ACOUSTICAL COMMUNICATION IN ARTHROPODS1

By RICHARD D. ALEXANDER Museum of Zoology and Department of Zoology, The University of Michigan, Ann Arbor, Michigan

Prior to the early 1950's, the study of arthropod acoustical behavior had been in a relatively stable state for a long time. Although hundreds of papers had been published on sound production and reception in insects, they had dealt chieflywith the morphology and physiology of devices that were either known or suspected to produce or respond to sounds [see bibliography (55)}. Only a few critical experiments on acoustical behavior had been performed (66, 68, 96, 113, 128-130). An abundance of review articles and books (13, 14, 37, 49, 50, 65, 111, 112, 123, 125, 131, 142) had failed to bring about any sustained growth of interest comparable to that enjoyed more recently by the field. The accelerating development of electronic recording and analyzing equipment following World War II ushered in a new era, attracting a large number of workers into many aspects of the field of animal communication. In the course of 10 or 15 years, several hundred papers were published on arthropod acoustics, including fivebooks (24, 51, 76, 85, 150) and an impres­ sive array of review articles (1, 3, 6---8, 43-45, 54, 77, 124 and others). The recent volume on acoustical behavior of animals edited by Busnel (25) de­ votes 285 pages to articles dealing solely with arthropods by six different authors, and insects are prominently discussed in several of the other chap­ ters. Nearly 500 genera of arthropods are mentioned, including representa­ tives of 15 orders of insects. The great preponderance of this recent work, inspired by the availability of new equipment and techniques, has involved descriptions and comparisons of the physical structure of the sounds themselves and of the ranges of re­

by Brown University on 06/06/12. For personal use only. sponsiveness of auditory organs. Relatively little direct study of the com­ municative significance of the various signals has been carried out, though probably more than has been accomplished for any other animal group. I t seems clear that we are now on the threshold of still another era in the Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org study of arthropod acoustics. The flurry of interest that generates whenever any new kind of biological information becomes available has largely faded. In some fields, such as systematics, applications have become well established and are incorporated into the methodologies of those active in the field (2, 5, 10, 146, 155, 156, 158). In other areas, such as insect control, there have been few or no encouraging developments (17, 56---58, 77, 89). Many of the workers who stepped into this field with the advent of new methods and equipment have stepped out again, and review articles seem to be proliferating faster than the research papers necessary for their sustenance. In short, the band-

1 The survey of the literature pertaining to this review was concluded in May 1966.

495 496 ALEXANDER

wagon of the late 1950's has disappeared , and we are faced with the question of what to do ultimately with information derived from the study of arthro­ pod acoustical behavior which, in turn, determines how hard we are going to work at studying it, and who is going to do the studying. Part of the answer to these questions derives from what has been happen­ ing in related fields. The rise of interest in arthropod acoustical behavior has coincided with an intensifying of concern among zoologists with the whole field of animal behavior-sparked by the extensive contributions of Euro­ pean ethology, the examples of investigators such as Karl von Frisch and his students in their work on honey bee biology, and a growing realization of the importance of behavioral information to the kinds of syntheses with which zoology is increasingly discovering itself to be concerned. One might say that, together, the various specialized fields of animal behavior-of which arthropod acoustics is one--have, once again, produced an embryo. If we can agree that this one is not a monster which ought to be aborted as quickly as possible, then our problem is how best to nourish it and guide its development. The study of animal behavior has had trouble before because this problem was not solved. In fact, only one of the many such embryos that zoology has produced has survived; this is psychology, whose foster parents, medicine and philosophy, have provided it with an adequate livelihood and considerabl e security, though in large part well out­ side the zoological family. Perhaps the problems involved in behavioral study by zoologists will be solved this time before it is too late. I think the nucleus of an answer lies in the early efforts of such biologists as William Morton Wheeler and Konrad Lorenz to focus attention on the role of natural selection in shaping behavior. Only when biological attributes are examined under the continuing realiza­

tion that they are, in one way or another, always a result of long, compli­ cated sequences of selective action, can we be confident that the most appro­ priate routes have been taken toward their understanding-whether in terms

of physiological mechanisms, ontogeny, or heredity-and their eventual by Brown University on 06/06/12. For personal use only. incorporation into reconstructive and predictive frameworks relative to the process of organic evolution. But there is another requirement, and this is that we must also acknowledge finally that behavior has always played a central role--perhaps the central role--in mediating the effects of natural Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org selection upon animals. Simpson (141) has said it this way: "Behavior is

subject to particularly strong selection , and it is probably farthest removed from the genes.... As a rule, with exceptions, the effect [of selection} be­ comes more, not less, diffuse, and less, not more, direct as the level of the gene is approached." Specialized acoustical behavior,· unlike specializations associated with chemical and visual input or output, is always a communicative phenomenon in all kinds of animals. It does not matter whether the signals are functional intraspecifically or interspecifically, or even if they are used solely by the individual producing them, as in echo-location; whether they are transmitted ACOUSTICAL BEHAVIOR 497

aerially, aquatically, through solid substrate (with air-transmitted portions that we hear only incidental to the signals themselves), or even only through direct bodily contact. To be examined in terms of selective action they must be studied as communicative units. Communicative functions, in turn, cannot be hypothesized effectively without comprehensive knowledge of the species involved: their life histories, ecology, and systematic positions -most particularly, their hour-by-hour, day-by-day, season-by-season ac- tivities. . In light of these considerations, I believe that the biggest problems and the most important contributions in the study of arthropod acoustics lie in analyzing it directly as a communicative phenomenon on a much more extensive scale than has been the rule, and in developing the available in­ formation in such a way as to make it more useful in a comparative sense, particularly with regard to the broader fields of animal communication and animal behavior in general. The present review has been written with this theme in mind; its organization has been influenced by a few recent papers dealing with the general aspects of animal communication (79, 115-117, 167).

SOME GENERAL CONSIDERATIONS

Communication can be defined as the transfer of information from one organism to another, detectable to an outsider only through the appearance of an observable response in the receiving individual. In its more complex forms it may become reciprocal in nature, and it may involve anticipation, delayed response, and other special complexities, depending upon the kind of system and the animal involved. But the near-universality of phenomena of this nature among animals, the continuity from simple expressions of communication to complex ones, and the certainty that all complex systems have evolved from simple ones, militate against restricting the idea of com­ munication, as many authors have done, to its more complex expressions and thereby to certain systems occurring only in humans or the higher verte­ brates. by Brown University on 06/06/12. For personal use only. Information can be transferred between organisms by means of chemicals (olfaction, taste), light waves (vision), sound waves (hearing), substrate vibrations, direct contact, or even by temperature and (at least theoretically)

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org humidity changes. Callahan (33-35) even speculates that moths communi­ cate by "high-frequency microwave electromagnetic radiation." Communication can be either intraspecific or interspecific [sometimes the latter has been termed "extraspecific"-Leston (98)J, though it is more apt to be complex and multifaceted in intraspecific contexts, for the obvious reason that members of the same species are more likely to possess a variety of mutually significant communicative contexts. For example, with a few exceptions (such as alarm calls in some birds and mammals), only conspecific individuals interact in interchangeable roles. As Wilson & Bossert (167) propose and exemplify for chemical signals, response to a communicative signal may be immediate and direct (releaser 498 ALEXANDER

effect) or delayed and indirect, through some kind of physiological adjust­ ment (primer effect). Most communicative responses studied so far are of a releaser nature, and except for mammals primer effects in acoustical systems have been demonstrated only in birds. Included in this category are such phenomena as the delayed effects of exposure to adult songs during critical periods in the lives of some birds (118, 147); production, by one member of a pair, of phrases previously uttered only by the other member, following removal of the latter (148); and changes in the nesting and molting cycle of budgerigars resulting from the addition or deletion of budgerigar sounds from the environment (52). With regard to nonacoustical kinds of communication, primer effects (changes in morphology, physiology, and behavior associated with "phase" differences) have been demonstrated for tactual, chemical, and visual sig­ nals in migratory locusts (47, 92, 93, 109), and tactual and visual signals in field crickets (69, 100). Examples given by Wilson & Bossert for chemical signals include the inhibiting of worker ovary development by queen sub­ stances in social insects such as ants (18), termites (110), honey bees (32), and the timing of female reproductive cycles by the odor of male urine in mice (121). The number and kind of communicative signals in the repertoire of an animal species depend upon the complexity of its life activities (the number of contexts in which signals can be used), the number and kind of communi­ cative systems it employs (each with its own peculiar limitations and poten­ tialities), and the number and kind of potentially confusing signals produced by other species within its habitat. Selective action on communicative sys­ tems ought to: (a) maximize the effective range and directionality of signals; (b) increase the number of useful contexts for any given kind of communica­ tive system; and (c) either minimize or maximize aspects of signal similarities within and between species repertoires, depending on the context (for ex­ amples, compare the functions of reproductive isolation and mimicry). These changes increase the amount of information transferred per unit time, per by Brown University on 06/06/12. For personal use only. situation, and per communicative system.

