Vibrational Communication in Animals 9780674273825

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Vibrational Communication in Animals

Vibrational Communication in Animals ◆ ◆ ◆

PEGGY S. M. HILL

HARVARD UNIVERSITY PRESS

Cambridge, Massachusetts London, England 2008

Copyright © 2008 by the President and Fellows of Harvard College All rights reserved Printed in the United States of America Library of Congress Cataloging-in-Publication Data Hill, Peggy S. M., 1948– Vibrational communication in animals / Peggy S. M. Hill. p. cm. Includes bibliographical references and index. ISBN-13: 978-0-674-02798-5 (alk. paper) 1. Animal communication. 2. Bioacoustics. 3. Vibration. I. Title. QL776.H55 2008 591.59—dc22 2007038954

Contents

Preface

vii

ONE

Vibration as a Channel for Information Transfer

TWO

Communication and the Medium

THREE FOUR FIVE SIX

Receiving Signals Sending Signals

39 86

Predator-Prey Interactions Mating

119

135

SEVEN

Group Information Transfer

EIGHT

Why Vibration?

References

203

211

Species Index

249

Subject Index

259

183

12

1

Preface

grew into this book was planted during a symposium on vibration as a communication channel held at the annual meeting of the Society for Integrative and Comparative Biology (SICB) in Chicago on January 4, 2001. This symposium was sponsored and funded by the National Science Foundation, SICB’s Divisions of Animal Behavior and Neurobiology, and the Animal Behaviour Society. Papers were given and later published in one of the last issues of American Zoologist (the predecessor of Integrative and Comparative Biology) by myself and my University of Tulsa collaborator, John R. Shadley, Jan A. Randall, Caitlin O’Connell-Rodwell and Lynette Hart, Peter M. Narins, Edwin R. Lewis, Reginald B. (Rex) Cocroft, Randy E. Hunt, and Philip H. Brownell. The discussions after the final paper and over dinner stimulated us all, I think, to speak and publish more often and more widely to educate the scientific community and general public about this fascinating world about which so little has been written. Anyone from the symposium could have taken up the challenge of writing this book, so I hope my efforts will meet with their approval. Vibration communication is ubiquitous indeed, and this book is essentially a broad overview of the literature by someone who is hardly an expert on any aspect. Even with the best of intentions, I am sure there are glaring omissions, and so I apologize in advance for my lapses and failures. I hope each of you still likes this book. I think I do. I would first like to thank my editor, Ann Downer-Hazell, for all her enthusiasm and encouragement of this project. It took Ann’s vision

THE SEED THAT

viii

Preface

of a book, and about five years of her patience, before I agreed to tackle the project. The book would literally not have been written if not for Ann’s advocacy. Special thanks also go to Ted Lewis, Rex Cocroft, and one anonymous reader whose comments and suggestions helped to improve the manuscript during revision. I am grateful to Vanessa Hayes, editorial assistant, and Elizabeth Gilbert, senior editor, at HUP, as well as Susan Rescigno, production editor at Westchester Book Services, and Pat Cattani, copy editor, for all their encouragement and technical help on the production side of the project. I would not have been able to think about vibration with any clarity, much less to understand any of the physics or to sort out the field experiments, if it had not been for the patience, tutelage, and kind mentoring of my professional mechanical engineer, friend, colleague, and field companion, John R. Shadley. I thank the University of Tulsa and its College of Engineering and Natural Sciences and Faculty of Biological Sciences for supporting me during a semester sabbatical leave while I wrote. I further thank the outstanding scientists working in the field of vibration communication, whose work I hope to have accurately summarized in these pages. Special thanks go to Peter Narins, Rex Cocroft, Caitlin O’Connell-Rodwell, Lynette Hart, Philip Brownell, Glenn Morris, and Andrew Mason. I also thank Karen Warkentin, Becky Talyn, David Clayton, Kevin Johnson, and Clint Kelly for their sometimes long-distance comments and encouragement. I further thank my two stalwart PhD students, Dan Howard and Charlotte Sanderson, who spent many hours listening and encouraging, and for Dan’s presubmission comments. I also thank my extended professional family who have listened and prodded: Janice Burnett, Sallie Trecek, William Rosche, Harrington Wells, and Randy Wymore. Lastly, the project could not have been finished without the careful attention and professional care of Ricardo Ortega, who edited and prepared the figures for publication, thus removing a major burden from my shoulders. I wish to dedicate this book to my family, who have given me the space and time to complete the project, as well as a great deal of love and laughter along the way: my husband, Robert; my children, Angela and Yevgeni Kachuyevski and Bobi and Joe Deere; my grandchildren,

Preface

ix

Jordan P. H. and R. J. Yonah Hill Deere, Alexander Y. and Nikolai Y. Kachuyevski, Kristina M. and Timothy J. Whatley; and my mother, Cara Staten Morrison. They have taught me to love my life without taking myself too seriously, and Bobi and Jordan have been a tremendous help for years with my field research.

ONE ◆ ◆ ◆

Vibration as a Channel for Information Transfer

most compelling outcomes of the process of science is that we tend to find what we seek. This observation is not meant to suggest that we search for support for a pet hypothesis while intentionally ignoring other alternatives, but that we tend to look for things when we already have a pretty good idea that they are there. The “normal science” of Kuhn (1996) is spent in working on small questions within the larger framework of a paradigm. We have a good general idea of how things work, but we question the smaller details, and we follow leads, looking for inconsistencies—the anomalies that lead us to other questions. Answers bring a new doorway with a heretofore-unknown world on the other side. We say, “The more I learn, the less I know.” However, rarely does an answer shift a paradigm. Only with major insights, or the use of new tools, or with a question asked of exactly the right person who is prepared to think of it in a novel way do we break away from the nested boxes that define most of our work in normal science. Such is the story of animal communication through substrate vibration: the idea that individuals send and receive signals using the substrate as the medium. Our study of vibrational communication is in its infancy, but the glimpse we have of the mechanisms employed leads us to believe that this is a very ancient system, that it is perhaps the primary channel of communication in some animal groups, and that it is ubiquitous, at least in vertebrates and arthropods (Hill 2001a,b). For example, the very loud signaling via airborne sounds in cicadas is actually a derived modality that evolved from a substrate vibration precursor

ONE OF THE

1

2

Vibrational Communication in Animals

still employed by its “little cicada” relatives in the Hemiptera (Claridge, Morgan, and Moulds 1999). Cocroft and Rodríguez (2005) conservatively suggest that 150,000 described species of insects communicate exclusively through substrate vibration, and another 45,000 species use vibration signals together with other forms of mechanical signaling. Those who work outside the field of animal communication may justifiably be skeptical that humans could have missed stumbling on this phenomenon before, even if by accident, were it really as widespread and primary as we now argue. The answer, of course, is that we have encountered it, but we were not looking for it. We described and documented the function of all sorts of mechanical receptors that could detect substrate vibrations in a large number of arthropod and vertebrate taxa, and we observed animals drumming or thumping appendages, heads, and abdomens against various substrates while producing no sounds audible to humans. We attributed the anomalies that led us to suspect something else was going on to anything more plausible than communication through vibration signals—or the anomalies persisted as anomalies, to be examined again later when it was more practical to do so. For example, Jones and Dambach (1973) reported that the cricket Gryllus campestris was able to respond to loud airborne signals even after the tympanal organs, antennae, and cerci had been removed. They did not speculate that the airborne sounds might have been picked up by the substrate and channeled to the cricket nervous system as vibration, but two decades later Kalmring et al. (1997) cite the Jones and Dambach paper as reporting on a vibratory communication system—not just vibration detection, but vibratory communication. Likewise, an early description of maternal care in the short-tailed cricket, Anurogryllus muticus, mentioned that the very aggressive female only retreated in response to “violent substrate vibration” (21) and that in her aggressive displays she “shook her body in the manner characteristic of aggression in many kinds of crickets” (West and Alexander 1963, 21). This behavior might strongly suggest the use of substrate vibration as a communication channel, but at that time, this interpretation was not really as intuitive as it might appear today. The community bound by a paradigm does not purposefully make square pegs fit round holes, but through the carrot-and-stick approach of peer review of publications and grant proposals, practitioners determine

Vibration as a Channel for Information Transfer

3

which questions are worth pursuing. Sometimes the weight of accumulating data is required to shift interpretations of events. Some investigators in the first half of the twentieth century were studying vibrational communication, especially in invertebrates, but the scientific community was not fully engaged. For example, Ossiannilsson (1949) published an extensive treatise on leafhoppers that suggested vibrations produced by the tymbal apparatus were conducted through the substrate. He summarized the literature to date, including a 1907 paper that reported “sounds” of the otherwise “silent” leafhoppers that had been transferred from a leaf to the air. Ossiannilsson himself used musical notation to describe substrate vibration of some leafhoppers that he was able to hear by inducing individuals to signal from leaves in a test tube that he held to his ear. He also analyzed recordings of signaling species and published the waveforms in his monograph, including one of two alternating males. He described substrate vibration signals used in a chorus, suggested that male-female duets were important mating signals, and determined that pitch varied with temperature (1949). However, up through the 1970s, conventional wisdom held that substrate-borne vibration could not transfer any biologically meaningful information among organisms, especially the very small. The medium of soil or water or plant stems was too inelastic, and propagation speeds were too great to provide anything more than a nonspecific alerting mechanism to inform the animal of a disturbance nearby (Schwartzkopff 1974). Then technology in the form of faster, cheaper computers and seismic sensors, such as the geophones that had been developed for oil exploration (and detecting advancing enemy troops in the jungles of Southeast Asia), became accessible to more scientists. Affordable transducers made detection, simulation, and manipulation of signals possible. Faster, smaller, cheaper computers provided the opportunity for rigorous analyses of the data gathered (Hill 2001b). Sometimes the right person was in a position to think of a new way to test an anomaly (see Miles et al. 2001). At the same time, perhaps, the anomalies encountered in asking other questions became too massive to be set aside for another time. My own interest in vibration began with a frustrating experience trying to manipulate male prairie mole crickets (Gryllotalpa major) in the field using a playback experiment (see Hill and Shadley 2001). These rare burrowing endemics of the south-central United States construct

