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Adaptive Sounds and Silences: Acoustic Anti-Predator Strategies in Insects
Abstract
There has been a recent resurgence of interest in the evolution of adaptive 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 acoustic interactions between predator and prey in behavioral, physiological, and evolutionary contexts similar to those used by visual ecologists.
... According to Conner (2014), all traits including visual, chemical tactile, electric, and acoustic cues, that minimize the probability of a prey being detected when potentially detectable to an observer, can be called Crypsis. For example, certain moths interrupt their sexual acoustic calls in the presence of acoustic predators, to avoid detection by the predator (Greenfield, 2014;Spangler, 1984). ...
... For example, certain moths interrupt their sexual acoustic calls in the presence of acoustic predators, to avoid detection by the predator (Greenfield, 2014;Spangler, 1984). Similar adaptive silence behaviors have been reported in crickets and katydids (Bailey and Haythornthwaite, 1998;Conner, 2014;Faure and Hoy, 2000;Spangler, 1984). ...
... Ostrinia furnicalis, male Asian corn borer moths, use specialized very low intensity courts cm) produced by sex-specific scales on the forewings and mesothorax. In order to protect the pair from nonspecific competitors and predators, this male moth produces the sounds in the immediate vicinity of the female's ear, which provide a private communication channel between the male singer and the female listener (Conner, 2014). ...
Studies into insect nervous systems have greatly advanced our knowledge of how the brain functions and how connections between its individual neurons evolve during development. It reveals the mechanics by which a brain combines a massive
amount of sensory information to produce proper movements and behavior. Various specialized cells that process information, drive impulses, support the functional integration of organs and systems, and produce specific behavior in response to the
environment are characteristics of a complex nervous system, such as those found in insects. It begins by outlining the fundamental composition of an insect’s brain. The cellular characteristics of the various neuronal types and how neuro-secretions affect them are then examined in relation to the integrative functions of these neurons during behavior. To highlight specific aspects of integrative processing, the
numerous movements that an insect makes are examined at the cellular level. The book emphasizes throughout how understanding these simpler neural systems helps us understand more complicated brains while also offering the functional synthesis that can be incorporated into the next molecular and computational studies.
... When visibility is low, such as at night, visual displays may be replaced with acoustic or olfactory signals (e.g. Pomini, Machado, Pinto-da-Rocha, Macías-Ord oñez, & Marsaioli, 2010; and see Conner, 2014;Masters, 1980;Ratcliffe & Nydam, 2008;Rowe & Halpin, 2013). ...
... An acoustic defensive mechanism common among arthropods is stridulation (Masters, 1980). This may startle the predator due to the sudden transition from silence to a burst of sound and/or if it is associated with other defences it may act as a warning signal (Alexander, 1967;Conner, 2014;Masters, 1980). Stridulation may occur before contact and thus may lead to the predator aborting its pursuit or, more often, the sound is emitted when the prey is restrained and may result in the predator dropping the prey allowing it to escape (Bura, Rohwer, Martin, & Yack, 2011;Dookie et al., 2017;Smith & Langley, 1978). ...
... As with vision-based aposematism, acoustic signals can have recognizable characteristics that provide the conditions for a predator to learn to associate the signal with a defensive mechanism (Hristov & Conner, 2005;Rowe & Halpin, 2013;Schmidt & Blum, 1977). In turn, and just like visual signals, the acoustic elements of a stridulation pattern, used by a well-defended animal, can be exploited by acoustic mimics (Conner, 2014). To date though, acoustic mimicry, in which a mimic imitates sounds produced by a defended model, has rarely been documented, with the only confirmed cases being found among moths. ...
The importance of vision-reliant defensive traits (e.g. warning colours) in mimicry studies is well established, but their effectiveness is limited by visibility. In low light conditions, for instance, acoustic or tactile channels may be more effective. The juvenile and adult stages of the nocturnal hunting Palpimanus spiders audibly stridulate when harassed. Given this we hypothesized that the sound produced by Palpimanus has a defensive role against interspecific predators. Palpimanus though are poorly defended especially against something as large as a gecko. Hence we hypothesized that the stridulation is effective because the spider mimics co-occurring mutillid wasps. We staged predator feeding experiments in which mutillid wasps, sham-operated Palpimanus, silenced Palpimanus and a nonstridulating spider were offered to Eusparassus spiders and geckoes. Stridulating spiders had significantly greater survival against both predators than the nonstridulating treatments and comparable survival to the mutillid wasps. This result represents the first confirmed case of a spider using stridulation against an interspecific predator. Stridulation deterred Eusparasus spiders, while in geckoes stridulation acted postcapture as they dropped the prey instead of attempting to swallow them. For mutillid wasps this dropping response was typically more rapid than with Palpimanus but attempts to swallow silenced individuals were more frequent than sham-operated individuals, which were more likely to be dropped before any attempt to swallow. Analyses of stridulation characteristics of Palpimanus showed they were similar to acoustic signals of four of the co-occurring mutillid wasps and far more so than distress signals of control insects. Our study overall supports the notion that Palpimanus spiders are Batesian mimics of sympatrically occurring mutillids through the use of an aposematic acoustic signal and not just an example of a startle response.
