 2013). Several key aspects of bat behavior are a part of predation avoidance, including emergence from roosts, choices of day roosts, landscape-related movement patterns, habitat selection, nature of sleep and torpor, and lunar phobia (Lima and O’Keefe, 2013). One type of behavioral antipredator responses of bats includes their reaction to direct encounter with a predator. For example, bats may respond to the presence of bird predators near a roost by clustering during emergence (Petr
zelkova´ and Zukal, 2003; Brighton et al., 2021), changing their access ports (Gu¨ttinger, 1990), delaying (Welbergen, 2006) or advancing emergence time (Fenton et al., 1994). Geoffroy’s bats (Myotis emarginatus) avoided or abandoned roosts in the long-term presence of owl (Spitzenberger et al., 2014). Bats also possess the ability to
´ lek, actively mob a predator (Kno¨rnschild and Tschapka, 2012; Lu
can and Sa 2013). Another antipredator mechanism includes long-term and fixed behavioral patterns. Bat sociality at roosts per se may be a part of antipredator behavior (Wilkinson, 1985). Unihemispheric sleep could have predator detection function and reduce bats’ risk of predation on bats (Downs et al., 2015), as could the structure of sleep in some bats (Zhao et al., 2010). Nocturnal torpor in lesser long-eared bats (Nyctophilus geoffroyi) may minimize energy expenditure and foraging activity outside the roost, helping these bats to avoid predators (Stawski and Geiser, 2010). Several temperate vespertilionid bats select commuting routes among roosts and foraging sites in more vegetated areas and near linear landscape elements such as tree lines and lanes, reflecting the perceived risk of predation (Verboom and Huitema, 1997; Jenkins et al., 1998). Another example is Rafinesque’s big-eared bat (Corynorhinus rafinesquii) which prefers tree cavities with smooth walls which may impede attacks by predators (Clement and Castleberry, 2013). Some bat species may evade predators by using roosts with smaller openings and located higher above the ground (Lausen and Barclay, 2002). Switching roost frequently has been also noted as a strategy to reduce predation risk (Lewis, 1995). Hopkins and Hopkins (1982) suggested that brief visits to flowers by nectarivorous bats could be a strategy to avoid predation by snakes. Additionally, lunar phobia has been documented especially in tropical bats, which could be due to the higher risk of predation in the tropics than in temperate regions, but the evidence so far is not convincing (Lima and O’Keefe, 2013). Finally, Stone et al. (2015) has reported reduced foraging activity and delayed emergence time of bats in the presence of increased artificial light pollution.

Bat predation and nocturnality

Bat predation and nocturnality The common ancestor of all modern mammals, including bats, was probably nocturnal (Maor et al., 2017). But this pattern is so ubiquitous in bats that the main question is why do bats not exhibit diurnal activity in situations, seasons, or areas, where it could be beneficial to them? For example, the nocturnal behavior of bats may be energetically and nutritionally disadvantageous, especially for insectivorous bats of temperate regions. Here, summer nights are short and insect activity often peaks before sunset and after sunrise, mismatching the time of peak foraging activity of bats (Rydell et al., 1996; Speakman et al., 2000; Malmqvist et al., 2018). Most arguments attempting to explain strict bat nocturnality have focused on functional explanations considering the direct disadvantages of diurnal activity in bats, including competition with and predation by diurnal birds or risk of hyperthermia (Rydell and Speakman, 1995; Speakman, 1995). The avian predation hypothesis received increased attention and some evidence indicates that diurnal avian predation risk might explain bats’ strict nocturnal behavior (Rydell and Speakman, 1995; Speakman, 1995; Mikula et al., 2016). The first line of evidence is based on predation rates. When accounting for the difference in bat flight time during the day and night, the predation rate by diurnal birds could be 100e1000 times higher than the nocturnal predation rate (Speakman, 1991b, 1995; Speakman et al., 1994). However, this estimate does not account for the risk of diurnal predation in roosts. Another support for selection pressure on bat nocturnality from diurnal predators comes from locations free of bird predators, typically oceanic islands where the risk of predation by diurnal birds is low. Frequent diurnal flying and feeding activity is exhibited by Noack’s roundleaf bat (Hipposideros ruber) on Sa˜o Tome´ Island (Russo et al., 2011), Blyth’s horseshoe bat (Rhinolophus lepidus) on Tioman Island (Chua and Aziz, 2019), and black-eared flying fox (Pteropus melanotus) on Christmas Island (Tidemann, 1987). The Azores noctule (Nyctalus azoreum), an endemic island species, was originally also reported to exhibit an unusually high degree of diurnal activity (Moore, 1975). However, later observations revealed that increased daytime activity was spatially restricted (Speakman and Webb, 1993). Similarly, several pteropodids including Samoa flying fox (P. samoensis) on Tutuila Island (Thomson et al., 1998) or Livingstone’s fruit bat (P. livingstonii) and Seychelles fruit bat (P. seychellensis) on the Comoro Islands (Trewhella et al., 2001) showed high diurnal activity despite the presence of the known bat predator, peregrine falcon (Lee and Kuo, 2001). Finally, bats exhibit flexible trade-offs between predation risk and foraging needs such as changes in emergence time in the presence of avian predators (Fenton et al., 1994; Welbergen, 2006) or lunar phobia (Lima and O’Keefe, 2013). Altogether, the importance of predation risk during diurnal activity of bats may be taxonomically, spatially, and temporally variable, and there remain large gaps in our knowledge

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on this phenomenon (Speakman, 1995). However, in general, it seems that predator activity may directly and indirectly exert sufficient pressure to keep bat activity concentrated mainly to the night and the crepuscular periods of day.

Predators of bats Predation is probably the most important source of external mortality in wild-living animals, including bats. Traditionally, the main predators of bats were presumed to be owls (Speakman, 1991a; Sieradzki and Mikkola, 2020), raptors (Mikula et al., 2016), snakes (Esbe´rard and Vrcibradic, 2007), small carnivores (Cichocki et al., 2021; Oedin et al., 2021), and humans (O’Shea et al., 2016). For example, opportunistic predation on bats by generalist predators such as owls and diurnal birds could account for 11% of the annual mortality of British bats (Speakman, 1991a). Before 2000, intentional killing by humans (often but not exclusively for food) was responsible for 39% of reported multiple mortality events in bats (O’Shea et al., 2016). However, other predators, including some bats and even invertebrates, also catch and eat bats (Valdez, 2020; Gual-Sua´rez and Medellı´n, 2021). A general absence of specialized bat predators does not necessarily mean that predation does not impact the lives of bats (Gillette and Kimbrough, 1970).

Birds The most common flying predators of vertebrates exploiting nocturnal niche are owls. Hence, owls have traditionally been considered major bat predators. Owls attack bats mainly during the evening emergence or morning return to the roosting places, but their hunting success is often low (Baker, 1962; Spitzenberger et al., 2014; but see Brighton et al., 2021). Owls may selectively hunt freshly volant inexperienced juveniles (Petr
zelkova´ et al., 2004) or immobilized bats (e.g., caught in mist-nets) (Serra-Gonc¸alves et al., 2017). Owls prey upon bats regularly, but bats usually represent only a minor part of their diet (e.g., on average < 0.1% of prey items in European owls; Sieradzki and Mikkola, 2020). However, in bat-rich environments such as near roosting sites of bats, the proportion of bat prey in the diet of individual owls may sharply increase up to 40% (Sieradzki and Mikkola, 2020). The current perception of the generally low importance of owl predation on bats may also be strongly biased toward the situation in temperate regions. In the British Isles, 97% of bats killed by birds were preyed upon by owls, whereas only 3% fall prey to diurnal birds (Speakman, 1991a). However, the general scarcity of bat predation by diurnal birds is largely caused by the mismatch in the dominant activity of extant bats and diurnal birds. Mikula et al. (2016) showed that bat predation by diurnal birds is a global phenomenon documented from every continent (except Antarctica), covering at least 143 species of diurnal raptors and 94 species (28 families) from other diurnal avian groups, including corvids or shrikes.

Predators of bats

Bats of at least 124 and 50 species are preyed upon by raptors and other diurnal birds, respectively. Most diurnal birds prey upon bats only opportunistically, but, similar to owls, large aggregations of bats are prone to attract their attention (Sprunt, 1950; Twente, 1954; Fenton et al., 1994; Tanalgo et al., 2020). Raptors typically limit their predation of bats to the outside of roosts, especially close to their entrances (Baker, 1962; Fenton et al., 1994; Brighton et al., 2021). Nonraptorial birds are often only capable of preying on young, typically nonvolant bats that have fallen or injured and torpid bats during hibernation (Herreid, 1960; Esto´k et al., 2010). However, some corvids may also successfully catch flying bats (Tanalgo et al., 2020).

Mammals Predation by mammals can represent a serious threat to roosting bats, sometimes strongly influencing the survival of entire bat colonies (Fellers, 2000; Haarsma and Kaal, 2016). Mammals may use olfactory cues for the detection of bat roosts (Threlfall et al., 2013) and, unlike birds, may even follow bats to deep and completely dark roosts, such as caves or mines (Rodrı´guez-Dura´n et al., 2010; Cichocki et al., 2021). Mammalian bat predators include various taxonomic groups, including opossums (Faria, 2014), carnivorans (Cichocki et al., 2021; Oedin et al., 2021), rodents (Haarsma and Kaal, 2016), nonhuman primates (Boinski and Timm, 1985), humans (O’Shea et al., 2016), as well as other bats (Gual-Sua´rez and Medellı´n, 2021). Of particular importance is the effect of nonnative mammals on native bat populations and species. Due to human activity, many mammal species were introduced to novel areas and some, such as cats or rodents, become invasive, threatening native wildlife and ecosystems (Doherty et al., 2016). Recently, Oedin et al. (2021) reviewed the global impact of predation by domestic cats (Felis catus) on bats. Bats generally represent only a small amount of cat diet (w0.7%), but this proportion is higher on islands than on the mainland. Cat predation threatened at least 86 species (12 families) of bats with a disproportionate number of species with an elevated extinction risk. Even a single cat may be responsible for a significant depredation of local bats (Scrimgeour et al., 2012). The widespread invasive rodents such as rats (Rattus spp.) and domestic mouse (Mus musculus) are also responsible for the decline and extinction of numerous native vertebrates, particularly island endemic species (Harris, 2009). However, direct observations of bat predation by rodents are extremely rare in the literature. This indicates that the effect of rodent predation on bats may generally be low, but it does not necessarily imply that rodent predators cannot have a significant impact locally. In one well-documented case, predation by wood mouse (Apodemus sylvaticus) at bat hibernacula in the Netherlands was responsible for up to 84% of the annual mortality of local bats (Haarsma and Kaal, 2016).

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Bats Gual-Sua´rez and Medellı´n (2021) reviewed the diets of 17 bat species known to eat vertebrates and found bat prey in 10 species representing four families. Five were Phyllostomidae bats: spectral bat (Vampyrum spectrum), big-eared woolly bat (Chrotopterus auritus), greater spear-nosed bat (Phyllostomus hastatus), fringe-lipped bat (Trachops cirrhosis), and greater round-eared bat (Tonatia bidens). Others were Megadermatidae (ghost bat Macroderma gigas, greater false vampire bat Megaderma lyra, and heart-nosed bat Cardioderma cor), Nycteridae (large slit-faced bat Nycteris grandis), and Vespertilionidae (pallid bat Antrozous pallidus) bats. In a cave roost in Puerto Rico, Rodrı´guez-Dura´n and Rosa (2020) reported greater bulldog bats (Noctilio leporinus) eating the young of other species of bats roosting in the cave.

Humans and primates Hunting of bats for bushmeat is a common practice across the Old-World tropics (Mickleburgh et al., 2009; O’Shea et al., 2016). In Asia and the Pacific islands, large fruit bats of the genus Pteropus are often consumed, whereas, in Africa, strawcolored fruit bats (Eidolon helvum) were commonly hunted for food (Mickleburgh et al., 2009). Insectivorous bats are also taken in Asia, particularly free-tailed bats of the genus Tadarida, or these of genus Rhinolophus and Hipposideros in Africa (Mickleburgh et al., 2009). Among nonhuman primates, Boinski and Timm (1985) reported an interesting case of tent-making bat predation by squirrel monkeys (Saimiri oerstedi), which on several occasions leaped on the leaf tents of bats and consumed bats knocked to the ground.

Reptiles Among reptiles, snakes are the main bat predators. Predation events involving snakes can be found practically all around the world but with a higher incidence in tropical than temperate regions. Most records are for boid (Boidae) and colubrid (Colubridae) snakes (Esbe´rard and Vrcibradic, 2007; Barti et al., 2019). They often prey on bats emerging from their roosts (Herreid, 1962; Rodriguez and Reagan, 1984; Dinets, 2017) or may also actively hunt and attack bats in roosts during daytime and night (Sorrel et al., 2011; Cha´vez-Arribasplata et al., 2016). Hopkins and Hopkins (1982) reported an arboreal constrictor catching bats visiting flowers. Other snake families may also prey on bats, including cobras (Naja spp.) (Elapidae) (Digana et al., 2000), brown house snake (Boaedon capensis) (Lamprophiidae) (Maritz and Maritz, 2020), pythons (Pythonidae) (Shine and Fitzgerald, 1996), and pit snakes (Viperidae) (Szczygie1 and Page, 2020). Predation by the invasive brown tree snakes (Boiga irregularis) may have contributed to the disappearance of Guam fruit bats (P. tokudae) and Pacific sheath-tailed bat (Emballonura semicaudata) on Guam Island (Rodda et al., 1999). On Christmas Island, the introduction of the common wolf snake (Lycodon aulicus) coincides with the declines in the populations of the Christmas Island flying fox (P. melanotus) (Fritts, 1993) and the extinct Christmas Island pipistrelle (Pipistrellus murrayi) (Lumsden et al., 2007).

Conclusions and suggestions for further research

Monitor lizards (Varanus spp.) are the most reported bat hunting lizards and seem to be the only ones that occasionally can forage actively for bats (Clarkson and Massyn, 2020; Tanalgo et al., 2020). The rest of the reports appear to be exceptional cases such as bat consumption by green basilisk (Basiliscus plumifrons) (Corytophanidae) (Hirth, 1963), and flapneck chameleon (Chamaeleo dilepis) (Chamaeleonidae) (Maritz and Maritz, 2020). Finally, crocodiles can opportunistically capture bats when they perch close to the water level or fly low to drink (Ratcliffe, 1932; Ceden˜o-Va´zquez et al., 2014). The only species regularly predating on bats (as far as we know) are local dwarf crocodiles (Osteolaemus tetraspis) in Abanda cave in Gabon (Shirley et al., 2017).

Other vertebrates Mikula (2015) reported 21 and 37 cases where bats were consumed by fishes and amphibians, respectively, particularly in tropical regions. These reports included at least 14 fish species and 14 species of frogs and 6 and 16 species of bats, respectively. Yager and Williams (1988) on several occasions observed several gray snappers (Lutjanus griseus) lurking below maternal colony of buffy flower bats (Erophylla sezekorni) in Lucayan Cavern (Bahamas) and taking bats that had fallen from their roosts.

Invertebrates Arthropods, especially scolopendrid centipedes (Scolopendromorpha) and large spiders (Araneae), also catch and eat bats (Nyffeler and Kno¨rnschild, 2013; Valdez, 2020). Bats represent half of all mammals taken by arthropods and a majority of such predation events have been documented in tropical regions (Valdez, 2020). For example, venomous giant centipedes (Scolopendra gigantea) actively searched for bats inside Cueva del Guano cave (Venezuela), and they were recorded to diurnally and nocturnally catch and subdue flying or perching bats much heavier than they are (Molinari et al., 2005). Orb-weaver spiders are known for their strong and large webs and most cases of spider predation included consumption of bats passively caught to their webs (Nyffeler and Kno¨rnschild, 2013). Several tarantulas (Lasiodora sp.) were observed to feed or wait in a sit-and-wait position for Wagner’s mustached bats (Pteronotus personatus) falling on the floor in Urubu Cave (Brazil) (Dias et al., 2015). This indicates that in some natural systems, bat predation by invertebrates may be relatively frequent.

Conclusions and suggestions for further research Currently, natural ecosystems are rapidly changing due to anthropogenic activity. Anthropogenic change drivers, including destruction and overexploitation of natural ecosystems, exotic species invasions, and climate change, may alter interactions between bats and their predators and eventually put bat populations in danger. For

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example, availability of human-made objects representing counterparts of natural cave-like structures in human-altered ecosystems is rapidly increasing (Russo and Ancillotto, 2015; Jung and Threlfall, 2016), but we are unaware of any study comparing predation pressure between rural and urban sites or the impact of predation by different predator groups along an urbanization gradient. Disappearing or decreasing populations of bats could affect severe trophic cascades (Schmitt et al., 2021), jeopardizing their various ecosystem services (Kunz et al., 2011). Unfortunately, our knowledge on this topic is still scarce to determine the detailed ecological processes implied in bat predation at population or higher levels, and much less about how they will respond to natural or anthropogenic changes. How can we advance our understanding of these antagonistic interactions? Large, predictable aggregations of bats can serve as a suitable study system for the analysis of predatoreprey interactions between bats and their predators. Despite the nocturnality of bat activity, virtually all observations of predatoreprey interactions between flying bats and their predators involved bat species or populations that emerge from roosts earlier, with rare documentation of such events during the dark hours of the night or for bat groups emerging later after sunset (Lima and O’Keefe, 2013). The use of new technologies such as infrared video cameras could bring new and exciting results (Rodrı´guez-Dura´n et al., 2010; Threlfall et al., 2013; Spitzenberger et al., 2014). Moreover, increased attention should also be paid to amateur and anecdotic reports, as these can offer insights on new or rare interactions or from poorly studied regions. Growing the quantity and quality of bat predation evidence will allow a more accurate analysis of these interactions, for example, through interaction networks. Detailed knowledge on what factors that make bats vulnerable to predation and the level of local, but also large-scale impacts of predators on bat populations may provide critical implications for the conservation of particularly important or endangered bats. Hence, we call for a greater emphasis on the study of interactions between bats and their predators and interdisciplinary collaboration in the coming decades.

Dedication and/or acknowledgments We thank to all people who shared their photographs on interactions between bats and predators with us. We would also like to thank two reviewers for valuable comments on the chapter.

References Alves, D.M.C.C., Diniz-Filho, J.A.F., da Silva e Souza, K., Gouveia, S.F., Villalobos, F., 2018. Geographic variation in the relationship between large-scale environmental determinants and bat species richness. Basic Appl. Ecol. 27, 1e8. Baker, J.K., 1962. The manner and efficiency of raptor depredations on bats. Condor 64, 500e504.