CLASSIFICATION OF COMMUNICATIVE FUNCTIONS

Various schemes of classification have been proposed for the purpose of Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org generalizing the contexts of animal communication. Dethier et al. (39), refer­ ring to the kind of action involved in the response and moving from the general to the specific, provided a logically exhaustive list of six possible functions of communicative signals: 1. locomotor stimulants, 2. locomotor depressants, 3. attractants, 4. repellents, 5. stimulants of specific acts, and 6. deterrents of specific acts. Wilson & Bossert (167) described six functional contexts for chemical-releasing stimuli which correspond to the above classi­

fication as follows: 1. trail marking (attractant), 2. sexual stimulation (stimu ­ lation of a specific act), 3. aggregation (attractant), 4. nonterritorial dis­ persal (locomotor stimulant), 5. territory and home range marking (repel- ACOUSTICAL BEHAVIOR 499

lent), and 6. alarm (stimulant of specific act, attractant, repellent, and lo­ comotor stimulant, under different conditions of intensity and other accom­ panying stimuli). Alexander (6), in classifying acoustical signals in crickets, referred first to the kinds of individuals between which the signals passed. To make such a classification reasonably complete, even for arthropod communication and including provision for signals passing both ways between different kinds of individuals, a rather large number of categories would be necessary: 1. male -female, 2. male--male, 3. parent-offspring, 4. juvenile--juvenile, 5. species-species, and (for social insects), 6. reproductive--sterile caste, 7. juvenile-sterile caste, 8. sterile caste-sterile caste. The list would have to be further complicated by, among other things, provision for distinctive signalling involving different kinds of sterile castes and different juvenile stages. For crickets, Alexander described only six acoustical signals, all in the first three categories : (a) calling (pair-forming) 1,2; (b) aggressive 1, 2; (c) courtship 1, 2?; (d) courtship interruption (pair-reforming?) 1, 2; (e) post­ copulatory (pair-maintaining) 1,2; (f) "recognition" 1?, 2?, 3? An unpub­ lished observation by Daniel Qtte (personal communication) on stridulation by a South African Brachytrupes species (Brachytrupinae) as it was being dug out and seized in the bottom of its burrow, indicates that a disturbance sound (g), presumably in category 5 above, should be added, giving the prob­ ability of seven functional kinds of signals in the collective acoustical reper­ toire of all crickets. Three factors complicate any attempt to generalize and classify commu­ nicative functions: 1. The functions of signals, measurable responses to them, and their structural nature may "blend" imperceptibly or vary independently between obvious functional foci. 2. Intensity, context, physiological condition of potential respondents, and, in some kinds of animals, individual recognition or prior experience, can h g by Brown University on 06/06/12. For personal use only. c an e effects of signals. 3. Any signal can have an effect on members of other species, either with­ out selective significance or in a way that will (at least initially) have a prin­ cipal selective significance only with regard to the responding species (for

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org example, predators may be attracted by the sexual signals of prey species). To illustrate some of these complications, there is evidence that under different circumstances the calling sound of male crickets can (a) attract predators (157); (b) attract females (3, 129, 154); (c) act as a locomotor de­ pressant (at high intensities) for females; (d) cause aggressive chirping and other aggressive actions; (e) stimulate calling by other males; (f) inhibit calling by other males; and (g) cause other males to move away (3, 4). Every one of Dethier's six signal functions is included in this list. In effect, it almost seems that one can devise an appropriate classification of communicative functions only when one is able to devise an appropriate classification of all functions in animal behavior. It was evidently for this 500 ALEXANDER

reason that Wilson & Bossert (167) found it necessary to restrict their discus­ sion of selective action on chemical communicative systems to "several spe­ cific cases within a narrowly definedfunction." On the other hand, studies of animal communication have, in many cases, led the way in the establishment of significant generalizations in behavioral work, and the obvious and strik­ ing parallels among signalling functions in insect communication indicate that an appropriate system of classification would offer more than mere nomenclatural convenience. Thus, it appears that all of the known and sus­ pected functions of arthropod acoustical signals can be arranged in nine categories, using nomenclature that is at least roughly comparable to that used by the investigators studying them in different kindsof arthropods: 1. Disturbance and alarm (predator-repelling and conspecific-alarming signals). 2. Calling (pair-forming and aggregating) signals. 3. Aggressive (rival-separating and dominance-establishing) signals. 4. Courtship (insemination-timing and insemination-facilitating) signals. S. Courtship interruption (pair-reforming?) signals. 6. Copulatory (insemination-facilitating and pair-maintaining) signals. 7. Post-copulatory or intercopulatory (pair-maintaining) signals. 8. Recognition (pair- and family-maintaining) signals (limited to sub­ social and social species). 9. Food and nest site directives (limited to social species). This classification is not comprehensive, even for arthropod communica­ tive systems. For example, a context not included in a clear fashion involves signals resulting in the transfer or exchange of food, chemicals, or other ma­ terials, most often in social species, and frequently referred to as "trophal­ laxis" (138, 165). Another example worthy of mention is the findingby Lloyd (107) that predaceous females in the firefly genus Photuris "attract and devour males of the genus Photinus by mimicking the Rash-responses of Photinus females." by Brown University on 06/06/12. For personal use only. GLOSSARY OF TERMS FOR DESCRIBING ARTHROPOD ACOUSTICAL SIGNALS

Two systems of nomenclature for arthropod acoustical signals have been

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org proposed (20, 36), but neither has been widely accepted or used; Broughton's terminology (20) was not even used by many of the other authors writing in the same book. There seem to be two reasons for the failure of these efforts. First, each has been unwieldy and rigid, and has attempted to assign one­ word labels to signals that are too complicated and unusual for any signifi­ cant information to be transferred without detailed description. Second, each has departed so violently from common everyday usage as to cause awkward, strained effortsby investigators attempting to use the terms, and to make the learning of an entire new vocabulary necessary for every reader of a paper on insect acoustical behavior. A useful glossary must be short, natural, and open to the addition of terms describing kinds ()f signals not yet encountered. It ACOUSTICAL BEHAVIOR 501

must also take into account all of the different reasons for naming signals or ways of naming them-the known or presumed function of the signals, the nature of the movements or the device involved in making the signal, the onomatopoetic effectof the sound produced, and the physical nature of the sound. Onomatopoetic terms ought to be used in ways that conform closely to their dictionary definitions. Physical descriptions ought to use terms in conformity with their usage by acousticians, with the exception that acousti­ cal signals of animals involve some combinations and kinds of units for which the acousticians have no adequate names, or for which the terms used by acousticians can be employed only through some slight stretching of their original meanings. Labels depending upon knowledge of function should be used when possible because of their high communicative value, but not before some reasonable basis for their introduction is established. Labels relating to movements of the sound-producing apparatus are least controversial, and can be applied with relatively little difficulty. The following Jist of terms, in the preparation of which I have been helped by Dr. Thomas J. Walker of the University of Florida and Dr. Thomas E. Moore of the University of Michigan, seems in large part to meet the above requirements:

Frequency: Cycles per second (not too different in meaning h'om the subjec­ tive word "pitch" when simple sounds within the sonic range are being considered). Any other repetitive units should be described in terms of rates (pulse rate, phrase rate, chirp rate, trill rate, wingstroke rate, tooth­ strike rate, etc.). The principal or dominant frequency is the physically most intense one (not necessarily the loudest to human ears); a pure fre­ quency (only theoretically possible) is a single one; the fundamental fre­ quency is usually the lowest one. (Multiples in terms of cycles per second are termed harmonics. Any additional frequencies higher or lower than the fundamental can be termed overtones or undertones, respectively; it is usu­ ally easier to avoid this term "fundamental" frequency than it is to be

by Brown University on 06/06/12. For personal use only. certain you're using it accurately. The main problem is that passing a sound through any kind of analyzing or recording device may introduce into it new harmonics or change the relative intensities of those originally present). Frequencies can be down-slurred or up-slurred (changed in a

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org gradual fashion), modulated (changed regularly) in either intensity or fre­ quency (the latter by regularly changing the frequency up and down), or pulsed (broken into separated units). If a frequency is above the (maximal) human hearing range (about 20,000 cycles per second), it is termed super­ sonic or ultrasonic; if it is below the (minimal) human range (about SO cycles per second), it is subsonic. Pulse (example: a very brief human whistle): a physically unitary or homo­ geneous sound-in the most restricted sense, a brief succession of sine waves (which, among insect sounds, is approached principally in cricket stridulations and wingbeat sounds). This term has been used by most bio­ acousticians in a slightly less restricted sense than the physical acousti- 502 ALEXANDER

cians had intended, more or less to include any sound that seems unitary by the methods being used to analyze it. In this broader usage, a pulse may be up-slurred or down-slurred, and it may contain more than one fre­ quency. I think this extension is reasonable and believe that it will increas­ ingly be accepted [but see Broughton (20) for a different opinion]. The words "chirp" and "syllable" have been substituted here by some authors, but I don't see how they help, except possibly in placating purists with regard to the word "pulse." They do not eliminate the problem of deciding, in various animal sounds produced in various fashions, just how much is to comprise the "chirp"; and in many cases they don't help in deciding how little is to be a "syllable." Much of the difficulty is owing to confusion of the different reasons or bases for naming sound units; phoneme and mor­ pheme, defined below, solve part of this problem. Wingstroke, tymbal pop, toothstrike, head-jerk, wing-snap, abdomen-waggle, leg-stroke, stridulation, crepitation, etc.): descriptive terms for the sound­ producing movements of insects with different kinds of acoustical devices. Such movements may be acoustically effective in two directions or in one direction only, and this should be specified when possible. In crickets and insects such as mosquitoes that make flight sounds with strongly dominant frequencies, a toothstrike and wingstroke, respectively, produce one cycle or wave. In some katydids, a toothstrike produces a pulse. Click, rasp, lisp, rattle, tick, beep; these and innumerable other onomatopoetic terms are used whenever they seem to assist in description. They cannot be defined rigidly and it is futile to try either to restrict greatly or to eliminate their use. Chirp (example: the caIl of a male house cricket): an onomatopoetic and subjective term tha.t is useful in describing any short, sharp sound, espe­ ciaIly a fairly high-pitched one (bass sounds are not usually caIled "chirps"). A chirp may be composed of one or several pulses. Some people would like to put a definite maximal length on the chirp, but it probably will have to remain a subjective term, with a meaning close to that given in by Brown University on 06/06/12. For personal use only. the dictionary. "Chirp" has a special usefulness in that it functions easily as both noun and verb, sometimes rendering a discussion much less cumbersome.