4

Vibrational Communication in Animals

burrows from which they project airborne sexual-advertisement calling songs to attract flying females for mating. Males sing from a fixed location inside an underground “acoustic horn” for about 30 min just at sunset on spring evenings when it is not too hot or too cold, not raining and not too windy. I wanted to test a scramble competition model that required me to evoke a response from a male when I simulated a competitor. Anecdotal reports were that prairie mole cricket males did not respond to conspecific song when the playback methods used to study other orthopterans and frogs were employed, but to test my hypothesis, I had to try. Males ignored the taped sounds I played for them, but as I moved about the area as darkness settled in night after night, males stopped singing whenever I was within 1–3 m of their burrow openings. It was entirely within my worldview at the time that these males could detect my footfalls and consider my presence a threat, but it took some investigation before I could ask whether they could also use this same sort of information to interact with conspecific neighbors. Could a person in the twenty-first century a.d. hope to write an account of animal communication through any other sensory modality? Would it be possible to describe visual or hearing or olfactory pathways that included a short history of use of the channel, background of the nature of the signal, production of signals as well as reception of them, and the contexts within which the signals were used by species known to use them across Kingdom Animalia? Yet even with the groundswell of interest in vibration since the dawn of the twenty-first century, we still speculate about the breadth and depth of the importance of substrate vibration as a communication pathway. We may know something about a behavior, but nothing yet about the signal or the neurophysiology of how the behavior is elicited and controlled. We may understand the technical aspects of a receiver, but not the ecological context that might have promoted its selection, or the selection for production of the signal, or even the behavioral interactions that were influenced by its selection. The ecologist with questions is not likely to be trained as a neuroethologist, a histologist, or a neurophysiologist. The functional morphologist may not have the tools to pursue questions beyond a point, and luring colleagues with these tools away from their own chosen research lines to help pursue a potential illusion is difficult, at best. An examination of the literature reveals early descriptions of anomalies and guarded suggestions of a link to substrate vibration. As recently

Vibration as a Channel for Information Transfer

5

as the 1980s, experiments in anatomy, physiology, ecology, and behavior still bolstered support for only tentative interpretations that animals really are using substrate vibration detection in as many contexts as they would use any other major sensory pathway. The pioneering work of Philip Brownell and Roger Farley (Brownell 1977; Brownell and Farley 1979a,b,c) showed us that scorpions not only can detect prey but can use information contained in substrate-borne vibrations created by the prey themselves to locate and capture them. It was Brownell and Farley’s carefully controlled and executed experiments, published in the best mainstream journals, that encouraged others to examine the possibility that baffling behaviors observed in their study species might be linked to sensory input via a substrate vibration channel. Hadley and Williams had already reported in 1968 that scorpions appeared to use tactile senses rather than vision to recognize prey and would attack forceps drawn along the substrate nearby (Hadley and

BT

H

SS B T

PS 1 mm

LC

B MC

Figure 1.1. Dorsal-anterior view of right fourth leg of the sand scorpion, Paruroctonus mesaensis, showing tarsal hairs (H) and the basitarsal slit sensillum (SS). B = bristle hairs, BT = basitarsus, LC = lateral claw, MC = medial claw, PS = pedal spur, T = tarsus.

Adapted and reprinted with kind permission of Springer Science and Business Media and The Journal of Comparative Physiology from Brownell and Farley (1979a, 24).

6

Vibrational Communication in Animals

Williams 1968). Yet Brownell knew that the sandy substrate on which he observed scorpions was supposed to absorb, or damp, low-frequency sound rather than transmit it, because sand is granular and would not support propagation of a wave from one particle to the next in the fashion of a more homogenous substrate. Further, waves traveling at higher frequencies would have a wavelength similar to the size of the sand grains, and these waves would be scattered as they traveled through the medium. What he found, however, was that sand was a good conductor of both compressional (P) waves and Rayleigh waves, that these waves traveled much slower in sand than predicted by current theory, and that in the range of several decimeters, animals with the right sort of receivers should be able to use information contained in these waves to make decisions that promote fitness. Specifically, he concluded that Rayleigh waves were detected by the basitarsal compound slit sensilla (BCSS) in scorpion legs (Figure 1.1) and used by scorpions to determine source direction, whereas P-waves were detected by mechanosensitive tarsal hairs and used to determine source distance (Brownell 1984). We now have uncovered evidence of use of the substrate vibration channel, especially in the Arthropoda, in contexts from predation or pathogen defense, to foraging coordination, to mate location and choice, to family dynamics. Of special note is the observation that if we find an unusual morphological feature that empirical evidence supports as a sender or receiver in substrate vibration communication, we then can find behavioral contexts in which this communication can be shown to occur, and vice versa. In examining related taxa, we often will find the same behavior or morphology, and sometimes an evolutionary trail can be followed by studying a feature in a phylogenetic framework. Again, if we find that a species gathers substrate vibration cues in one context, we often can find that it also uses vibration signals in conspecific communication. When our worldview expands to suspect that substrate vibration might be a key to explaining a behavior or morphology, we very often find that it is. What the Fossils Tell Us The fossil record and comparative morphology studies tell us a great deal about the possibilities for sensory input in ancient taxa, even if the central nervous system (CNS) does not fossilize. We can fall back on

Vibration as a Channel for Information Transfer

7

comparative evidence from the skeletal material in which the nervous system has been housed, as we do with modern forms, and modern taxa may not be that much different from their extinct ancestors. Morphologists can see that ancient amphibians, the first vertebrates on land, would have been able to detect substrate vibrations as their massive heads lay on the ground. Their lower jaws, coupled with the soil, could conduct vibrations through the quadrate bone to the inner ear through a bony pathway (Hildebrand and Goslow 2001). Thus, the earliest land vertebrates could “hear” substrate vibrations before they had the acoustic apparatus required to hear airborne sounds as terrestrial forms do today. Furthermore, the vibration pathway is still in use by amphibians, and the sacculus and lagena of the inner ear of modern frogs are the sites of their exquisite sensitivity to substrate-borne vibrations (Ashcroft and Hallpike 1934; Caston, Precht, and Blanks 1977; Lewis 1984). The story of the evolution of vertebrate animals and their head skeleton is a fascinating one (see review in Northcutt and Gans 1983). The process of cephalization that accompanied the earliest bilateral symmetry in invertebrates not only defined the head end of an individual, but it focused sensory structures, and then feeding structures and a brain, in this region. Details of the head so define vertebrates as a group, and in turn the classes into which they are sorted, that a wellreasoned and logical argument can be made to call them the Craniata. All vertebrate animals have a brain enclosed by a skull, but not all have jaws, and the earliest jaws in the fishes were integrated into the rest of the head skeleton in a different way than the jaws later seen in terrestrial forms. Elements of the visceral skeleton, which supported gills in the fish, were freed up by terrestrial life where the gill arches had no role. Some of these elements were incorporated into new hearing structures, the auditory ossicles of the middle ear, and others were incorporated into the vocal apparatus of the larynx and hyoid apparatus, which anchors the tongue and supports the floor of the mouth (Figure 1.2). At the same time, the number of elements in the lower jaw, or mandible, was dramatically decreased in a manner that gained stability but lost flexibility. The jaw joint itself was “reinvented” and was moved forward, while the muscles that closed the jaw shifted to a position where they attached outside the skull, rather than inside, as they had in the earlier fishes. The skull developed windows, or fenestrae, to accommodate these external muscles, and the options for food choices were

8

Vibrational Communication in Animals

rather suddenly, for geologic time, increased. We might also argue that the options for communication also were multiplied by these changes in the head skeleton. In primitive bony fish (Class Osteichthyes) skulls, the visceral skeleton includes an element, the hyomandibula, in association with the quadrate bone in the jaw joint. In the early amphibians, this hyomandibula was reduced and took on a new role as an early ear ossicle, the stapes, or columella (Hildebrand and Goslow 2001). Modern amphibians and

Figure 1.2. Phylogeny of the vertebrate jaw articulation and ear ossicles.

Note angular/ectotympanic, articular/malleus, quadrate/incus, and hyomandibula/stapes relationships between lobe-finned fish and mammal. Reprinted with kind permission of John Wiley & Sons, Inc., from Hildebrand and Goslow (2001, 128).