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can, R.K., Jones, D.N., Tryjanowski, P., 2016. Bats as prey of diurnal birds: a global perspective. Mamm. Rev. 46, 160e174. Mikula, P., 2015. Fish and amphibians as bat predators. Eur. J. Ecol. 1, 71e80. Molinari, J., Gutie´rrez, E.E., Ascenc¸a˜o, A.A., Nassar, J.M., Arends, A., Ma´rquez, R.J., 2005. Predation by giant centipedes, Scolopendra gigantea, on three species of bats in a Venezuelan cave. Caribb. J. Sci. 41, 340e346. Moore, N.W., 1975. The diurnal flight of the Azorean bat (Nyctalus azoreum) and the avifauna of the Azores. J. Zool. 177, 483e486. Nyffeler, M., Kno¨rnschild, M., 2013. Bat predation by spiders. PLoS One 8, e58120. Oedin, M., Brescia, F., Millon, A., Murphy, B.P., Palmas, P., Woinarski, J.C.Z., et al., 2021. Cats Felis catus as a threat to bats worldwide: a review of the evidence. Mamm. Rev. 51, 323e337. O’Shea, T.J., Cryan, P.M., Hayman, D.T.S., Plowright, R.K., Streicker, D.G., 2016. Multiple mortality events in bats: a global review. Mamm. Rev. 46, 175e190. Petr
zelkova´, K., Zukal, J., 2001. Emergence behaviour of the serotine bat (Eptesicus serotinus) under predation risk. Neth. J. Zool. 51, 395e414. Petr
zelkova´, K.J., Zukal, J., 2003. Does a live barn owl (Tyto alba) affect emergence behavior of serotine bats (Eptesicus serotinus)? Acta Chiropterol. 5, 177e184. Petr
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Rodrı´guez-Dura´n, A., Pe´rez, J., Montalba´n, M.A., Sandoval, J.M., 2010. Predation by freeroaming cats on an insular population of bats. Acta Chiropterol. 12, 359e362. Rodrı´guez-Dura´n, A., Rosa, J., 2020. Remarkable variation in the diet of Noctilio leporinus in Puerto Rico: The fishing bat turns carnivorous. Acta Chiropterologica 22 (1), 175e178. Russ, J.M., Jones, G., Mackie, I.J., Racey, P.A., 2004. Interspecific responses to distress calls in bats (Chiroptera: Vespertilionidae): a function for convergence in call design? Anim. Behav. 67, 1005e1014. Russo, D., Ancillotto, L., 2015. Sensitivity of bats to urbanization: a review. Mamm. Biol. 80, 205e212. Russo, D., Maglio, G., Rainho, A., Meyer, C.F.J., Palmeirim, J.M., 2011. Out of the dark: diurnal activity in the bat Hipposideros ruber on Sa˜o Tome´ Island (West Africa). Mamm. Biol. 76 (6), 701e708. Rydell, J., Speakman, J.R., 1995. Evolution of nocturnality in bats: Potential competitors and predators during their early history. Biol. J. Linn. Soc. 54, 183e191. Rydell, J., Entwistle, A., Racey, P.A., 1996. Timing of foraging flights of three species of bats in relation to insect activity and predation risk. Oikos 76, 243e252. Schmitt, L., Greenberg, R., Ibarra-Nu´n˜ez, G., Bichier, P., Gordon, C.E., Perfecto, I., 2021. Cascading effects of birds and bats in a shaded coffee agroforestry system. Front. Sustain. Food Syst. 5, 512998. Scrimgeour, J., Beath, A., Swanney, M., 2012. Cat predation of short-tailed bats (Mystacina tuberculata rhyocobia) in Rangataua Forest, Mount Ruapehu, Central North Island, New Zealand. N. Z. J. Zool 39, 257e260. Serra-Gonc¸alves, C., Lo´pez-Baucells, A., Rocha, R., 2017. Opportunistic predation of a silky short-tailed bat Carollia brevicauda by a tawny-bellied screech-owl Megascops watsonii, with a compilation of predation events upon bats entangled in mist-nets. Barbastella 10, 41e46. Shine, R., Fitzgerald, M., 1996. Large snakes in a mosaic rural landscape: the ecology of carpet pythons Morelia spilota (serpentes: Pythonidae) in coastal eastern Australia. Biol. Conserv. 76, 113e122. Shirley, M.H., Burtner, B., Oslisly, R., Sebag, D., Testa, O., 2017. Diet and body condition of cave-dwelling dwarf crocodiles (Osteolaemus tetraspis, Cope 1861) in Gabon. Afr. J. Ecol. 55, 411e422. Sieradzki, A., Mikkola, H., 2020. A Review of European Owls as Predators of Bats. In: Mikkola, H. (Ed.), Owls. IntechOpen, pp. 1e20. Sinclair, A.R.E., Mduma, S., Brashares, J.S., 2003. Patterns of predation in a diverse predatoreprey system. Nature 425, 288e290. Sorrel, G.G., Boback, S.M., Reed, R.N., Green, S., Montgomery, C.E., de Souza, L.S., et al., 2011. Boa constrictor (Boa constrictor): foraging behavior. Herpetol. Rev. 42, 281. Speakman, J.R., Webb, P.I., 1993. Taxonomy, status and distribution of the Azorean bat (Nyctalus azoreum). J. Zool. 231, 27e38. Speakman, J.R., Lumsden, L.F., Hays, G.C., 1994. Predation rates on bats released to fly during daylight in south-eastern Australia. J. Zool. 233, 318e321. Speakman, J.R., Rydell, J., Webb, P.I., Hayes, J.P., Hays, G.C., Hulbert, I.A.R., et al., 2000. Activity patterns of insectivorous bats and birds in northern Scandinavia (69 N), during continuous midsummer daylight. Oikos 88, 75e86. Speakman, J.R., 1991a. The impact of predation by birds on bat populations in the British Isles. Mamm. Rev. 21, 123e142.

References

Speakman, J.R., 1991b. Why do insectivorous bats in Britain not fly in daylight more frequently? Funct. Ecol. 5, 518. Speakman, J.R., 1995. Chiropteran nocturnality. In: Symposia of the Zoological Society of London, vol. 67, pp. 187e201. Spitzenberger, F., Engelberger, S., Kugelschafter, K., 2014. Real time observations of Strix aluco preying upon a maternity colony of Myotis emarginatus. Vespertilio 17, 185e196. Sprunt, A., 1950. Hawk predation at the bat caves of Texas. Tex. J. Sci. 2, 463e470. Stawski, C., Geiser, F., 2010. Fat and fed: frequent use of summer torpor in a subtropical bat. Naturwissenschaften 97, 29e35. Stephens, D.W., Krebs, J.R., 1986. Foraging theory. Princeton University Press, Princeton, New Jersey, USA. Stone, E.L., Harris, S., Jones, G., 2015. Impacts of artificial lighting on bats: a review of challenges and solutions. Mamm. Biol. 80, 213e219. Szczygie1, H.A., Page, R.A., 2020. When the hunter becomes the hunted: foraging bat attacked by pit viper at frog chorus. Ecology 101, e03111. Tanalgo, K.C., Monfort, N., Hughes, A.C., 2020. Attacked from above and below: new ethological evidence on the predation strategies of corvid and varanid on a cave-roosting bat. Ethol. Ecol. Evol. 32, 596e610. Thomas, A.J., Jacobs, D.S., 2013. Factors influencing the emergence times of sympatric insectivorous bat species. Acta Chiropterol. 15, 121e132. Thomson, S.C., Brooke, A.P., Speakman, J.R., 1998. Diurnal activity in the Samoan flying fox, Pteropus samoensis. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 353, 1595e1606. Threlfall, C., Law, B., Banks, P.B., 2013. Odour cues influence predation risk at artificial bat roosts in urban bushland. Biol. Lett. 9, 20121144. Tidemann, C.R., 1987. Notes on the flying-fox, Pteropus melanotus (Chiroptera: Pteropodidae) on Christmas Island, Indian Ocean. Aust. Mammal. 10, 89e91. Trewhella, W.J., Rodriguez-Clark, K.M., Davies, J.G., Reason, P.F., Wray, S., 2001. Sympatric fruit bat species (Chiroptera: Pteropodidae) in the Comoro Islands (Western Indian Ocean): diurnality, feeding interactions and their conservation implications. Acta Chiropterol. 3, 135e147. Twente, J.W., 1954. Predation on bats by hawks and owls. Wilson Bull. 66, 135e136. Valdez, J.W., 2020. Arthropods as vertebrate predators: a review of global patterns. Global Ecol. Biogeogr. 29, 1691e1703. Verboom, B., Huitema, H., 1997. The importance of linear landscape elements for the pipistrelle Pipistrellus pipistrellus and the serotine bat Eptesicus serotinus. Landsc. Ecol. 12, 117e125. Welbergen, J.A., 2006. Timing of the evening emergence from day roosts of the grey-headed flying fox, Pteropus poliocephalus: the effects of predation risk, foraging needs, and social context. Behav. Ecol. Sociobiol. 60 (3), 311e322. Welch, J.N., Leppanen, C., 2017. The threat of invasive species to bats: a review. Mamm. Rev. 47, 277e290. Wilkinson, G.S., 1985. The social organization of the common vampire bat. Behav. Ecol. Sociobiol. 17, 111e121. Wilson, D.E., Mittermeier, R.A., 2019. Handbook of the mammals of the world. In: Bats, vol. 9. Lynx Edicions, Barcelona. Yager, J., Williams, D., 1988. Predation by gray snapper on cave bats in the Bahamas. Bull. Mar. Sci. 43, 102e103. Zhao, X., Sun, H., Tang, Z., Flanders, J., Zhang, S., Ma, Y., 2010. Characterization of the sleep architecture in two species of fruit bat. Behav. Brain Res. 208, 497e501.

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Energetics of foraging bats

10

Liam P. McGuire1, Justin G. Boyles2 1

Department of Biology, University of Waterloo, Waterloo, ON, Canada; 2School of Biological Sciences, Southern Illinois University, Carbondale, IL, United States

Energy budgets and metabolism At the core of life history theory is the idea that animals function to convert energy into offspring. Bats, in particular, are a fascinating group of animals to consider from the perspective of energetics. Bats are nearly cosmopolitan, and different species have adapted to a wide range of environments and environmental conditions. Bats (along with birds) represent a unique confluence of energetic constraints because as flying animals, locomotion incurs great energetic cost, and as generally smallbodied animals, thermoregulation can impose a substantial energetic challenge. The cost of reproduction is also very high, especially for females. For these reasons and more, there is a rich history of energetic studies on bats. For readers that do not generally dabble in the worlds of physiology, energetics, and thermoregulation, an excellent place to begin your adventure is Speakman and Thomas’ (2003) chapter on the physiology and energetics of bats. Much of that chapter is relevant to considerations of foraging energetics, but we do not attempt to recreate that chapter here. Instead, we rather hope that this chapter will serve as a supplement or extension to that chapter, with specific focus on foraging energetics. Energy balance is a key determinant of fitness, and as we will explore, there are many aspects of energy balance related to foraging, including energy gained from food and the environment, the energy costs to obtain and digest food, and strategies to maintain energy balance despite spatial and temporal variation in food availability.

Energy balance [ energy in L energy out Ecological energetics is traditionally framed in the concept of energy balance. In the simplest sense, energy inputs must equal energy expenditure over the life of the animal. More realistically, energy budgets represent a dynamic balance between energy input and energy expenditure occurring simultaneously on several timescales, ranging from minutes to hours to years. How an animal manages the energy budget depends on physiology, morphology, life history traits, the environment, and other factors. At one extreme, some organisms balance energy on short timescales, A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.00012-7 Copyright © 2024 Elsevier Inc. All rights reserved.

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essentially expending energy as soon as it is consumed and converted into a useable form with very little buffer against environmental perturbations. At the other extreme, some organisms consume food and store energy for later use when necessitated by life history demands (e.g., reproduction) or an environmental nadir (e.g., winter or drought). Thus, we can consider a spectrum of capital to income energy balance strategies, where capital strategies involve pre-emptive energy storage to survive future energetic challenges and income strategies represent a “just in time delivery” approach to obtaining energy resources as they are required. Animals maintain different pools of energy, most commonly in form of three major macronutrientsdlipids (fat), carbohydrates, and proteins. Fat is the primary energy store, comprised of high-energy-density triglycerides which can be stored in large quantity in adipose tissue. Carbohydrates are typically stored in the form of glycogen (primarily in the liver) which is critical for maintaining homeostasis (e.g., blood glucose), but glycogen stores are limited and low in energy density because of extensive bound water associated with the storage polymers. Protein is not stored per se, rather can only be deposited as functional tissues such as muscles and organs. Thus, drawing on energy or nutrients stored in protein requires the catabolism of functional tissues and leads to their degradation. Nevertheless, there may be dramatic seasonal changes in lean tissue composition, whether providing energy storage, as a functional consequence of fat storage (e.g., larger flight muscles to carry larger fat loads), or for aspects of maintaining homeostasis such as replenishing intermediate compounds of the citric acid cycle. Heat is also important in energy balance equations. All metabolic processes generate heat as a by-product. Heat is not directly useful metabolically and is considered low-grade energy because it cannot be used to perform physiological work. However, environmental sources of heat can effectively replace metabolic heat production in some cases. Basking may be an important energy saving thermoregulatory strategy for some species (Vaughan, 1987), and many species of bats regularly reduce the energetic costs of rewarming from torpid body temperatures by taking advantage of environmental sources of heat (e.g., solar radiation or social thermoregulation) to passively rewarm (Chruszcz and Barclay, 2002; Ruczy
nski, 2006; Currie et al., 2015). Conversely, excessive heat is a problem as clearly evident in recent extreme heat events (Ratnayake et al., 2019). Excessive heat gain from solar radiation has also been hypothesized to explain why bats may be constrained to nocturnal active periods (Speakman et al., 1994; Voigt and Lewanzik, 2011). The trade-offs and implications of energy balance vary across time scales. Energy inputs must equal energy expenditure over the life of the animal, but variation on shorter, ecologically relevant time scales drives behavioral decisions. For example, within a nocturnal foraging period, the short-term balance of foraging success and foraging cost might determine if a bat should continue foraging, adopt a different foraging strategy, or abandon foraging effort for the night and return to the roost (behavioral decisions as described by foraging theory;

Energy budgets and metabolism

Stephens and Krebs, 1986). On weekly or monthly schedules, energy balance might influence a bat to move to a new roost and forage in different places. Seasonally, energy balance might determine if reproduction or overwinter survival is successful, and over many years or generations, local population persistence and distribution ranges may be affected.

Metabolic rate: Basal, resting, torpid, and flight Understanding energy balance requires an understanding of both energy intake (energy taken in from food and exogenous sources) and energy output. Energy intake is an intuitive idea (which we expand on below), but there are many ways to measure and describe energy expenditure. The unifying concept for understanding energy expenditure is a metabolic rate. Technically, the metabolic rate describes the rate of energy expenditure as a result of all biochemical processes in the organism. Conceptually, it might be easier to think of metabolic rate as the amount of energy converted from chemical energy in food to work energy used to power life processes. In ecology and physiology, we measure and describe several different aspects of metabolic rate, depending on the question at hand. A standard measurement of the metabolic rate that is used to compare the rate of energy expenditure across animals is the basal metabolic rate (BMR; Fig. 10.1), the rate of energy expenditure of an endothermic animal at rest within the thermoneutral zone (the range of temperatures which do not cause an increase in metabolic rate to maintain euthermic body temperature). Under these conditions, the metabolic rate is at a minimum (for a normothermic individual) and is not increased by digestive processes, activity, thermogenesis, stress, or any other process that requires energy. As a common benchmark, BMR is a useful measurement, but animals rarely experience BMR outside of experimental conditions specifically designed for such measurements. In practice, we often consider resting metabolic rate (RMR) instead. Outside the thermoneutral zone, the metabolic rate increases as animals expend energy to maintain body temperature, warming themselves at cooler temperatures and cooling themselves at warmer temperatures (Fig. 10.1). At rest, there is little remarkable about the BMR of bats as it falls within the expected range for their body size (Speakman and Thomas, 2003). Like other smallbodied endotherms (body mass of most bat species is 50 km to foraging areas (Fahr et al., 2015). However, bats adjust flight speed to reduce the cost of transport in response to wind conditions encountered during commuting, whether decreasing airspeed with tailwind assistance, or increasing airspeed in response to crosswinds (Sapir et al., 2014). There are also several studies that document bats flying at speeds near Vmp when foraging, including Kuhl’s pipistrelles (Grodzinski et al., 2009), Nathusius’ pipistrelles (Troxell et al., 2019), and noctule bats (Nyctalus noctula; Jones 1995). Kuhl’s pipistrelles and noctule bats foraged at speeds slightly greater than predicted Vmp (Jones, 1995; Grodzinski et al., 2009), consistent with flight speed theory, but Nathusius’ pipistrelles foraged at speeds somewhat less than Vmp (Troxell et al., 2019). In

Energy required to get food

a contrary example, eastern red bats (Lasiurus borealis) and hoary bats (Lasiurus cinereus) were observed foraging at flight speeds greater than predicted Vmr (Salcedo et al., 1995). Providing context to foraging flight speed requires a consideration of the specific actions during foraging. Pursuing prey that require rapid responses and highly maneuverable flight may require slower flight speeds, while direct pursuit of fast flying prey may result in flight speeds that are greater than predicted by theory. Flight performance related to the nature of the prey being pursued may affect flight cost. As noted above, the foraging gain ratio, where bats balance the energetic benefits of foraging against the costs of foraging flight, is likely more informative than the simple cost of foraging. Whether due to foraging flight style or wing morphology (which is adapted to foraging flight; Norberg and Rayner, 1987; Bullen and McKenzie, 2001), the energetic cost of flight drives behavioral trade-offs for many species. The long and narrow wings of molossids are adapted to rapid flight in open spaces but are not suited to more cluttered environments. In enclosed environments such as forest gaps, the increased costs of highly maneuverable flight more than double flight metabolic rate (Voigt and Holderied, 2012). Therefore, bats adapted to rapid, direct flight in open spaces are likely excluded from foraging in more cluttered environments by the increased energetic cost of highly maneuverable flight. The cost of maneuvering flight is also related to a perch hunting foraging strategy, as illustrated by a comparison of Mediterranean horseshoe bats (Rhinolophus euryale) and Mehely’s horseshoe bats (Rhinolophus mehelyi). Both species have similar wing area, but Mehely’s horseshoe bats are heavier and thus have higher wing loading. Greater wing loading increases flight cost, and a 20% increase in wing loading between the two species translated into 50% greater flight cost (Voigt et al., 2010a). Consequently, Mehely’s horseshoe bats adopt a perch hunting strategy rather than aerial hawking like Mediterranean horseshoe bats (Dietz et al., 2009). Perch hunting is not a common foraging strategy in bats (most common in Rhinolophidae), but given the energetic constraints associated with wing morphology and wing loading, it is not surprising that most perch-hunting species are larger bodied with low aspect ratio wings (Lee et al., 2021). Wing morphology is important to understand aerodynamics and flight costs, but it is also important to consider the aerodynamic impacts of other body structures. For many species of bats, large ears adapted for echolocation affect aerodynamics and flight performance. The costs and consequences of large ears are demonstrated by comparisons of brown long-eared bats and Pallas’ long-tongued bats flying in a wind tunnel (Ha˚kansson et al., 2017). Large ears increase drag but also generate additional lift. The resulting increased power required for flight leads to lower Vmp. Thus, there is an evolutionary trade-off, where larger ears may improve echolocation performance but limit flight performance. Similarly, there are flight performance consequences for aspects of the head and face, body shape, pelage, feet, and tails (Bullen and McKenzie, 2009). Aerial hawking molossids that forage in open spaces with fast forward flight have the most aerodynamic morphology, which contrast with perch hunting species, while gleaning species and species that forage

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along edges or cluttered habitat are intermediate in terms of aerodynamic cleanliness (Bullen and McKenzie, 2009). The hovering flight of nectarivorous bats represents an extreme form of foraging flight, where hovering represents the speeds far below Vmp (forward flight speed ¼ 0). Although there are many examples of nectarivorous bats that hover while foraging, hovering flight can typically only be sustained for a few seconds (Voigt and Winter, 1999; Welch et al., 2008; Suarez et al., 2009). In small-bodied nectarivores, hovering flight may cost 50% more than forward flight (Voigt and Winter, 1999). Furthermore, allometric scaling of flight cost increases the relative cost of hovering, and likely imposes an upper limit of w30 g body mass for hovering bats (Voigt and Winter, 1999).

Variation in wing loading With fixed wing morphology, as mass (and hence wing loading) is increased, flight cost is also increased (Fig. 10.2B). Aerodynamic theory predicts that flight cost should scale to the power of 1.56, consistent with empirical observations of Pallas’ long-tongued bats (Voigt, 2000). In addition to flight cost, increased wing loading can also compromise various aspects of maneuverability and flight performance (Brigham, 1988; MacAyeal et al., 2011; Voigt and Lewanzik, 2012). Variation in wing loading may thus result in changes in foraging habits (i.e., individuals with high wing loading foraging in less cluttered habitats), and different access to prey resources (Kalcounis and Brigham, 1995). There are several ecologically relevant scenarios under which a foraging bat may contend with increased wing loading. Female bats face great variation in flight cost as body mass increases through pregnancy. At birth, pups often weigh >20% of their mother’s body mass (Barclay and Harder, 2003), and pregnant female body mass may be 50% greater than during the postlactation period (e.g., Brazilian freetailed bats; Sommers et al., 2019). With a 50% increase in body mass, a pregnant female is predicted to experience a 45%e50% increase in flight cost (Norberg, 1995). Consistent with the predictions of aerodynamic theory, observations of free-flying lesser long-nosed bats resulted in a 40% increase in flight cost during late pregnancy. Wing loading also varies on short time scales as bats gain or carry mass during foraging. Insectivorous bats can consume prey that represent a substantial proportion of their body mass (e.g., 20%e30% of body mass in cave myotis Myotis velifer; Kunz, 1974) and can do so in a very short period of time. In Mexico, black mastiff bats (Molossus rufus) were observed to forage for only w25 min per night, but during that brief foraging time, they consumed w15% of their body mass in insects, providing enough energy to offset their flight costs and the energetic costs incurred during roosting for the coming day (Fenton et al., 1998). Increased wing loading is also experienced by frugivorous species that carry fruits in flight (Norberg, 1995). For example, Jamaican fruit-eating bats in Panama preferentially selected the largest figs available from fruiting trees, representing up to w20% of body mass (Morrison,

Energy required to get food

1978). Carrying these fruits was estimated to increase flight cost by w10%, and bats made repeated foraging flights throughout the night, but the energy content of the fruit was more than enough to offset the increased cost of commuting flight while carrying the heavy load (Morrison, 1978). Notably, differences in roosting ecology resulted in commuting costs that were half as much for male bats that roosted in foliage near available fruiting trees than for females that roosted in tree hollows that were more limited in availability and thus required longer commuting distances.

Energetic cost of terrestrial locomotion Although very rare, terrestrial locomotion is important for some bats. Common vampire bats (Desmodus rotundus) are well known for great terrestrial agility (Riskin and Hermanson, 2005). However, the New Zealand lesser short-tailed bat (Mystacina tuberculata) is the only species for which terrestrial foraging is important (but see Hand et al., 2009 for discussion of fossil species), spending 30%e40% of their time foraging on the ground (Carter and Riskin, 2006). Measurements of the metabolic rate in crawling Thomas’ mastiff bat (Voigt et al., 2012) provide useful context for considering the energetics of terrestrial foraging. At a speed of w0.5 m/s, the metabolic rate of crawling bats was equivalent to that of flying bats. While metabolic power (cost per unit time) may be similar, the costs of transport (cost per unit distance) remain 10
greater for terrestrial locomotion than flight. Despite these energetic costs, it has been hypothesized that the evolution of terrestrial foraging in New Zealand lesser short-tailed bats may have been driven by the ready availability of diverse prey sources. From the energy balance perspective, the energy output of terrestrial foraging is not reduced (and may be increased) compared to flight, but the energy intake side of the equation may drive net energetic benefit (increased foraging gain ratio).