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org Phrase (examples: such insect sounds as might be paraphrased "zip-zip-zip" or "zzzzzzeee-zee-zee" or "rasp-raasp-raaaasp," etc.): any multiple-pulse sound that the term chirp does not seem to fit; most often used for groups of sounds that (a) are either low-pitched or nonuniform (the pulses within it are not alike), and (b) are noiselike (have a wide frequency spectrum rather than a noticeable dominant frequency or a tone) . A group of slowly delivered pulses is likely to be called a phrase, though it might also be termed a group of one-pulse chirps. Trill (example: a long blast on a police or referee's whistle of the sort that utilizes a vibrating ball): any succession of pulses, most often strongly dominated by a single or a few frequencies (having a definite tone if it is ACOUSTICAL BEHAVIOR 503 sonic), which lasts too long to be called a chirp and is too uniform and rapidly delivered to be called a phrase. Unless a trill extends indefinitely (which should be specified), length and uniformity of both trills and their intervals (as with chirp and phrase sequences) ought to be specified. A ringing telephone is a short trill, but on a party line there will be groupings of variable numbers of trills of the same or differentlengths. The pulses in a trill need not all be of the same frequency or length or delivered at the same rate. The label complex trill can be used, but, depending upon the kind and degree of complexity, each such sound will probably have to be described. Thus, it wouldn't be very communicative to refer to a whistled rendition of Yankee Doodle merely as a "complex trill." Broughton (20), using strict musical definitions, would like to restrict this term to sequences in which two differenttones are alternated and use "tremolo" for successions of like tones. While I cannot disagree with his definitions, this would practically eliminate the quite widely used and understood term "trill;" I doubt that this is possible, or important to try to do. Buzz (example: a telephone buzzer signal): sounds that are patterned like trills, but because they have more or less wide frequency spectra are much different in quality (lack tone), and don't bring to mind the word "trill" in the sense of cricket sounds, or whistles. Phone buzzer signals are usually short buzzes, or perhaps a broken buzz, while most electric alarm clocks produce continuous buzzes (or trills). Group: This simple term is so useful, particularly as a descriptive modifier, that it deserves special mention. All of the rhythm units described above are either grouped or ungrouped in different insect sounds. An ungrouped series or succession of pulses would be a succession of chirps, phrases, or short trills. A group of three pulses may be called a chirp or a phrase, de­ pending upon the speed of delivery and uniformity of length of intervals and pulses; a group of SO pulses would be a short trill. There are secondary and tertiary grouping of all of the above rhythm units in the most complex

by Brown University on 06/06/12. For personal use only. insect sounds. Sentence: Broughton (20) suggests the use of this word, more or less in the dictionary sense of "a complete musical expression" to refer to the long, sometimes complicated units of sound made by several kinds of insects, for

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org example, Amblycorypha uhleri StiLl (3). I have not previously used the term, but if its meaning becomes widely understood it may be a good addi­ tion to the bioacoustical vocabulary. Phoneme (from linguistics): Structural units in communicative sounds which are too small to have meaning (transmit information; cause responses) by themselves (analogous to letters in a written language and individual sounds in a spoken language). Morpheme (from linguistics): The smallest structural units which have mean­ ing (analogous to words in written and spoken language). Phoneme and morpheme are terms used by the linguists specifically for human language. Hockett (79) would prefer that the more general terms, "ceneme" and 504 ALEXANDER

"plereme," be used for "nonlinguistic" signals, by which designation he would include nonvocal signals of all sorts, such as arthropod acoustical signals and all tactual, chemical, and visual signals. It seems to me that the break might better be made between acoustical and nonacoustical kinds of signals.

Any sound too complex to be described by one or more of the above terms might as well be described in detail. Examples are sounds involving gradual or sequential chan�:es in rates of delivery of rhythm units, or different kinds of groupings following one another in some regular succession. The usefulness of any kind of generalized terminology diminishes as the involved patterns increase in complexity and individuality. A point that perhaps should be made here concerns the tendency of some investigators to designate as "complex," sounds that are essentially without rhythm or tone and within which, therefore, the information-bearing compo­ nents are difficult to identify. As mere physical entities, such sounds may indeed be "complex" (compared to, say, a three-pulse house cricket chirp), but as acoustical signals, they are much more likely to be merely rudimentary and simple.

DEMONSTRATIONS OF COMMUNICATIVE FUNCTIONS

GENERAL Stridulatory organs and other devices known to produce sound or sus­ pected of producing it have been described in thousands of arthropods, in­ cluding practically all of the insect orders (7, 8, 43, 55, 95). Likewise, vibration-sensitive devices believed to be capable of responding to substrate­ or contact-transmitted vibrations are almost universal among insects (38, 55, 139). Recent experiments suggest that if sounds are produced at unnatur­ ally high intensities, almost any insect can be made to respond-at least in a "phonokinetic" or nonoriented, spasmodic fashion (22, 23); by this, the

by Brown University on 06/06/12. For personal use only. necessity of giving some indication of intensity in all experimental studies is underscored. Clear demonstrations of response to air-transmitted sounds resembling some known stimulus in the arthropod's environment have so far been re­

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org stricted to a few orders of insects: Orthoptera (26-31, 66-68, 122, 128-130, 154), Homoptera (9, 144, 145), Lepidoptera (7, 132-135), Coleoptera (114), and Diptera (89, 136, 168). Demonstrations of response to air-transmitted sounds produced by conspecificindividuals are still restricted to Ensifera and Caelifera (Orthoptera), Auchenorrhyncha (Homoptera), and Culicidae (above references). Specialized responses to substrate-transmitted sounds (or vibrations) produced by conspecific individuals have been demonstrated in bees (105, 106, 161, 162), termites (80), and crabs (137). In this and following accounts, investigations may be known to readers which have been omitted, yet seem to illustrate phenomena being discussed. I have excluded numerous publications often included in similar discussions ACOUSTICAL BEHAVIOR 505

because I have restricted examples to what seem to me to be actual demon­ strations of function. Doubtful papers excluded fall mostly into three cate­ gories: (a) anecdotal descriptions of behavior without specification of ade­ quate controls or sufficientrepetitions of improbable sequences to lend credi­ bility; (b) experiments in which sound intensities were not indicated, so that phonokinetic effects, for example, could be involved; or (c) experiments in which substrate transmission could not be ruled out and is not unlikely on the basis of the animal involved and the experimental set-up described. It is most difficult to survey the literature so exhaustively that flatly exclusive state­ ments can be made, and some errors of omission may occur. I feel, however, that the effects of a few such errors are outweighed by the value of the kind of straightforward generalizations that inclusion of doubtful results often precludes.

INTERSPECIFIC INTERACTIONS Responses to substrate-transmitted vibrations have been extensively analyzed in spiders (101, 152) in connection with methods of detection of prey struggling in the web, and (less extensively), in ant lions in connection with detection of prey struggling on the sloping walls of the larval burrows (127). Responses to air-transmitted sounds produced by other species of animals in a natural situation have been demonstrated only in certain Lepi­ doptera, in connection with the strong likelihood that flying moths avoid predatory bats by responding to their echo-location signals (132-135, 149). In spite of considerable speculation, summarized and discussed by Walker (157), there is only one demonstration of a vertebrate predator locating arthropod prey by its noise. Walker observed two domestic cats apparently locating crickets and katydids by their sounds and demonstrated that one of the cats was attracted to the electronically reproduced sound of a katydid from 30 feet away. One claim has been made for acoustical mimicry in an arthropod (97). The authors believe that the disturbance stridulations of burying beetles by Brown University on 06/06/12. For personal use only. (Silphidae: Necrophorus spp.) have been selected toward resemblance to the buzzing of disturbed bumble bees, and that the leg-waving behavior and froth-covered appearance of a disturbed, stridulating beetle lying on its back

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org furthers the resemblance. The report is detailed and the suggestion not unreasonable, but in the absence of experimental tests with animals that might have been responsible for such selection, no conclusions can be reached. Many of the described facets of resemblance, including the general nature of the sounds of bumble bee and beetle compared, are by no means restricted to these two kinds of arthropods. The report by Broughton (21) of song "learning" in Tettigoniidae, based on two chirps supposedly produced by an individual of Platycleis sabulosa and resembling a sound he otherwise had heard only from P. ajfirmis, can be mentioned here, since it, too, is the only such claim to be made for an arthro­ pod in recent years. The only parallel seems to be the reports by several 506 ALEXANDER

investigators of inducing changes in the lengths of chirps made by males of the true katydid, Pterophylla camellifolia, by playing long chirps to them (3, 123, 140). In these cases, however, the same change occurs in natural situations and seems to be related physiologically to simple inhibitory and stimulative effects between neighboring katydids, and functionally to ag­ gressive signalling: and whatever effects accrue from long-continued alterna­ tion (see PHONORESPONSES AND AGGREGATION below).