Vibration as a Channel for Information Transfer

9

reptiles that lie flat on the soil in direct contact with the Earth over much of their body surface have not developed a tympanum (ear drum) or middle ear cavity that promotes the most efficient conduction of airborne sound. They, like their ancient, extinct ancestors, are more suited to receiving information from vibration in the substrate than from sounds transmitted through the atmosphere. Aberrant Behavior and Vibration Sensitivity Humans have actually taken note of various animal responses to substrate vibration for at least 3,000 years (Snarr 2005). Tributsch (1982) rather extensively discussed documented reports of anomalous animal behavior that occurred minutes to days prior to an earthquake, beginning with a detailed description of the 373 b.c. destruction of Helice in ancient Greece for which the primary source has been lost. Many people have heard that animals “act funny” before, after, and during earthquakes (see Anderson 1973), and I, myself, have been interviewed by the BBC on how animals might be able to predict earthquakes. However, after the 2004 tsunami in Southeast Asia, most of us were surprised to hear anecdotal reports that animals such as elephants and tigers did not die from the wave as humans did (i.e., Kenneally 2004, 2005), and even the indigenous people did not die as the more “civilized” ones did (Parker 2004; McAdoo et al. 2006; Nowak 2006). Before the tsunami arrived in Thailand, elephants carrying tourists reportedly broke free from handlers to move away from the area. Elephants, their riders, and the handlers who chased them survived, while other humans who stayed did not (Kenneally 2005). Of the survivors of the tsunami in Thailand who responded to a formal survey within three months of the event, only 21% remembered any unusual animal behavior prior to the arrival of the first wave, but only 24% recalled noticing unusual shaking of the ground (Gregg et al. 2006). Even though interest in this phenomenon is high, empirical evidence is sparse, especially in what would be considered natural, nondomestic, or noncaptive settings. Two radio-collared Asian elephants (Elephas maximus) being monitored with their herds at Yala National Park in Sri Lanka provided an unplanned opportunity to gather data on 26 December 2004. No evidence in their movement behavior suggested either was using anything other than immediate environmental cues as they avoided the wave

10

Vibrational Communication in Animals

(Wikramanayake, Fernando, and Leimgruber 2006). However, the wave did not reach either area where the two herds were actually located, unlike the situation of the elephants in Thailand in the anecdotal reports, whose position was inundated and human lives were lost. Mantled howlers (Alouatta palliata) in northeast Honduras that were being studied in Cuero y Salado Wildlife Refuge provided an opportunity to gather opportunistic data when an earthquake occurred in El Salvador in February 2001 with its epicenter at a distance of 341 km from the field site. Because behavioral data were already being collected on these habituated, but free-ranging, individuals at 10 min intervals, trained observers were on hand to document precisely the sequence of population responses to the surprising occurrence of the earthquake. Individuals responded much as they had been noted to do to a threat from the ground and rapidly moved higher into the trees, switching from a resting to an alert state. This behavior was in response to Modified Mercalli Intensity Scale Level IV motion at the site, or an incident where automobiles would rock visibly and dishes, windows, and doors would be disturbed but not broken. Although individuals did not display any anomalous preseismic activity, seismic body waves were detected by the howlers almost instantly, as “the P-waves arrived at the field site approximately 60 s post-origin, with the S-waves arriving 87 s post-origin” (Snarr 2005, 281). Kirschvink (2000) made an interesting argument that even with a short life span that would preclude an animal’s being able to “remember” a seismic event and respond to it, individuals might “inherit” an ability to respond appropriately to a seismic event. “A population-genetic model indicates that such a seismic-escape response system can be maintained against random mutations as a result of episodic selection that operates with time scales comparable to that of strong seismic events” (312). The oldest known fossils of mammals that survived the Permian extinction are most commonly found as pairs in a collapsed burrow; therefore, selection pressure for a response to seismic events was present at least 250 million years ago (Kirschvink 2000). We speculate that those burrowing mating pairs that did not respond were killed where their remains were found, whereas those that exited the burrow complex survived to be parents. If individuals detect P-waves, as reported for the mantled howlers by Snarr (2005), they might avoid death by responding rapidly before

Vibration as a Channel for Information Transfer

11

the S-waves arrived. The greater the distance from the epicenter of the earthquake, the more time individuals would have to respond because P-waves travel through the crust at about 2–4 km/s faster than S-waves (Kirschvink 2000). The response time provided by the difference in the arrival of these two wave types would have been sufficient to allow the escape from the 2004 tsunami, as well. We thus know a bit about a lot with regard to the substrate as a communication channel. More data must be gathered before we can convert anecdotal reports into questions with testable hypotheses in many areas. Evidence from the fossil record and behavior associated with earthquakes has mostly been incidentally gathered, rather than being in response to the question driving the research. Very few systems have even been superficially studied. A handful of research groups are linking communication studies with morphology and neurophysiology and asking questions about selection for a particular type of signal in a given habitat or social environment. However, an entire planet full of potential research subjects awaits our interest. One purpose of this book is to document what we do know, in the broadest possible sense, from others’ work to identify promising areas for future research. Another is to simply provide a glimpse into a fascinating world of animal interactions that we otherwise might happily continue not to see.

TWO ◆ ◆ ◆

Communication and the Medium

a broad range of potential signals merely as incidental events, or byproducts, or epiphenomena, of routine activities. These events can only be labeled signals after empirical testing to confirm that they transfer information among or between individuals (see Bradbury and Vehrencamp 1998). Animals generate airborne, or waterborne, or substrate-borne vibrations; display colors or patterns; and emit chemicals as they live their lives. However, even if an event is stereotypical and species specific (Doherty and Gerhardt 1984), it cannot be classified as a signal unless it functions to transfer information from the sender to a receiver and then modifies the behavior of the receiver in a predictable way that has adaptive value for one or both (Markl 1983). This concept of a signal, though by all means not the only one available in the literature, will be used throughout this book. The definition clearly applies to conspecific communication used in mating, parental care, and coordinated group living, but it would also include information transferred incidentally between prey and predators. The signal need not be directed toward a specific individual; in other words, it may be broadcast in hopes of its encountering a receiver. Further, the time delay between sending and receiving may be rather short, or the signal could be persistent, as in scent marking of a mammal’s territory. A signal could even be a thread spun and deposited by a spider (Krafft 1982). The essential requirements, then, of any communication system include that an individual acts to initiate an event that encodes information (intentionally or incidentally), that the informa-

ANIMALS GENERATE

12

Communication and the Medium

13

tion is carried through some medium in a format that will deliver it to a receiving individual, and that the receiver is able to both detect and decode the message, ultimately acting on the information received. All of these steps must be present and detectable by a researcher for the event to be formally classified as a signal. However, signals may also be multimodal, and scientists must remain open to the idea that cryptic signals, or certain aspects of signals, may be repeatedly overlooked. Determining the range of information that can be transmitted via vibration in solids of all kinds, translating the signals, and estimating the contribution of such signaling to overall fitness will likely be a focus of study for some time, as will determining which anatomical features are specialized for sending and receiving the signals, and whether the same behaviors and features are present or absent in related taxa. A further challenge is to communicate to the reader a concise view of a complex, hidden process, where, for example, signal intensity “can be expressed either in terms of acceleration (m/s2), velocity (m/s), or displacement (m)” (Dambach 1989, 179). Still, the search for these answers and our attempts to incorporate them into our communication paradigm are rather young. Ehrenberg’s mole-rat, or the Palestine mole-rat, Spalax ehrenbergi (but work also reported under the generic name Nannospalax, or Nanospalax: see Mason and Narins 2001), has been observed to bang its flat head against the top of its subterranean tunnel in a way that could be explained as part of tunnel building activity. However, when individuals were shown to respond in a highly repeatable way to playback stimuli of thumping by conspecifics (Heth et al. 1987) and to respond to simulations in artificial tunnels as well as in the field (Rado et al. 1987), this head banging could be referred to as signaling. Thus, the first confirmation of vibrational communication in terrestrial mammals was as recent as 1987. Our information on invertebrate communication via vibration signals is currently restricted essentially to the literature of Arthropods, but behavioral observations of other taxa at least suggest that looking for such signals might be worthwhile (i.e., Beesley, Glasby, and Ross 2000 on the extreme vibration sensitivity of feather-duster worms in Annelida, and Newbury 1972 on use of vibration in prey detection by the Chaetognatha). Vibrational communication has only been a research focus of primarily the last 30 years, even though we have been

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Vibrational Communication in Animals

able to build on century-old observations of novel, or anomalous, behaviors. One example is our study of the fiddler crabs in the genus Uca, which inhabit intertidal beaches around the world. Males have long been of interest to those studying communication because they have one larger claw, or chela, which they are seen to wave and also to rap on the ground. Male Uca pugilator have been observed in both laboratory and field settings as they drummed their large chelae against the substrate. Teasing apart the waveforms showed that drumming created three types of waves. Study of this and related species is providing a great deal of information on how substrate vibrations contribute to animal communication. If conspecific animals, in particular the females targeted by male courtship, are able to perceive waves with different properties and propagation velocities as different vibration events, they should be able to use the information encoded in the drumming signal to locate the male who is producing them (Aicher and Tautz 1990). However, what does this drumming say to other males, or to any members of the population in a context other than mating? Again, work continues to reveal a fascinating world of information transfer. Distinguishing strictly between sound and vibration may not be a useful enterprise. We can somewhat distinguish them based on sensory perception, if we hold that sound is detected by pressure, or pressure difference, receivers, and vibration by particle displacement in a medium (Kalmring 1985). Vibrations that propagate through both the air and the substrate are produced simultaneously by the same action (Gogala 1985a). Especially in the Orthoptera (Markl 1983), it appears that airborne sound and substrate-borne vibration signals are used in combination in both mating and aggressive interactions. The tympanal organ used for “hearing” and the subgenual organ that detects substrate vibration are located adjacent to each other in the cricket prothoracic legs. The sensory cells in the subgenual organ are “structurally indistinguishable from those in the ear, and these sensory cells respond to substrate vibration as well as to low-frequency sound” (Ball, Oldfield, and Rudolph 1989, 391). Not only is teasing apart the signal functions a daunting task, but it is entirely possible that the two function in combination, as well. Therefore, the more we learn about the channels animals use to gather information about the environment,