Cost of echolocation Echolocation is also important to consider in context of foraging energetics. Whether used to navigate cluttered habitats in search of fruit or flowers, or to detect volant prey, echolocation is an important aspect of foraging for most bats (pteropodids being a notable exception). At rest, echolocation imposes substantial energetic costs for bats, with estimates of echolocation cost equivalent to 7e12 times BMR (Speakman et al., 1989), approaching the energetic cost of flight. However, the costs of flight and echolocation are not additive (Speakman and Racey, 1991; Voigt and Lewanzik, 2012) and bats can couple echolocation, exhalation, and muscle contractions of the wing beat cycle to offset the costs of echolocation (Arita and Fenton, 1997). Still, echolocation is not always energetically negligible during flight, and high-intensity echolocation calls do indeed incur metabolic costs (Currie et al., 2020). One potential implication is for the energetics of foraging associated with anthropogenic noise pollution. It is clear that anthropogenic noise affects bat foraging behavior (Schaub et al., 2008; Wang et al., 2022; Hooker et al., 2023), possibly due to distraction (Allen

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et al., 2021; Domer et al., 2021), and although bats alter the structure of their echolocation calls in noisy environments (Bunkley et al., 2015; Song et al., 2019), it is not clear whether intensity and echolocation cost are increased.

Energy in food

Variation in diet composition Dietary items vary in composition of the three major macronutrients (lipids, carbohydrates, and protein). Generally, arthropods are high in protein and lipids and low in carbohydrates, while fruits are high in carbohydrates and lower in protein and lipids. Although all contain energy and may be interconverted among pools in the body (Karasov and Martinez del Rio, 2007), the composition of the diet requires digestive physiology suitable for accessing the energy and nutrients in the ingested food. Bats are renowned for their diversity on many axes, and especially dietary diversity. Most species are insectivorous or frugivorous, but others consume nectar, vertebrate prey, or blood. With this variation in diet comes variation in digestive physiology (Schondube et al., 2001). For example, insectivorous bats have high trehalase and aminopeptidase-N activity, allowing them to digest the carbohydrates (trehalose is the primary storage carbohydrate in arthropods) and proteins in their insect prey, but low sucrase and maltase activity because there are few plant sugars in the diet. Carnivorous species and vampire bats have high aminopeptidase activity and low maltase and sucrase activity but also have low trehalase activity, reflecting their high-protein, nonarthropod diets. Vertebrate or arthropod prey is high in protein, but fruit and nectar diets are low in protein. Therefore, while frugivorous and nectarivorous species have high sucrase and maltase activity to digest dietary sugars, they often consume insects to meet protein demands (Barros et al., 2013; Clare et al., 2014) and maintain aminopeptidase-N activity to digest insect protein in their diet.

Refractory content and implications for the energetics of different diets Most dietary items consumed by bats contain refractory, or indigestible, material (Fig. 10.3). Refractory content of fruits is primarily lignin, cellulose, and hemicellulose (Wendeln et al., 2000), and refractory material in arthropods is primarily chitin in the cuticle3 (Bell, 1990). Nectar is one exception and contains no refractory

3

Some species of bats produce an endogenous chitinase enzyme (Strobel et al., 2013) and bats may also benefit from chitinase produced by gut microbes (Whitaker et al., 2004). However, it is unclear whether chitinase would release enough energy to make a meaningful difference in the energetics of day-to-day active season foraging. Chitinase may instead help break apart insect tissues for easier digestion or may provide a slow release of nutrients during hibernation.

Energy in food

FIGURE 10.3 Refractory content is highly variable among diets. High refractory content diets would require bats to fly with increased gut content mass, increasing wing loading and flight cost. Seeds and leaves are both very high in refractory content, and there are no species of bats that are primarily folivorous or granivorous. Fruit and arthropods span a wide range of refractory content, but bats can use behavioral strategies to reduce refractory content and increase digestibility (white arrows). Frugivores spit out pulp and insectivores can remove body parts such as wings and legs. On average, an insect diet is expected to be comprised of w18% refractory content, indicated by a star (Bell, 1990). Nectar may be lower energy content on a dry mass basis, but it is nearly 100% digestible.

material; it is therefore essentially 100% digestible. Refractory material must be passed through the digestive tract and creates a load that must be carried by the animal. In terrestrial animals, this additional load might be negligible. However, the high cost of flight means that, in general, bats are precluded from consuming food sources with low energy and high refractory material, even if they are found in very high densities. This likely explains why no bats are granivorous or heavily herbivorous, even though granivory and herbivory are successful feeding adaptations that have evolved repeatedly in ungulates, primates, rodents, marine mammals, marsupials, and others. This is, in part, because liberating energy from fibrous plant materials (high in refractory content) is slow and inefficient (some bats chew on and occasionally eat leaves, but this is likely for protein or calcium, not energy; Kunz and Ingalls, 1994; Nelson et al., 2005). Many mammalian herbivores have enlarged

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sections in the digestive tract to facilitate microbial fermentation of otherwise indigestible materials, but for flying bats, this strategy would be doubly counterproductive. Bats would have to ingest large quantities of leaves and have enlarged digestive tracts, both of which are precluded by increased flight cost associated with greater wing loading. Even when bats consume foods that might have high refractory content like insects, they often have behavioral adaptations to maximize efficiency in obtaining energy while minimizing costs associated with doing so. Arthropods are highly variable in refractory content. Wings, elytra, and legs are largely cuticle and scales, with little digestible content. Unsurprisingly, many insectivorous bats discard parts of moths and beetles that have low energy density and/or digestibility (Jones, 1990; Barclay et al., 1991; Czaplewski et al., 2018), effectively reducing the refractory content of the diet and increasing digestibility. When fed mealworms (Tenebrio molitor) under captive conditions, Bechstein’s myotis (Myotis bechsteinii) and brown long-eared bats were able to extract 97% or more of the energy available in the diet (Becker et al., 2012). However, when fed natural prey (various moth species), little brown myotis (Myotis lucifugus), long-eared myotis (Myotis evotis), and long-legged myotis (Myotis volans) extracted approximately 75% of the energy available in the diet (Barclay et al., 1991). Furthermore, digestive efficiency was positively correlated with moth body size because bats removed legs, wings, and sometimes heads from larger moths before consuming the body parts that were lower in refractory content, but small bodied moths were consumed whole (Barclay et al., 1991). A general avoidance of food sources with low energy to mass ratios might also explain why bats sometimes limit consumption of food items that would seem otherwise acceptable. For example, mosquitoes are cosmopolitan and often ubiquitous, but no bat species has ever been shown to consume mosquitoes in quantities even approaching their availability in the environment. The most likely explanation for this is that mosquitoes are small and when full, carry substantial water weight in blood. They are therefore relatively high in refractory content and water, and not energy dense enough to make them feasible as a main prey item for flying bats (Wetzler and Boyles, 2018). Fruit is also variable in refractory content, as skin, pulp, seeds, and juice are differently digestible. Skin, pulp, and seeds are all relatively high in cellulose and lignin and therefore have low digestibility. Like insectivorous bats discarding wings or legs, frugivorous species often suck the juice from fruits and discard the fibrous pulp (Funakoshi et al., 1993). Jamaican fruit-eating bats suck the juices and eject the difficult to digest pulp from figs. They are able to extract 96% of the metabolizable energy in the swallowed juice, but they discard upward of 75% of the total energy in the fruits in the pulp (Morrison, 1980). The raw fruit consumed by a bat over the course of a night could weigh several times more than the bat if consumed whole. By discarding the pulp and focusing on the juice, frugivorous bats obtain a highly digestible diet while not paying the energetic cost of flying with a large mass of refractory content in the digestive tract.

Energy in food

The constraints of flight also impose trade-offs on digestive morphology. Bats have smaller digestive tracts (shorter intestines, less surface area) than comparably sized terrestrial mammals (Price et al., 2015). Reduced digestive tracts decrease intestinal volume by more than 50%, which also leads to decreased mass of gut contents and short retention times (Cabrera-Campos et al., 2021). Short digestive tracts and short retention times (e.g., 30 min for Jamaican fruit-eating bats; Ortega and Castro-Arellano, 2001) are normally associated with lower digestive efficiency (less time to digest and less surface area over which to absorb nutrients), which could pose a further energetic constraint for bats. Bats, especially frugivorous bats, have instead evolved increased paracellular absorption to achieve increased digestive efficiency despite short retention times (Caviedes-Vidal et al., 2007, 2008). Paracellular absorption is a process by which nutrients are absorbed into the body through the gaps between cells of the intestinal lining rather than being absorbed through cells (i.e., transcellular absorption) as is typical for mammals. Paracellular absorption is passive and rapid and may account for as much as 70% of glucose absorption in some fruit-eating bats (Tracy et al., 2007; Caviedes-Vidal et al., 2008). Paracellular absorption is also important for insectivorous bats, including paracellular absorption of amino acids (Price et al., 2013), with paracellular nutrient absorption rates double the rates observed for insect-eating rodents (Price et al., 2014).

Rapidly accessing dietary energy As flight is an exceedingly expensive form of locomotion, nightly foraging creates a short-term mismatch between energy availability and energy demand, and bats have evolved a suite of physiological “tricks” to compensate. Most mammals are limited in their ability to quickly convert exogenous (i.e., recently ingested) food into useable energy (ingest, digest, absorb, assimilate) and transport it to muscles to be oxidized to power locomotion. Thus, most mammals power locomotion largely with endogenous energy stores, with recently ingested food providing only 25% e30% of the energy required for exercise (Welch et al., 2008). At no time is the mismatch between energy availability and energy demand greater than at the beginning of the foraging period. When leaving the roost for the first foraging bout of a night, most bats have been fasting for 12 or more hours, and during the reproductive period, females have the added energy demands associated with pregnancy and lactation. This means readily available endogenous energy is likely low as bats begin their nightly foraging bouts, but unlike terrestrial mammals, bats must immediately begin expending huge amounts of energy to power foraging flight. Stored fat (which may be converted to ketones; see discussion in Boyles et al., 2016; Baloun et al., 2019) is used to fuel initial periods of flight (Welch et al., 2008), but bats can quickly switch over to powering foraging flight with the nutrients they ingest while foraging. Nectar is easily digestible with no refractory content (Fig. 10.3) and can quickly be digested to simple sugars that can be rapidly absorbed by paracellular transport.

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Within 10 min of their first drink of nectar, Pallas’ long-tongued bats use exogenous nutrients to fuel flight and nutrients in the diet can account for almost 80% of the energy expended on current foraging flight (Welch et al., 2008). Even with higher refractory content diets, similar patterns have been documented for frugivores and insectivores. Egyptian fruit bats (Rousettus aegyptiacus) are frugivores, and much larger than any nectarivorous bats (w15
the body mass of Pallas long-tongued bats) yet within 10 min are also able to fuel flight with energy from food they have just eaten (Amitai et al., 2010). Lesser bulldog bats (Noctilio albiventris) took slightly longer to use dietary nutrients to fuel flight (27 min) but were able to fuel over 90% of flight costs with energy in the food they had just eaten (Voigt et al., 2010b). Thus, foraging bats, regardless of body size or diet, are exceptional among mammals in being able to rapidly use energy from the diet to fuel current exercise and cover most flight costs with recently ingested energy. The high cost of flight requires bats to rapidly mobilize stored energy (primarily from fat stores) at the beginning of the night, but bats are able to quickly overcome the mismatch in energy availability and demand early in the foraging bout by feeding alone.

Spatial and temporal variation in the foodscape The rate of energy and nutrient acquisition possible for any animal is ultimately limited by the amount and density of energy and nutrients available in the environment and mediated by the ability of the animal to detect, capture, consume, digest, and assimilate energy and nutrients. This interaction between environment and physiology dictates the “foodscape” available to an animal (Searle et al., 2007). From the perspective of a foraging bat, the goal is to gather energy and nutrients on the foodscape in the most efficient way possible given the current conditions.4 The foodscape varies depending on foraging behavior of a species, which we have covered above, and spatial and temporal variability in food availability, which we focus on here. Some insectivorous species might experience a relatively homogenous distribution of energy on the landscape (at least during summer months), while some nectarivorous and frugivorous species might experience a patchy distribution of energy. Within foraging guilds, the foodscape might vary based on specific prey items, competition with conspecifics, or small-scale habitat variation. As a general approximation, patchy food sources (e.g., fruit, nectar, blood) tend to be high in useable energy per item, while more uniform food sources (e.g.,

4

As a brief aside, energy is of course not the only consideration during foraging. Bats must also obtain a suitable balance of macro- and micronutrients, minerals, and vitamins, while coping with or avoiding noxious dietary items such as plant secondary metabolites or toxins sequestered in prey tissues. There are many fascinating avenues to consider dietary ecology in the context of these issues, but we focus here more generally on energetics.

Spatial and temporal variation in the foodscape

insects) tend to be low in useable energy per item (compare with refractory content; Fig. 10.3). This variation strongly affects the foraging ecology and behavior of bat species and puts constraints on the niches available to bats. The foodscape also varies on multiple timescales. Strong seasonality in temperate climates can lead to extreme fluctuations in food availability across the annual cycle. Seasonal fluctuations in food availability are also common in subtropical and tropical climates but are more muted. In any environment, bats must have behavioral and physiological mechanisms that allow them to weather extended periods when the energetic cost of foraging would outweigh the energy gained by that foraging (extended periods of negative energy balance). Temperate-zone insectivorous species accomplish this through migration or hibernation (Wojciechowski et al., 2007; Boyles et al., 2013; Webber and McGuire, 2022). Migrating bats that remain active through winter continue to incur the high energetic costs of foraging yearround by taking advantage of continent-level variation in the foodscape. Hibernating bats instead use physiological mechanisms (decreased metabolic rate and body temperature) to avoid the high energetic costs of foraging when the foodscape is unfavorable. Because tropical and subtropical bats face less extreme seasonal fluctuations in the foodscape, their responses are also less extreme. Here, bats tend to migrate on regional scales to follow food availability or use short-term torpor as opposed to hibernation (Stawski et al., 2014). The foodscape also fluctuates within or across nights, during all seasons (Fig. 10.4). During the active season, fluctuations can be related to prey life history (e.g., insect emergences), prey movements (e.g., large mammals fed on by vampire bats), or abiotic factors like weather. When available food resources are temporarily limited during the active season, negative energy balance can quickly become critical because of limited energy stores. In perhaps the most extreme and famous example, common vampire bats can only go two nights without successfully feeding. A third night without a blood meal risks driving negative energy balance to the point of starvation (McNab, 1973). There are far more general causes of short-term nadirs in energy availability on the foodscape. For example, rainstorms may preclude foraging for most species as rain limits availability of some prey (e.g., insects) and interferes with echolocation making detection of prey more difficult (Griffin, 1971), while also increasing the energetic cost of flight (Voigt et al., 2011). In all but the lightest rain (Belwood and Fullard, 1984), the energetic costs of foraging therefore usually outweigh the energetic gain. Likewise, hoary bats which had recently returned to their summer breeding grounds were faced with late spring storms that brought cold temperatures and a mix of snow and rain over multiple days. To cope with this challenge, pregnant females became torpid for up to 5 days, and when conditions improved bats became active, resumed foraging, and gave birth within a few days (Willis et al., 2006). Daily torpor is a common response to inclement weather among temperate bats, and while sub-tropical and tropical species are not generally considered heterothermic, there is increasing evidence that some species are able to use torpor in response to short-term energy limitation (Stawski and Geiser, 2010).

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FIGURE 10.4 Model-predicted temporal variation in the quality of the foodscape for a northernhemisphere insectivorous bat (e.g., little brown myotis) based on real weather data from Carbondale, Illinois, USA (37.52 N, 89.25 W) in 2016. Notice that variation happens on both daily and seasonal temporal scales. During the summer (active season), the foodscape is favorable on most nights, except when it rains. During the winter (inactive season), the foodscape is unfavorable on most nights, except for a few warm nights. The model (from Boyles, Brack, Marshall, and Brack, in review) estimates the likelihood of a population of bats foraging on each night given the availability of flying insects. It accounts for life cycle of the insects (e.g., emergence and diapause), the probability of insects flying based on temperature, and the effect of precipitation on insect activity. Little brown myotis photo by Sherri and Brock Fenton.

During the inactive season, insectivorous bats that use prolonged hibernation must cope with long periods in which the foodscape is unfavorable and energetic costs of foraging would greatly outweigh the energy gained. Bats prepare for hibernation by depositing large fat and lean mass stores (Kunz et al., 1998; McGuire et al., 2022) which represent the primary energy source until they emerge from hibernation in spring (but see below for discussion of winter foraging). The energy balance perspective is helpful in considering the strategies to deposit fat stores prior to hibernation. Building a substantial fat store requires positive energy balance, which can be achieved either by increasing energy intake or decreasing energy output. There is evidence for both strategies. When preparing for hibernation, bats may become hyperphagic, greatly increasing foraging effort and energy intake (McGuire et al., 2009; Suba et al., 2010). However, other studies have found no evidence of prehibernation hyperphagia (McGuire et al., 2016). Alternatively (or additionally), bats may reduce daily energy expenditure by increasing the expression of daily torpor, thus driving an increasingly positive energy balance without increasing energy intake

Conclusion

(Krzanowski, 1960; Kokurewicz and Speakman, 2006). In an experimental study, brown long-eared bats selected colder roosting temperatures in the prehibernation period, which allowed them to increase torpor expression and deposit more mass, despite having lower digestive efficiency (Speakman and Rowland, 1999). Thus, bats can manipulate both energy intake and energy output to drive positive energy balance when foraging in preparation for hibernation. Historically, it was thought that foraging was limited during the inactive season (Whitaker and Rissler, 1993), in part because of low insect activity. More recently, there is accumulating evidence that hibernating bats take advantage of warm nights for foraging, especially at low-temperate latitudes (Boyles et al., 2006; Zahn and Kriner, 2016; Bernard et al., 2021). Further, climate change has strongly shifted insect activity in spring and autumn, which may be leading to a more favorable foodscape later in the autumn and earlier in the fall for hibernating bats (Boyles, Brack, Marshall, and Brack, In Review).

Conclusion The ability to fly makes bats exceptional among mammals. Flight has been important in the radiation of bats, and while flight is associated with a low cost of transport (cost per unit distance), flight incurs exceptionally high cost per unit time. Thus, regardless of the varied and diverse food sources that bats consume, all bats must obtain sufficient energy from foraging to overcome the cost of flight. Accordingly, bats use a combination of behavioral and physiological adaptations to either increase energy gain or reduce energy cost, whether optimizing the immediate foraging gain ratio, or balancing the energy budget on shorter or longer timescales. We have touched on many of these energetic considerations here, but there is much more that can be done from an energetic perspective of foraging. Many studies have worked through calculations of daily energy expenditure to evaluate aspects of foraging costs and dietary energy. For example, Morrison (1978) calculated that Jamaican fruit-eating bats expended 43.9 kJ of energy each day, of which foraging flight accounted for 4.33 kJ, but that the energy available in the figs eaten exceeded flight and daily maintenance costs by more than 40%. Similarly, Kurta et al. (1989) calculated daily energy expenditure for pregnant and lactating little brown myotis. Foraging flight was the costliest component of the daily energy budget (4.46 kJ/h), compared with 0.52 kJ/h for day roosting and 0.82 kJ/h for night roosting. Lactating females are predicted to require 6.7 g of insects to meet these costs, which may require 4 h of foraging. The purpose of such energetic calculations is not to demonstrate that bats can obtain enough energy from foraging to survive.clearly, they do. But taking an energetic perspective on foraging can provide useful context for many behavioral and physiological adaptations and help us to understand many aspects of the ecology of bats.

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Acknowledgments Thanks to Danilo Russo and Brock Fenton for the invitation to contribute this chapter and thanks also to the many colleagues, collaborators, and students with whom we have discussed bat energetics over the years. LPM was supported by the Natural Sciences and Engineering Research Council of Canada during the preparation of this manuscript.