DISTURBANCE AND ALARM SIGNALS Sounds made by arthropods held in the hand, or disturbed in various manners such as by pinching, probing, or restraining, are known in almost every order of insects (3, 7, 8, 55, 76). This kind of response exists in one or more species in every major arthropod group suspected or known to have specialized sound production. In no case, however, has a function been dem­ onstrated for the air-transmitted portions of stridulations or other noises made during disturbance, except, of course, that humans can hear such noises and often react to them. The sudden squawk of a seized cicada or katydid might cause one to drop it or allow it to escape; Leston & Pringle (99) state that "The sudden loud outbursts of a large reduviid when picked up by a trained observer often causes him to drop it .. .. " Except for the unproved possibility that similar reactions have been given by vertebrate predators in the past, however, such human responses do not afford much insight into the evolutionary processes leading to elaboration of disturbance sounds. I have witnessed the seizing of cicadas, both in mid-air and in trees, by several dif­ ferent species of birds, but I have not yet seen a cicada escape following its squawk when so seized. Cicada squawks may cause other cicadas to fly (3), but there is no clear evidence of this. Howse (80) has reported the only detailed experimental investigations of the probable causes and effectsof an arthropod disturbance or alarm sound in the termite, Zootel'mopsis angusticollis (Hagen). He found that the tapping

by Brown University on 06/06/12. For personal use only. noise reported from termite colonies is caused by soldiers striking their heads against both the roof and the floor of tunnels and by workers striking their heads against the roof, producing sounds with a frequency (in termite­ infested wood) of around 1000 cycles per second in bursts of two to eight

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org pulses delivered at rates equivalent to 24 per second at 20 to 210 C. These sounds are elicited by some kinds of stimuli that elicit so-called disturbance sounds in other arthropods-substrate vibration, sudden exposure to bright light, and puffs of air. Howse was able to obtain responses only by transmit­ ting the sound through the substrate, and his findings indicate that termites change their responses to chemical, tactual, and gravitational stimuli when presented with substrate vibrations, that they often respond to a vibration by making one themselves, that they produce vibrations upon encountering other termites, and that they receive the vibrations through the tibial sub­ genual organs which are tuned somewhat to the frequency and pulse rate in their particular disturbance response. ACOUSTICAL BEHAVIOR 507

Howse's papers offeran example of how to approach the problem of com­ municative function and selective significance of so-called disturbance "sounds" in arthropods. Interest in this subject is obviously great. More papers are published on stridulatory structures and sounds in arthropods with this general kind of behavior than on any other aspect of arthropod acoustical behavior, and more arthropods fall into this category of having only a disturbance sound of unknown function than into all other categories of acoustical behavior combined. Two general suggestions seem pertinent for investigators involved with these problems: (a) view the stimuli as possibly being elaborate tactual or vibratory communicative signals rather than as strictly rudimentary acoustical signals, and proceed as if the air-transmitted portions of the signals (the parts we hear) might be incidental; (b) expect the principal functions to be intraspecific and learn enough about the biology of the species involved to know what kinds of interactions, either at close range or during actual bodily contact, might be mediated by tactual or vibratory stimuli. Discovery of specific signals in courtship situations in various Cole­ optera (11, 114, 151) and Hemiptera [see review by Leston & Pringle, (49)J previously known to produce noises only when disturbed, emphasizes the likelihood that several intraspecific functions exist. However, it should be emphasized that the study of some of these groups has yet to pass beyond the anecdotal stage in which our knowledge of orthopteran and homopteran acoustical behavior had largely remained until a short time ago.

PAIR FORMATION AND REPRODUCTIVE ISOLATION

The usual events of sexual behavior, in order, are pair formation, court­ ship, copulation (or better, insemination), and sometimes pair-maintenance and further inseminations; in some species, pairs are formed chiefly or only within previously formed aggregations of sexually responsive individuals.

Aside from the influenceof predators, selective action on these various events may be viewed as solely a matter of maximizing efficiency of the sequence within by Brown University on 06/06/12. For personal use only. species-that is, decreasing the percentage of unmated individuals and the percentage of prematurely aborted, sexually significant encounters (the amount of wasted time and energy). But, for any species, the particular nature of individual units in the sequence may be explainable only in the

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org context of reproductive isolation, in other words, only in relation to the na­ ture of the same units in the behavior of other species living in the same area and sufficiently alike to be potentially confusing to the animals themselves. If two similar species live together long enough, it seems probable that events occurring early in the sexual sequence will eventually become sufficiently differentthat they will operate as the functional reproductive isolating mech­ anisms regardless of the nature of the original difference that made inter­

breeding or interaction between the species deleterious (5, 40, 46). Thus, differences in the manner of pair formation would prevent deleterious inter­ action between similar species more effectively (that is, involve less wastage of time and energy), than, say, courtship differences; courtship differences in 508 ALEXANDER

tUrn would be more efficient than mechanical barriers to copulation. As a result, selection ought to continue to promote divergence in pair-forming signals (or aggregating signals) even following the appearance of differences in the nature of other events occurring later in the sexual sequence; in con­ trast, diverging selection on later events would cease when early events be­ came completely effective. This is why calling or pair-forming signals of any sort, in any kind of animal, are more than just another taxonomic character (5) ; they alone (as a definable group of characteristics) can be expected to distinguish all the species in any well-established situation. Such character­ istics include not only aggregating or pair-forming chemical, visual, and acoustical signals, but the separation of adults of different species during breeding time by differences in daily or seasonal cycles, or by habitat differ­ ences. These are features of arthropod biology that cannot be ignored in any effort to distinguish the species in any group. In some animal groups, such as many birds, humans use the same things the animals evidently do to distin­ guish the species (plumage, song, eye and bill color) j in most arthropods this is not true, and I must confess to a large amount of skepticism whenever any insect group is treated as if the species had been defined when pair-forming mechanisms have not yet been studied. Part of the lesson deriving from this theme involves the value of the "local fauna" beginning in the taxonomy of any group. Perhaps the closest parallels to acoustical signalling in this regard, and excellent recent examples, are the studies of Barber (15) and Lloyd (108) on fireflies.

CALLING SIGNALS

Function has been demonstrated more frequently for pair-forming or calling signals than for any other kind of insect acoustical signal. Most often, pair formation is accomplished by the simple attraction of the sexually re­ sponsive female to the signalling male. Such responses have been demon­ strated in Gryllidae (3, 129, 154), Tettigoniidae (26-28, 42), and Cicadidae ,

by Brown University on 06/06/12. For personal use only. (9), and are likely in crabs of the genus Uca (137). In some insects males are attracted to acoustical females j such a response has been demonstrated in Culicidae (136, 168) and Ceratopogonidae (41), and is possible in beetles (Trogidae) (11) . In still other cases, then! is movement by both males and

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org females as a result of hearing the other's sound, and a series of phono­ responses as well. Such interactions have been demonstrated in Acridinae (29-3 1, 75, 85) and Tettigoniidae (12, 67, 143). Recently, Mampe & Neunzig (114) reported that males and females of the plum curculio, Conotrachelus nenuphar, are attracted to cages of stridulating individuals of the opposite sex, but not to cages containing silent individuals with their elytra removed or glued down. Most of the evidence by which we can decipher how selective action has operated upon insect acoustical systems is still of an indirect nature. Not all such evidence, however, is completely unreliable or lamentably tenuous, as can be illustrated with the role of pair-forming acoustical signals in the effi- ACOUSTICAL BEHAVIOR 509 ciency of reproductive isolation among sympatric, synchronic species. If a particular signal is chiefly responsible for pair formation in any group of species, then differences between signals of species living together would prevent wasted time and energy in deleterious interspecificint eractions. This says nothing about why the interspecificinte ractions are deleterious-a ques­ tion worth more attention than it has received in the light of our increasing awareness of the prevalence of the potential of closely related animal species both vertebrate and invertebrate, to produce viable hybrids on a wide scale (5, 19, 71, 72, 81)-and it says little about the manner in which such inter­ spccific signal differences might arise. But it does give us a basis for further investigation. Thus, if insect acoustical signals are important in reproductive isolation, then we should expect firstthat species reproductively active in the same places at the same times would not have identical acoustical behavior. This expectation has proved justifiable. In spite of the fact that more than half of the 1000 or so species of Orthoptera and Homoptera in North America and Europe have been studied to some extent, no case of identical or confusingly similar acoustical behavior has been discovered between sympa­ tric, synchronic species (3, 6, 24, 25, 49, 50). Second, we should expect that some recently diverged species that are still isolated either temporally or geographically would have identical or very similar sounds. Several such cases have been reported for insects (5) ; evidently, none has been reported for vertebrates. Gryllus veletis (Alexander and Bigelow) and Gryllus pennsylvani­ cus Burmeister, seasonally isolated sympatric field cricket species in North America, each have a wingstroke rate of 25 to 27 per second at 75° F, a mode number of four pulses in the calling chirp, variable, similar chirp rates, and the same frequencies (cycles per second) in their calling songs. Gryllus camp­ estris Linnaeus in Europe, with a wingstroke rate of 27 to 28 per second, has an identical (or extremely similar) calling song in all other respects, even to the variable chirp rate (about 100 to 300 per min), the mode pulse number in the chirp (four), the range of from three to six pulses per chirp, and the fre­

by Brown University on 06/06/12. For personal use only. quency of the sound (about 4.5 kc per sec) . These species have perhaps been isolated since the Oligocene period, G. campestris living almost alone in Europe, with no congeneric sympatric species except for an apparent slight overlap with G. bimaculatus De Geer near the Mediterranean (a detailed

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org description of the geographic, seasonal, and ecological overlap between these two widely studied species has, to my knowledge, never been published). G. bimaculatus has a song that seems to be identical to that of G. campestris except for a pulse rate of 25 to 26 at 75° F. This difference is probably too slight to be effectively significant to the crickets, especially since the figures given here are based on recordings of only a few individuals. For instance, Walker (154) found that the pulse rate differences between the trills of Oecanthus quadripunctatus and o. argentinus-36.5 and 44.25 per second, respectively, at 74° F-could be eliminated by less than a 10° F difference in temperature. Such a shift would cause the song to attract females of the wrong species. The closest relative of G. pennsylvanicus and G. veletis in North 510 ALEXAN DER