Communication and the Medium

15

the less valuable a distinction between sound and vibration becomes. Ossiannilsson (1949) commented on this distinction as follows: This discussion has been made more complicated by many workers having felt obliged to separate a perception of air-born vibrations by a specific auditory sense from a perception of the vibrations by the tactile sense. This presentation of the problem will, in my opinion, very easily turn into a battle of words. Even in insects with a well developed tympanal organ apparently specially constructed for the interception of vibrations of the air, we shall of course never be able to gain a real conception of how the animal subjectively apprehends these . . . I believe that the vibrations produced by the tymbal organ of one specimen are conducted to other individuals mainly by the solid substratum—as a rule some part of a plant—and only in a less degree by air. If it could be established that the animals do in this way apprehend calls of each other as such—is this to be termed hearing or not? A matter of taste! (136)

The Problem of Ambiguous Terminology Within the context of human interactions, we all have a fair understanding of what is meant by words such as sound, hearing, vibration, song, acoustic, and audible. However, one of the greatest challenges of trying to organize and review what is known about communication via substrate signaling has been the lack of a consistent, cohesive vocabulary that is used by researchers studying disparate taxa. A common experience of any emerging academic discipline is to borrow terminology from mostly compatible, or closely related, fields, and then to develop jargon when the established vocabulary fails. In the case of vibrational communication studies, terms have been imported from, for example, physics and mechanical engineering, but their use has evolved and definitions have been sculpted in isolation to the point that communication among groups of researchers is impeded. In many cases first descriptions were published before substrate signaling was suspected, and then the same terms were subsequently used, even after confirmation that the signals were carried via the substrate. Merely repeating the terms that authors have used to describe their systems creates a jumble of roadblocks for the intended audience of a review. Trying to translate the authors’ descriptions by substituting standard terms carries with it

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Vibrational Communication in Animals

all the dangers inherent in any translation and may unintentionally alter or misrepresent the original observer’s perspective. However, after first relying on individual authors’ use of terms for this book, the decision was made to convert them, and accept the criticism, by using terminology based on the considerations discussed here. A large and comprehensive literature exists on senders and receivers used in animal communication via airborne or waterborne compressional waves (i.e., the Springer Handbook of Auditory Research volumes), but that literature and other conventional literature on hearing do not include substrate-borne vibration communication. The topics covered in this book are mostly distinguished from that literature by the medium (substrates of one kind or another) and the direction of particle motion detected by receivers (perpendicular to the direction of propagation), where detection of the particle motion usually involves some sort of inertial motion sensor, or sensing mass (see Lewis 1984). However, attempting to strictly separate airborne sound from substrate-borne vibration signaling leaves a gray, or fuzzy, area of behaviors that we have yet to successfully categorize, especially when the same words are used to describe very different phenomena. The first distinction must be made between sound and vibration. Use of these terms is not as clear-cut as we might think (e.g., Webster 1992; Lewis and Fay 2004), even though they are generally understood to be distinct when used in a popular connotation. Sound is typically used to describe airborne or waterborne compressional acoustic waves that can be “heard” after detection by some specialized sensory organ (such as an ear), but authors may also use sounds to describe substrateborne vibrations detected by other sensory organs. The use of sound has thus been minimized in this book, even when it is the term most used in the source material to describe signals. Using the strictest definition, vibration can be airborne, waterborne, or substrate-borne in that it represents particle motion in a fluid or elastic body. Particle motion, rather than the medium, is the issue in defining vibration. Further, vibrations in a fluid always accompany vibrations in a solid with which it is in contact. We tend to use vibration to refer to substrate-borne waves, and this convention is followed in this book, even though this is an ambiguous usage that engineers will find appalling. Vibration signals that are propagated via the substrate, atmosphere, or surface waves of water, as well as airborne and waterborne signals propa-

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gated as compressional waves, could all be considered acoustic, and so acoustic is not used in this book except in direct quotations. Likewise, for those who study animals whose signals are carried in soil or sand, seismic and substrate are synonymous. However, vibrations carried in plants are not seismic, by strict definition, because they are not carried through the earth. For all those authors who wrote of seismic signals, the alternatives vibration signal or substrate-borne vibration signal have been used. The terms song and noise are also not restricted to medium. Signals can be songs, or they can be noisy, but they are distinguished by whether they contain a fundamental frequency with harmonic overtones (song) or whether energy is broadly represented in frequencies that are not whole number multiples of the fundamental. Songs can be propagated via the substrate, air, or water and are distinguished in this book with terms such as airborne song or vibrational song. Somewhat easier to elucidate, but not significantly so, is the distinction among the types of waves produced and detected by animals in their communication. A Primer on Wave Theory Markl (1983) distinguishes among vibration events that induce contact vibrations (when one individual directly touches another with varying pressure: tapping, drumming, antennating, etc.), nearfield medium motions (generated in the fluid medium surrounding the sender and perceived by movement detectors such as hairs or cerci), or boundary vibrations (substrate vibrations at the interface between solid/air, water/air, solid/water, solid/solid, etc.). Most of our focus is on boundary vibrations; however, examples of both contact and nearfield motion are included in subsequent pages, especially when they are difficult to tease apart from other events, or where an evolving story would be truncated and incomplete without their inclusion. Markl (1983) subdivides boundary waves into subcategories: pure longitudinal, quasi-longitudinal, transverse, torsional, and bending waves. However, we are cautioned to remember that “different wave types are characterized by their different kinds of motions in relation to the direction of wave energy propagation, by their different speeds of propagation and—depending on the conducting material and its geometry—by the different attenuations with which they are propagated” (Markl 1983, 338) (Figure 2.1). Likewise, one disturbance

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Vibrational Communication in Animals

Figure 2.1. Types of waves in elastic solids: (1) compressional, or P-waves,

(2) shear, or S-waves, (3) Rayleigh waves, and (4) Love waves. The arrow shows the direction of propagation. Reprinted with kind permission of Springer Science and Business Media and The Journal of Comparative Physiology from Aicher and Tautz (1990, 346).

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event may excite different types of vibrations in the same substrate, and when passing through some sort of junction (e.g., where a twig meets a larger stem) a given wave may even be converted into an entirely different type (Markl 1983). Pure longitudinal waves, also known as compressional waves (Brownell 1977), are restricted to “the interior of a medium that extends over many wavelengths in all directions” (Markl 1983, 338), and particle oscillation is in the direction that the wave is propagating. A variety of surface waves are produced when pure longitudinal waves arrive at boundaries, and the ideal vibration pattern is changed (Gogala 1985a). Quasi-longitudinal waves, also known as symmetric waves, are produced by pure longitudinal waves at the boundary with rod- or plate-like structures and have a slightly lower propagation velocity than the pure longitudinal waves (Gogala 1985a). Quasi-longitudinal waves are often propagated through structures such as plant stems or leaves, or spider web strands, where one or two dimensions are small in relation to the wavelength. The displacement perpendicular to the surface, where an animal might be found, would only be 1/100 to 1/1000 times the displacement in the longitudinal wave’s propagation direction, but very sensitive receptors could perceive that level of displacement (Markl 1983). Quasi-longitudinal waves are thought to be a likely candidate when looking for a mechanism for vibrational signaling (Gogala 1985a). Transverse waves only exist in solids (Gogala 1985a) and “can only be propagated in solid materials, which are able to sustain and transmit elastic shearing forces. Particle motion in them is perpendicular to the direction of wave propagation and in the plane of the surface of a body boundary” (Markl 1983, 339). The propagation velocity of plane transverse waves is about 60% that of quasi-longitudinal waves (Markl 1983). Rayleigh waves are produced by a combination of longitudinal and transverse waves at boundaries of solids and have a shear component that is perpendicular to the plane of the body surface. Their propagation velocity is even lower: 4–13% less than transverse waves (Gogala 1985a). Love waves are transverse surface waves (Markl 1983). Torsional waves, which appear similar to transverse waves and are likely to be seen in parts of plants (Gogala 1985a), have not been explored as a source of biologically relevant information. They are “the type of transverse vibrations transmitted in long structures whose diameters are small in comparison to their length. If the structure has rotational symmetry

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Vibrational Communication in Animals

(as in a circular rod) there is no component of motion perpendicular to the surface and wave propagation along the rod’s axis is the same as that for a plane transverse wave” (Markl 1983, 339). Bending waves appear similar to transverse waves and are sometimes referred to as transverse waves, but in the strictest interpretation they are quite different. One difference is that their propagation velocity is frequency dependent, and bending waves are propagated with dispersion (Markl 1983). This means that the different frequency components in dispersion waves travel at different speeds, are not in phase with each other, and arrive at a given distance from the source at different times. Animals might be able to use these phase differences in locating the signal source (Gogala 1985a). A second difference between bending waves and plane transverse waves is that “the phase and group velocity are not the same, the latter being twice the phase velocity” (Gogala 1985a, 119). The group velocity “can be regarded as the propagation velocity of the carrier wave envelope of a wave bundle or wave packet” (Markl 1983, 339). Bending waves occur in a structure with a small diameter in relation to either the structure’s length or the wavelength: the diameter must be less than 1/6 the wavelength (Markl 1983). “Particle motion in bending waves is perpendicular to the structural surface at rest because the whole structure is rhythmically bent” (Markl 1983, 339). Boundary waves on the surface of water present a special case. A disturbance event will generate waves in which particle movement (in ellipses or circles) is dependent on water depth in relation to the wavelength. Likewise, propagation velocity at wavelengths greater than or equal to 10 cm (or frequency of less than or equal to 4 Hz) is dependent on gravity (gravity waves), whereas at higher frequencies (greater than or equal to 46 Hz or wavelength less than or equal to 0.6 cm) it is dependent on surface tension (capillary waves). In between, propagation velocity is dependent on both (capillary-gravity waves). Gravity waves in shallow water, like bending waves, are propagated with dispersion, while the dispersive waves in deeper water are more complicated. Attenuation of surface waves is also frequency dependent (Markl 1983). Since this book is intended as a study of vibrational communication in animals, the focus has been on substrate vibrations, whether those are via the surface of water, soils of various kinds, plant tissues, or spider webs. These vibration signals all involve at least some particle motion that is perpendicular to the direction of propagation. The

