Entomology Monographs Masaki Sakai Editor Death-Feigning in Insects Mechanism and Function of Tonic Immobility Entomology Monographs Series Editor Hideharu Numata, Graduate School of Science, Kyoto University, Kyoto, Japan Insects are the most diverse group of organisms, and many biological advances have been derived from this group. Although entomology is considered to be a classic science, recent developments in molecular methods, application of modern theoretical concepts and collaboration with related sciences have opened new directions in entomology. Japanese scientists play a signifcant role in these felds, and this book series will focus on such developments. The book series Entomology Monographs publishes refereed volumes on all aspects of entomology, including ecology, ethology, physiology, taxonomy, systematics, morphology, evolutionary developmental biology, genetics, biochemistry, and molecular biology in insects and related arthropods. Authors are not restricted to Japanese entomologists, and other international experts will also be considered on the basis of their recent contribution to these felds. More information about this series at http://www.springer.com/series/15687 Masaki Sakai Editor Death-Feigning in Insects Mechanism and Function of Tonic Immobility Editor Masaki Sakai Graduate School of Natural Science and Technology Okayama University Okayama, Japan ISSN 2522-526X ISSN 2522-5278 (electronic) Entomology Monographs ISBN 978-981-33-6597-1 ISBN 978-981-33-6598-8 (eBook) https://doi.org/10.1007/978-981-33-6598-8 © Springer Nature Singapore Pte Ltd. 2021 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifcally the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microflms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specifc statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affliations. This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore Preface The so-called death-feigning is a well-known behavior because the term is com- monly used in daily life. Death-feigning means taking an irresponsive attitude toward others by appearing to be dead. In biology, death-feigning means the behav- ior of an animal assuming an immobile posture as if had fainted. Death-feigning is often called tonic immobility (TI) and this term is used hereafter. TI is a peculiar but not so rare behavior. Many animal species from invertebrates to vertebrates show TI. In the natural habitat, TI occurs when the prey is attacked by a predator. The prey lies down in a paralyzed manner and remains immobile some- times for up to several hours. TI has been studied since a long time ago and there are lots of reports on TI. However, there are not so many researchers who have interests in mechanism and function. One reason is probably TI seems to be a kind of physiologically abnormal state and another reason is that there is not a suitable way to demonstrate the function of TI in the natural habitat. Knowledge of TI is informally used in labo- ratory procedures and animal husbandry, for example, where techniques of TI induction are needed to quiet large animals like a sheep and a rabbit for injections and blood samples in stock farming. In fshery, they need to quiet large fsh such as sharks and rays quickly after capturing on the ship. On the other hand, some researchers are interested in TI behavior itself. Here I introduce my experience. I found that the cricket Gryllus bimaculatus, a popular insect bred in the laboratory, showed distinct TI. This fnding led me to investigate its neural mechanism since I had an interest in narcolepsy in cats. I speculated that TI in crickets might be a model of sleep paralysis in cats. This model seemed prom- ising because the nervous systems of insects are much simpler than those in mam- mals. However, during the course of my searching the central nervous system for neural correlates with TI, I gradually realized that it was still premature to associate the mechanism of TI in crickets with that of narcolepsy in cats. Since then, a quarter of a century has passed, but it seems that not much progress has been made in the study of the TI mechanism. I was asked by Prof. Hideharu Numata, the series editor of Entomology Monographs in Springer, to make a book on TI (May 2017). At frst, I hesitated to v vi Preface accept it because TI occupies only a small portion of behavioral science. However, there are several researchers in Japan who have studied TI by different approaches. Besides, almost no monographs on TI had been published. This led me to believe that a book on TI would gain “scarcity value” in entomology. I frst discussed this matter with Hiroshi Nishino, who was my former collabora- tor, and then asked two Japanese researchers Atsushi Honma and Takahisa Miyatake to participate in the project. Atsushi Honma is a feld worker on TI research and Takahisa Miyatake is a specialist in the functional signifcance of TI. At the same time, I requested three German researchers, Hans-Joachim Pfüger, Ansgar Büschges and their mentor Ulrich Bässler, to take part in the project. This is because experi- mental studies on insect TI have been conducted mainly in Germany and a neuro- physiological study on insect TI was performed for the frst time by Bässler’s group at Kaiserslautern University. After the main plan for the book had been established, another topic, freezing came to issue. Freezing is a behavior that is similar in some ways but distinctly dif- ferent from TI. Freezing occurs when the prey encounters a predator, being earlier in the sequence of a predator’s attack. The prey stops all the movements and usually assumes a crouching posture so as not to be spotted by the predator and waits for a chance to escape. Freezing has been well investigated as one of the fear responses including fight and fght, and its neural mechanism has been established in mam- mals. On the other hand, TI is placed peripherally in the context of fear response and its neural mechanism remains uncertain. What is worse still, TI is sometimes mixed up with freezing. I, therefore, decided to incorporate freezing behavior to clarify both behaviors. I asked Ryo Nakano, Takuma Takanashi, Wataru Kojima, and Shigehiro Namiki who are specialists of insect freezing to join us. Finally, Masayuki Yoshida, a specialist in fsh behavior, was asked to support us. This is because stud- ies on TI and freezing have been done more in vertebrates than in invertebrates. As a result, one chapter was set up for vertebrates to present examples of not only pre- ceding but also advanced studies on TI and freezing. Neurobiology in insects has been rapidly developing, and the gap between the nervous structures in insects and vertebrates has been narrowing. Insects are easy to handle and suitable for the use of new technologies such as molecular and genetic analyses. Therefore, it is expected that studies on TI and freezing in insects will progress rapidly and that knowledge of the neural mechanism and function will make an important contribution to TI study in vertebrates. In this trend, this book covering (1) two defense immobility behaviors (TI and freezing), (2) their two main issues (mechanism and function) in insects, and (3) immobility behavior in verte- brates is unique and valuable. I hope that this book will be read by many students and researchers and will help them to understand immobility behavior. I would like to thank Dr. Hideharu Numata for his offer of making this book and Fumiko Yamaguchi and Selvakumar Rajendran in Springer for their great help in editing. Okayama, Japan Masaki Sakai Contents 1 Freezing and Tonic Immobility: Their Definitions and Naming. 1 Masaki Sakai 2 Historical Review on Thanatosis with Special Reference to the Work of Fritz Steiniger ���������������������������������������������������������������������������� 15 Hans-Joachim Pfüger, Ansgar Büschges, and Ulrich Bässler 3 The Function of Tonic Immobility: Review and Prospectus ���������������� 23 Atsushi Honma 4 Environmental, Physiological, and Genetic Effects on Tonic Immobility in Beetles . 39 Takahisa Miyatake 5 Ultrasound-Induced Freezing Response in Moths �������������������������������� 55 Ryo Nakano 6 Vibration-Induced Immobility in Coleopteran Insects ������������������������ 73 Takuma Takanashi and Wataru Kojima 7 Tonic Immobility in a Cricket: Behavioral Characteristics, Neural Substrate, and Functional Significance . 93 Hiroshi Nishino and Masaki Sakai