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Ortega, J., Castro-Arellano, I., 2001. Artibeus jamaicensis. Mamm. Species 2001, 1e9. Pennycuick, C., 1975. Mechanics of flight. Avian Biol. 5, 1e73. Pennycuick, C.J., 2008. Modelling the Flying Bird. Elsevier. Price, E.R., Brun, A., Caviedes-Vidal, E., Karasov, W.H., 2015. Digestive adaptations of aerial lifestyles. Physiology 30, 69e78. Price, E.R., Brun, A., Fasulo, V., Karasov, W.H., Caviedes-Vidal, E., 2013. Intestinal perfusion indicates high reliance on paracellular nutrient absorption in an insectivorous bat Tadarida brasiliensis. Comp. Biochem. Physiol. Mol. Integr. Physiol. 164, 351e355. Price, E.R., Rott, K.H., Caviedes-Vidal, E., Karasov, W.H., 2014. Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level. J. Exp. Biol. 217, 3483e3492. Ratnayake, H.U., Kearney, M.R., Govekar, P., Karoly, D., Welbergen, J.A., 2019. Forecasting wildlife die-offs from extreme heat events. Anim. Conserv. 22, 386e395. Rayner, J., 1999. Estimating power curves of flying vertebrates. J. Exp. Biol. 202, 3449e3461. Rayner, J.M., 1988. The evolution of vertebrate flight. Biol. J. Linn. Soc. 34, 269e287. Riskin, D.K., Hermanson, J.W., 2005. Independent evolution of running in vampire bats. Nature 434, 292. Ruczy
nski, I., 2006. Influence of temperature on maternity roost selection by noctule bats (Nyctalus noctula) and Leisler’s bats (N. leisleri) in Bia1owie_za Primeval Forest, Poland. Can. J. Zool. 84, 900e907. Sahley, C.T., Horner, M.A., Fleming, T.H., 1993. Flight speeds and mechanical power outputs of the nectar-feedint bat, Leptonycteris curasoae (Phyllostomidae: glossophaginae). J. Mammal. 74, 594e600. Salcedo, H., Fenton, M., Hickey, M., Blake, R., 1995. Energetic consequences of flight speeds of foraging red and hoary bats (Lasiurus borealis and Lasiurus cinereus; Chiroptera: Vespertilionidae). J. Exp. Biol. 198, 2245e2251. Sapir, N., Horvitz, N., Dechmann, D.K., Fahr, J., Wikelski, M., 2014. Commuting fruit bats beneficially modulate their flight in relation to wind. Proc. Biol. Sci. 281, 20140018. Schaub, A., Ostwald, J., Siemers, B.r.M., 2008. Foraging bats avoid noise. J. Exp. Biol. 211, 3174e3180. Schmidt-Nielsen, K., 1972. Locomotion: energy cost of swimming, flying, and running. Science 177, 222e228. Schondube, J.E., Herrera-M, L.G., del Rio, C.M., 2001. Diet and the evolution of digestion and renal function in phyllostomid bats. Zoology 104, 59e73. Searle, K.R., Hobbs, N.T., Gordon, I.J., 2007. It’s the “foodscape”, not the landscape: using foraging behavior to make functional assessments of landscape condition. Isr. J. Ecol. Evol. 53, 297e316. Sommers, A.S., Rogers, E.J., McGuire, L.P., 2019. Migration and reproduction are associated with similar degrees of phenotypic flexibility in an insectivorous bat. Oecologia 190, 747e755. Song, S., Lin, A., Jiang, T., Zhao, X., Metzner, W., Feng, J., 2019. Bats adjust temporal parameters of echolocation pulses but not those of communication calls in response to traffic noise. Integr. Zool. 14, 576e588. Speakman, J., Anderson, M., Racey, P., 1989. The energy cost of echolocation in pipistrelle bats (Pipistrettus pipistrellus). J. Comp. Physiol. 165, 679e685. Speakman, J., Hays, G., Webb, P., 1994. Is hyperthermia a constraint on the diurnal activity of bats? J. Theor. Biol. 171, 325e339.

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Voigt, C.C., Schuller, B.-M., Greif, S., Siemers, B.M., 2010a. Perch-hunting in insectivorous Rhinolophus bats is related to the high energy costs of manoeuvring in flight. J. Comp. Physiol. B 180, 1079e1088. Voigt, C.C., So¨rgel, K., Dechmann, D.K., 2010b. Refueling while flying: foraging bats combust food rapidly and directly to power flight. Ecology 91, 2908e2917. von Busse, R., Swartz, S.M., Voigt, C.C., 2013. Flight metabolism in relation to speed in Chiroptera: testing the U-shape paradigm in the short-tailed fruit bat Carollia perspicillata. J. Exp. Biol. 216, 2073e2080. Wang, W., Gao, H., Li, C., Deng, Y., Zhou, D., Li, Y., Zhou, W., Luo, B., Liang, H., Liu, W., 2022. Airport noise disturbs foraging behavior of Japanese pipistrelle bats. Ecol. Evol. 12, e8976. Webber, Q.M., McGuire, L.P., 2022. Heterothermy, body size, and locomotion as ecological predictors of migration in mammals. Mamm. Rev. 52, 82e95. Welch Jr., K.C., Herrera M, L.G., Suarez, R.K., 2008. Dietary sugar as a direct fuel for flight in the nectarivorous bat Glossophaga soricina. J. Exp. Biol. 211, 310e316. Wendeln, M.C., Runkle, J.R., Kalko, E.K., 2000. Nutritional values of 14 fig species and bat feeding preferences in Panama 1. Biotropica 32, 489e501. Wetzler, G.C., Boyles, J.G., 2018. The energetics of mosquito feeding by insectivorous bats. Can. J. Zool. 96, 373e377. Whitaker Jr., J.O., Dannelly, H.K., Prentice, D.A., 2004. Chitinase in insectivorous bats. J. Mammal. 85, 15e18. Whitaker Jr., J.O., Rissler, L.J., 1993. Do bats feed in winter? Am. Midl. Nat. 129, 200e203. Willis, C.K., Brigham, R.M., Geiser, F., 2006. Deep, prolonged torpor by pregnant, freeranging bats. Naturwissenschaften 93, 80e83. Winter, Y., Von Helversen, O., 1998. The energy cost of flight: do small bats fly more cheaply than birds? J. Comp. Physiol. B 168, 105e111. Wojciechowski, M.S., Jefimow, M., Tegowska, E., 2007. Environmental conditions, rather than season, determine torpor use and temperature selection in large mouse-eared bats (Myotis myotis). Comp. Biochem. Physiol. Mol. Integr. Physiol. 147, 828e840. Wolff, J.O., 1985. The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus. Can. J. Zool. 63, 2657e2662. Zahn, A., Kriner, E., 2016. Winter foraging activity of Central European Vespertilionid bats. Mamm. Biol. 81, 40e45.

CHAPTER

Bat migration and foraging: Energydemanding journeys on tight budgets

11

Christian C. Voigt1, Shannon E. Currie2, Liam P. McGuire3 1

Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany; 2Institute for Cell and Systems Biology, University of Hamburg, Hamburg, Germany; 3Department of Biology, University of Waterloo, Waterloo, ON, Canada

Introduction In many regions, seasonal environmental conditions limit foraging opportunities, requiring bats to either migrate to more favorable locations or hibernate until conditions improve (Hutterer et al., 2005; Heim et al., 2016; Jastroch et al., 2016; Geiser, 2020). Alternatively, bats may travel long distances to take advantage of large foraging resource pulses, such as the case of the straw-colored fruit bat (Eidolon helvum) in Africa (Hurme et al., 2022). Indeed, migration is often considered a response to seasonal thermoregulatory challenges (i.e., cold winters in temperate regions), but foraging limitations and food resource opportunities are important factors of a more general and inclusive framework for understanding the drivers of torpor use and large-scale movements (Wojciechowski et al., 2007). A variety of behaviors involve long-distance movements, whether dispersal or seasonal movements including migration and nomadism (Jonze´n et al., 2011; Teitelbaum and Mu¨ller, 2019). Therefore, a taxonomy of movement is necessary to clarify the type of movements made by bats and also their underlying drivers (Dingle, 2014). We currently lack information on nomadism in bats, but it is likely that this form of movement is more common than currently appreciated. Therefore, we focus on migration in the remainder of the text and use this term to describe seasonal bidirectional movements (to-and-fro migration) of animals over long distances (Dingle and Drake, 2007). Long distance is a relative term that we use here for continent-wide migration. Such movements generally have a latitudinal component (i.e., north to south), contrasting with the generally shorter distance stellate pattern typical of regional movements bats make to and from hibernacula (Hutterer et al., 2005). At even smaller scales, some bats travel altitudinally (McGuire and Boyle, 2013; Voigt et al., 2014a). However, our focus here is on long-distance bat migration for the simple reason that these activities, and associated foraging behaviors, may present extreme situations for bats. This enables us to focus on the strong selective A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.00006-1 Copyright © 2024 Elsevier Inc. All rights reserved.

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pressures these bats face and may illustrate specializations in physiology and foraging behavior when traveling over long distances. We are, by and large, biased in our understanding of bat migration because the larger body of literature has been created on studies from North America and Europe. Consequently, by reviewing the literature, we mostly report studies from these two continents with a few notable exceptions, such as the migration of flying foxes in Africa and Australia (Thomas, 1983; Richter and Cumming, 2006; Ossa et al., 2012; Hurme et al., 2022) or insectivorous bats in Madagascar (Reher et al., 2019). Specifically, we have taken an ecophysiology approach to explore the facets of foraging in migratory bats. We first ask questions about the diversity and drivers of migration (which species migrate and why?). Then, we address physiological questions (how much energy is needed for migration, which nutrients are most important?) and foraging ecology questions (where do bats find these food items and what kind of landscapes are used for migration?).

What species of bats migrate? Long-distance migration is widespread but relatively uncommon among bats and has evolved repeatedly and independently (Fleming and Eby, 2003; Bisson et al., 2009). There is great diversity in long-distance migratory movements. Complete to-and-fro migration where all individuals migrate from a common summer distribution to a common winter distribution is likely the exception, with most species engaging in some form of partial and/or differential migration, such as the European common noctule bat (Nyctalus noctula; Lehnert et al., 2018) or silver-haired bat (Lasionycteris noctivagans; Rogers et al., 2022). Widely distributed species may comprise sedentary populations that remain in a region throughout the whole year and populations in other regions (often higher latitude) that migrate to more southern areas in winter. For example, soprano pipistrelles (Pipistrellus pygmaeus) are nonmigratory in Central Europe, whereas they show seasonal migration at higher latitudes, such as in the Baltic countries (Lindecke et al., 2019). Partially migratory populations may also include a mix of individuals that migrate and individuals that remain sedentary, and many species exhibit differential migration with certain subsets of the population that migrate differently (e.g., different timing or longer distance in females). Ultimately, it is important to remember that migration is a characteristic of individual animals and is not a fixed species-specific trait. When describing a species as migratory, this is an emergent property describing a regularly observed pattern among the individuals in all or some populations of that species. Details of migration have been described for the major feeding guilds of bats, including insect-feeding bats, fruit-eating bats, and nectar-feeding bats. However, the drivers of migration likely vary by latitude. In temperate regions of North America and Europe, migratory species are primarily tree-roosting or foliage-roosting insectivores that either hunt insects in the uncluttered open aerial column or that forage along structures such as forest edges (Cryan, 2003; Denzinger and Schnitzler, 2013).

What species of bats migrate?

For example, among the most well-known migratory bats in North America, Eastern red bats (Lasiurus borealis) and hoary bats (Lasiurus cinereus; Shump and Shump, 1982a,b) roost in foliage and silver-haired bats (L. noctivagans; Kunz, 1982) roost in tree hollows. In Europe, migratory bats such as the Nathusius’ pipistrelle (Pipistrellus nathusii; Fig. 11.1A) and N. noctula are also insectivorous and similarly roost mostly in tree hollows (Voigt et al., 2014b). In both regions, migration may be partly related to roosting ecology and its relationship to thermal biology, where species hibernating above ground are more likely to migrate south to avoid harsh winter conditions, where other species hibernate more locally below ground (e.g., in caves, mines, or rock crevices). In sub-tropical and tropical regions, there is more variation among migratory species related to diet and roosting ecology. Flying foxes in Australia (little red flying fox Pteropus scapulatus, gray-headed flying fox Pteropus poliocephalus, and black flying fox Pteropus alecto; Vardon & Tidemann, 1999; Ratcliffe, 1932; Eby, 1991; Roberts et al., 2012, Pa´ez et al., 2018; Welbergen et al., 2020) engage in long-distance nomadic movements. In Southeast Asia, Pteropus species are known to cover long distances (Epstein et al., 2009). Yet evidence for bidirectional seasonal movements (migration) is weak for these pteropodid species. The best-known migratory bat from Africa is E. helvum, a foliage-roosting frugivore, which moves seasonally mostly within the subtropical and tropical belt of Africa (Richter and Cumming, 2006; Ossa et al., 2012; Hurme et al., 2022, Fig. 11.1B). In the southwestern United States and Mexico, common migratory species include the insectivorous Brazilian free-tailed bat (Tadarida brasiliensis; Cockrum, 1969) and nectarivorous species such as the lesser long-nosed bat (Leptonycteris yerbabuenae; Rojas- Martı´nez et al., 1999, Fig. 11.1C). Populations of these species at the northern limit of their distribution would face more challenging winter conditions, but both species roost in caves which would buffer the exposure to winter conditions supporting the importance of foraging resources as a migratory driver.

FIGURE 11.1 Three examples of migratory bats with different dietary habits and from different continents: European insect-feeding Pipistellus nathusii (A); breeding range in light orange), fruit-eating Eidolon helvum from Africa (B) and nectar-feeding Leptonycteris yerbabuenae from North America (C). Credit for inlet pictures: Pipistrellus (C) Emily S. Damstra, Eidolon (C) Brian Cressman, Leptonycteris (C) Gillian Harris.

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Resource fluctuations as a driver of migration Migration may be caused by seasonal fluctuations of resources. In temperate regions, one driver of these resource fluctuations is the dramatic drop in ambient temperature over the winter. When temperatures fall so too does insect activity, while energy demand is increased to remain active in cold temperatures. During winter, insect abundance drops to levels where food is effectively unavailable for many months, forcing insectivorous bats (as the vast majority of temperate bat species is) to either hibernate or move to more suitable places. Even among species which hibernate over winter, there are limitations to the length of time individuals can persist without access to food, and the minimum temperatures they can withstand during hibernation, meaning that many bats migrate to spend the winter in more suitable hibernacula. Foliage-roosting bats in North America also lose access to suitable foliage roosts during this time, forcing them to move to southern areas (Weller et al., 2016) when no alternative hibernacula are used (see Kurta et al., 2018). This is also true for many European bats that roost in thermally labile tree hollows which provide limited insulation when temperatures drop below zero. In northern Europe, tree-roosting P. nathusii likely cannot sustain the costs of thermoregulation, even in torpor, when temperatures fall below the freezing point, and thus, these 8 g bats migrate up to 2486 km to hibernate in western and southern Europe where temperatures are more favorable (Vasenkov et al., 2022). For fruit and nectar feeding bats, temperature and rainfall drive seasonal fluctuations in food resources resulting in different migratory behaviors across a species range. For example, L. yerbabuenae in North America only migrates at latitudes near 30 N, whereas at latitudes lower than 21 N, this species is present throughout the year, as is their primary nectar source (Rojas-Martı´nez et al., 1999; Cole and Wilson, 2006). Similarly, the local occurrence of L. yerbabuenae is usually related to the availability of nectar and pollen, mainly driven by the seasonally flowering agave plants. A modeling approach confirmed that simulated fluctuations of nectar availability concur with observed variation in nectar-production throughout the year (Moreno-Valdez et al., 2000). Following these seasonal fluctuations in food resource, the model also explained the seasonal occurrence of L. yerbabuenae and L. nivalis (Moreno-Valdez et al., 2000; Stoner et al., 2003). Seasonal availability of food is also a driver of migratory behavior in E. helvum, which depend on the availability of ripe fruits (Hurme et al., 2022). Similar predictive models have been used to map the movements of these bats in relation to the productivity and phenology of their resources across the landscape and found that these bats time their migrations to match short-lived explosions of resources potentially via collective sensing (Hurme et al., 2022). Large colonies upwards of six million E. helvum aggregate in Kasanka National park each year to benefit from the local abundance of fruits in the adjacent forests and these large colonies provide avenues for collective sensing of rapid changes in available resources (Richter and Cumming, 2006, 2008; Hurme et al., 2022). Australian flying foxes (P. poliocephalus and P. alecto)

The energetics of migratory flights

similarly make long distance movements to large flowering pulses, but these pulses are unpredictable in time and space driving a more nomadic movement pattern (Eby et al., 2023).

The energetics of migratory flights Bat migration is intrinsically linked to the ability of bats for powered flight. Flight is the most energetically expensive mode of locomotion when considered per unit time, yet active flight enables bats to cover long distances in short periods of time. For example, E. helvum fly near 2000 km over their 3-month migration traveling w90 km per night but are capable of covering up to 370 km in a single night. Comparatively, 8g P. nathusii can travel 100e150 km in a night and fly continuously for 1.5e3 h when crossing a marine waterbody (Bach et al., 2022). Such extended periods of flight in small bats equate to 5.4e10.8 kJ energy at an assumed metabolic power of 1 W during flight (Troxell et al., 2019). This is equivalent to about 18% e36% of the estimated daily energy expenditure (30 kJ d 1; Speakman and Thomas, 2003). Outside of the migration season, foraging activity is often limited to the first 2 h after sunset, sometimes with a second period of activity in the hours just before sunrise. Yet during migration, long-distance flights are likely to last the whole night. Even though many bats balance the costs of flight via torpor use when inactive, especially during the migration season, the high costs of migratory flights are likely to dramatically increase daily energy expenditure. Several lines of evidence indicate that migratory periods are especially energetically stressful, even for aerial hawking insectivores that may spend several hours in foraging flight each night (McGuire and Guglielmo, 2009). Consistent with optimal flight speed theory (Hedenstro¨m and Alerstam, 1995), migrating P. nathusii choose a flight speed at which least energy is expended in relation to distance traveled per unit time under optimal conditions (Hedenstro¨m, 2009; Troxell et al., 2019). Notably, efficiency of converting metabolic energy into kinetic energy increases from 7% at the minimum power speed up to 10% at the maximum range speed (Currie et al., 2023). Peak conversion efficiency in this species occurs near maximum range speed, where the cost of transport is minimized (Currie et al., 2023); a pattern that is expected for this species given its long-distance movements. The exercise demands of migration are also apparent in the fact that migrating L. cinereus increase the size of exercise organs (McGuire et al., 2013a). Migration-related phenotypic flexibility is also observed in a reduction in the size of digestive organs, which reduces flight cost by reducing body mass, but it is unclear how this may affect foraging and refueling (McGuire et al., 2013a). Tadarida brasiliensis enter a period of hyperphagia before spring and fall migration and increase fat stores to fuel migratory flight (O’Shea, 1976; Widmaier et al., 1996; Rogers et al., 2019). Female L. cinereus similarly increase fat storage during migration, although no difference in fat storage is apparent for males (McGuire et al., 2013a). During migration, female L. cinereus and

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L. noctivagans had greater fuel loads than males, consistent with predictions of optimal migration theory (Clerc et al., 2021). Migrating bats also have increased aerobic capacity and elements of lipid metabolism pathways are upregulated during migration (McGuire et al., 2013b). Further, oxidative stress likely increases during migration. For example, oxidative status of Nathusius’ pipistrelles was different during migration compared to the premigration season; specifically bats exhibited a higher oxidative damage and different expression of both nonenzymatic and enzymatic antioxidants (glutathione peroxidase) (Costantini et al., 2019). Oxidative damage might be lower for fruit-eating and nectar-feeding migratory bats, given their high antioxidant level (Schneeberger et al., 2014), which could support long distance movements of bats with these feeding habits. Immune function may also trade off with the energetic cost of migration. Some aspects of immune function were related to migration distance in L. noctivagans, but others were apparently unrelated to migration distance (Rogers et al., 2022). In summary, the metabolic cost of migration is high for bats, and thus, selection should favor behaviors that optimize acquisition and expenditure of energy in migratory bats. Migratory bats may be on an energetic knife-edge and need to balance the energy demands of long-distance movements with the acquisition of sufficient energy sources to fuel their journeys.