Communication and the Medium

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distinction between sound and vibration underwater is not a clear one, and the discussion of communication through water has been limited to very specific cases, as has that of infrasound and tactile (contact) communication signaling. The Issue of the Medium Animals create substrate vibrations, including those used in communication, through a variety of behaviors. Substrates can be soils, plants, water, honeycombs, and spider webs, but even within these broad groupings, great variation often exists in the characteristics of any given substrate (i.e., sand vs. clay soils, wet vs. dry sand, soft vs. rigid stems, leaves with parallel veins vs. leaves with netted veins, or even leaves vs. stems of the same plant). How much damping or filtering of the emitted signal occurs during propagation? How much of the signal is reflected, and do vibrations composed of energy across broad frequency bands propagate with dispersion, or are they phase locked? We have made progress in 30 years of study of vibration signaling, but much is still unknown. Further, the same behavior generates different kinds of waveforms, depending on the substrate, and different behaviors create waves of varying types even within the same substrate. For example, drumming is a percussive event, and we would expect that a drumming individual would produce longitudinal, or compression, waves (Morris 1980). Drumming on sand, or tree bark, or dry leaves are similar events from a behavioral perspective, but the transmission of the signals may be quite different, or they may not. Do drumming on a plant stem and stridulating while standing on a plant leaf create the same type of wave? Should and might are still part of the discussion until more data are gathered. Can we account for the tendency of animals to tremulate on plants but drum on sand because of the types of waves created by the behavior? Perhaps. Soils Soil is not a static substrate. Propagation properties of soil change from day to day with changes in temperature and moisture content (Hill and Shadley 2001). Further, generalizations and extrapolations

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Vibrational Communication in Animals

from one habitat to another are difficult to make (and to support empirically) because of variations in such things as particle size, degree of heterogeneity, and overall complexity of a soil. Some animals, such as the jumping spider Habronattus dossenus, routinely traverse an environmentally heterogenous substrate on a daily basis. H. dossenus can be located on sand, rock, and leaf litter in the Sonoran desert of North America and will court on all three substrates. The three substrates have very different filtering properties, and most successful courtship was on leaf litter, which was also the most favorable signaling substrate of the three (Elias, Mason, and Hoy 2004). In observing animals and designing simulations to test their responses, characteristics of the medium must be considered and incorporated into the design because “seismic waveforms (observed with geophones) produced by impulsive mechanical stimuli (including those produced by the thumper) are largely determined by the physical properties of the ground and largely independent of the stimulus source” (Lewis et al. 2001, 1195). In studying terrestrial or burrowing vertebrates or invertebrates, in rain forest or desert or prairie, the issue of the medium is nontrivial. As long as the temporal pattern and intensity of the simulated signal are a good approximation of a naturally produced one, the receiving animal will respond, whether the signal is produced by a living source or a mechanical one (Brownell and Farley 1979c; Hill and Shadley 2001; Lewis et al. 2001). In grasslands soils, attenuation of vibration signals is strongly dependent on frequency. For example, in a test of signal propagation at a frequency of 142.5 Hz, “the vibration level fell off at a rate of 44 dB per decade increase in distance” (Hill and Shadley 1997, 462). In addition, the soil is not a noise-free environment. Soil organisms produce vibrations as they move, forage, and perhaps communicate. Anyone who has ever listened to the Earth using a geophone in a desert or grassland when the wind is blowing knows the sounds of the tugging of grasses against the soil, which are much like the creaking and groaning of a wooden ship, or an old house, in the wind. There is also incidental noise in most inhabited regions due to vehicle traffic, and engineers are aware, even if biologists are not, of a rather ubiquitous 60 Hz vibration signal (50 Hz in Europe) from transducers in both substrate and atmosphere that could be interpreted by the unwary as evidence of vibration produced by animals. “It is not uncommon for recordings

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from electrical transducers to contain noise at 60 Hz and multiples of 60 Hz. In outdoor measurement, these are often due to emissions from electrical power transmission lines” (Hill and Shadley 2001, 1204). Thus, collaborative research across disciplinary lines is a wise choice for all those hoping to disentangle the part of a putative signal that is from the animal and the part that is from its environment. Even though Brownell (1977) knew that sand was supposed to absorb low- frequency vibrations instead of propagate them, he identified two separate waves propagating through desert sand when a piezoelectric crystal generated displacement pulses on the sand surface (Figure 2.2). A fast wave varied in velocity with sand compaction from 95 to 120 m/sec and was determined to be a compressional body wave, or P-wave. The slower wave velocity was 40 m/sec in loose sand and 50 m/sec in lightly compacted sand. This slower wave was determined to be a Rayleigh wave, and both wave types traveled at about 1/10th their documented velocities in other natural substrates. Both waves were detected when the receiver axis was placed radially to the source, but amplitude of the Rayleigh wave increased, and that of the P-wave decreased, when the receiver was oriented perpendicular to the surface. Likewise, the Rayleigh wave could be damped by placing an absorbant object between source and receiver, whereas the P-wave was not affected (Brownell 1977). Rayleigh waves and Love waves, which are boundary waves, are the principal components of the vibrations produced by drumming fiddler crabs, and the surface P-waves, or primary waves, carried much lower energy (Aicher and Tautz 1990).

Vibrational Wave Transmission in Sand Source

R

sand

V (m/s) Freq (Hz) (cm) G(r) 10(db/cm) Surface waves (>70%) 45–50 300–400 ~10–15 cm ~1/r 0.20–0.40 Rayleigh (R)

----~1/r Love (L)

P Body waves ( 60 kHz) airborne sexual advertisement calls (Morris et al. 1994), and an undescribed species in the genus Arachnoscelis from Columbia actually sings a pure-tone song at 129 kHz (Montealegre-Z, Morris, and Mason 2006). Bushcrickets sing these very high-frequency calls with significant intervals of silence that result in a reduced duty cycle for the song. The signal bursts are short, but at these very high frequencies they would also attenuate rapidly with distance and could thwart eavesdropping predators. The signals would be of less importance in long-range advertisement to females, but they are thought to have evolved in areas where katydids are heavily preyed upon by bats, and so the high-frequency signals would also be less conspicuous, though not undetectable, to nearby bats. Many of the same katydid species have developed elaborate vibration signaling that employs a mechanism separate from stridulation, and in some cases the vibration event is the only calling song produced by males. Tremulation of the male body often produces the substrate signal, but in contrast to temperate zone tremulation, neotropical species actually employ the behavior in “rhetorical” sexual advertisement in the absence of females, rather than for close-range pairing. Trade-offs are always present, however, because in gaining privacy from bat eavesdropping through the evolution of substrate-borne vibration signals, the door would have been opened for eavesdropping on vibration signals by wandering spiders in the genus Cupiennius (Morris et al. 1994). It should be noted that the concept of privacy is not unique to communication via the vibration channel and may simply be a human construct used to explain phenomena about which we are short on information. The neotropical katydid Copiphora rhinoceros may also have evolved tremulation-induced substrate signaling in response to bat predation.

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However, an additional selective mechanism may have been avoidance of cuckoldry. Males of this species produce very large spermatophores, which are passed to females during copulation, and they invest both time and body mass in spermatophore assembly. One male was observed to spend five hours in courtship and copulation, whether or not this is standard for the species. Males within a refractory period after mating can still copulate and pass sperm packets, but the tremulation signals they produce with and without the burden of a spermatophore are substantively different. Signals produced by males should thus provide an honest signal to females of ability to invest direct nutritional benefits because tremulation signals would be changed for any given male with the weight loss that follows passing a spermatophore. Neighboring males that have already passed spermatophores could take advantage of the airborne signal of a male with a spermatophore to offer, but tremulation signals would only be detectable by a female on the same branch of vegetation. Thus, cuckoldry could be avoided by the male who actually is investing nutrients for the benefit of future offspring (Morris 1980). Likewise, in a species such as the black-horned tree cricket, Oecanthus nigricornis, where the male feeds his mate secretions from a metanotal gland, attracting too many females could be a problem. Immediately following mating and before he is capable of inseminating others, females that were able to find him based on his airborne or pheromonal signaling could harvest his nutritional contribution without providing him the benefit of parenthood. Use of vibrational signals in courtship at the last stage of pair formation thus affords some privacy (Bell 1980a). Epiphenomena Associated with Other Behaviors Randall (2001) suggested that footdrumming in mammals evolved independently in different lineages, possibly as a ritualization of other behaviors. The conflict between running away from a threat and moving toward it, in inspection and for risk assessment, could have led to drumming as a displacement activity. This hypothesis has stronger support than a suggestion that footdrumming evolved from a digging behavior because some kangaroo rats drum just before they run to chase an intruder. Evolution of a signal, however, is perhaps linked in

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an unexplored way to body mass in kangaroo rats: large-bodied territory defenders drum, whereas medium-sized species have a rudimentary signal, and the smallest species do not drum (Randall 2001). The days of arguing in a brew pub whether or not communication through the substrate vibration channel even exists are happily gone. Scientists are working across vertebrate and arthropod taxa to document and test hypotheses for behaviors and to describe sending and receiving mechanisms. When a baffling behavior is encountered, it is no longer rare for someone to suggest that vibration signaling may be involved. However, a great deal of alpha-level work is still required before a unified theory of vibrational communication can be formulated. So much has been accomplished in the last five years that we are justifiably encouraged to hope that energetic young scientists will accept the challenge to use their interdisciplinary training and creativity to make a name for themselves through revealing the mysteries surrounding this communication channel. Einstein was chided near the end of his life for “wasting” so much time searching for answers that would reveal the unified field theory. We are told he replied that he could afford the time because he had already made his reputation, whereas young scientists were expected to work on problems that held promise that a solution actually did exist. Now the standard model in physics includes an explanation for everything but the gravitational field. Perhaps the study of vibration communication will develop in the same way. Those who have worked so hard to study vibration as side projects to other, sponsored research are seeing younger scientists begin to attract funding for projects where vibrational communication plays a key role. The torch is being passed. Do not let it fall.

