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Acoustic Anti-Predator Strategies in Insects

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Acoustic Anti-Predator Strategies in Insects Chapter 5 Adaptive Sounds and Silences: Acoustic Anti-Predator Strategies in Insects William E. Conner Abstract There has been a recent resurgence of interest in the evolution of adap- tive coloration and a new appreciation of the mechanisms, functions, and evolution of crypsis, aposematic coloration, and mimicry. I here apply these principles to the acoustic modality using insect examples and discuss adaptive silence, acoustic crypsis, stealth, acoustic aposematism, acoustic mimicry, and sonar jamming. My goal is to inspire students of bioacoustics to explore the full richness of the acous- tic interactions between predator and prey in behavioral, physiological, and evolu- tionary contexts similar to those used by visual ecologists. 5.1 Introduction Adaptive coloration encompasses a variety of concepts, including the beautiful and intricate exemplars of crypsis, warning coloration, and mimicry plus many other lesser-studied visual phenomena such as masquerade, countershading, and disruptive coloration. Early naturalists and insect lovers played a critical role in defining the behavioral significance of the color patterns of animals. Among them were Erasmus Darwin (1794), the father of Charles Darwin, who commented on the utility of concealing coloration for animals; Edward B. Poulton (1890), who coined the term “aposematism” for warning coloration; and Henry W. Bates and Fritz Müller, who defined Batesian mimicry (1862) and Müllerian mimicry (1878), respectively. Yet adaptive coloration is but a reflection of selective pres- sures imposed by predators that hunt visually as appreciated by a primarily visual audience—man. Predators that rely on sound rather than vision have selected for an entirely different suite of characteristics, and it is those adaptive sounds and W. E. Conner (*) Department of Biology, Wake Forest University, Winston-Salem, NC 27106, USA e-mail: [email protected] B. Hedwig (ed.), Insect Hearing and Acoustic Communication, 65 Animal Signals and Communication 1, DOI: 10.1007/978-3-642-40462-7_5, © Springer-Verlag Berlin Heidelberg 2014 66 W. E. Conner silences that I examine here. I admit to being inspired by a book titled Avoiding Attack: the Evolutionary Ecology of Crypsis, Warning Signals and Mimicry by Ruxton, Sherratt, and Speed (2004), and I happily recommend it to those looking for an insightful and a detailed treatment of adaptive coloration. The authors by their own admission, however, focus exclusively on the visual modality and rarely mention sound (but see Ruxton 2011). Given the number of predators that hunt orienting by sound that omission should be corrected. I hope to do that here. Many predators use a combination of sensory modalities to hunt insects: vision, hearing, and olfaction are the major ones, with a bias toward vision in diurnal ani- mals and toward hearing and olfaction in those that hunt at night. Acoustic spe- cialists include nocturnal hunters such as owls, rodents, felids, canids which are all passive listeners, and bats which are both passive listeners and active echolo- cators. Insect counteradaptations often affect both types. The key predators are vertebrates which allow us to appreciate, at least in a rudimentary way, the prob- lems associated with finding prey and interpreting acoustic prey signals. I will focus on the antipredator adaptations of terrestrial insects vis-à-vis these predators. I would be remiss not to include parasites as well. Whenever an insect uses the acoustic modality to communicate, it becomes vulnerable to parasites that eaves- drop on their sound signals (Zuk and Kolluru 1998; see Chap. 4 by Hedwig and Robert). Parasitism may prove equally important in shaping the acoustic commu- nication systems of insects. Defenses can be divided into two categories: primary and secondary (Edmunds 1974). Primary defenses are those that prevent detection by the predator. Secondary defenses promote survival after detection. The primary defenses discussed below are adaptive silence, stealth as in the modern military sense of the word, and acoustic crypsis. Secondary defenses will include preven- tion of localization, acoustic aposematism, mimicry, and sonar jamming. 