America is C. firmus Scudder, an Atlantic and Gulf Coast cricket, with a pulse rate of 17 to 18 per second at 75" F-almost surely a significantdiff er­ ence. C. bermudiensis Caudell, found only on Bermuda, is undoubtedly de­ rived from G. firmus, perhaps during the Pleistocene, and is allopatric with G. firmus. One individual recorded had a pulse rate of 14.0 per second at 75° F, probably not communicatively different (to the crickets) from the song of G. firmus. Finally, we should expect that species which overlap would differ more in regard to acoustical behavior where they overlap than where they do not. Only two possible cases have been reported. Alexander (2) suggested that Gryllus fultoni (Alexander) may have developed a faster, more regular chirp in the northern part of its range. In that region it overlaps ecologically with two chirping species absent in the southern part of its range--Gryllus veletis (Alexander and Bigelow) and C. vernalis Blatchley. Character displacement, it must be emphasized, is still a highly speculative possibility in this case. The change involved does respresent a divergence from the song characteristics of these two species, and only a single trilling species overlaps ecologically and temporally with G..fultoni in the south where its chirp is less regular and more slowly delivered. Walker (155) suggests a similar and probably more positive case in North American tree crickets. Oecanthus fultoni Walker shows geographic variation in chirp rate, western individuals that overlap with the similar and more slowly chirping species, O. rileyi, having a faster chirp rate. On the other hand, Thomas & Alexander (146) failed to locate evidence of character dis­ placement in song among three meadow grasshoppers with distributions that provide an almost optimal model for this phenomenon-linear distributions with geographic and ecological overlap only at the two extreme ends of the distribution of each of three species. Why are there so few cases of song identity among allopatric and allo­ chronic species and so few cases of local divergence in regions of overlap

by Brown University on 06/06/12. For personal use only. between similar species? Thomas & Alexander suggest that the three meadow grasshoppers they studied may have diverged in this regard before acquiring their present extensive ranges; that is while living together in a restricted southern location near their present southern overlap. Pulse rates in the Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org songs are almost as different as is possible--nearly multiples of one another. Another possibility is that song change, while seeming necessarily to be a relatively conservative evolutionary feature because of the communicative function (which requires that response capability change each time signal structure changes), nevertheless may occur between two species even while they are still allopatric or allochronic because of some confusing similarity of the song structure to the songs of other related or unrelated species in the same habitats. In a region such as North America, where 40 or 50 insect species may be stridulating simultaneously, it seems likely that any large adjustment of the complement of a species' acoustical neighbors would surely result in an adjustment of one sort or another in that species' calling sound. ACOUSTICAL BEHAVIOR 511

Several experiments have been done on iriterspecific song discrimination. Walker (154) showed that females of the two tree crickets cited above, Oecanthus quadripunctatus and o. argentinus, were able to discriminate their own species' song, and by juggling pulse rates and temperatures until the females responded to the wrong species' song, he further showed that the discrimination was based solely on rate of delivery of pulses in these simple trills. Perdeck (122) demonstrated that two grasshopper species (Acridinae) are able to discriminate one another's songs, and that this is a most impor­ tant factor in preventing hybridization where the species overlap. Alexander & Moore (9) showed that two species of synipatric, synchronic cicadas are unable to respond to each other's songs because of their wide differences in both frequency and rate of delivery of temporal units. Roth (136) and Kahn & Offenhauser (89) demonstrated species differences in mosquito responses. An important study bearing on this question is the demonstration by Wever & Vernon (164) that an American Gryllus species (probably pennsylvanicus) has an abruptly lowered auditory threshold at just the frequency (pitch) of its song (ca. 4.5 kps.) This cannot be an accident, and one immediately specu­ lates that other crickets must have their auditory organs similarly "tuned" to their frequencies. This means that the frequencies of rhythmically similar songs in different genera of crickets could be so different as to render the two kinds of songs almost inaudible between species belonging to the two differ­ ent genera. In other words, although not selected in the context of reproduc­ tive isolation, frequency differences could be the effective distinction be­ tween songs; in such cases the rhythm patterns could evolve without refer­ ence to one another. For example : songs of Nemobiinae (ground crickets) , which often live with field crickets, are usually pitched between 8 and 10 kilo­ cycles per second. I believe that all demonstrations of identity in acoustical behavior among allochronic and allopatric species of ar thropods, and all demonstrations of interspecific acoustical incompatibility involving closely similar species, are cited above. by Brown University on 06/06/12. For personal use only.

PHONORESPONSES AND AGGREGATION

Perhaps the most widely observed and easily demonstrated acoustical response in all arthropods is that which Busnel and his co-workers (31, 45) Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org refer to as the "phonoresponse"-the production of sound upon hearing a sound. This behavior takes several forms, varying from a simple "reply" to the sound of a conspecific individual, or repeat of it (usually involving male calling sounds or aggressive sound only) to a consistent, rhythmic alterna­ tion or synchronization of calling phrases between males for indefinitely long periods of time. Specialized alternation and synchronization of calling phrases by Orthoptera and Cicadidae can be observed easily in many species in almost any part of the world, and in some cases have been analyzed in some detail (3, 9, 29, 31, 66, 68, 87, 88, 123, 130, 140, 159). Curiously, no function has yet been demonstrated for phonoresponses 512 ALEXANDER

when they involve, as they do in most cases, two individuals of the same sex. Four possibilities can be suggested (3) : (a) elaboration of the role of auditory feedback in rhythmical, long-continued calling of individual males may have incidentally rendered them "captive" phonoresponders to close neighbors in many species; (b) two or more males singing in alternation or synchrony may produce sound more regularly for longer periods of time (make up a more stable sound-producing unit) than lone-singing males because of stimulative and inhibitory effects upon one another [Barlow (16) has commented on a similar possibility for synchronous firefly flashing]; (c) phonoresponses may assist in the formation and maintenance of aggregations of males in situations in which individual males increase their chances of securing mates by joining such groups; and (d) rhythmic interaction (chorusing) by numerous males within a restricted area may prevent obscurement of the species-specific and female-attracting portions of the song or even enhance their distinctiveness. I t can be seen that these four possibilities represent possible stages in the evolution of complex phonoresponses, and that the last three involve pair formation by way of specialized aggregations of calling males. To demonstrate that any of the above functions has been elaborated as a result of selective action would be difficult. But the circumstantial evidence is often impressive, as can be illustrated with the 17 -year and 13-year cicadas. Alexander & Moore (9, 10) demonstrated that individual males are stimu­ lated into song by hearing tape recordings of calling males (and evidently would be similarly stimulated by hearing neighbors) , and that in a synchro­ nizing species with a song consisting of two parts alternated with one an­ other, males hearing only part one of the song will respond by producing part

two, and vice versa. They also found that most mating takes place within groups of chorusing males, and that males are attracted to the calls of other males. To the human ear, the rhythm of individual song phrases is more discernible when chorusing synchrony is achieved in those species showing it. The fact that one calling male stimulates another to call indicates that two

by Brown University on 06/06/12. For personal use only. males caIling together make up a more stable sound-producing unit than one alone. In other words, every one of the above four functions is strongly sug­ gested by these data on periodical cicadas, though none can be proved to have developed as a result of direct selective action.

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org Recently, Wynne-Edwards (169) has advanced another "explanation" for elaborated phonoresponses, namely that "mass-stridulation" as illus­ trated by choruses of crickets, cicadas, and katydids (as well as mass perfor­ mances by male fireflies and males of many other species) ought to be viewed as "epidiectic" behavior, which he defines as concerned chiefly with dispers­ ing the males and "regulating" the population density (or size, for he uses the terms more or less interchangeably), by which he evidently means specifically keeping it from going above a certain point. Wynne-Edwards uses as a prin­ cipal argument the fact that other explanations have not been available for these phenomena, which is a doubtful justification even if it were not true

that he cites only papers thirty or more years old on this subject. It is sur- ACOUSTICAL BEHAVIOR 513

prising that the fallacies in his schemes of selection to acount for this and other phenomena have not been more widely recognized [but see (166)]. In this case it will suffice to point out that the chorusing of periodical cicadas, which he specifically cites as a principal example: (a) renders the populations more dense, not less (for the effect is aggregation, not dispersal); and (b) presumably is chiefly responsible for increasing the size of the population, not decreasing or otherwise "regulating" it (since mating success is largely re­ stricted to choruses in those species with the more elaborate chorusing be­ havior) . Both of these facts are the reverse of what would be necessary to support Wynne-Edwards' hypotheses. It is perhaps appropriate to note here that he has made similar errors in dealing with the behavior of other insects. Thus, territorial and aggressive behavior in crickets is most pronounced during times of low population density rather than high (4) ; likewise, the apparent functions are increases in the reproductive potential of their posses­ sors, not decreases. Among other things, Wynne-Edwards has erroneously lumped the territoriality of crickets, which seems to be functional solely in obtaining a mate, with that of birds and other parental animals which must obtain not only a mate but sufficient territory to provide for food and the other necessities involved in rearing offspring. When cricket populations are dense, aggressive behavior disappears, and is even replaced by a clustering­ together (4) ; no evidence yet exists to support the idea that adult behavior has been selected in connection with the dispersion of subsequent genera­ tions.

AGGRESSION

Elaborate fighting behavior associated with special acoustical signals is known among arthropods only in crickets. Sounds evidently causing separa­ tion of individuals have been described in Crustacea (78, 126) Tettigoniidae (140, 143), Acrididae (51, 74, 85), and Passalidae (Coleoptera) (11). In Acrid­ idae, such sounds have been termed the "rivals' duet" when a male intrudes

by Brown University on 06/06/12. For personal use only. during courtship of a female by another male, and "copulation song" when the intrusion occurs during copulation. The only detailed examination of the effect of aggressive acoustical signals in arthropods is that of Alexander (4), who summarized his findings as follows:

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org The aggressive stridulation of the males of GrylJinae is distinct from the sounds made in other situations. Stridulation by one male during combat usually causes the other male to stridulate, and in most species, both males stridulate during intense

aggression . Dominant males stridulate during aggression more frequently than subordinate males, and the dominant male in an intensively aggressive encounter nearly always stridulates after antennal contact has been lost through the retreat of the subordinate. The subordinate male rarely chirps after an encounter, and if he does, it signals an impending change in his status. A relatively specific set of artificial stimuli, such as simultaneous playback of aggressive sounds and simulated antennal lashing, is required to elicit the full dis­ play of aggressive behavior in a male unless he has just stopped behaving aggres­ sively after winning a fight, is behaving territorially, or has just copulated. In sllch .5 14 ALEXANDER

cases, a male can be stimulated into aggressive activity with either tactile or audi­ tory stimuli alone, indicating a temporary "conditioning" or "priming" effect.... Recent losses decrease a male's inclination to fight, and the dominance status of two males can be reversed over and over again by "defeating" the dominant repeat­ edly between encounters by means of artificial stimuli. Fighting or retreat is induced more quickly when aggressive sounds are played as the male is lashed with bristles simulating cricket antennae, and conditioning is stronger.