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Species Index

MAMMALIA Order Monotremata Ornithorhynchus anatinus Gray, 63 Tachyglosss aculeatus (Shaw), 63 Order Dasyuromorpha Sarcophilus harrisii Boitard, 91–92 Order Diprotodontia Macropus eugenii Desmarest, 63–64, 91–92 Macropus giganteus Shaw, 91–92 Order Afrosoricida Chrysochloris asiatica (Linnaeus), 46 Eremitalpa granti Broom, 44–46, 120–121, 205 Order Proboscidea Elephus maximus Linnaeus, 9–10, 43–44, 61, 89–91, 178 Loxodonta africana Blumenbach, 89–91, 178 Order Primates Alouatta palliata Gray, 10 Homo sapiens sapiens Linnaeus, 56, 60 Order Rodentia Cryptomys Gray sp., 205 Dipodomys deserti Stephens, 46, 88, 128 Dipodomys heermanni LeConte, 88–89 Dipodomys ingens (Merriam), 46, 88, 128 Dipodomys spectabilis Merriam, 46, 88, 127–128, 183 Georychus capensis (Pallas), 44, 87–88 Heterocephalus glaber Rüppell, 47 Nannospalax ehrenbergi, 13, 43, 87. See also Spalax ehrenbergi Nehring Notomys Lesson sp., 47 Pseudomys Gray sp., 47 Rhombomys opimus (Lichtenstein), 129

249

250

Species Index

Spalax ehrenbergi Nehring, 13, 43–44, 47, 61–62, 87, 136, 205. See also Nannospalax ehrenbergi Order Soricomorpha Condylura cristata Linnaeus, 62–63 Order Carnivora Spilogale interrupta (Linnaeus), 89 Vulpes macrotus Merriam, 128 Order Artiodactyla Odocoileus virginianus Zimmermann, 89 Order Cetacea Tursiops truncatus Montagu, 42 AVES Columba livia Gmelin, 41 Fulica atra Linnaeus, 92 REPTILIA Order Squamata Cerastes Laurenti sp., 121 Chamaeleo calyptratus Duméril & Bibron, 65, 92 Chamaeleo höhnelii (Steindachner), 48 Chamaeleo jacksoni (Boulenger), 48 Chamaeleo quilensis Bocage, 48 Chamaeleo senegalensis Daudin, 48 Dispholidus typus (Smith), 49 Erix miliaris (Pallas), 129 Pituophis melanoleucus affinis Conant & Collins, 127, 129 Pseudechis porphyriacus Shaw, 64–65. See also Pseudechis porthyriacus (sic) Pseudechis porthyriacus (sic), 64–65 Scincus scincus Linnaeus, 50, 121 AMPHIBIA Order Urodela Salamandra Laurenti sp., 49 Triturus Rafinesque sp., 49 Order Anura Agalychnis callidryas Cope, 129–130 Eleutherodactylus coqui Thomas, 53 Leptodactylus albilabris (Gunther), 50, 92–93, 179 Leptodactylus syphax Bokermann, 93 Lithobates catesbeiana (Shaw), 48, 50. See also Rana catesbeiana (Shaw) Lithobates clamitans (Latreille), 32. See also Rana clamitans (Latreille) Lithobates pipiens (Schreber), 51. See also Rana pipiens (Schreber) Lithobates sphenocephala (Cope), 130–131. See also Rana sphenocephala (Cope) Rana catesbeiana (Shaw), 48, 50 Rana clamitans (Latreille), 32 Rana pipiens (Schreber), 51 Rana sphenocephala (Cope), 130–131

Species Index

251

Rana temporaria Linnaeus, 51 Telmatobius halli Noble, 94 Telmatobius montanus Lataste, 94 Telmatobius marmoratus Duméril & Bibron, 94 Telmatobius pefauri Veloso & Bibron, 94 Telmatobius peruvianus Weigmann, 94 Telmatobius zapahuirensis Veloso, Sallaberry, Navarro, Iturra, Valencia, Penna & Díaz, 94 Xenopus laevis Daudin, 53–55 OSTEICHTHYES Cottus bairdii Girard, 52, 95 Oncorhynchus keta Walbaum, 136 Oncorhynchus nerka (Walbaum), 136 Opsanus tau (Linnaeus), 94–95 INSECTA Order Plecoptera Acroneuria abnormis (Newman), 141 Capnia bifrons Newman, 140 Dinocras cephalotes Curtis, 140 Nemoura spiniloba Jewett, 138 Isogenoides zionensis Hanson, 140 Isoperla Banks sp., 140 Oconoperla innubila (Needham & Classen), 141 Perla marginata Panzer, 140 Perlinella drymo (Newman), 139 Pteronarcella badia (Hagen), 139 Taeniopteryx burksi Ricker & Ross, 140 Order Megaloptera Sialis fuliginosa Pictet, 98, 141–142 Sialis lutaria Linnaeus, 98, 141–142 Order Orthoptera Ametrus Brunner von Wattenwyl sp., 99, 145 Anurogryllus muticus (DeGeer), 2 Arachnoscelis Karny sp., 207 Balamara gydia Otte & Alexander, 143–144 Chorthippus parallelus (Zetterstedt), 96 Conocephalus nigropleurum (Bruner), 108, 144 Copiphora rhinoceros Pictet, 107, 207 Decticus verrucivorus (Linnaeus), 175 Docidocercus chlorops Nickle, 107 Ephippiger ephippiger Fiebig, 107, 143 Gryllotalpa major Saussure, 3–4, 177–181 Gryllus bimaculatus DeGeer, 142 Gryllus campestris Linnaeus, 2 Hadrogryllacris Karny sp., 99, 145 Hemiandrus pallitarsis (F. Walker), 112, 145

252

Species Index

Hemideina crassidens (Blanchard), 111–112, 144–145 Hemideina femorata Hutton, 111–112, 144–145 Hemideina ricta (Hutton), 111–112 Meconema thalassinum (DeGeer), 99, 145 Melanonotus powellorum Rentz, 107 Myopophyllum speciosum Beier, 107 Oecanthus nigricornis F. Walker, 25, 143, 208 Ornebius aperta Otte and Alexander, 144 Phaeophilacris spectrum Saussure, 112 Polysarcus denticauda (Charpentier), 72 Stenopelmatus Burmeister sp., 98–99 Tettigonia cantans Fuessly, 142, 176 Order Blattodea Arenivaga investigata Friauf & Edney, 133 Periplaneta americana Linnaeus, 69–70 Order Isoptera Macrotermes bellicosus (Smeathman), 133, 184 Macrotermes subhyalinus (Rambur), 133, 184 Pseudacanthotermes militaris (Hagen), 133 Pseudacanthotermes spiniger (Sjöstedt), 133 Reticulitermes flavipes (Kollar), 96 Zootermopsis angusticollis (Hagen), 133, 184–185, 188 Zootermopsis nevadensis (Hagen), 133, 184 Order Hemiptera (Heteroptera: Gerromorpha) Aquarius remigis, 32. See also Gerris remigis Say Gerris buenoi Kirkaldy, 32 Gerris lacustris (Linnaeus), 31 Gerris odontogaster (Zetterstedt), 32 Gerris remigis Say, 31–32. See also Aquarius remigis Limnoporus dissortis (Drake & Harris), 33 Limnoporus notabilis (Drake & Hottes), 33 Limnoporus rufoscutellatus (Latreille), 33 Rhagadotarsus spp. Breddin, 32–33 Order Hemiptera (Heteroptera: Nepomorpha) Corixa dentipes (Thomson), 106, 150 Corixa punctata (Illiger), 106 Notonecta glauca Linnaeus, 30–31, 67–68 Notonecta kirkii, 32 Notonecta lutea Müller, 32 Order Hemiptera (Heteroptera: Cimicomorpha) Corythucha hewitti Drake, 198–199 Dipetalogaster maxima (Uhler), 105 Nabis kinbergii Reuter, 128 Rhodnius prolixus Stål, 105 Triatoma guasayana Wygodzinsky & Abalos, 105 Triatoma infestans (Klug), 105 Triatoma sordida (Stål), 105