5.2 Avoiding Detection: Primary Defenses Before proceeding, it would be wise to define a concept that is too frequently used without a precise definition: crypsis. To put it simply, crypsis is avoiding detection while remaining in plain sight. It includes a range of color and pattern strategies that prevent detection (Stevens and Merilaita 2009), including background match- ing, a general matching of the color, intensity, and pattern of the background; self-shadow concealment, the use of pattern to cancel telltale shadows that betray position; obliterative shading, similar shading that cancels other three-dimensional cues to recognition; disruptive coloration, markings that disrupt outlines and other recognition patterns; flicker-fusion camouflage, the blurring of fast-moving stripes to match general background color; distractive markings that draw attention away from recognition cues; transparency, allowing the background to show through decreasing visibility; and silvering, a high degree of reflectivity that prevents sil- houettes in nondirectional light (for details see Stevens and Merilaita 2011). All of these examples describe visual phenomena. I would like to extend the definitions 5 Adaptive Sounds and Silences: Acoustic Anti-Predator Strategies in Insects 67 of Stevens and Merilaita (2009) to include all traits—visual, chemical, tactile, electric, and, here, acoustic cues—that minimize the probability of being detected when potentially detectable to an observer. 5.2.1 Adaptive Silence In his massive tome on Adaptive Coloration in Animals H. B. Cott (1940) states that “cryptic silence is to the ear what cryptic appearance is to the eye.” His exam- ples refer to the stealth with which predators approach prey, but the concept can equally be applied to prey characteristics. Technically this is more akin to hiding in the visual modality, and some have referred to it as acoustic avoidance (Curio 1976). Certain moths, for instance, interrupt their sexual displays in the pres- ence of acoustic predators (see Chap. 6 by Greenfield). Males of lesser waxmoth, Achroia grisella, advertise their presence to potential mates by producing ultra- sonic 100 μs pulses at a rate of 100/s. Females are attracted by and walk toward those acoustic displays. In the presence of sounds mimicking, the search calls of gleaning bats with long pulse lengths >1 ms and lower pulse rates <30/s, the male moths shut down their acoustic advertisement calls (Spangler 1984; Greenfield and Baker 2003) to avoid predator detection. Similar adaptive silences have been reported in katydids and crickets (Spangler 1984; Belwood and Morris 1987; Faure and Hoy 2000; Bailey and Haythornthwaite 1998; ter Hofstede et al. 2010). The advantages and costs of such a strategy are straightforward; silence not only prevents detection by predators that hunt by listening, but also it prevents commu- nication with conspecifics. Tradeoffs in such cases are inevitable. “Whispering” moths illustrate another antidetection strategy (Nakano 2008). Male Asian corn borer moths, Ostrinia furnicalis, use specialized sex-specific scales on the forewings and mesothorax to produce very low intensity courtship songs with frequencies between 40 and 80 kHz. The male produces the sounds in the immediate vicinity of the female’s ear. The implication is that the song pro- vides a private communication channel between the male singer and the female listener, protecting the pair from conspecific competitors and predators. A variety of moths produce similar hushed songs, presenting new technical challenges to researchers studying moth courtship (Nakano 2009). One of the most interesting examples of adaptive silence can be found in the cricket Teleogryllus oceanicus (Zuk et al. 2006, see Chap. 4 by Hedwig and Robert). In field crickets, the male stridulates by scissoring the wings and slid- ing a scraper on one wing across a file on the other. Females are attracted to the males’ songs. T. oceanicus, an Australian and Pacific Island species, has been forced to alter that strategy. The species was introduced to the Hawaiian Islands in the late 1990s. On the islands of Oahu, Hawaii, and Kauai, it overlaps in distribu- tion with the acoustically orienting parasitoid fly Ormia ochracea. Like the female cricket, the female fly is attracted to the male cricket’s calling song. After locat- ing the male cricket, the fly deposits her young on and in the vicinity of the male. 68 W. E. Conner The voracious larvae burrow into the male, killing him as they develop. Within a remarkably rapid timeframe of about 20 generations intense selection by the fly has resulted in a morphological change in the wings of the male crickets on Kauai (Zuk et al. 2011). So-called flatwing males have wings similar in appearance to those of females. They have lost their file and scraper and are thereby silenced. These males produce no calling song and do not attract the parasitoid. It is not clear how the silent flatwing males now attract mates, although it has been sug- gested that they function as satellite males, waiting in the vicinity of calling males, and intercepting females as they move toward them (Cade 1980). 5.2.2 Stealth In addition to shutting down acoustic signals that could attract gleaning preda- tors, a prey insect may be able to dampen its echo signature to aerial hawking and gleaning bats
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