COURTSHIP

Courtship signals can be defined as those occurring after pair formation and culminating in copulation or insemination when the courted individual is sexually responsive. This definition means that in some species courtship signals must be absent, and this is a reasonable prediction, based on the supposition that some courtship functions can be accomplished during pair formation arid others may be absent in certain species. The independence of pair formation and courtship in some cases in which courtship is in evidence, has been noted by Haskell (75) as being demonstrated in Acridinae by the fact that if a pair is formed by chance meeting, calling or pair-forming signals are omitted, the sexual sequence beginning instead with the courtship signals. This seems to be true in all of the groups discussed below in which acoustical courtship signals are known. According to the above definition, no acoustical courtship signals are known for any female arthropod. Acoustical courtship signals by males are known in Acridinae, Oedipodinae (Orthoptera: Acrididae) , Gryllidae (Orth­ optera), and Cicadidae (Homoptera) , and are presumed on good evidence in crabs (137), and certain bugs (84, 99), and on rather scanty evidence in numerous other insects, including Drosophila (153). Responses to courtship signals are difficultto demonstrate, partly because they seem often to be no more than "allowing" the male to copulate (for example, in both cicadas and grasshoppers) . The presence or absence of such readiness to copulate, as a specific reaction to courtship sounds, must be

by Brown University on 06/06/12. For personal use only. tested, using normal and silenced males ; such tests have not been performed. But Haskell (76) tested the responses of deafened and nondeafened grass­ hopper females (Acrididae) to male calling stridulations and attempts at copulation. Deafened females did not allow copulation, while nonoperated Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org females did; there were no sham-operated controls. The only other demonstration of response to courtship sounds is that of Alexander (3, 4) for neld crickets (Gryllus), which indicated that females are caused to walk forward without directional orientation unless tactual stimuli are present. Ordinarily, this would cause the female to touch the rear end of the courting male and walk up on his back into the copulatory position. Artificial playbacks to a group of sexually responsive females caused them to locomote more or less without direction and to antennate one another when they came into contact, so that pairs of females often walked in circles around one another ; presumably, if either of two such females stopped walking, as a male in that situation would, a copulatory position would be assumed be- ACOUSTICAL BEHAVIOR SlS

tween them. Coinciding with this evidence is my (unpublished) observation that when a male field cricket is placed with several females and begins to court, one 'can identify the sexually responsive females with a high degree of confidence as those which begin immediately to locomote. Generally speaking, courtship signals have three possible contexts of significance: (a) they may be selected as reproductive isolating mechanisms in cases in which the chances of accidental pair formation are high ; (b) they may be responsible for timing inseminations or insemination bouts by in­ forming the individuals in a pair when both are sexually responsive; (c) they may facilitate insemination directly by moving the pair into the copulatory position. All other possible effects of courtship signals, as defined above, such as "bringing the female into a sexually responsive state," or "causing the female to recognize males of her own species," can be subsumed under these three headings. The presence or absence of specific courtship signals in the sexual se­ quence of a species may be related to the above three effects. Thus, if several congeneric species live together so that the chances of interspecific pair for­ mation are relatively high, we should expect to find courtship signals in at least all but one (probably all) of the involved species. Further, courtship signals selected in this context ought to be about as species-specific as the pair-forming signals. Species-specific courtship signals, however, do not necessarily denote a reproductive isolating function: the species-specificity may merely be a result of the derivation of the courtship signals from calling signals that are species-specific as a result of direct selective action (5). For example, if the pulse rate is about the same in all of a cricket's signals and its calling song is caused to change under selective pressure associated with reproductive isolation, then the courtship song (as well as all the other signals in this case) will have to make the same change. It is also possible that a signal can be species-specific as a result of selective action that is no longer operating, for example, if a courtship signal once was the principal species­ by Brown University on 06/06/12. For personal use only. isolator, but the calling signals subsequently became species-specific and prevented all interspecific pair formations, or if a species no longer lives with another species which was potentially confusing to it and from which its courtship signals had diverged on this account. The significance of species­ Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org specificity must always be evaluated in terms of the particular species group

involved. The same questions, incidentally , must be asked about all charac­ teristics functioning late in the mating sequence and showing some species­ specificity-for example, genitalic differences among species. Courtship signals, then, may be expected to be vestigial, rudimentary, or absent when few congeneric or confusingly similar species live together, and when, in addition, accidental pair formation is minimal and pairs are formed only briefly in association with one or a few copulations. In the latter case, the pair-forming signal itself would accomplish the courtship function of timing inseminations. If pairs are maintained through successive insemina­ tions or successive bouts of insemination, then courtship signals ought to be 516 ALEXANDER

expected as timing devices. If pair formation normally occurs through unori­ ented locomotion or without specific signals (in other words, accidentally), then courtship signals should be expected in the timing function. vV e can test the predictive value of these generalizations by applying them to specific groups of arthropods in which courtship signals are known. Thus, among arthropods with acoustical signals in their sexual behavior, an extreme of long-term pair formation involves a social beetle in the family Passalidae, Popitius disjunetus (Illiger) , in which the pair isolates itself and rears its offspring, with the adults living two or more years. Juveniles possess stridulatory organs of independent origin from those of the adults, but prob­ ably their sounds are perceived by the adults' auditory organs, and vice versa (11, 70). Unpublished observations on courtship behavior (Laura Berkeley, personal communication) indicate that a special courtship signal does occur, even though this species has lived for some time in North America without relatives, even in the same family. The pair-forming mechanisms are still unknown. Various crickets maintain pairs through several copulations (4, 5). West & Alexander (163) thought that in the subsocial species, A nurogryllus mutieus (De Geer), females copulate but once and then ensconce themselves in a burrow from which they exclude all other crickets and lay their eggs and bring in food which their newly hatched offspring consume. Subsequent unpublished observations on this and a South African species indicate, in­ stead, that a female will copulate several times in one session, at intervals of fifteen minutes or so, but will not copulate following some unknown period after one or more copulations; in other words, after she has ensconced herself in the brood chamber. A. mutieus possesses a distinctive courtship signal (163), even though no species in the same genus or otherwise potentially confusing to it, occurs with it in North America, and evidently not in Central or South America either. Most of the crickets that are known to copulate several times in succes­ by Brown University on 06/06/12. For personal use only. sion possess acoustical courtship signals. Alexander (5) lists eleven of fifteen studied genera in this category ; among the four remaining, courtship is not clearly known in one case, and metanotal glands producing chemicals during courtship occur in two cases, replacing acoustical signals (in one of these, Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org Hapithus, the female also eats the male's wings during copulation. Alexander erred in omitting reference to metanotal glands possessed by this species) . In one genus, Cyrtoxipha, lacking both glands and a courtship song, the single observed copulation took place extremely rapidly, without evidence of any specific signals by the male. Among Cicadidae, courtship signals have been sparsely known. One would predict that Tibicen species in eastern North America, on the basis of relatively low population densities and few species living together, should provide a contrast with the Magieicada species which live together in great abundance in groups of three species over most of their range. Present evi­ dence suggests that this is true. Alexander and Moore (unpublished data) ACOUSTICAL BEHAVIOR 517

have discovered that all Magicicada species have two courtship signals which are always or nearly always produced in succession prior to copulation ; no courtship song is yet known for any Tibicen species, although it must be admitted that the members of this genus have not been studied thoroughly, and Alexander & Moore (9, 10) did not discover the true nature of the acous­ tical courtship signals in Magicicada until the sixth year they studied periodi­ cal cicadas in the field.

POST-COPULATORY BEHAVIOR

Three kinds of signals have been described which should be considered in this category. Among crickets and grasshoppers, sounds that closely resemble aggressive stridulations are produced whenever courtship is interrupted. No function has been actually demonstrated for these signals, but it is probable that they call back departing females if the interruption was accidental or have the usual aggressive effects upon other males if the interruption was caused by intrusion. In many crickets, specific stridulations occur following each copulation, or perhaps more properly between copulations in a "bout" of copulations (3-5). Two functions are evident. First, females involved in the behavioral interaction including this kind of signal, are kept with the male until he has produced another spermatophore. Alexander (6) notes that the female among some crickets is ready to copulate again before the male. This function is very much like the timing function of courtship signals described above, but the two classes of signals are not necessarily alike: courtship and post-copulatory signals are similar in Oecanthinae; aggressive and post-copulatory signals in most Gryliinae ; and calling and post-copulatory signals in Miogryllus (Gryl­ linae) and Anurogryllus (Brachytrupinae) (6). The second function of post-copulatory signals in crickets is evidently preventing the female from removing the spermatophore before insemination is complete. Huber (82) found that females of Gryllus campestris did not re­ by Brown University on 06/06/12. For personal use only. move the spermatophore until about 15 minutes had passed even when isolated from males, and that this was sufficient time for emptying of the spermato­ phore. However, there is no way to determine the delaying effect of the dis­ turbance created by the separation, and it is significant that many orthop­ Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org terans, in which the spermatophore ampulla remains outside the female, have a mucous mass or cap on the spermatophore. In the subfamily Gryl­ linae, this cap appears only in Gryltodes sigillatus Walker among crickets so far studied, and there are two noteworthy specializations associated with it: (a) the post-copulatory behavior of the male is weak, contact being lost between a pair in laboratory cages more frequently than in other Gryllinae; and (b) the female turns immediately following copulation and without interference from the male bites the cap offthe spermatophore and chews it slowly and for several minutes. In other Gryllinae any movement by the female of the sort involving spermatophore removal causes a quick forward lurching and anten­ nation by the male, this stopping further action by the female. 518 ALEXANDER

In certain Acrididae (51, 76), the male often stridulates during copula­ tion, apparently when the female's movements or intrusion by another indi­ vidual threaten disruption of copulation. This signal seems to be analogous to the post-copulatory signals of crickets, since its function is apparently main­ tenance of the pair until insemination is completed. The essential differenceis that the genitalia are engaged while this is going on in Acrididae; in effect, the male holds the ampulla or bulb of the spermatophore while the female is being inseminated, while in most (but not all) crickets, the male inserts the spermatophore tube and immediately disconnects from the female's genitalia and the spermatophore. In most crickets with post-copulatory signals, in­ semination occurs after the genitalia have been disconnected, though in tree crickets the female remains on the male's back. The analogy between grass­ hoppers and crickets is furthered by the fact that in some grasshoppers the male rides on the back of the female without the genitalia engaged either before or between copulations.