Species Index Order Hemiptera (Heteroptera: Cydnidae), 68, 97, 117 Sehirus (Canthophorus) dubius Scopoli, 24 Sehirus (Canthophorus) impressus Horváth, 24 Sehirus (Canthophorus) melanopterus (Herrich-Schäffer), 24 Sehirus (Tritomegas) bicolor (Linnaeus), 24 Order Hemiptera (Heteroptera: Pentatomidae) Acrosternum hilare (Say), 149–150 Euschistus conspersus (Uhler), 150 Holcostethus strictus (Fabricius), 150 Murgantia histrionica (Hahn), 27, 150 Nezara viridula (Linnaeus), 27, 29, 71, 75, 122, 145–150 Podiscus maculiventris (Say), 122–123 Thyanta custator accerra ( Jones), 150 Thyanta pallidovirens (Stål), 150 Order Hemiptera (Auchenorrhyncha Dictyopharidae) Dictyophara europea (Linnaeus), 151 Order Hemiptera (Auchenorrhyncha: Delphacidae) Euides speciosa (Boheman), 24 Javesella Fennah sp., 152 Laodelphas striatellus Fall, 24, 114–115, 151 Nilaparvata lugens (Stål), 24, 28, 111, 114–115, 151–152, 175 Oliarus Stål sp., 153 Prokelisia dolus Wilson, 152 Prokelisia marginata (Van Duzee), 152 Ribautodelphax Wagner sp., 152 Sogatella furcifera (Horváth), 24, 114–115, 151 Solonaima Kirkaldy sp., 153 Tachycixius Wagner sp., 153 Order Hemiptera (Auchenorrhyncha: Cicadidae) Okanagana rimosa (Say), 116–117 Tettigarcta crinita Distant, 114 Tettigarcta tomentosa White, 114–115 Order Hemiptera (Auchenorrhyncha: Membracidae) Calloconophora pinguis (Fowler), 198 Enchenopa binotata (Say), 156 Ennya chrysura Fairmaire, 158, 175 Tomogonia vittatipennis (Fairmaire), 133 Umbonia crassicornis (Amyot & Serville), 27, 156, 200 Vanduzea arquata Say, 158–159 Order Hemiptera (Auchenorrhyncha: Cicadellidae) Agallia constricta Van Duzee, 154 Agalliopsis novella (Say), 154 Amrasca devastans (Distant), 28, 154. See also Empoasca fabae (Harris) Balclutha incisa (Matsumura), 128 Circulifer tenellus (Baker), 113, 115–116 Empoasca fabae (Harris), 115 Euscelidus variegatus Kirshbaum, 24

253

254

Species Index

Euscelis lineolatus Brulle, 24 Graminella nigrifrons (Forbes), 155–156, 164, 180 Oncopsis avellanae Edwards, 154–155 Oncopsis flavicollis (Linnaeus), 75, 154–155 Oncopsis tristis (Zetterstedt), 154–155 Spissistilus festinus (Say), 155 Order Hemiptera (Sternorrhyncha: Aleyrodidae), 111 Order Hemiptera (Sternorrhyncha: Psylloidea), 105, 159 Order Hemiptera (Coleorrhyncha) Hackeriella veitchi (Hacker), 96 Order Neuoptera Brinckochrysa Tjeder sp., 109 Chrysocerca Weele sp., 109 Chrysopa carnea Stephens, 160. See also Chrysoperla carnea (Stephens) Chrysoperla agilis Henry, Brooks, Duelli & Johnson, 161 Chrysoperla carnea (Stephens), 25, 67–68, 71, 160–161 Chrysoperla downesi (Smith), 160 Chrysoperla lucasina (Lacroix), 67–68 Chrysoperla pallida Henry, Brooks, Duelli & Johnson, 161 Chrysoperla plorabunda Fitch, 160–161 Dichrostigma flavipes (Stein), 71 Hemerobius micans Olivier, 71 Meleoma (Fitch) sp., 109 Myrmeleon formicarius Linnaeus, 123 Osmylus fulvicephalus (Scopoli), 71 Semidalis aleyrodiformia (Stephens), 71 Sisyra terminalis Curtis, 71 Order Coleoptera Aphodius ater (DeGeer), 104 Aphodius granarius (Linnaeus), 104 Aphodius pectoralis LeConte, 104 Aphodius rainieri Hatch, 104 Aphodius sigmoideus Van Dyke, 104 Dineutes discolor Aubé, 33, 76 Epilachna varivestis Mulsant, 122 Eupsophulus castaneus (Horn), 161–162 Eusattus convexus LeConte, 161 Eusattus muricatus LeConte, 161 Eusattus reticulatus Say, 161 Eusattus robustus LeConte, 161 Hylotrupes bajulus (Linnaeus), 105–106 Lepidochora discoidalis (Gebien), 74 Onymacris plana plana (Peringuey), 74 Onymacris rugatipennis (Haag), 74 Phelypera distigma (Boheman), 199 Phrynocolus somalicus Wilke, 162 Physodesmia globosa (Haag), 74 Platypus quercivorus (Murayama), 104

Species Index Polychalma multicava (Latreille), 198 Psammodes striatus (Fabricius), 204–205 Xestobium rufovillosum (DeGeer), 162 Zophosis orbicularis (Deyrolle), 74 Order Mecoptera Panorpa alpina (Rambur), 162 Panorpa communis Linnaeus, 162 Panorpa germanica Linnaeus, 162 Order Diptera Anastrepha suspense Lowe, 125 Drosophila cyrtoloma Hardy, 163 Drosophila fasciculisetae Hardy, 163 Drosophila heteroneura Perkins, 163 Drosophila melanogaster (Meigen), 163 Drosophila silvestris Basden, 163 Formicosepsis hamata, 175 Lipara japonica Kanmiya, 84, 112, 164, 175 Order Hymenoptera Aphaenogaster Mayr sp., 185 Apis cerana Fabricius, 196 Apis dorsata Fabricius, 196 Apis florea Fabricius, 196 Apis laboriosa Smith, 196 Apis mellifera Linnaeus, 73–74, 112, 190–198 Apis mellifera scutellata Lepeletier, 195 Atta cephalotes (Linnaeus), 73, 98, 186–188 Atta sexdens (Linnaeus), 98, 103–104, 186 Belonogaster Saussure sp., 189 Biosteres longicaudatus Ashmead, 125 Bombus hortorum (Linnaeus), 37 Bombus terrestris (Linnaeus), 37 Camponotus ligniperda Latreille, 73, 98, 185 Cotesia rubecula (Marshall), 164 Dasymutilla foxi (Cockerell), 164 Euglossa imperialis Cockerell, 37 Formica rufa Linnaeus, 123 Iridomyrmex anceps (Roger), 132 Leptogenys chinensis Mayr, 188 Megaponera foetens (Fabricius), 133, 188–189 Melipona seminigra Friese, 192 Messor capitatus (Latreille), 186 Metapolybia aztecoides Richards, 194 Monomorium Mayr sp., 188 Novomessor albisetosus (Mayr), 185–186 Novomessor cockerelli (André), 185–186 Perga dorsalis Leach, 198 Pimpla instigator Fabricius, 101–102 Pimpla turionellae (Linnaeus), 101–102, 206

255

256

Species Index

Pogonomyrmex Mayr sp., 186 Polistes dominulus (Christ), 99, 190 Polistes fuscatus (Fabricius), 99, 189–190 Polistes metricus Say, 189 Polyrhachis Arnold sp., 98 Sympiesis sericeicornis Nees, 124–125 Tapinoma Foerster sp., 188 Vespa orientalis Fabricius, 190 Order Lepidoptera Barathra brassicae (Linnaeus), 82 Caloptillia serotinella (Ely), 117 Drepana arcuata Walker, 199 Jalmenus evagoras (Donovan), 132 Phyllonorycter blancardella Fabricius, 124–125 Phyllonorycter cydoniella (Denis & Schiffermüller), 124 Phyllonorycter malella (Gerasimov), 123–125 Plathypena scabra (Fabricius), 122 Semiothisa aemulataria (Walker), 131 Thisbe irenea (Stoll), 131–132 AR ACHNIDA Order Scorpiones Paruroctonus mesaensis (Stahnke), 5–6, 76–78, 86, 122, 133 Order Acariformes Neumania papillator Marshall, 172 Order Araneae Acanthoscurria suina Pocock, 101 Agelena Koch sp., 83 Agelenopsis aperta (Gertsch), 169 Araneus (or Araneous) sericatus Clerck, 79, 83 Argiope argentata (Fabricius), 126 Argyrodes elevatus Taczanowski, 126 Cupiennius coccineus Pickard-Cambridge, 28, 171, 207 Cupiennius getazi Simon, 28, 109–110, 171, 173–174, 207 Cupiennius salei (Keyserling), 28–30, 76–81, 110, 126, 169–172, 207 Cyrtophora cicatrosa (Stoliczka), 168 Dolomedes triton (Walckenaer), 33, 77, 79 Eupalaestrus weijenberghi (Thorell), 101 Habronattus dossenus Griswold, 22, 164–165 Habronattus pugillis Griswold, 165–166 Heteropoda venatoria (Linnaeus), 109 Hygrolycosa rubrofasciata (Ohlert), 99–100, 166–167 Isopoda immanis (Koch), 109 Leucorchestris arenicola Lawrence, 175 Lycosa tarentula fasciiventris Dufour, 99, 171–173 Micrathena sagittata (Walckenaer), 126 Nephila clavipes (Linnaeus), 36, 83, 126 Phidippus johnsoni (Peckham & Peckham), 205