Stopover behavior and torpor-assisted migration Given the long distances covered during migration, bats must make stopovers along their route. For example, suitable stopover sites are critical for straw-colored fruit bats that migrate up to 2500 km (Ossa et al., 2012). Migratory bats may conduct multiple-day stopovers, for example, when approaching large waterbodies (McGuire et al., 2012) or after having crossed such large water bodies (Bach et al., 2022). However, stopover durations may be much shorter than typically observed in migrating songbirds that make extended refueling stopovers. For example, only 30% of fall migrating silver-haired bats made multiday stopovers, and of those, most only stopped for 2 days (McGuire et al., 2012). Similarly, only 36% of springmigrating L. noctivagans made multiday stopovers, although longer stopovers were more common (Jonasson and Guglielmo, 2019). During both fall and spring, multiday stopovers were associated with weather, either rain during fall migration (McGuire et al., 2012) or cold ambient temperatures during spring migration (Jonasson and Guglielmo, 2019). Only a few records of stopovers greater than 2e8 days have been observed in P. nathusii that were banded or tagged in Latvia and Lithuania (Petersons, 2004; Bach et al., 2022). In contrast to most birds, migratory bats use torpor during such stopovers to save energy (Wikelski et al., 2003; McGuire et al., 2014), a strategy referred to as torporassisted migration. Not all migratory bat species are capable of using torpor (e.g., E. helvum and other pteropodids), and while few species have been explicitly studied in this regard, the common use of torpor among many bats throughout the year

Stopover behavior and torpor-assisted migration

(Stawski et al., 2014) suggests that torpor-assisted migration is widespread among insectivorous migrants. The ability to use torpor enables bats to save up to 90% of the energy costs that would have been incurred had they remained homeothermic (i.e., not reducing metabolic rate via torpor) through the inactive period (McGuire et al., 2014) and to effectively replenish their limited fat stores (Clerc and McGuire, 2021). Furthermore, migrating bats use torpor flexibly in response to variation in ambient conditions such that daily energy expenditure can be moderated, effectively independent of ambient conditions (McGuire et al., 2014; Baloun and Guglielmo, 2019). The energetic savings of torpor use during migration have major implications for the overall energetics of migration. For songbirds that do not use torpor, approximately 70% of the total energy cost of migration is incurred at stopover sites (Hedenstro¨m and Alerstam, 1997; Wikelski et al., 2003), whereas for migrating bats that use torpor, it is estimated that stopover represents only 15%e20% of the total energy cost of migration (Baloun and Guglielmo, 2019). Synthesizing these findings, Clerc and McGuire (2021) conclude that heterotherms such as bats will engage only in brief stopovers and have a lower fuel load compared with homeotherms. Torpor-assisted migration theory predicts that heterothermic migrants will have smaller fat stores, and this is supported by field observations. During fall migration, both sexes readily use torpor (McGuire et al., 2014) but during spring migration females are pregnant and therefore use less torpor than males (Cryan and Wolf, 2003; Baloun and Guglielmo, 2019). Consistent with theoretical predictions (Clerc and McGuire, 2021), females that use less torpor than males have frequently been observed to carry larger fat stores than males (McGuire et al., 2013a; Jonasson and Guglielmo, 2019; Baloun and Guglielmo, 2019; Clerc et al., 2021). Given the energy savings of torpor, brief stopover durations, reduced digestive organs, and smaller fuel loads in heterothermic migrants, there is an interesting question of how important foraging is at stopover sites. Based on radiotracking data, McGuire et al. (2012) inferred that only one-third of L. noctivagans tracked during fall migration engaged in foraging while at the stopover site. Subsequent studies have indicated that foraging is more common than this. Several studies have used stable isotopes to determine that foraging is common at stopover sites (Voigt et al., 2012; Baloun et al., 2020; Clerc et al., 2021) and temporal patterns of body composition similarly indicate refueling at stopover (Jonasson and Guglielmo, 2019). However, several authors suggested that foraging occurs opportunistically and may not be a primary goal of stopover (McGuire et al., 2012; Jonasson and Guglielmo, 2019; Baloun et al., 2020). While opportunistic foraging at stopover sites may be important, migrating bats may rely to some degree on fat stores deposited in advance of migration (Clerc et al., 2021). Wetlands could play an important role as stopover sites because these habitats produce large insect biomasses and because insects with a limnic larval stage are rich in polyunsaturated fatty acids, which could be helpful for high exercise performance (Price, 2010; Pierce and McWilliams, 2014).

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Food for migration Bats are capable of using recently ingested nutrients as an oxidative fuel for flight. As a consequence, bats can make use of energy shortly after ingestion, a strategy that  has been termed “aerial refueling” (Voigt et al., 2010). Later Suba and colleagues phrased the term “fly-and-forage strategy,” yet, this does not capture the essence of the underlying physiological process because virtually all insect-feeding bats  are foraging while flying (Suba et al., 2012). Furthermore, previous bird migration literature has used the term “fly-and-forage migration” in a different context, leading to potential confusion about the intended meaning of the term (see for example, Strandberg and Alerstam, 2007). Voigt et al. (2012) described a mixed-fuel strategy for P. nathusii migrating in late summer from the Baltic countries to southwestern Europe, with breath isotope signatures intermediate between those expected for insect prey and stored fat. Baloun and colleagues confirmed these observations in migrating L. noctivagans (Baloun et al., 2020). Furthermore, stable isotope ratios were more variable among bats captured later in the night, suggesting variation among individuals in the use of foraging and reliance on stored fat (Voigt et al., 2012). Clerc et al. (2021) observed larger fuel load in spring migrating female L. noctivagans and L. cinereus but did not observe any difference in foraging (based on breath stable isotope ratios) or digestive efficiency (based on isotope tracer assay) and concluded that the difference in fuel storage may be due to females relying to a greater extent on fat deposited prior to migration. Optimal flight speed theory (Hedenstro¨m and Alerstam, 1995) predicts that foraging bats should fly slower (near the minimum power speed) than bats engaged in commuting or migratory flight (near maximum range speed). Thus, foraging during a migratory flight may pose a trade-off between the optimal speed for migration and the optimal speed for foraging. Given that the efficiency with which some migratory species are capable of converting metabolic power to aerodynamic power increases linearly with flight speed (Currie et al., 2023), it is likely that variation in speed will impact overall costs of migratory flights. However, based on comparisons of bats flying in a wind tunnel and free-flying bats, Troxell et al. (2019) concluded that aerial refueling would not dramatically affect overall migration flight speed. However, it is unclear whether search time and deviations from the migratory flight path to forage may reduce overall migration rate or the efficiency of migratory flight. It may be that migrating bats partition time into bouts of foraging and bouts of migratory flight (McGuire et al., 2012; Troxell et al., 2019; Haddaway and McGuire, 2022). In addition to exogenous substrates such as recently ingested insects, fruits, and nectar, bats may also use endogenous substrates, such as fatty acids from adipocytes. Studies on migrating P. nathusii have shown that endogenous substrates are relevant as an oxidative fuel, yet bats may use exogenous substrates to a larger extent (Voigt et al., 2012). Fat stores of migratory bats such as European N. noctula and North

Food for migration

American Lasiurus consisted mostly of unsaturated fatty acids (primarily oleic acid) similar to those observed in migrating birds, yet migratory birds generally have higher polyunsaturated fatty acid content in muscle and adipose tissues compared to higher monounsaturated fatty acids in bats (Voigt et al., 2019; McGuire et al., 2013a). Unsaturated fatty acids in adipose tissue are beneficial for high metabolic rate exercise (flight) because they can be more rapidly mobilized than saturated fatty acids (Price, 2010; McGuire et al., 2013a), although polyunsaturated fatty acids yield less energy than the saturated fatty acids (Price, 2010; Pierce and McWilliams, 2014). Unsaturated fatty acids in muscle membranes (especially omega-3 and omega-6 polyunsaturated fatty acids) are beneficial during low metabolic rate torpor because they have lower melting points and thus contribute to maintaining membrane fluidity at reduced body temperature (Ruf and Arnold, 2008; Rosner and Voigt, 2018). In addition, these fatty acids are essential for sarcoendoplasmic reticulum calcium ATPase activity, which supports cardiac function at low body temperature, promoting deeper torpor and greater energy savings (Giroud et al., 2013). Oxidative fuel of nectar-feeding and fruit-eating bats is facilitated by the fact that plant-derived carbohydrates are easily oxidized shortly after ingestion in nectarivorous bats (Voigt and Speakman, 2007; Suarez and Welch, 2011) and fruit-eating bats (Voigt et al., 2008; Amitai et al., 2010). Consequently, nectar- and fruit-eating bats make rapid use of ingested carbohydrates from flowering and fruiting trees, while migrating across landscapes. Migrating nectar-feeding bats of the genus Leptonycteris from North America seem to follow a so-called nectar corridor provided by the flowering of Agave and Saguaro cacti plants (Burke et al., 2019). In contrast, resident populations of L. yerbabuenae consume mostly nectar of nonsucculent plants (Ceballos et al., 1997). Insectivorous bats seem to follow migratory insects in North America (Lee et al., 2005), yet empirical evidence is inconsistent. For example, North American T. brasiliensis adjust the altitude of foraging to the presence of migratory moths (Krauel et al., 2018), yet it remains unclear whether these bats follow migratory insect prey to other places or whether they commute back and forth over longer distances to ephemeral aggregations of migratory insects. Where T. brasiliensis may take advantage of moths that migrate through their home range, L. cinereus seem to time migration to benefit from seasonally abundant noctuid and geometric moths (Valdez and Cryan, 2009, 2013). However, metabarcoding studies in North American and European bats suggest a similar diet of bats during the migration and nonmigration period (Reimer et al., 2010; Kru¨ger et al., 2014). Rydell and colleagues suggested that the high fatality rates of migratory bats at wind turbines are associated with nocturnal insect migration at higher altitudes (Rydell et al., 2010), yet a recent metabarcoding study confirmed instead a large fraction of nonmigratory insects in the diet of migratory bats killed at wind turbines (Rydell et al., 2016; Scholz and Voigt, 2022). This argues for overall insect abundance rather than insect nutrient composition (e.g., fatty acid composition) being relevant in the phenology of migratory bats.

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Flight corridors Migratory corridors have been suggested for insectivorous bats, such as P. nathusii along coastlines and river valleys via acoustic surveys and stable isotope methods (Furmankiewicz et al., 2009; Rydell et al., 2014; Ija¨s et al., 2017; Kruscynski et al., 2021). Lately, this was confirmed by radio-tracking data for P. nathusii flying along the German, Dutch, and Belgian coastlines (Bach et al., 2022). Yet, it is unclear whether the use of these corridors is associated with insect availability or whether these bats use quasi-linear landscape elements such as coastlines as landmarks for navigation over longer distances. Population genetic studies confirmed that L. yerbabuenae most likely use a migration corridor along the Pacific coast of Mexico or along the foothills of the Sierra Madre Occidental (Wilkinson and Fleming, 1996). This corridor is mostly caused by the corridor-like availability of nectar by Agave and Saguaro plants, similar to the nectar-corridor observed when nectar-feeding bats migrate from south-central Mexico to south-western United States (Fleming et al., 1993; Burke et al., 2019). The migratory movements of E. helvum appear to be more sporadic and are suggested to be driven by communal sensing of resource pulses (Hurme et al., 2022), rather than driven by specific corridors in the landscape. In the absence of ecological barriers (e.g., coastlines, mountain ranges) or discrete patches of food resources (e.g., flowering cacti for nectarivorous migrants), it is unclear how migrants move across the landscape, and whether broadfront migration may be more common than defined movement corridors.

Open research questions In general, we lack comprehensive data on where migratory bats move during the full annual cycle. New tracking technologies may enhance our understanding of the migratory movements of bats. For example, tracking VHF-tagged insectivorous bats by planes offer new insights into the travel distances and heading directions of European N. noctula (Dechmann et al., 2014, 2017). In pteropodid bats, which roost at sun-exposed trees, solar-powered GPS units may illuminate the whereabouts of bats during migration. Notably, we miss data on full migratory journeys of individual bats, and no data on the actual energy expenditure during migratory flights and for the full migratory journeys. New sensor technologies provide opportunities for understanding fine-time scale data on flight behavior and energy expenditure via on-board accelerometry and heart rate. Acceleration data have already been used to determine wingbeat frequencies and infer information about flight behavior in response to windspeed in migratory E. helvum (O’Mara et al., 2019). The broader application of these devices, which now weigh $5 million

Malaysia

Indonesian Bureau of Statistics (1986); Fujita and Tuttle (1991) Indonesian Bureau of Statistics (1986); Fujita and Tuttle (1991) Fujita and Tuttle (1991)

the number of damaged kernels per ear of corn (Maine and Boyles, 2015). Bats also suppress pests in pine (Pinus spp) plantations, where higher bat activity has been correlated with a decrease in colonies of the pine processionary moth (Thaumetopoea pityocampa), a major defoliator of pines (Charbonnier et al., 2014). By eating crop pests, bats help farmers reduce their expenditures on insecticides. Insectivory by Brazilian free-tailed bats allows cotton growers to reduce the frequency of insecticide applications (Federico et al., 2008), minimizing costs and negative ecological impacts such as pollinator declines and pollution of aquatic ecosystems (Potts et al., 2016; Stoler et al., 2017). Bats can also reduce crop damage by pests even when not directly feeding on them; some insects with bat-detecting ears avoid areas where bats are active, creating a “soundscape of fear” (Russo et al., 2018). In the evolutionary arms race between bats and moths, crop pest moths have evolved tympanic organs that allow them to hear echolocation calls (ter Hofstede and Ratcliffe, 2016). When these tympanate moths are exposed to broadcast bat echolocation calls in agricultural landscapes, there is lower pest infestation and a disruption of moth mating behaviors (Acharya and McNeil, 1998; Belton and Kempster, 1962; Huang et al., 2003; Huang and Subramanyam, 2004).

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As pests damage leaves of crop plants, fungal infections and their mycotoxins and metabolic byproducts increase (Diekman and Green, 1992; Fennell et al., 1975). In corn, fungi such as Aspergillus flavus and Fusarium graminear commonly infect ears damaged by corn earworm moths (Fennell et al., 1975). Fumosin (a fungal mycotoxin) can make livestock vomit and eat less feed, while other mycotoxins can disrupt the reproduction of livestock (Diekman and Green, 1992). Mycotoxin contamination has large economic costs, with one estimate of 197 million USD in losses due to contaminated corn (Shane, 1984). By feeding on corn earworm moths, bats indirectly suppress these fungal infections and mycotoxins (Maine and Boyles, 2015), thereby rendering a critical ecosystem service to livestock producers and crop farmers (Diekman and Green, 1992). Bats also consume blood-sucking pests, with DNA analysis of fecal samples show that bats eat mosquitos and biting midges, which can be harmful to human and nonhuman animals (Cohen et al., 2020; Puig-Montserrat et al., 2020). Although there is no study to our knowledge that has directly examined the effect of bat insectivory on cattle, foraging on blood-sucking pests can potentially minimize weight loss and reduction in milk production in cattle (Ancillotto et al., 2017). Although we found no studies that directly examined the effect of bat insectivory on human health, bats eating mosquitos may bring direct benefits, as half the world is at risk of mosquito-borne diseases (Aguiar et al., 2021; World Health Organization, 2014).

Pollination and seed dispersal All members of the family Pteropodidae are phytophagous, and most of them are frugivorous (Muscarella and Fleming, 2007). Within Pteropodidae, 15 species are morphologically adapted to drink nectar with elongated snouts and tongues. The rest are mainly frugivorous with some opportunistically visiting flowers (Kunz et al., 2011; Nogueira et al., 2009). Over half of phyllostomids are plant-visitors, with 52 species specializing in nectar (Muchhala and Tschapka, 2020) and ca. 90 species primarily eating fruits (Kunz et al., 2011). Unlike insectivorous bats, plant-visiting bats may provide ecosystem services through mutualistic interactions, moving plant gametes and propagules in return for fruit and nectar. These mutualistic interactions may provide benefits for humans as well since many plants that are dispersed and pollinated by bats are eaten by humans (Table 15.1). Bats frequently visit plants that are cultivated and traded for the production of fruits, seeds, and nuts (Aziz et al., 2021). However, there has been limited research evaluating the economic value of fruit crops dispersed by bats. This difficulty arises from challenges in accurately identifying and quantifying the economic values of locally sold crops (Kunz et al., 2011). Other plants visited by bats have provisional values, such as having oil for scenting items, being used as pulp or timber, or being cultivated as ornamentals (Gardner, 1977; Lobova et al., 2009). In the neotropics, the five plant families (Cactaceae, Arecaceae, Sapotacea, Moraceae, Myrtaceae) dispersed by the greatest number of

Pollination and seed dispersal

phyllostomid genera include 1.6% by volume of exported timber (Muscarella and Fleming, 2007). In tropical Asia and Australia, the five plant families (Sapotaceae, Anacardiaceae, Meliaceae, Arecacea, Rubiaceae) dispersed by the greatest number of pteropodid genera includes 3.7% by volume of exported timber. In tropical Africa, the five plant families dispersed by the greatest number of pteropodid species include 34.3% by volume of exported timber (Muscarella and Fleming, 2007). Some nectarivorous bats are the sole or major pollinators for plants with economic and provisional benefits such as Agave (Rocha et al., 2005; Trejo-Salazar et al., 2016) and two species of columnar cacti, Carnegiea gigantean and Stenocereus thurbei (Fleming and Valiente-Banuet, 2002). Pollination and seed dispersal by bats indirectly benefit humans as well through the maintenance of healthy and biodiverse ecosystems. Many people value conservation of certain habitats or species that are dependent on bats (Oguh et al., 2021). Healthy ecosystems also allow recreational activities and benefit ecotourism and are the foundation of regulating services humans depend on for clean air and water (Oguh et al., 2021). Nectarivorous bats are particularly effective at promoting genetic connectivity between plant populations because they can fly long distances. For instance, in the Brazilian Amazon, bat pollinators of West Indian locust (Hymenaea courbaril) move pollen up to 18 km (Biscaia de Lacerda et al., 2008), while in the Australian rain forest, the common blossom bat (Syconycteris australis) can fly 6 km when foraging for nectar (Law and Lean, 1999). In Mexico, both Pallas’s long-tongued bat (Glossopahaga soricina) and the southern long-nosed bat (Leptonycteris curasoae) visit flowers of isolated Ceiba grandiflora in agricultural fields and pastures (Quesada et al., 2004). In frugivorous bats, long distance seed dispersal is partially mediated by feeding behaviors. Those that contribute to long distance seed dispersal are “fast feeders,” and consume fruits within a few minutes, swallow most or all of the seeds, and defecate them within 30 min (Dumont, 2003). These bats include the genus Carollia, with some species traveling 1e2 km between foraging areas (Dumont, 2003). “Slow feeders” will eat fibrous fruits, chewing on them and swallowing the juices before spitting out the seeds (Dumont, 2003) but still swallow and defecate fig (Ficus spp) seeds (Tang et al., 2007). The Jamaican fruit bat (Artibeus jamaicensis), a “slow feeder,” can carry figs up to 250 m away before feeding again, and within a single night will visit trees 1 km apart from each other (Morrison, 1978; Tang et al., 2007). The Jamaican fruit bat and the great fruit-eating bat (A. lituratus) have even been found to consume up to 200% of their body mass in pulp each day, dispersing a large number of seeds daily (Charles-Dominique, 1991; Morrison, 1978). The Egyptian fruit bat (Rousettus aegyptiacus) facilitates asynchronous germination, which increases the probability in unpredictable environments, by either spitting out or digesting and passing seeds (Izhaki et al., 1995). Behaviors also vary among individuals, as pregnant and lactating females have higher energy requirements and will increase fruit consumption while foraging over shorter distances (Charles-Dominique, 1991; Korine et al., 2013; Morrison, 1978).

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Pteropodids are key seed dispersers in Old World tropical islands due to their flying distances (Oleksy et al., 2015). The Mauritian flying fox (Pteropus niger) is an important disperser on Mauritius, traveling 6e9 km between forest fragments (Oleksy et al., 2019). In the case of the greater short-nosed fruit bad (Cynopterus sphinx), they can digest fig seeds for more than 12 h, potentially aiding dispersal across islands (Shilton et al., 1999). In fact, pteropodid-dispersed Ficus were early colonists on islands, attracting other frugivores that sequentially brought seeds from other species, leading to forest regeneration (Kunz et al., 2011; Muscarella and Fleming, 2007; Shilton and Whittaker, 2009). In the New World tropics, frugivorous bats are critical for tropical succession because they are the most abundant seed-dispersers (Medellin and Gaona, 1999). Volant vertebrates (bats and birds) are responsible for more than 80% of seed rain in the neotropics (Galindo-Gonza´lez et al., 2000). Although not all phyllostomids are primarily frugivorous, all species that do eat fruit include at least one of five main neotropical plant genera in their diet (Cecropia, Ficus, Piper, Solanum, Vismia) (Lobova et al., 2009), of which Cecropia, Solanum, and Vismia are dominant pioneer species (Foster et al., 1986; Mesquita et al., 2001; Oleksy et al., 2017; Saldarriaga et al., 1988; Toledo and Salick, 2006; Uhl, 1987). Bats also forage relatively frequently in forest fragments in lowland tropics (Arteaga et al., 2006; Estrada et al., 1993; Schulze et al., 2000), minimizing habitat fragmentation by dispersing seeds under isolated trees in abandoned agricultural lands or defecating seeds mid-flight in open areas (Duncan and Chapman, 1999; Galindo-Gonza´lez et al., 2000; Muscarella and Fleming, 2007). Long distance seed dispersal can be critical because seeds dispersed too close to parent plants may suffer increased mortality from predation, pathogens, and intraspecific competition (Harms et al., 2000). It is important to acknowledge that while bats contribute to seed dispersal, the ecosystem services derived from frugivory rely on the successful germination of dispersed seeds. This successful germination is contingent not only upon seed viability but also habitat quality of the locations where the seeds are deposited (Chan et al., 2021). Plant pollinated and dispersed by bats are also important for community structure and ecosystem function. One classic example is the dispersal of tropical figs, which are considered keystone species (Shanahan et al., 2001). Bats pollinate mangroves, which are involved in many ecosystem functions (Coupland et al., 2006), providing habitats for diverse assemblages of plants and animals, as well as reproductive habitats and shelter, and play important roles in nutrient cycling and water purification (Barbier et al., 2011). Mangroves are crucially important to humans, serving as a vital source of physical protection against storms, flooding, and tsunamis (Barbier et al., 2011). These ecosystems play a significant role in mitigating the destructive impacts of natural disasters, providing valuable coastal defense and safeguarding coastal communities and infrastructure.