FOOD AND NEST SITE DIRECTIVES As mentioned earlier in this review, one of the most prominent and stimu­ lating series of investigations on animal behavior in this century has been that begun by von Frisch on the communication of honey bees more than forty years ago (60) , and best known now from his 1950 and 1957 books (61, 62) and the subsequent book by Lindauer (102). Numerous papers have been published on this subject since von Frisch's books [for example, von Frisch & Lindauer (64) ; Lindauer (104)]; but only a few are pertinent here. The investigations of von Frisch, Lindauer, and others have shown that honey bee workers returning from distant sources of food vibrate their abdo­ mens during the straight run portion of a "dance" during which a figureeight is roughly traced out by the bee. Direction of the food source (or potential hive site in swarminl� bees) is roughly indicated by the angle of the straight run relative to the perpendicular, which averages about the same as the angle by Brown University on 06/06/12. For personal use only. of the food source relative to the direction of the sun from the hive. This relationship between angle with regard to a light source on a horizontal sur­ face and angle with regard to the perpendicular on· a vertical surface is a familiar component of the light-compass reaction known to exist in many Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org arthropods (53). The additional speciality of the bee's dance is that the dis­ tance of the food source was found by von Frisch to be roughly proportional to the time taken by the bee to complete its figure-eight run. Subsequently, von Frisch & Jander (63) and Wenner (160) discovered that the length of the straight run itself is a more accurate reflection of distance. The angle of the dance remains accurate by virtue of continual shifting during the day as the sun moves, a shifting which continues even in bees that are not being exposed to the sun at short intervals. Bees in north temperate climates (with a southern sun) shift their dance angles counterclockwise and bees in south temperate climates shift their dance angles clockwise. Some intriguing results have been obtained by investigators interested in the problems of the ACOUSTICAL BEHAVIOR 519 sun passing through the zenith in a few days' time, and in what happens to northern bees transported to southern climates and vice versa (90, 119, 120), but, unfortunately, the results do not all agree (91, 103, 104). Some of these studies are peripheral to the subject of this review, but I present them because of their relationship to the following curious fact. Al­ though several investigators have indicated that the particular bees receiv­ ing the message about food source or potential hive sites can be recognized because they run alongside or behind the dancer with their antennae either being struck by the vibrating abdomen or touching the thorax of the dancer (several commercially available movies can be used to illustrate this behav­ ior) , no investigator has yet discovered what classes of stimuli are actually received by these presumed "responder" bees and how each is used. Even more curious is the fact that no one has presented data based on marked bees proving that particular "responder" bees have indeed received specific infor­ mation as to distance and direction of food sources. Wenner (160) analyzed statistically the best data presented on this topic (63), and concluded that because bees visiting wrong locations were not destroyed, a clumping of visits at the right post based on multiple scent post visitations was not precluded. Furthermore, the training of bees to feeding sites involves two odors, one provided by the experimenter and one added by the bees (Starzeldujt) (104) ; precisely how these variables enhance the infor­ mation received during dances, and therefore the extent to which there is correspondence between what humans have been deriving from bees' dances and what another bee can derive, seems to have been measured less accu­ rately than is generally supposed. Dancing bees make a noise when they waggle the abdomen, which Esch (48) and Wenner (160) found to be pitched at 200 to 250 cycles per second and made up of pulses of sound delivered at 35 to 40 per second. Wenner found this rate to be from 2 to 6 times the rate at which the abdomen struck a tiny cellophane flap glued to the microphone and held to one side of the by Brown University on 06/06/12. For personal use only. bee's abdomen during waggling, and could not account for this rate. The number of sound pulses per burst, however, correlated as closely with dis­ tance as any other feature of the dance. Lindauer (104) refers to sound as a characteristic of more "vivid" dances, resulting from food sources of a high Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org quality, and he refers to the acoustical part of the waggle dance as "addi­ tional (secondary) vibrations of the abdomen." He does not cite Wenner's (160) paper. Heran (170) found that honey bee antennae are most sensitive to vibra­ tions at the frequencies of sounds produced during the dance (162) . Lindauer & Kerr (105, 106) believed that tibial receptors (perhaps the subgenual organs) are receptors for such vibrations in stingless bees. Otherwise, the mechanics of any possible sound reception as well as that of sound produc­ tion are still completely unknown. It may be significantthat other work with the effects of acoustical stimuli on honey bees has indicated that substrate transmission is almost mandatory. Wenner (161) caused a virgin queen bee 520 ALEXANDER

to "pipe" in response to an artificially produced imitation through the sub­ strate but was unable to secure a reaction to more intense air-transmitted vibrations. Lindauer & Kerr (94, 105, 106) found that workers of the stingless bees in the genus Melipona can alert members of the hive and cause them to locate food sources in greater numbers as a result of a buzzing noise (varying be­ tween 326 and 588 cycles per second among several species) made in the hive, which must be transmitted through the substrate. Bees in one compartment of a hive were alerted by buzzing workers .i n another compartment, and bees on soft substrates could not alert other bees. The only other work on the question of the effects of acoustical stimuli on Apidae has been that of Hansson (73), Jarvis (86), and Frings & Little (59), who were able to stop the activity of honey bees by subjecting them to ex­ tremely intense sounds between 300 and 1000 cycles per second.

CONCLUDING REMARKS This review has been highly selective, as was hinted in the introductory remarks. I have concentrated strictly on communicative functions of acous­ tical signals. Recent studies on hereditary aspects, developmental influences, effectsof environmental variables such as temperature, and sensory, muscle, and neurophysiology have been almost entirely ignored. For information on these subjects prior to 1961, the reader is referred to Busnel (24, 25), Frings & Frings (54), and Haskell (76), and the reviews by Alexander (7, 8) covering the years 1961 and 1962. Haskell (77), Dethier (38), Roeder (134), and Huber (83) furnish recent reviews on related topics.

LITERATURE CITED 1. Alexander, R. D. Sound production 7. Alexander, R. D. Invertebrate bio­ and associated behavior in insects. acoustics: 1961. Bio-A coustics Bull., Ohio J. Sci., 57, 101-13 (1957) Z, 7-10 (1962) 2. Alexander, R. D. The taxonomy of the 8. Alexander, R. D. Invertebrate Bio­ field crickets of the eastern United 1962. Bio-A caustics by Brown University on 06/06/12. For personal use only. Acoustics: States. Ann. Enlomo!. Soc. Am., 50, Bull., 3, 13-18 (1963) 584-602 (1957) 9. Alexander, R. D., and Moore, T. E. 3. Alexander, R. D. Sound communica­ Studies on the acoustical behavior tion in Orthoptcra and Cicadidae. of seventeen-year cicadas. Ohio J. In Animal Sounds and Communica­ Sci., 58, 107-27 (1958) Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org tion, Chap. 3, 38--92 (Lanyon, 10. Alexander, R. D., and Moore, T. E. W. E., and Tavolga, W. N., Eds., The evolutionary relationships of Am. Inst. Bio!. Sci. Pub!. No. 7. 17-year and 13-year cicadas and 1960) Washington, D. C., 443 pp., three new species. Univ. Mich. 4. Alexander, R. D. Aggressiveness, terri­ Museum Zool. Misc. Publ., 121, toriality, and behavior in sexual 1-59 (1962) field crickets. BehaViour, 17, 130-223 11. Alexander, Moore, E., and (1961) R. D., T. Woodruff, R. E. The evolutionary 5. Alexander, R. D. The role of behav­ differentiation of st ridulatory sig­ ioral study in cricket classification. System. Zool., 11, 53-72 (1962) nals in beetles. A nimal Behaviour, 6. Alexander, R. D. Evolutionarychange 11, 111-15 (1963) in cricket acoustical communica­ 12. Allard, H. A. Remarkable musical tion. Evolution, 16, 443-67 (1962) technique of the larger angular- ACOUSTICAL BEHAVIOR 521