Species Index Pisaura Simon sp., 83 Portia fimbriata (Doleschall), 126–127 Schizocosa ocreata (Hentz), 99–100, 167 Schizocosa rovneri Uetz & Dondale, 100, 167 Schizocosa stridulans Stratton, 100, 167–168 Scytodes pallida Doleschall, 130 Sericopelma Ausserer sp., 83 Stegodyphus lineatus Latreille, 168–169 Theridion saxatile (Koch), 200 Zygiella Pickard-Cambridge sp., 35, 83 CRUSTACEA Gecarcinus lateralis (Fréminville), 97 Heloecius cordiformis (Milne-Edwards), 137 Nephrops norvegicus (Linnaeus), 83 Ocypode jousseaumei (Nobili), 81–82, 97–98, 102–103 Ocypode platytarsus Milne-Edwards, 81–82, 97–98, 102–103 Ocypode rotundata Miers, 81–82, 97–98, 102–103 Ocypode saratan (Forskål), 81–82, 97–98, 102–103 Ocypode sinensis Dai, Song & Yang, 81–82, 97–98, 102–103 Uca longidigitum (Kingsley), 137 Uca minax LeConte, 81–82 Uca pugilator (Bosc), 14, 81–83, 97–98, 165, 205 NEMATODA Heterorhabditis megidis Poinar, Jackson & Klein, 123 Steinernema carpocapsae (Weiser), 123 Steinernema feltiae (Filipjev), 123

257

Subject Index

Abdominal rubbing, 140–141 Abdominal wagging, 169, 189. See also Tremulation Acceleration detector, 50, 81–82 Acoustic fat, 42–43 Advertisement signal, 4, 53, 87, 92–93, 95–96, 99, 107, 119, 137, 141–142, 145, 154, 159, 161, 173, 176, 179, 182, 207 Aggressive mimicry, 126–127 Aggressive signal, 32–33, 93, 97, 106, 156, 159, 175, 180 Alarm signal, 87, 89–92, 94–95, 103, 129, 133, 184–185, 197, 200 Annelida, 13 Ant-associated, 131–133, 158–159 Auditory ossicle, 7–8, 40–41, 43–48, 52 Barth’s organ, 67, 81–82 Basitarsal compound slit sensilla (BCSS), 6, 66, 76–79, 82 Bending wave, 17, 20, 25, 30, 142 Bone conduction, 7, 41–49, 52 Boundary vibration, 17–20 Brownell, Philip, 5–6, 23 Buzz pollination, 36–37 Calling song, 4, 24, 29, 32, 83, 93, 98–99, 104–107, 111, 128, 142–143, 146–159, 161, 164, 175–181, 207

Campaniform sensilla, 66–68, 75–76, 105, 143, 192 Cave-dweller, 152–153 Cerebral cortex, 59–60, 62, 65–66 Chaetognatha, 13 Chela, 14, 97–98, 137, 205 Chordotonal organ, 66–69, 74–75, 81–82, 192 Chorusing, 3, 137, 158, 177, 180–181 Cocroft, Reginald (Rex), 2 Columella (stapes), 8, 47–48, 54 Common sound, 153–154 Contact vibration, 17, 21, 32–33, 66–67, 94, 104, 106, 143 Courtship signal, 24, 29–30, 32–34, 80–81, 92, 97–99, 101, 104, 106–107, 109–111, 115, 128, 137, 142, 144, 146–148, 151, 153–154, 156, 158, 160, 163–175, 186, 200, 205, 208 Defense signal, 95, 102, 111–112, 132, 144, 187 Dialects, 139 Dicotyledonous leaf, 27–29, 81 Directional information, 33, 49, 77, 83, 121–122, 133, 140, 146, 149, 155–156, 162, 203 Distance estimation, 6, 25, 30, 33, 80, 82–83, 122, 133, 142, 155, 170, 173

259

260

Subject Index

Disturbance sound, 97, 104–105, 119–120, 133, 154, 184, 189, 199 Dorso-ventral abdominal movement, 109–112, 114, 141, 143, 162, 168, 191, 193, 196. See also Tremulation Drumming, 14, 21, 23, 30, 46–47, 62, 80, 82, 87–102, 107, 109, 111–112, 125, 127–129, 133, 136–145, 154, 156, 158, 161–162, 164–175, 183–185, 188–190, 198–199, 205, 208–209 Duet, 26, 87–88, 98, 106, 128, 135, 139–140, 145–146, 150–151, 154, 156, 159–162, 169–171 Eimer’s organ, 62–63 Farley, Roger, 5 Female abdominal vibration (FAV), 111, 115, 151–152. See also Tremulation Female choice, 144, 152, 157–158, 166–167, 169, 171–172 Flight muscles, 36–37, 112, 163–164, 192–194 Footdrumming, 46–47, 87–88, 127–129, 183, 208. See also Drumming Frequency discrimination, 31, 79–80, 83 Gas bladder, 52, 94–95 Geophone, 22, 89, 120, 178–179, 206 Gogala, Matija, 68, 97 Hair sensilla, 66, 82–84 Harmonics, 28, 69, 103, 156, 158, 164, 177–178, 194 Herbst corpuscle, 63–65 Honeycomb, 34, 112, 190–191, 196–197 Hunt, Randy, 181 Hyomandibula, 8

Longitudinal wave, 17, 19, 21, 35–36, 79 Love wave, 18–19, 23 Lyriform organ, 34, 66, 78–81, 83–85 Meissner’s corpuscle, 56–57, 61–62 Merkel’s receptor, 56–57, 63 Mid-coxal protuberance, 84 Modulatory communication, 149, 185, 191–197, 199 Monocotyledonous leaf, 28–29, 81, 169 Multimodal signal, 13, 143, 165–168, 186, 206 Narins, Peter, 206 Nearfield motion, 17, 75, 168 Nest moving, 188, 194–195 O’Connell-Rodwell, Caitlin, 202 Opercularis, 48–49 Opisthosoma, 30, 99, 109–110, 170–174 Ossiannilsson, Frej, 3, 15, 96, 113–115, 181 Pacinian corpuscle, 56–65, 69–70, 81, 84–85, 120 Pathogen alarm, 184–185 Pedipalp, 30, 80, 99, 167–174 Percussion. See Drumming Pheromones, 109, 146, 149–150, 164, 169, 172, 185, 188, 208 Pneumatic duct, 52 Predator-induced hatching, 129–131 Propagation with dispersion, 20–21, 25 P-wave (compressional), 6, 10–11, 17–18, 23, 82, 121, 175 Quadrate bone, 7–8, 48–49 Quasi-longitudinal wave, 17, 19 Queen piping, 164, 194

Infrasound, 21, 41, 112 Johnston’s organ, 33, 66–67, 74–76, 105, 192 Juvenile hormone ( JH), 195 Lagena, 7, 50–51 Lateral vibration (LV), 189–190 Lewis, Edwin (Ted), 206

Randall, Jan, 202, 208 Rapping, 82–83, 98, 102. See also Drumming Rayleigh wave, 6, 18–19, 23, 46, 48–49, 59, 77, 86, 88–90, 93, 121, 162, 175, 206 Recruitment, 103, 133, 186–188, 190, 194–195, 197–198

Subject Index Repelling vibration, 146, 186 Rivalry song, 24, 147, 149–150, 159, 180 Rodríguez, Rafael, 2 Ruffini’s corpuscle, 56–57 Sacculus (saccule), 7, 50–52, 121 Sand, 6, 17, 21–23, 33, 45–46, 74, 76, 86, 95, 104, 120–123, 128, 165, 171, 175, 206 Scolopidia, 67, 70–72, 75 Scraping, 30, 117, 190, 199 Shaking signal, 191, 193 Sibling-group signal, 200–202 Signal, 12–13, 37–39, 94, 135–136, 181–182, 208 Signal jamming, 158, 175 Slapping. See Drumming Slit sensilla, 6, 66, 76–85 Soil, 3, 7, 9, 17, 21–23, 43, 86–87, 92–93, 97–98, 103–104, 123, 125, 141–142, 165, 177–179, 204–205 Sounding, 71–72, 101–102, 125 Spacing, 87–88, 90, 98, 117, 162, 176–177, 181–182 Spider webs, 19, 34–36, 80, 83, 126–127, 168–169 Stamping. See Drumming Stance, 33, 73, 77–79, 82, 122, 149 Stapes (columella), 8, 40, 45–49, 54 Stridulation, 21, 96–107, 109, 111–112, 117, 120, 128, 132–133, 142–145, 150–151, 159, 162, 164–165, 167–168, 172, 176–177, 185–189, 207 Subgenual organ, 14–15, 66–76, 81, 84–85, 98, 102, 105, 125, 143, 181, 192, 197 S-wave, 10–11, 18 Swim bladder, 52, 71, 94. See also Gas bladder

261

Synthetic signals, 80–81, 84, 124–125, 160, 170, 175, 179–180, 194, 197 Tapping. See Drumming Tarso-pretarsal organ, 68 Temperature dependent, 110, 138 Temporal pattern, 22, 30, 95, 97, 105, 110, 124, 130, 137, 139–140, 144–147, 152, 154, 159, 167, 170–173, 181 Thumping, 91, 93, 98. See also Drumming Ticking, 154 Torsional wave, 17, 19, 35 Transducer, 25, 39, 55, 68 Transverse wave, 17, 19–20, 35–36, 79, 107 Tremble dance, 196–197 Tremulation, 21, 30, 99, 107–112, 115, 117, 128, 140–141, 143–144, 151, 155, 160–162, 164–165, 167, 170, 172, 188–189, 191, 193, 196, 199, 207–208 Trichobothria, 34, 66, 83–84, 105 Trichoid sensilla, 66–67 Tsunami, 9–11, 59–60 Tymbal, 3, 15, 96, 112–117, 151, 154–155, 159 Tympanal organ, 14–15, 70, 97, 105–106, 114, 143 Utriculus (utricle), 50–51 Velum, 71–72 Vibration dance, 191–195 Vocalization, 91, 94 Water-borne, 20, 30–34, 55, 82–83, 122 Weberian ossicles, 52 Wind, 22, 29, 31, 74, 125, 127, 129, 205–206 Wing movement, 111–112, 116, 141, 143, 154, 156, 163–164