Conservation recommendations

Ecosystem disservices Although bats provide many benefits through foraging, their behaviors may also adversely affect ecosystem services. For example, insectivorous bats also feed on predatory arthropods, which may lead to a release of pest suppression at a lower trophic level (Maas et al., 2013). Experimental bat exclusions in agriculture show an increase in predatory spiders and ants in agriculture (Maas et al., 2013); however, some evidence suggests this does not affect yield (Denmead et al., 2017). In the case of frugivory, bats also consume commercial fruits, such as lychee (Litchi cinensis), arecanut (Areca catechu), and sapota (Achrus zaptoa), leading to economic losses (Chakravarthy and Girish, 2015; Oleksy et al., 2019). Finally, in some cases, bats disperse and pollinate exotics plants, particularly in urban areas (Chan et al., 2021; Corlett, 2005).

Conservation recommendations A key tool for effective conservation is raising awareness about the economic advantages that bats bring. However, the scarcity of studies focusing on the monetary value of bats’ ecosystem services is apparent. To address this gap, this review presents a compilation of diverse valuations related to bat’s ecosystem services (Table 15.1). Effective valuation of ecosystem services requires understanding not only the structure and function of the natural system but also its link with human systems, and how both affect consumptive (e.g., agriculture) and nonconsumptive (e.g., recreation) uses (National Research Council, 2005). Despite the availability of site-level analyses of economic contributions, there is difficulty in scaling those up to a global level as the value of ecosystem services varies spatially (Plummer, 2009). Although it is difficult to estimate economic values from a comprehensive analysis, effort should be directed to collecting detailed data on bats and the organisms they interact with, as well as other factors that influence ecosystem services (National Research Council, 2005). In this review, we have shown that, through foraging, bats play critical roles in ecosystem services, benefitting both natural processes and human well-being. Insectivorous bats are important arthropod suppressors, especially in agricultural systems where they minimize crop damage, saving millions in USD each year. Through seed dispersal and pollination, frugivorous and nectarivorous bats not only maintain genetic diversity of plant populations but also sustain ecologically and economically important plant species. The International Union for Conservation of Nature (IUCN) considers 80% of bat species as threatened, data deficient, or suffering from decreased populations (IUCN; Frick et al., 2020). Major threats include logging, agriculture, and the combination of hunting and persecution, with some hunting driven by public fears and

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misconceptions of bats (Frick et al., 2020; Tuttle, 2013). In light of these threats, addressing research gaps will aid in managing natural and altered environments to support biodiversity and ecosystem processes. For many plant species, we do not know the fate of seeds dropped and defecated by bats, and future work should investigate the germination and survival rates to determine bats’ true contributions to seed dispersal (Chan et al., 2021). This can help devise strategies to prioritize which plant species require conservation efforts. We also must understand how urbanization is affecting bat communities and in turn the ecosystem services they provide. The changes in habitat composition and food availability, introduction of nonnative plant and animal species, as well as light, noise, and chemical pollution are all factors in urban areas that can influence bat behaviors and their services. We can then better support bats in urban areas by managing green spaces, pollutants, and the presence of nonnative species.

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Russo, D., Ancillotto, L., 2015. Sensitivity of bats to urbanization: A review. Mamm. Biol. 80 (3), 205e212. https://doi.org/10.1016/j.mambio.2014.10.003. Russo, D., Bosso, L., Ancillotto, L., 2018. Novel perspectives on bat insectivory highlight the value of this ecosystem service in farmland: Research frontiers and management implications. Agric. Ecosyst. Environ. 266, 31e38. https://doi.org/10.1016/j.agee.2018. 07.024. Saldarriaga, J.G., West, D.C., Tharpt, M.L., Uhl, C., 1988. Long-term chronosequence of forest succession in the upper Rio Negro of Colombia and Venezuela. J. Ecol. 76 (4), 938e958. https://doi.org/10.2307/2260625. Schulze, M.D., Seavy, N.E., Whitacre, D.F., 2000. A comparison of Phyllostomid bat assemblages in undisturbed Neotropical forest in forest fragments of a slash-and-burn framing mosaic in Pete´n, Guatemala. Biotropica 32 (1), 174e184. Shanahan, M., Samson, S.O., Compton, S.G., Corlett, R., 2001. Fig-eating by vertebrate frugivores: A global review. Biol. Rev. Camb. Phil. Soc. 76 (4), 529e572. https://doi.org/ 10.1017/S1464793101005760. Shane, S.H., 1984. Economic issues associated with aflatoxins. In: Eaton, D.L., Groopman, J.D. (Eds.), The Toxicology of Aflatoxins. Sheherazade, Ober, H.K., Tsang, S.M., 2019. Contributions of bats to the local economy through durian pollination in Sulawesi, Indonesia. Biotropica 51 (6), 913e922. https:// doi.org/10.1111/btp.12712. Shilton, L.A., Altringham, J.D., Compton, S.G., Whittaker, R.J., 1999. Old World fruit bats can be long-distance seed dispersers through extended retention of viable seeds in the gut. Proc. Biol. Sci. 266 (1416), 219e223. https://doi.org/10.1098/rspb.1999.0625. Shilton, L.A., Whittaker, R.H., 2009. The role of pteropodid bats in re-establishing tropical forests on Krakatau. In: Fleming, T.H., Racey, P.A. (Eds.), Island Bats: Evolution, Ecology, and Conservation. University of Chicago Press, pp. 176e215. Simmons, N.B., Cirranello, A.L., 2023. Bat Species of the World: A Taxonomic and Geographic Database. Version 1.3. Stoler, A.B., Mattes, B.M., Hintz, W.D., Jones, D.K., Lind, L., Schuler, M.S., Relyea, R.A., 2017. Effects of a common insecticide on wetland communities with varying quality of leaf litter inputs. Environ. Pollut. 226, 452e462. https://doi.org/10.1016/j.envpol.2017. 04.019. Tang, Z.H., Mukherjee, A., Sheng, L.-X., Cao, M., Liang, B., Corlett, R.T., Zhang, S.-Y., 2007. Effect of ingestion by two frugivorous bat species on the seed germination of Ficus racemosa and F. hispida (Moraceae). J. Trop. Ecol. 23 (1), 125e127. https://doi.org/ 10.1017/S0266467406003737. Taylor, P.J., Grass, I., Alberts, A.J., Joubert, E., Tscharntke, T., 2018. Economic value of bat predation services e A review and new estimates from macadamia orchards. Ecosyst. Serv. 30, 372e381. https://doi.org/10.1016/j.ecoser.2017.11.015. ter Hofstede, H.M., Ratcliffe, J.M., 2016. Evolutionary escalation: The bat-moth arms race. J. Exp. Biol. 219 (11), 1589e1602. https://doi.org/10.1242/jeb.086686. Toledo, M., Salick, J., 2006. Secondary succession and indigenous management in semideciduous forest fallows of the Amazon basin. Biotropica 38 (2), 161e170. https://doi.org/ 10.1111/j.1744-7429.2006.00120.x. Trejo-Salazar, R.E., Eguiarte, L.E., Suro-Pin˜era, D., Medellin, R.A., 2016. Save our bats, save our tequila: Industry and science join forces to help bats and Agaves. Nat. Area J. 36 (4), 523e530. https://doi.org/10.3375/043.036.0417.

References

Tuneu-Corral, C., Puig-Montserrat, X., Riba-Bertolı´n, D., Russo, D., Rebelo, H., Cabeza, M., Lo´pez-Baucells, A., 2023. Pest suppression by bats and management strategies to favour it: a global review. Biol. Rev. https://doi.org/10.1111/brv.12967. Tuttle, M.D., 2013. Threats to bats and educational challenges. In: Adams, R.A., Pedersen, S.C. (Eds.), Bat Evolution, Ecology, and Conservation. Springer Science and Business Media, pp. 363e391. https://doi.org/10.1007/978-1-4614-7397-8. Uhl, C., 1987. Factors controlling succession following slash-and-burn agriculture in Amazonia. J. Ecol. 75 (2), 377e407. United Nations Millennium Ecosystem Assessment, 2005. Ecosystems and Human WellBeing: Synthesis. Island Press. Wanger, T.C., Darras, K., Bumrungsri, S., Tscharntke, T., Klein, A.M., 2014. Bat pest control contributes to food security in Thailand. Biol. Conserv. 171, 220e223. https://doi.org/ 10.1016/j.biocon.2014.01.030. Westbrook, J.K., Eyster, R.S., Wolf, W.W., Lingren, P.D., Raulston, J.R., 1995. Migration pathways of corn earworm (Lepidoptera: noctuidae) indicated by tetroon trajectories. Agric. For. Meteorol. 73 (1e2), 67e87. https://doi.org/10.1016/0168-1923(94)02171-F. Whitaker, J.O., 1972. Food habits of bats from Indiana. Can. J. Zool. 50 (6), 877e883. https:// doi.org/10.1139/z72-118. Williams-Guille´n, K., Perfecto, I., Vandermeer, J., 2008. Bats limit insects in a neotropical agroforetry system. Science 320 (5872), 70. https://doi.org/10.1126/science.1152944. Wolf, W.W., Westbrook, J.K., Raulston, J., Pair, S.D., Hobbs, S.E., Riley, J.R., Mason, P.J., Joyce, R.J., 1990. Recent airborne radar observations of migrant pests in the United States. Phil. Trans. Biol. Sci. 328 (1251), 619e630. World Health Organization, 2014. A Global Brief on Vector-Borne Diseases.

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Conserving bats and their foraging habitats

16

Winifred F. Frick1,2, Luz A. de Wit1, Ana Ibarra1, Kristen Lear1, M. Teague O’Mara1, 3, 4, 5 1

Bat Conservation International, Austin, TX, United States; 2Ecology and Evolutionary Biology, University of Santa Cruz, Santa Cruz, CA, United States; 3Southeastern Louisiana University, Hammond, LA, United States; 4Max Planck Institute of Animal Behavior, Radolfzell, Germany; 5 Smithsonian Tropical Research Institute, Panama City, Panama

Introduction Natural history stems from our limitless curiosity about nature and the organisms with which we share the planet. The focus of this book on the natural history of bat foraging animates our sense of wonder and fosters desire for further scientific inquiry and discovery into the adaptations and species interactions involved in bat foraging. Sadly, our appreciation of bat foraging must also include discourse on the reality of the global biodiversity crisis and an entreaty to protect bat species and their habitats. Although threats to bats vary with geographical and ecological context, by far the most pervasive threat to bats globally are land uses that destroy or degrade habitats (Voigt and Kingston, 2016; Frick et al., 2020). Bat conservation efforts are part of the broader conservation movement to protect and restore ecological integrity, recognizing the inexorable links between environmental and human well-being (Sokolow et al., 2019; Hopkins et al., 2022). With over 1460 species, bats are diverse and their conservation needs varied. Over a third of bat species assessed by the International Union for the Conservation of Nature (IUCN) are ranked as threatened or data deficient, with 23 species currently listed as critically endangered, 85 as endangered, 113 as vulnerable, and 236 as data deficient (IUCN 2023). Generally, for bat species to thrive, they need intact foraging grounds, a healthy aerosphere, access to safe roosts, and clean surface water for drinking (Fig. 16.1). By definition, bat foraging involves species interactions, whether those interactions are predator-prey dynamics of animalivorous bats or the mutualisms of nectivorous bats pollinating flowering plants or frugivorous bats dispersing seeds. Conservation actions focused on broad-scale habitat protection and restoration are the most relevant to bat foraging. Roost protection receives a lot of conservation attention and is a high priority for bat conservation. Bat roosts are good examples of Small Natural Features (SNFs), defined as spatially distinct habitats with potentially disproportionate importance on ecosystem function relative to their size, analogous to the concept of keystone A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.00002-4 Copyright © 2024 Elsevier Inc. All rights reserved.

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FIGURE 16.1 Conceptual metamodel showing pathways of anthropogenic threats to bats via four critical habitat components.

species (Hunter et al., 2017). From a conservation perspective, SNFs are highly attractive because they represent defined spaces to focus habitat protection or restoration activities (Davis et al., 2017; Hunter et al., 2017). Conservation practitioners must often prioritize limited resources to maximize conservation benefit. Focusing on SNFs is rational conservation planning given the potential for a high “impactto-action” ratio, a measure of the conservation benefit relative to the level of effort the action requires (Hunter et al., 2017). Large colonies concentrated in a cave or mine are priority conservation targets given they generally have small spatial footprints relative to the value to protecting species or populations and are vulnerable to threats of disturbance or persecution (Furey and Racey, 2015; Hunter et al., 2017; Medellin et al., 2017; Frick et al., 2020). For example, protecting the last remaining cave roost for a bat species could prevent the global extinction of a species (Frick et al., 2020). While roost protection is undeniably important for bat conservation, protecting and providing foraging habitats is also critical for supporting healthy bat populations, yet has received less attention. Sixty-two of IUCN species assessments consider the loss of foraging resources as a threat to bat species, and these are distributed across threat categories (1 critically endangered, four endangered; eight vulnerable; nine near threatened; 40 least concern) (IUCN, 2023). In most cases, the loss of foraging resources is associated with a loss of habitat generally, mostly due to anthropogenic causes (e.g., expansion of agriculture and logging). Loss of foraging resources also results indirectly from activities such as use of pesticides that reduce

Introduction

insect availability. In general, evidence of loss of foraging resources as a cause of species decline is indirect (habitat loss includes both roosting and foraging habitat) and is less widely available in the literature. Identifying important foraging areas and strategies to protect foraging habitat can be more challenging than identifying roost sites given the inherent complexity to defining high-quality foraging habitat. Determining the appropriate scale and configuration for foraging habitat protection is particularly daunting given the scale of nightly movements of bats (McCracken et al., 2016; Goldshtein et al., 2020; O’Mara et al., 2021). For example, many molossid species fly over vast areas in a night, often at high altitudes (McCracken et al., 2008; Gillam et al., 2009; O’Mara et al., 2021). For these aerial insectivores, foraging primarily occurs in the aerosphere, and the direct linkages to specific terrestrial habitats may be diffuse (Kunz et al., 2008, Box 16.1). Even species that forage directly on plants can have foraging areas that are spatially disjunct from their roosting habitats. Straw-colored fruit bats typically forage for fruit approximately 35 km from their roosts and can fly over 90 km in search of nectar (Fahr et al., 2015; Caldero´n-Capote et al., 2020). Similarly, nectar-feeding lesser long-nosed bat (Leptonycteris yerbabuernae) can fly over 60 km each way from a cave roost to foraging areas for cactus nectar (Goldshtein et al., 2020). Bats live at their energy ceilings, and many species rely on their daily foraging success to maintain positive energy balance (e.g. (O’Mara et al., 2017)). Research on conservation physiology and how energetic needs of bats relate to habitat quality

Box 16.1 Aeroecology Thomas Kunz introduced the term aeroecology in 2008 to recognize the importance of aerial habitats for species interactions, most notably of bats, birds, and insects (Kunz et al., 2008). Aeroecology integrates ecology and atmospheric science, defining the aerosphere as habitat (Chilson et al., 2012; Diehl, 2013; Diehl et al., 2018). The concept of airspace as habitat is intuitive yet was not traditionally recognized as a habitat biome on par with terrestrial or marine biomes (Diehl, 2013). The unifying concept of aeroecology is a focus on the planetary boundary layer and lower free atmosphere (i.e., the aerosphere) and the airborne organisms that inhabit and depend upon this aerial environment for their existence (Chilson et al., 2012). Because of their ability to move over large spatial scales, volant organisms such as birds, bats, and insects contribute to the ecological integrity of ecosystems that span geopolitical boundaries linked by migration or dispersal through the aerosphere. The abundance of insects aloft is an important food source for aerial consumers, such as aerial insectivorous birds and bats (Frick et al., 2018). The scope and scale of seasonal migrations of insects is far greater than previously recognized and an important driver of aeroecological dynamics (Satterfield et al., 2020). Gary McCracken was one of the first researchers to provide insights into high-altitude aerial foraging behaviors of Brazilian free-tailed bats (McCracken et al., 2021). Use of weather radars has advanced aeroecological work by providing observational data of aloft biomass at relevant temporal and spatial scales (Chilson et al., 2012). Aeroecology and its promotion of airspace as habitat draws attention to specific threats to aeroecological integrity, including structures that cause direct mortality (e.g., wind turbines) or disrupt behaviors (e.g., light pollution) (Kunz et al., 2008; Chilson et al., 2012). Conservation attention to the aerosphere is key to protect biodiversity, global health, and ecological integrity (Kunz et al., 2008).

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could provide useful information about how habitat protection and restoration actions can benefit bat conservation over broad spatial and temporal scales. With growing interest in protecting and restoring habitats to help meet global 30 by 30 targets and sustain biodiversity, a better understanding of how bat energetic needs maps to habitat use would help inform conservation planning.

Threats to bat foraging Bats occupy the widest range of ecological niches of any mammalian order. While the majority of bat species feed on arthropods, many include fruit, nectar, and vertebrates in their diets. However, the foraging requirements for many bat species remain unknown, and nearly 20% of bat species are classified as Data Deficient by the IUCN (https://www.iucnredlist.org/). Basic information about dietary composition and diversity as well as habitat preferences to find these resources remain poorly understood for most of these species. Because of this, conservation aimed to protect bat foraging faces a range of challenges, most of which are rooted in identifying and protecting access to quality foraging habitats or resolving conflict with humans. Top ranked threats in the IUCN Red List for bat species include logging and agriculture, indicating that habitat loss is the greatest threat to bat biodiversity globally (Frick et al., 2020). Changes and degradation of land cover can negatively impact insect abundance and quality, fruit and flower availability, and drinking water access, and built infrastructure can interfere with access to foraging habitat or result in direct mortality of foraging bats. Global declines in insect availability threaten the viability of many bat species (Thomas et al., 2004; Shortall et al., 2009; Hallmann et al., 2017; Lister and Garcia, 2018; Sa´nchez-Bayo and Wyckhuys 2019). The insect apocalypse is likely caused by a combination of factors including habitat loss, pesticide use, climate change, and increasing light pollution (Sa´nchez-Bayo and Wyckhuys, 2019). The loss of insects has far-reaching consequences, as insects and other arthropods play important roles in ecosystems, including as food sources for other animals, including the majority of bat species. Arthropods can have complex life cycles with distinct habitat needs requiring habitat protection efforts that achieve integrity of varied habitats that support entire life cycles (Arrizabalaga-Escudero et al., 2015). Given that approximately 70% of bat species are insectivores, the impacts of the insect apocalypse on bat conservation are, of growing concern (Goulson, 2019; IBPES, 2019). Many bats, especially those that do not forage directly on nectar or fruit, need regular access to pooled drinking water. Due to their large surface area to volume ratios and uninsulated wings, water loss can range between 15% and 31% of body mass per day through evaporation (Studier, 1970; Webb, 1995). This is elevated in arid environments that hold a third of global biodiversity hotspots (Durant et al., 2012) and contain a quarter of the world’s terrestrial vertebrate species, with high rates of endemism and species of highest conservation concern (Brito et al., 2014; Durant et al., 2014). Bat activity is highest around water where bats

Threats to bat foraging

drink (Kurta et al., 1990; Mclean and Speakman, 1999), hunt for arthropods (Adams and Thibault, 2006; Rebelo and Brito, 2007; Korine et al., 2015), and cool off. Bats drink in flight and, consequently, may require a minimum surface size of water to be able to approach while flying (Laverty and Berger, 2020). Experimental reductions of desert pond size have reduced bat activity and species richness, particularly for larger, less maneuverable species (Razgour et al., 2010; Hall et al., 2016). In some arid regions, bats comprise the largest proportion of mammal diversity and partition use of water resources (Razgour et al., 2018). As climate change exacerbates drought conditions, arid environments may no longer be able to support high diversity of bat species (Adams and Hayes, 2021). Environmental pollution threatens bat foraging by reducing insect populations (Sa´nchez-Bayo and Wyckhuys, 2019) as well as contaminating habitats, including water where bats drink and forage (Bayat et al., 2014; Korine et al., 2015; Oliveira et al., 2020). Agricultural pesticides can cause direct mortality in bats, or when chronically exposed, these compounds can bioaccumulate in their tissues and cause sublethal impacts that affect immune function and reproductive health (Bayat et al., 2014; Oliveira et al., 2020). Chemical spills in water sources have been linked to reduced survival in bats (Frick et al., 2007), and water quality can affect bat activity (Korine et al., 2015) and bat physiology (e.g. (Hill et al., 2016)). More studies on the effects of chemical pollutants on bats are needed, including ecotoxicology as well as population-level impacts (Bayat et al., 2014; Zukal et al., 2015; Oliveira et al., 2020). Sublethal effects or disruptions to food webs may be challenging to identify but could have cumulative or chronic effects on bat populations (Bayat et al., 2014). Bats have been suggested as useful bioindicators (Jones et al., 2009; Zukal et al., 2015), and efforts to expand global databases as well as bat monitoring programs like the North American Bat Monitoring Program (Loeb et al., 2015; Reichert et al., 2021) could be helpful in assessing the effects of pollution on habitat quality, bat health, and population trends (Russo et al., 2021). Sensory pollutants and the effects of anthropogenic light and noise on bats is an expanding area of conservation research. Noise pollution is increasingly recognized as disruptive to bat foraging success, especially for species that use passive listening to identify prey (Barber et al., 2010; Domer et al., 2021). Light pollution has mixed effects on bat communities and can simultaneously have negative effects on bats by reducing insect populations or disrupting foraging activity (Stone et al., 2015) but can also provide enhanced feeding opportunities for some insectivorous bat species that feed effectively at artificial lights that attract moths and other phototactic insects (Voigt et al., 2021; Barre´ et al., 2022; Frick et al., 2023). Responses of bat species to Artificial Light at Night (ALAN) vary with foraging behavior and landscape context but could influence bat community composition and habitat use at broad scales (Cravens et al., 2018; Seewagen and Adams, 2021; Barre´ et al., 2022). While many bat species exploit and use urban habitats, sensory pollutants and fragmented foraging habitats in urbanized areas likely reduce species richness and could also create chronic stressors even for species that have adapted readily to roosting in human structures (Russo and Ancillotto 2015; Voigt and Kingston 2016).