winged katydid. Science, 67, 613-14 Ie comportement acoustico-sexuel (1928) de la femelle d' Ephippiger bitter­ 13. Arrow, G. J. The origin of stridulation ensis. Campt. Rend., 242, 174-77 in beetles. Proc. Roy. Entomo!. Soc. (1956) London (A), 1'7, 83-86 (1942) 28. Busnel, R. G., DuMortier, B., and 14. Autrum, H. Schallempfang bei Tier Busnel, M. C. Recherches sur Ie und Mensch. Naturwissenschaften, comportement acoustique des 30, 69-85 (1942) ephippigeres. Bull. Bioi. France 15. Barber, H. S. North American fireflies Belg., 90, 219-86 (1956) of the genus Photuris. Smithsonian 29. Busnel, R. G., and Loher, W. Sur Inst. Misc. Collections, 117, 58 pp. l'etude du temps de la response au (1951) stimulus acoustique artificiel chez 16. Barlow, J. S. Discussion. In Biological lea CharthiPpus, et la rapidite de Clocks. Cold Spring Harbor Symp. ! 'integration du stimulus. Compt. Quant. Bioi., 25, 54-55 (1960) Rend. Soc. Bioi., 148, 862-65 (1954) 17. Belton, P. Responses to sound in 30. Busnel, R. G., and Loher, W. Memoire pyralid moths. Nature, 196, 1188- acoustique directionnelle du male 89 (1962) de Chorthippus biguttulus L. CampI. 1 8. Bier, K. Die Regulation der Sexualitat Rend. Soc. Bioi., 148, 993-95 (1954) in den Insektenstaaten. Ergeb. 31. Busnel, R. G., and Loher, W. De­ Bio)., 20, 97-126 (1958) c1enchment de phonoresponses chez 19. Blair, W. F. Genetic incompatibility Char/hippus brunneus (Thunb.). and species groups in U. S. toads A custica, 1 1, 65-70 (1961) (Bufo) . Te:x:as J. Sci., 11, 427-53 32. Butler, C. G. The scent of queen (1959) honey-bees (A. mellifera) that 20. Broughton, W. B. M ethod in bio­ causes partial inhibition of queen acoustic terminology. In Acoustic rearing. J. Insect Physiol., '7, 258- Beha7liour of A nimals, Chap. 1, 3-24 64 (1961) (Busnel, R. G., Ed., Elsevier 33. Callahan, P. S. A photoelectric-photo­ Pub!. Co., Amsterdam-London­ graphic analysis of flight behavior New York, 933 pp., 1963) in the corn earworm, Heliothis zea, 21. Broughton, W. B. Song learning in and other moths. Ann. Entomol. grasshoppers? New Scientist, 27, Soc. Am., 58, 159-69 (1965) 338-41 (1965) 34. Callahan, P. S. Intermediate and far 22. Busnel, M. C., and Burkhardt, D. An infrared sensing of nocturnal in­ electrophysiological study of the sects. Part 1. Evidences for a far phonokinetic reaction in Locusta infrared (FIR) electromagnetic the­ migratoria migratorioides (L.). ory of communication and sensing Symp. Zool. Soc. London, 7, 13-44 in moths and its relationship to the (1962) limiting biosphere of the corn ear­ 23. Busnel, M. C., DuMortier, B., and worm. A1In. Entomol. Soc. Am., 58,

by Brown University on 06/06/12. For personal use only. Busnel, R. G. Recherches sur la 727-45 (1965) phonocinese de certains insectes. 35. Callahan, P. S. Intermediate and far Bull. Soc. Zool. France, 84, 351 infrared sensing of nocturnal in­ (1959) sects. Part II. The compound eye of 24. Busnel, R. G., Ed. Colloque sur the corn earworm, H eliolhis zea, and I'acoustique des orthopteres. Inst. other moths as a mosaic optic­ Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org Nat. Rech. Agron., Paris, 448 pp. electromagnetic thermal radiom­ (1954) eter. Ann. Enlomol. Soc. Am., 58, 25. Eusuel, R. G., Ed. Acoustic Behaviour 746-56 (1965) of Animals. (Elsevier Pub!. Co., 36. Chavasse, P., Busnel, R. G., Pasqui­ Amsterdam-London-New York, 933 nelly, F., and Broughton, W. B. pp., 1963) Proposition de definitions concer­ 26. Busnel, R. G., and DuMortier, B. nant l'acoustique appliquee aux Phonotaxie de 9 d'Ephippigcr a des insectes. In L'A coustique des Or­ signaux acoustiques synthetiques. thopteres, Chap. 1, 21-25. (Busnel, CampI. Rend. Soc. Bioi. , 149, 11-13 R. G., Ed., lnst. Nat. Rech. Agron. (1955) Paris, 448 pp., 1954) 27. Busnei, R. G., and DuMortier, B. 37. Chen, S. H. Sound production in in­ Rapport entre la vitesse de deplace­ sects; its origin and specialization. ment et l'intensite du stimulus dans Sinensia. 14, 37-39 (1943) 522 ALEXANDER

38. Dethier, V. G. Th., Physiology of Insect terenstridulation Methodik der Senses. (Methuen & Co., Ltd., Bearbeitung und Auswertung von London, 266 pp., 1963) Stridulationsbeobachtungen. Ein­ 39. Dethier, V. G., Browne, L. B., and zeldarstellungen). Z. MorPhol. Oe­ Smith, C. N. The designation of kol. Tiere, 26, 1-93 (1932) chemicals in terms of the responses 51. Faber, A. Laut- und Gebardensprache they elicit from insects. J. Econ. bei Insekten. Orthoptera (Gerad­ En/omol., 53, 134-36 (1960) flUgler) . Mitt. Staatl. Museum 40. Dobzhansky, T. Ge-n etics alld the Origin Naturh., Stuttgart, 198 pp. (1953) of SPecies. (Columbia Univ. Press, 52. Ficken, R., van Tienhoven, A., Ficken, New York, 364 pp., 1951) M., and Sibley, F. Effects of visual 41. Downes, J. A. Observations on the and vocal stimuli on breeding in the swarming flight and mating of budgerigar (Melositacus tmdulatus). Culicoides. Trans. Roy. Entomol. Soc. Animal Behaviour, 8, 104-6 (1960) London, 106, 213-36 (1955) 53. Fraenkel, G. S. and Gunn, D. L. The 42. Duijm, M. and van Oyen, T. Het Orientation of Animals. Kineses, sjirpen van de Zadelsprinkhaan. Tines, and Compass Reactions. LefJende Natuur, 51, 81-87 (1948) (Dover Pub!., New York, 376 pp., 43. DuMortier, B. Morphology of sound 1961) emission apparatus in Arthropoda. 54. Frings, H., and Frings, M. Uses of In Acoustic Behaviour 0/ Animals, sounds by insects. Ann. Rev. EntD­ Chap. 11, 277-345. (Busnel, R. G., mol., 8, 87-106 (1958) Ed., Elsevier Pub!. Co., Amster­ 55. Frings, H., and Frings, M. Sound dam-London-New York, 933 pp., Production and Sound Reception by 1963) Insects: A Bibliography. (The Penn­ 44. DuMortier, B. The physical character­ sylvania State Univ. Press, Uni­ istics of sound emissions in Arthro­ versity Park, 108 pp., 1960) poda. In Acoustic Behaviour of 56. Frings, H., and Frings. M. Bio-acous­ Animals, Chap. 12, 346--73. (Bus­ tics and pest control. BiD-Acoustics nel, R. G., Ed., Elsevier Pub!. Co., Bull., 2, 21-24 (1962) Amsterdam-London-New York, 933 57. Friugs, H .• and Frings, M. Pest con­ pp., 1963) trol with sound. Part 1. Possibilities 45. DuMortier, B. Ethological and physi­ with invertebrates. Sound,. 1, 13-20 ological study of sound emissions in (1962) Arthropoda. In Amustic Behaviour 58. Frings, H., and Frings, M. Sound of Animals, Chap. 21 , 583-654. against insects. NtID Scientist. 3, (Busnel, R. G., Ed., Elsevier Pub!. 634-37 (1965) Co., Amsterdam-London-New York, 59. Frings, H., and Little, F. Reactions of 933 pp., 1963) honeybees in the hive to simple 46. Ehrman, L. Courtship and mating sounds. Science 125, 122 (1957) behavior as a reproductive isolating 60. Frisch, K. von. Uber die "Sprache" by Brown University on 06/06/12. For personal use only. mechanism in Drosophila. Am. der Bienen. Eine tierpsychologische Zool., 4, 147-53 (19M) Untersuchung. Zool. Jahrb. Abe. 47. Ellis. P. E. Learning and social aggre­ Allgem. Zool. Physiol. Tiere, 40, gation in locust hoppers. Animal 1-186 (1923) Behaviour, 7, 91-106 (1959) 61. Frisch, K. von. Bees : Theil' Vision,

Annu. Rev. Entomol. 1967.12:495-526. Downloaded from www.annualreviews.org 48. Esch, H. Uber die Schallerzeugung Chemical Senses, and Language. beim Werbetanz der Honigbiene. (Great Seal Books, Cornell Univ. Z. Vergleich. Physiol., 45, 1-11 Press, Ithaca, N. Y., 118 pp., 1950) (1961) 62. Frisch, K. von. The Dancing Bees. 49. Faber, A. Die Lautliusserungen der (Harcourt, Brace, and World, New Orthopteren. (Lauterzeugung, Lau­ York, 182 pp., 1953) tabwandlung und deren biologische 63. Frisch, K. von, and Jander, R. Ueber Bedeutung sowie Tonapparat der den Schwanzeltanz der Bienen. Z. Geradfiiigler) . Vergleichende Un­ Vergleich. Physicl., 40, 239-63 tersuchungen. I. Z. Morphol. Oekol. (1959) Tiere, 13, 754-803 (1929) 64. Frisch . K. von, and Lindauer, M. The 50. Faber, A. Die Lautausserungen der "language" and orientation of the Orthopteren. II. (Untersuchungen honeybee. Ann. Rev. Entomol., 1, iiber die biozonotischen, tierpsycho­ 45-58 (1956) \ogischen und vergleichendphysio­ 65. Frost, S. W. Sonification. General logischen Probleme der Orthol?- Entomology. Chap. 10, 198-211. ACOUSTICAL BEHAVIOR 523

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