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Some bats exploit urban areas for foraging (Egert-Berg et al., 2021), although whether urban areas function as ecological traps remains poorly understood for foraging (Russo and Ancillotto 2015). For example, recent work tracking Egyptian fruit bats (Rousettus aegyptiacus) in rural versus urban areas in Israel showed that these mobile fruit-eating bats commuted nightly into urban areas and shifted foraging behaviors to be more exploratory, including frequent switching among foraging patches in urban settings, which resulted in diversified diets (Egert-Berg et al., 2021). Climate change is a threat to biodiversity globally (Bellard et al., 2012). For bats, climate change presents a direct mortality threat when extreme temperatures cause mass mortality events (Welbergen et al., 2008; O’Shea et al., 2016; Festa et al., 2023). Heat stress causing die-offs of flying foxes in Australia has been observed over the past decade and extreme cold temperatures caused a mass mortality event of Mexican free-tailed bats in Texas during a “big freeze” event in 2021 (McSweeny and Brooks, 2022). These major die-offs often capture media attention and raise awareness of the impact of climate change on species conservation. In a more subtle and chronic way, climate change can amplify the impacts of other anthropogenic threats (Festa et al., 2023). Certain species, foraging guilds, and biomes are more sensitive to the effects of climate change than others indicating that the effects of climate change vary across phylogeny and geography (Festa et al., 2023). Bat species that rely on closely timed migration to feed on ephemeral flowering plants are more vulnerable to effects of climate change (Go´mez-Ruiz and Lacher, 2017) than those that have diverse diets or exploit human habitats and structures. Climate change heightens risks to bat foraging by intensifying drought (Adams and Hayes, 2021), increasing the strength and frequency of cyclones and hurricanes (Festa et al., 2023), and causing phenological mismatches between migrating consumers and food resources (Kubelka et al., 2022).

Conservation evidence Effective conservation of foraging resources requires knowing the impact of potential actions, and we are currently in an evidence crisis in conservation (Sutherland et al., 2004, 2022). Misguided actions have wasted millions of dollars and continue to leave species and ecosystems vulnerable (Sutherland et al., 2022). One challenge for bat conservation is the lack of evidence for conservation actions directed to benefit bats (Frick et al., 2020; Berthinussen et al., 2021). The Conservation Evidence program (www.conservationevidence.org) summarizes available conservation actions and systematically compiles the scientific literature available to evaluate efficacy of different actions (Sutherland et al., 2022). The conservation evidence database currently lists 200 conservation actions that could potentially benefit bat populations (Berthinussen et al., 2021). However, of these 200 actions, 60% currently have no studies reporting evidence and another 22% were ranked as “unknown effectiveness” due to the limited number of studies available. Furthermore,

The benefits to human well-being of protecting where bats eat

there is a bias toward actions in the global north, whereas bat diversity peaks in the global south. Forty-seven actions are directly related to bat foraging and categorized within two themes: education and awareness and land protection and management. These actions are mostly targeted at mitigating the effects of agriculture and modification of natural systemsdparticularly in applications toward annual and perennial nontimber crops, modifying natural systems to accommodate human housing and urban areas, and preserving surface water. Clearly, more work directly addressing diverse approaches and challenges to bat conservation are needed.

The benefits to human well-being of protecting where bats eat Protecting where bats forage by ensuring availability of food resources across their native ranges and across their active seasons is not only crucial for maintaining bat health but can also help to reduce humanebat conflict and risk of zoonotic pathogens spilling into humans (Plowright et al., 2021). The spillover and subsequent emergence of zoonotic pathogensdmicrobes transmitted from animal hosts to humans that cause diseasedis most often the result of close interactions between people, domestic animals, and wildlife (Plowright et al., 2021; Shapiro et al., 2021). Reservoir hosts are the species or populations in which a pathogen naturally occurs, and the availability, abundance, and quality of foraging resources largely determine their spatial distribution, their movement and feeding behaviors, and their physiological state (e.g., nutrition, reproduction, immunity and infection status) (Plowright et al., 2017; Kessler et al., 2018; Shapiro et al., 2021). However, anthropogenic changes to ecosystems driven by land-use change (i.e., transformation of natural habitats into agricultural and urban landscapes) and climate change (e.g., frequent and extreme droughts and storms) have shown to permeate the physical and physiological barriers between reservoir hosts and humans and induce the spillover of pathogens, including some for which several bat species are reservoir hosts (e.g., Nipah virus, Hendra virus, and Rabies) (Plowright et al., 2021; Reaser et al., 2022). Flying foxes native to Australia (Pteropus scapulatus, P. alecto. P. conspicillauts, P. poliocephalus) are natural reservoir hosts of Hendra virus, a paramyxovirus in the Henipavirus genus that has caused sporadic, often fatal, outbreaks of respiratory illness in horses and humans since the 1990s (Plowright et al., 2011; Kessler et al., 2018). Flying foxes infected with Hendra virus do not show apparent clinical symptoms of disease but can shed the virus in their saliva, urine, feces, and placental fluids (Halpin et al., 2011). Long-term empirical studies suggest nutritional stress and poor body condition in flying foxes caused by food shortages, combined with behavioral changes due to urban and agricultural resource provisioning, are key factors driving spillover of Hendra virus into horse and human populations (Plowright et al., 2021; Eby et al., 2022). Flying foxes rely on flowering trees for food, as their

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diet consists primarily of nectar and fruits, and they migrate long distances (up to thousands of kilometers) following seasonal food pulses provided by flowering plants (Welbergen et al., 2020; Eby et al., 2022). The progressive loss of native forests in Northeastern Australia, combined with increased frequency of climatic events that affect flowering plant phenology, has resulted in flying fox populations becoming sedentary in human-dominated landscapes, where they obtain a continuous, yet suboptimal supply of food resources (Eby et al., 2022). These agricultural and urban food resources do not meet the energetic and nutritional demands of flying foxes and can lead to immune deficiencies that increase risk of Hendra virus infection and shedding (Plowright et al., 2008; Kessler et al., 2018; Eby et al., 2022). Furthermore, these altered behaviors place flying foxes in close proximity to horses, creating opportunities for spillover of Hendra virus to horses and subsequently to humans (Kessler et al., 2018). Flying foxes native to South and Southeast Asia are natural reservoirs of Nipah virusdanother Henipavirus that has caused multiple outbreaks of respiratory disease and encephalitis in domestic animals and humans (Epstein et al., 2006). Decades of research on Nipah virus outbreaks and on the ecology of humanebat interactions in the region suggest that land-use change and agricultural and urban resource provisioning are key drivers of Nipah virus spillover dynamics (Pulliam et al., 2012; Islam et al., 2016; McKee et al., 2021). For example, the spatial overlap between commercial pig farms and agricultural production of mango in Malaysia facilitated the spillover of Nipah virus into a pig farm, where pigs consumed contaminated mango fruit that was partially eaten by local infected flying foxes (Pteropus hypomelanus) (Epstein et al., 2006; Pulliam et al., 2012). Infections in pigs led to subsequent transmission to pig farmers and abattoir workers and a country-wide outbreak that resulted in the death of 105 people and the culling of over one million pigs (Epstein et al., 2006; McKee et al., 2021). In Bangladesh, date palm sap, which is used to make palm wine and is obtained by tapping palm trees and collecting it in large clay pots, has become an easily accessible food resource for Pteropus medius. When infected P. medius visit date palm trees to consume this resource, they can contaminate the sap by shedding the virus through their saliva, urine, and feces, thereby transmitting the virus to people who consume the sap (Islam et al., 2016; McKee et al., 2021). In Latin America, Desmodus rotundus is one of the main reservoirs of the rabies virus, and the only species of vampire bat whose primary diet includes both wildlife (both mammals and birds) and livestock (Schneider et al., 2009; Streicker and Allgeier, 2016). Rabies is a lethal neurological disease that kills thousands of livestock annually and causes sporadic outbreaks in people from rural villages (Streicker and Allgeier, 2016). The feeding behavior and prey preference of D. rotundus are highly variable at both individual and population levels (Streicker and Allgeier, 2016), and such variability can be largely explained by anthropogenic disturbances that affect prey availability (Stoner-Duncan et al., 2014). In Uruguay and the Peruvian and Brazilian Amazon, agricultural expansion and other resource extractive industries have led to the displacement of D. rotundus’ natural prey and shifted this species’ feeding

The benefits to human well-being of protecting where bats eat

preferences to domestic animals and even very rarely humans (Stoner-Duncan et al., 2014; Streicker and Allgeier, 2016; Botto Nun˜ez et al., 2020). Interestingly, in villages where livestock are present, D. rotundus tend to preferentially feed on livestock, as livestock represent an abundant and reliable food source (Gilbert et al., 2012; Streicker and Allgeier, 2016). This shift in feeding behavior may have significant consequences for the health of bats if they are exposed to pathogens or antibiotics in the blood of livestock and may also have economic consequences to farmers from losing livestock to rabies disease or decreasing production due to anemia (Streicker and Allgeier, 2016). The loss of native foraging habitat and prey and the subsequent shifts in diet toward livestock and agricultural food sources has also led to conflict with livestock and fruit orchard farmers, which has resulted in the persecution and even legal culling of endangered bats (Streicker and Allgeier, 2016; Oleksy et al., 2021). For example, the Mauritian flying fox (Pteropus niger) is considered an agricultural pest because this species tends to feed on commercial fruit plants like mango and lychee, which have replaced the native fruit trees, causing economic losses to orchard farmers worth millions of dollars annually (Oleksy et al., 2021). Consequently, in 2015 and 2016, the Mauritian Government allowed the legal culling of almost 70,000 flying foxes in an attempt to control the damage caused in fruit orchards by P. niger, yet resulting in a 50% population decline of this species and its uplisting from Vulnerable to Endangered by the IUCN (Oleksy et al., 2021). Ecological interventions that protect where bats forage (and the quality of their foraging resources), could substantially reduce conservation threats to bats while also reducing risks to human health and reducing humanebat conflict (Sokolow et al., 2019). For example, researchers found that a massive winter flowering event in eastern Australia managed to feed hundreds of thousands of flying foxes, amid a landscape that was otherwise depauperate of food for these bats, thus protecting them from Hendra virus infection and reducing risk of spillover to horses and humans (Eby et al., 2022). They suggest that in addition to conventional medical approaches for disease prevention (e.g., vaccines and treatments), landscape restoration programs focused on restoring native forests that provide winter foraging habitat would ensure the reliability of these food sources during winter and draw flying foxes away from suburban landscapes (Plowright et al., 2016; Sokolow et al., 2019). Similarly, in addition to improving technologies for rabies vaccine delivery to vampire bats, habitat restoration and wildlife protection practices aiming to preserve D. rotundus’ native prey in the Amazon could switch vampire bat foraging back to natural feeding habits and reduce rabies transmission (Sokolow et al., 2019). Nipah virus outbreaks in pigs and humans in Malaysia have substantially decreased since the adoption of a policy that requires farmers to plant fruit trees at a minimum distance from pigsties (Pulliam et al., 2012). Prevention of Nipah virus outbreaks in Bangladesh are centered on human behavioral changes, which include placing bamboo skirts over date palm sap collection pots that prevent the sap from becoming contaminated with flying foxes’ saliva, urine and feces

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(Nahar et al., 2014; Sokolow et al., 2019). Likewise, covering fruit trees with nets has shown to be the most effective bat deterrent that prevents damage to fruit orchards without causing any harm to flying foxes; a practice that can be implemented alongside native forest restoration efforts and informational campaigns that address negative attitudes toward bats (Tollington et al., 2019; Oleksy et al., 2021). Reducing bat depredation on fruit orchards through netting could have an added benefit of reducing virus spillover risk at the bat-human-domestic animal interface. The health and biodiversity impacts of land-use change and climate change go beyond zoonotic spillover risk, and these zoonotic diseases are certainly not restricted to bats as potential reservoir hosts (e.g. (Sokolow et al., 2019)). Scientists continue to adopt systems-based approaches to understanding the biodiversity, health, and economic impacts of environmental degradation and identifying sustainable solutions that can protect biodiversity and human health (e.g. (Sokolow et al., 2015, 2019; de Wit et al., 2019; Cronin et al., 2022; Hopkins et al., 2022)). The emergence of Hendra, Nipah, and rabies viruses highlight how changes to ecosystems that affect the distribution, abundance, and quality of bats’ foraging resources not only represent a threat to bat populations but can also increase contact and spillover risk at the bat-human-domestic animal interface. As such, interventions that aim to protect where bats naturally forage can result in outcomes that benefit the conservation of bats and the ecosystems in which they forage (i.e., functions and services), as well as human health and people’s livelihoods (e.g. (Hopkins et al., 2021)).

Conservation initiatives targeting bat foraging

Restoring and conserving healthy habitat for nectarivorous bats, agaves, and people Conservation of bat foraging habitat can occur in both natural and human-dominated landscapes and can offer co-benefits to human communities through provisioning of ecosystem services, such as pollination. In North America, there are three nectarfeeding bats that migrate annually from Mexico to the southwestern United States and depend on flowering plants. The lesser long-nosed bat (Leptonycteris yerbabuenae), the Mexican long-nosed bat (Leptonycteris nivalis), and the Mexican longtongued bat (Choeronycteris mexicana). These three species rely on approximately 50 species of flowering plants across their ranges, extending from central Mexico into the southwestern United States, consuming nectar from agaves, columnar cacti (e.g., saguaro and organ pipe), and dry forest plants like Ceiba and Ipomoea (Arroyo-Cabrales et al., 1987; Cole and Wilson, 2006; USFWS, 2016; U.S. Fish and Wildlife Service, 2018). As pollinators of plants like agave and cactus, bats support critical functioning of ecosystems and economies. Yet, anthropogenic pressures combined with climate change threaten these species foraging resources and viability.

Conservation initiatives targeting bat foraging

Agave habitat is under threat from agricultural and urban expansion, grazing, drought, fire, and overharvesting (Reichenbacher, 1985; Alducin-Martinez et al., 2023). Agave plants have been used by people since pre-Colombian times and agaves continue to be used by communities throughout rural Mexico for food, fibers, construction materials, livestock fodder, medicinal uses, and distilled spirits. However, these uses involve harvesting the plant prior to blooming, thus reducing nectar availability for bats and other pollinators. Models predicting the future distribution of Mexican long-nosed bats and Agave species indicate the spatial overlap between these mutualistic species will be reduced by at least 75% in the next several decades (Go´mez-Ruiz and Lacher, 2019). Migration routes of Leptonycteris species follow a “nectar corridor” of blooming cacti and agave plants from central and southern Mexico into the Sonoran and Chihuahuan deserts of northern Mexico and the southwestern United States (Fleming et al., 1993; Go´mez-Ruiz and Lacher, 2017; Frick et al., 2018). For L. nivalis, agaves are often the only or main chiropterophilic plant and nectar source for this species during the energetically demanding period of migration and reproduction. For L. yerbabuenae, the importance of agave species to the bats’ diet increases in the northern portion of the migratory range. Agaves are the main nectar source for this species during mid- to late summer and fall, as well as during their fall migration southward (Cole and Wilson, 2006).

Bat Conservation International’s Agave Restoration Initiative In 2018, Bat Conservation International launched their Agave Restoration Initiative (batcon.org/agave), a binational and landscape scale effort to protect and restore critical agave foraging habitat surrounding known cave roosts and along migratory corridors for the Mexican long-nosed bat, lesser long-nosed bat, and Mexican long-tongued bat. The initiative involves dozens of partners from the United States and Mexico that span the conservation, civil, government, and business communities. BCI’s Agave Restoration Initiative aims to protect and restore agaves in Mexico and the United States to create a climate-resilient “nectar corridor” that benefits both bats and local communities. Initial efforts focused on restoring foraging habitat within a 50 km radius of known roosts of Leptonycteris species to reduce commuting distances bats must travel each night to find food, which is especially important for females nursing pups that must return to their cave multiple times per night (Medellin et al., 2018; Goldshtein et al., 2020). Protecting and restoring foraging habitat around known roosts may not be sufficient, given the long-distance seasonal migrations these bats make each year. Thus, the project was expanded to plant agaves in targeted areas within the migratory corridors of these species to help restore and recreate resilient foraging habitats along their migratory routes. The program focuses on creating climate-resilient foraging habitat by planting and restoring native agave species known to thrive in particular regions. Agave species are selected to maximize blooming at different times of the year to provide

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longer periods of nectar availability and to support any potential shifts in the timing of bat migration or flowering phenology. In addition, targeted regions for planting and restoring agaves encompass altitudinal gradients to account for suitable habitat for a diversity of agave species, with a particular emphasis on higher elevation areas that are projected to be climate strongholds for agave species diversity (Go´mez-Ruiz and Lacher, 2019). In the first 5 years of the initiative, over 80,000 agaves were planted at key sites in six U.S. and Mexican states, and over 9000 ha of land were protected for agave habitat. Restoration of agaves is not just focused on creating resilient nectar corridors for migratory bats but also supports farmers and communities in Mexico who rely on agaves as important parts of their livelihoods and culture (Lear 2020). In desert, scrubland, and montane ecosystems of the United States and Mexico, agave plants (Agave spp.) function as keystone species for both natural and human systems, supporting ecosystem integrity as well as human livelihoods. Agaves are both wildharvested and cultivated to make food and beverage products such as tequila, mezcal, agua miel, pulque, and agave syrup, and they are used for feeding livestock, controlling erosion, building fences, and supporting healthy water sources, among other uses (Lear, 2020). Agaves are especially important for many communities during periods of drought, as people harvest agaves to augment their income and diet and utilize agave as supplemental cattle feed when range forage is limited. BCI’s agave restoration program directly supports local communities through investment in local community infrastructures and business opportunities (e.g., community greenhouses for growing agave seedlings prior to planting), and co-creating bestpractices for sustainable agricultural and ranching techniques that aid rural communities through increasing landscape resilience through soil erosion control, improved water management, alternative sources of fodder for livestock during drought, and sustainable sources of income. The conservation of foraging habitat for long-distance migratory species such as Leptonycteris bats poses several challenges that stem from the ecological aspects of the system as well as human dimensions. Creating and protecting connected patches of foraging habitat along binational migratory corridors requires a coordinated vision and the involvement of many landowners and other stakeholders. Furthermore, the exact migratory pathways remain unknown, which limits the ability to target foraging habitat conservation efforts in the most critical areas. Work is ongoing to identify potential new roosts along these corridors as well as identify associated foraging areas. Novel approaches to identifying the migratory corridors and foraging areas, such as the use of environmental DNA (eDNA), are being tested to provide cost-effective surveys to identify foraging routes. Flowers of agaves can be sampled for the presence of bat DNA from salivary cells on flowers and eDNA has recently been successfully used to detect Mexican longnosed bats from both whole agave flowers and swabs of flowers (Walker et al., 2022). Use of eDNA surveys to identify foraging areas and migratory pathways are currently being explored.

Conclusion

Gardening for bats People often inquire how to help bats with their individual actions. Bat Conservation International (www.batcon.org) and Bat Conservation Trust (www.bats.org.uk) promote the concept of gardening for bats as an engagement strategy with potential benefits to improve bat foraging conditions. The idea of “bat gardens” is to encourage gardening practices aimed to increase local insect prey abundance and diversity and improve bat foraging habitats within residential areas. Guidance includes planting night-blooming plants that attract nocturnal insects as food resources for bats. Local varieties of native plants are recommended because they are best suited for local conditions and most likely to support native insects. Replacing invasive plants with natives can make gardens more biodiversity friendly (Burghardt and Tallamy, 2015). When available, local native plant nurseries or gardening clubs can help identify suitable local plants and gardening practices. General guidance for gardening for bats includes using plants with a diversity of floral structures, heights, and colors can help attract a diversity of insects (Bat Conservation Trust, 2015). Allowing grasses to grow long may also improve habitat value for insects and their larvae. Trees and shrubs can provide shelter for many insect larvae; hedges encourage concentrations of insects; and aquatic plants provide habitat for aquatic larvae such as mayflies (Bat Conservation Trust, 2016). Reducing or avoiding use of pesticides is recommended as best-practice for supporting local insect abundance and diversity (Frampton and Dorne, 2007). Additionally, reducing certain types of artificial light in and near gardens or garden features could reduce disturbance to some bats (Mathews et al., 2015; Seewagen and Adams, 2021). In larger gardens, features such as adding a pond or other water feature could provide drinking water for bats and may be particularly beneficial in arid climates with limited water availability. Lastly, gardens can become more bat friendly when people keep their cats indoors to prevent predation (Oedin et al., 2021), and gardens can support bat roosting habitat by protecting old trees or putting up an appropriately designed and located bat houses (Taylor et al., 2020). Bat gardens are an opportunity to engage the public and groups interested in wildlife and supporting conservation, such as parks, schools, nature centers, and churches, in bat conservation. In addition to improving habitats in the urban environment, they offer educational tools to teach the public about the habitat needs of bats and the importance of local and global bat conservation.

Conclusion Bats support ecological integrity through the ecological services they provide but also depend on intact habitats that can support both roosting and foraging needs to sustain viable populations. Conservation of bat foraging must be a priority for both conservation research and action to prevent further biodiversity loss and protect

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planetary function. We have much work to do to identify and implement strategies that can be effective at providing resilient foraging habitats for bats alongside protecting roost habitats from the effects of human disturbance or destruction. The escalating threat of climate change and how it amplifies and intensifies other threats, including intensification and expansion of agriculture and urbanization, stresses the urgency to use and build the evidence base for bat conservation to ensure our sustained progress on protecting bats and their foraging habitats around the world.

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17

Bat foraging: The next steps

Brock Fenton1, Danilo Russo2 1

Department of Biology, University of Western Ontario, London, ON, Canada; 2Animal Ecology and Evolution Laboratory (AnEcoEvo), Dipartimento di Agraria, Universita` degli Studi di Napoli Federico II, Portici, Italy

We hope that readers have found that some of the information in this volume has changed the way that they look at bats, perhaps with special reference to foraging. We believe that some aspects of bat foraging have not changed very much in the last 20 or even 50 years. Other substantial changes arose from new technology and techniques ¼ new discoveries. We hope that the diversity of chapters has made it “easier” for students and colleagues to reconsider some of the “tried and true” knowledge about bats. Reconsiderations could be particularly important when planning new research projects. Certainly, categorization of bats by food type has been at least shuffled by the combination of DNA barcoding of items in bat droppings, data from microbiomes, as well as from isotopes: all have repercussions for the way we view the structure of bat communities as well as how concepts of niches apply to bats and their diets. Information about social foraging by bats has advanced a great deal placing new emphases on just how foraging behavior is learned and how it can influence diet. This also has implications for the dynamics of bats and their prey, not to mention the energetic repercussions associated with diet, seasonal variations, and geographic variation. The importance of learning and evidence of long memories bears directly on bats’ social scenes. Advances in our knowledge of the adaptive radiation of bats put new perspectives on the central role of echolocation behavior in foraging. Our views of acoustic-based interactions between bats and their prey also have changed. Increased data about bats and ecosystems, as well as the impact bat foraging can have on agriculture, will surely change our view of bats as ecosystem service providers. This builds on new information about how bats use space and information coming from new techniques and equipment for tracking bats in their day-to-day, month-to-month, or even year-to-year comings and goings. When we relied on data from banding, we learned about point-to-point movements, without data on the times and courses involved in these movements. The small sizes of many, if not most species of bats, belie their capacity for movement, whether daily, seasonal, or annual. While a “typical” average flight speed for a Myotis lucifugus arriving at a swarming site is 5 m/s, other species A Natural History of Bat Foraging. https://doi.org/10.1016/B978-0-323-91820-6.00011-5 Copyright © 2024 Elsevier Inc. All rights reserved.

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FIGURE 17.1 Eptesicus fuscus in flightdbats do get around!

such as Lasiurus cinereus average 5.9 m/s. Recently, we have learned that Tadarida brasiliensis fly over 44 m/s and Tadarida teniotis over 37.5 m/s. One net effect of this combination of information is that bats do get around (Fig. 17.1). We are particularly intrigued by the realities of bats. The information in the chapters in this book set the stage for even more discoveries. Indeed, bats are the gift that keeps on giving.

Index Note: ‘Page numbers followed by “f” indicate figures and “t” indicate tables.’

A Achroia grisella, 45 Actias luna, 50 Active gleaning foraging strategy in animalivorous bats, 92 of phytophagous bats, 93 Adaptive social information, 127e129 Aegyptonycteris (Aegyptonycteridae), 8e9, 16 Aerial hawking, 63e64 Aerial hawking foraging strategy, 87e90 Aerial-hawking mode, 85 Aerial refueling, 206 Aeroecology, 307b Agricultural pesticides, 309 Agricultural pests, 146t Airflow sensing for flight control, 73e74 “Allotonic frequency hypothesis”, 48 Aminopeptidase-N activity, 184 Ancient bats dentitions, 14e17 foraging strategies in, 25e27 Animalivores, 244 Animalivorous bats, 12 active gleaning foraging strategy in, 92 passive gleaning foraging strategy of, 91e92 Animalivorous taxa, 10e12 Animal physiology and ecology, 4 Anthropogenic activity, 165e166 Anthropogenic foods, 272 Anti-inflammatory drugs (NSAIDs), 271e272 Antrozous pallidus, 64e65, 114e115, 235e237, 236f Aquatic ecosystems, 262e263 Archaeonycteris, 18e19 Arid zone bats, 109e110 Arid-zone dwelling bats, 109e115 diet habits, 114e115 nightly movements, 110e111 seasonal movements, 111e112 temporal activity, 112e114 Arthropods, 114, 308 suppression, 288e292 Artificial Light at Night (ALAN), 309 Aspergillus flavus, 292 Assemblage-wide assessment of diet in bats, 247e250

Atmospheric boundary layer (ABL), 141e142 Auditory signals, 62e68 Autographa gamma, 143, 149

B Barbastella barbastellus, 67e68 Barbestella, 48e49 Basal metabolic rate (BMR), 175, 176f Basic epidemiological model, 270f Bat Conservation International’s Agave Restoration Initiative, 315e316 Bat-dependent ecosystem services, 4 “Bat gardens”, 317 Bat-human-domestic animal interface, 313e314 Bat migration and foraging, 199e200 energetics of migratory flights, 203e204 flight corridors, 208 food for migration, 206e207 open research questions, 208e209 resource fluctuations as driver of migration, 202e203 species, 200e201 stopover behavior and torpor-assisted migration, 204e205 Bats, 1, 2f, 47e49, 164 changes, behavior of, 148 diets, 144e145 ecosystem services of, 146e147 extinct families of, 9t foraging strategies of. See Foraging strategies of bats life history features of, 147e148 migration or hibernation of, 147e148 predation and nocturnality, 161e162 responses to predation, 160 sensory systems and specializations, 68e74 Bat X, 251e252 Belize-specific and global analysis, 262e263 Bertholdia trigona, 67 Betaherpesvirus transmission, 265e268 Bioaccumulation, 261e264, 273e274 Biodiversity and sustainability, 4e5 Birds, 162e163 Brazilian free-tailed bats, 158, 201, 289 Broadcast bat echolocation calls, 291 Bufo marinus, 65

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Index

C Callosobruchus maculatus, 144 Carbohydrates, 174, 184 “Carnassiform notches”, 12e13 Carnegiea gigantean, 292e293 Carnivores, 244e245 Carnivorous bats, 12 Carnivorous species, 83, 184 Carollia perspicillata, 73, 241e242 Carollia sowelli, 248e249 Chaerephon plicatus, 139 Choeronycteris, 239 Choristoneura fumiferana, 141 Chrysoperla rufilabris, 66e67 Climate change on bat populations, 149 Commuting behavior in bats, 100e101 Conservation evidence, 310e311 Conservation initiatives targeting bat foraging, 314e316 Constant frequency (CF), 58, 93 Cooperative interactions, 265e268 Corn earworm moths, 292 Corynorhinus townsendii, 48e49 Costa Rican bat, 264e265 Cryptobune (Necromantidae), 16 Cytokines, 221

D Decision-making hypotheses, 126e127 Dental morphology and diet, 9e14 Desmodus rotundus, 72e73, 312e313 Dietary energy, 187e188 Dietary exposure to contaminants, 262e264 to parasites, 264e269 Diet composition, variation in, 184 Diet habits, 114e115 Diets of bats Antrozous pallidus, 235e237 assemblage-wide assessment of, 247e250 carnivores, 244e245 collapse of traditional guild, 234 frugivores, 241e242 Glossophaga, 240e241 insectivores, 234e235 nectarivores, 237e239 omnivores, 251e252 Trachops, 245e246 widely distributed pteropodids, 242e244 Direct health effects, 269e272 Diurnal birds, 162e163 Doppler shift compensation (DSC), 60

Doppler-shift echolocation, 20e21 Doppler shifted echoes, 58e60

E Early Eocene Climatic Optimum (EECO), 23e24 Echolocating bats, 57e58, 83e95, 123e124 auditory signals and ecological niche, 62e68 bat sensory systems and specializations, 68e74 commuting behavior, search behavior, and social foraging, 83e84 constraints, 85e86 foraging habitats, 84 foraging modes, 85 habitat types, 84 nonlaryngeal echolocation, 60e61 sonar call structure and duty cycle, 58e60 sonar scene analysis, 61e62 Echolocation, 3, 58e62, 83, 88t, 127f, 327 cost of, 183e184 evolution of, 20e22 Ecoimmunology, 276 Ecological and faunal diversity, 28e30 Ecological energetics, 173e174 Ecological niche, 62e68 Ecosystem disservices, 295 Ecosystem services of bats, 146e147 Egyptian fruit bats, 69, 187e188, 242, 265e268, 293, 309e310 Eimeria hessei, 271 Emballonuridae, 19 Energetics cost of terrestrial locomotion, 183 of different diets, 184e187 Energy balance, 173e175 budgets and metabolism, 173e177 in food, 184e188 required to get food, 177e184 Environmental DNA (eDNA), 316 Eocene bats, 14, 15f Eonycteris spelaea, 61 Eptesicus bottae foraging, 98f Eptesicus fuscus, 62, 70e71 Escherichia coli, 265 Euderma maculatum, 48 Euxoa auxiliaris, 147 Evolutionary biology, 41 Exogenous and endogenous factors, 109 Experimental bat exclusions, 295

F “Fast feeders”, 293

Index

Feed blood sucking pests, 288f Ficus colubrinae, 268 Firmicutes, 222e224 Fish-eating bats, 127e129 “Fishing” bats, 244 Flight boundary layer (FBL), 141e142 Flight morphology, 86 Flutter detecting foraging strategy, 93e94 “Fly-and-forage strategy”, 206 Foliage-roosting bats, 202 Food for migration, 206e207 Foraging-dependent ecosystem services, 287e288 arthropod suppression, 288e292 conservation recommendations, 295e296 ecosystem disservices, 295 pollination and seed dispersal, 292e294 Foraging habitats, 84 Foraging modes, 85 Foraging over water, 64 Foraging strategies of bats, 85e95, 308e310, 327e328 active gleaning foraging strategy in animalivorous bats, 92 aerial hawking foraging strategy, 87e90 flutter detecting foraging strategy, 93e94 passive/active gleaning foraging strategy of phytophagous bats, 93 passive gleaning foraging strategy of animalivorous bats, 91e92 search and commuting behavior of foraging bats, 95e101 trawling foraging strategy, 91 Fossilized stomach contents, 8, 17e18 Frequency modulated (FM), 58, 93 “Fringe-lipped bat”, 245e246 “Frog-eating bat”, 245e246 Frugivores, 241e242 Frugivorous bats, 186, 241e242, 287e288 Frugivorous phyllostomids, 13e14 Frugocarnivores, 244 Fruit-eating bats, 207, 218e219 Fungal infections and mycotoxins, 292 Fusarium graminear, 292

G Gardening for bats, 317 Gastric morphology, 218f Gastrointestinal structure, 217e220 Gastrointestinal (GI) tract, 217e218 GEM project, 150 Germ-free (GF), 220 Gleaning for prey on substrates, 64e65

Global biodiversity, 145 Global Union of Bat Diversity Networks (GBatNet), 252 Glossophaga, 115, 237e241 Glossophaga mutica, 243e244 Glossophaga soricina, 218e219 Glycosphingolipids, 225 Gray-headed flying fox, 159f Greater spear-nosed bats, 125 Great fruit-eating bats, 273 Green River Formation of Wyoming, 28 Gut microbiota, 220e222

H Habitat types, 84 Hassianycteris, 17, 19e20 Hasstilesia tricolor, 268 Healthy habitat, 314e315 Hemodynamic mop, 238f Hendra virus, 311e312 in flying foxes, 221e222 Heterospecific information, 133 Hg-impaired neutrophil production, 271 High duty cycle (HDC), 58, 93 High population growth rates, 143e144 Hipposiderids, 93 Hipposideros, 164 Host diet influences taxonomic composition, 222e224 Human activities pose threats, 4 Human health interconnections, 4 Humans and primates, 164 Human well-being, benefits to, 311e314 Hunting bats, 288 Hypocone basin, 12e13 Hypothesized diets, 14e17 Hypsignathus monstrosus, 179e180

I Icaronycteridae, 8e9 Icaronycteris, 18e19 Immune development, 220e222 Immunoregulation, 221e222 Indirect health effects, 272e273 Individual bats, 248f Insectivores, 65e68, 234e235 Insectivorous bats, 14, 66f, 139, 142e144, 184, 207, 218e219, 290te291t Insectivorous desert-dwelling species, 114e115 Insectivorous species, 83 Insect migration, 141e149

331

332

Index

International Union for the Conservation of Nature (IUCN), 295e296, 305 Interspecific interactions, 109 Intraspecific competition, 131e132 Invertebrates, 165

J Jamaican fruit-eating bats, 179f, 186

K Kerivoula, 90

L Lasiurus cinereus, 327e328 Lepidoptera, 43e44 Leptonycteris species, 315 Leptonycteris yerbabuenae, 71e72, 222e224 Livingstone’s fruit bat, 161 Local dwarf crocodiles, 165 Locusta migratoria, 66e67 Lonchophylla robusta, 239 Longer-term dietary ecology, 234 Low duty cycle (LDC), 58

M Macrolepidoptera, 17 Macronutrients, 184 Macrophyllum macrophyllum, 91, 94e95 Madagascan rousette, 268e269 Mammalian bat predators, 163 Mammalian order, 7e8 Mammals, 163e164 Mangroves, 294 Mathematical models, 262 Mauritian flying fox, 313 Mediterranean horseshoe bats, 181 Mehely’s horseshoe bats, 181 Metabolic rate, 175e177 Mexican free-tailed bats, 272 Mexican long-nosed bat, 314 Microbiome functions and diet, 224e226 Microbiomes of bats, 226e227 gastrointestinal structure, 217e220 host diet influences taxonomic composition of microbiome, 222e224 interactions between gut microbiota and immune development, 220e222 interactions between microbiome functions and diet, 224e226 Micronycteris microtis, 62 Migratory bats, 201f Migratory flights, energetics of, 203e204

Migratory insect species, 149e150 Miniopterus species, 265 Model-predicted temporal variation, 190f Molossus molossus, 99 Monitor lizards, 165 Monitor migratory insect infestations, 147 Mosquito-borne diseases, 292 Multivariate dental topographic analysis, 10e12 Murina, 90 Musonycteris, 237e239 Mutualistic relationships, 4 Myotis, 244 Myotis daubentonii, 101 Myotis lucifugus, 139, 327e328 Myotis myotis, 100 Myotis sodalis, 70 Myotis species, 89e90 Myotis vivesi, 114e115

N Nathusius’ pipistrelle, 200e201 Necromantis (Necromantidae), 8e9, 16 Nectar- and fruit-eating bats, 207 Nectarivores, 237e239 Nectarivorous bats, 233, 287e288, 293 Nectarivorous species, 110e111 Neotropical bats, 264f, 273e274 Neuroethological model, 43e44 New Zealand lesser short-tailed bats, 158 Nightly movements, 110e111 Nipah virus, 312 Noack’s roundleaf bat, 161 Noctilio albiventris, 99 Noctilio leporinus, 64 Nocturnality, 22e25 Noise pollution, 309 Nonlaryngeal echolocation, 60e61 North American Bat Monitoring Program, 309 Nyctalus aviator, 244e245 Nyctalus lasiopterus, 244e245 Nyctalus lepidopterus, 89 Nyctalus noctula, 99 Nycticeius humeralis, 124e125

O Olfaction, 71e72 Omega-3 fatty acids, 225 Omnivores, 240e241, 251e252 One Health Strategy, 4 Onychonycteridae, 8e9 Onychonycteris, 18e19 “Oogenesis flight” syndrome, 141

Index

Open research questions, 208e209 Optimal flight speed theory, 180e182, 206 Orb-weaver spiders, 165 Organochlorine (OC) pesticides, 262 Otonycteris hemprichii, 110e111, 236f Oxidative fuel of nectar-feeding, 207

P Palaeochiropteryx, 17, 19e20 Paleocene/Eocene Thermal Maximum (PETM), 23e24 Pallas’ long-tongued bats, 181e182 Paracellular absorption, 187 Passive gleaning foraging strategy of animalivorous bats, 91e92 of phytophagous bats, 93 Passive listening to sounds of prey, 65 Pesticide residues or heavy metals, 262 Peyer’s patches, 219e220 Phragmatobia fuliginosa, 67 Phyllostomidae bats, 164 Phyllostomus discolor, 243 Phyllostomus hastatus, 17, 129 Phylogenetic comparative methods, 10e12 Phylogenetic trees, 47e48 Physalaemus pustulosus, 65 Phytophagous bats, 83 active gleaning foraging strategy of, 93 passive gleaning foraging strategy of, 93 Pipistrellus kuhlii, 89e90 Plecotini, 49 Plecotus species, 147e148 Pollination and seed dispersal, 287e288, 292e294 Polyfluoroalkyl substances (PFAS), 275 Postcranial clues, 18e20 Postparacrista, 14 Predatoreprey interactions, 158 Predators of bats, 162e165 Premetacrista, 14 Prey counter strategies, 65e68 Primarily folivorous or granivorous, 185f Proinflammatory signaling molecules, 221 Proteobacteria, 222e224 Protozoans and fungi, 227 Pseudomonas species, 222e224 Pteronotus bats, 139 Pteronotus mesoamericanus, 235, 247 Pteropus giganteus, 221e222 Pteropus poliocephalus, 179e180, 201 Pteropus scapulatus, 201 Pyrrolizidine alkaloids, 45

Q Quantitative examination, 42

R Red bats, 131f Refractory content, 184e187 Reproductive cycle, 109 Reptiles, 164e165 Resting metabolic rate (RMR), 175 Rhinolophids, 93 Rhinolophus, 164 Rhinolophus ferrumequinum, 60 Rhinopoma hardwicki, 100 Rhinopoma microphyllum, 99, 110e111, 140 Rousettus, 60e61 Rousettus aegyptiacus, 59f, 242

S Saccopteryx bilineata, 72 Sample size corrected ellipse area (SEAc), 251f Scale organization influence thermoregulation, 50 “Screech calls”, 125 Search and commuting behavior of foraging bats, 95e101 “Search phase calls”, 124 Seasonal movements, 111e112 Sensory systems, 57 Sexual acoustic signaling, 43 Silver-haired bats, 200e201 “Slow feeders”, 293 Small Natural Features (SNFs), 305e306 Social communication, 72 Social foraging, 123e124 in bats, 132e133 in bats feeding, 95e100 cons of, 131e132 Social information transfer, 124f Social information use in bats, 123e130 Sonar call structure and duty cycle, 58e60 Sonar scene analysis, 61e62 Soprano pipistrelles (Pipistrellus pygmaeus), 200 Source levels (SL), 86 Spodoptera exempta, 144 Spodoptera frugiperda, 143, 146e147 Spodoptera litura, 45 “Stealth echolocation”, 67e68 Stenocereus thurbei, 292e293 Straw-colored fruit bat, 199

T Tachypteron, 19

333

334

Index

Tadarida brasiliensis, 63e64, 111, 139, 148, 203e204, 327e328 Tadarida teniotis, 327e328 Taphozous melanopogon, 19 Temporal activity, 112e114 “Terminal feeding buzzes”, 124 Terrestrial locomotion, energetic cost of, 183 Thermoreception, 72e73 Torpid metabolic rates (TMR), 175e177 Torpor-assisted migration, 204e205 Toxoplasma gondii, 268 Trachops, 245e246, 245f Trachops cirrhosus, 245e246 Trawling mode, 85 Tribosphenic bats, 12e13

U Ultrasonic vocalizations, 61e62 Ultrasound production, 44 Unihemispheric sleep, 160 Uroderma bilobatum, 72

V Vampire bats, 10, 184, 265e268 Vertebrates, 165 Vision, 22e25, 68e71 Vitamin B1, 225e226 Vitamin B5 metabolism, 225e226

W Warm blooded animals, 74 White-nose syndrome (WNS), 271e272 Widely distributed pteropodids, 242e244 Wing loading, variation in, 182e183 Wing morphology, 181e182 and body mass, 178e179 Witwatia (Philisidae), 16 Wood mouse, 163 W-shaped ectoloph, 10e12

Y Yangochiroptera, 287 Yinpterochiroptera, 287 Yponomeuta genus, 46e47

Z Zealand lesser short-tailed bats, 183 Zoonotic pathogens, 311 Zoonotic viruses, 269e270