... They occur in species ranging in size from tiny beetles (Lewis and Cane, 1990) to giant wetas (Field, 1980) and are generated by a variety of mechanisms including stridulation, forced air, percussion and tymbalation (Ewing, 1989). Despite their prevalence and diversity, surprisingly little is known about the effects of these sounds on predators, and this subject has generated ongoing debate (Conner, 2014;Rowe and Halpin, 2013;Siddall and Marples, 2011). Proposed functions can be broadly categorized according to the target audience of the signals; those directed at conspecifics and some heterospecifics may function as alarm signals to warn of impending danger or to recruit help (Cocroft, 1999;Hager and Kirchner, 2013). ...
... Proposed functions can be broadly categorized according to the target audience of the signals; those directed at conspecifics and some heterospecifics may function as alarm signals to warn of impending danger or to recruit help (Cocroft, 1999;Hager and Kirchner, 2013). Alternatively, signals may be directed at predators, where proposed functions include but are not limited to, acoustic aposematism, startle, enhancement of visual signals, sonar jamming, and mimicry of something dangerous (Conner 2014;Masters, 1980;Rowe and Halpin, 2013). Our understanding of the protective value of defence sounds is limited because live insects may have multiple components to their displays, making it difficult to isolate the effects of the sounds alone (Rowe and Halpin, 2013;Siddall and Marples, 2011). ...
... Yet, there has been little rigorous experimental investigation of the functions of these signals on predators. Currently, studies are mostly restricted to the unique relationship between tiger moths and their echolocating bat predators (Corcoran et al., 2010;Conner and Corcoran, 2012;Conner, 2014). It has been recently argued that bio-acousticians fall behind visual ecologists in understanding the complexity between predator-prey interactions involving acoustic defence signals (Conner, 2014). ...
Many insects produce sounds when attacked by a predator, yet the functions of these signals are poorly understood. It is debated whether such sounds function as startle, warning or alarm signals, or merely serve to augment other defences. Direct evidence is limited owing to difficulties in disentangling the effects of sounds from other defences that often occur simultaneously in live insects. We conducted an experiment to test whether an insect sound can function as a deimatic (i.e. startle) display. Variations of a whistle of the walnut sphinx caterpillar (Amorpha juglandis) were presented to a predator, red-winged blackbirds (Agelaius phoeniceus), when birds activated a sensor while feeding on mealworms (Tenebrio molitor). Birds exposed to whistles played back at natural sound levels exhibited significantly higher startle scores (by flying away, flinching, and hopping) and took longer to return to the feeding dish than during control conditions where no sounds were played. Birds habituated to sounds during a one-hour session, but after two days the startling effects were restored. Our results provide empirical evidence that an insect sound alone can function as a deimatic display against an avian predator. We discuss how whistles might be particularly effective ‘acoustic eye spots’ on avian predators.
... In 1867, Charles Darwin wrote to fellow naturalist Alfred Wallace asking, "why are caterpillars so beautifully and artistically coloured?" to which Wallace replied explaining that the bright colours helped caterpillars to avoid bird predation by signaling their distastefulness (Darwin, 1887). Since then hundreds of studies have focused on these bright displays in insects, but comparatively little has been reported on the function of defences of the acoustic nature (Conner, 2014). ...
... Despite the large and diverse repertoire of defence sound types and mechanisms distributed across the class Insecta, there is a lack of understanding of how they function to protect prey against predators (Conner, 2014). These insufficiencies in the literature are partially because there has been a greater focus on visual defences, and also because there have been few studies that have tested the effects of defence sounds on live predators (Conner, 2014). ...
... Despite the large and diverse repertoire of defence sound types and mechanisms distributed across the class Insecta, there is a lack of understanding of how they function to protect prey against predators (Conner, 2014). These insufficiencies in the literature are partially because there has been a greater focus on visual defences, and also because there have been few studies that have tested the effects of defence sounds on live predators (Conner, 2014). Several hypotheses have been proposed which fall in two major categories based on whether they are directed at conspecifics, or predators (Table 1.1). ...
Defence sounds are widespread and diverse amongst insects. Despite their ubiquity and variability, hypotheses explaining their functions and evolutionary origins have been understudied. My thesis focused on these topics using silk and hawkmoth Bombycoidea caterpillars as a model system. In Chapter Two I investigated why defence sounds have evolved in some caterpillars but not others by testing the hypothesis that large body size is a factor in the evolution of defence sounds. To test this hypothesis, I followed the development of defence sounds in four Bombycoidea species from hatching to pupation. I predicted that early instars would not produce defence sounds, and that within sound producing instars defence sounds would be more likely to occur in larger caterpillars. Results showed that defence sounds were absent in the first and second instar, and that they developed in the third through to the fifth instar in all species. Moreover, the onset of sound production occurred when all species were the same relative size (~1.12 g, ~26.37 mm), despite the fact that the species differed in their final instar size. I concluded that early instar caterpillars do not make defence sounds, and that there is a critical size when defence sounds develop. I further tested the hypothesis that smaller caterpillars do not have enough energy to make defence sounds, by analyzing the relationship between size and several temporal characteristics of the sounds. I predicted that smaller caterpillars would signal less than larger caterpillars, and produce shorter signal units and trains, with lower duty cycles. Results partly supported the hypothesis, showing that in two species there was a positive relationship between size and the number of units produced within two seconds following an attack, the mean number of units per train, and the mean duration of the units in one species. I also tested the hypothesis that sounds of small caterpillars are not in the hearing range of predators. I predicted that there would be a relationship between caterpillar size, and the sound pressure levels and dominant frequencies of the sounds. Results showed no significant relationships with dominant frequencies or sound pressure levels and size. I concluded that the caterpillars made sounds that were within the hearing range of major predators from the onset of sound production. In Chapter Three I followed the other antipredator defences of the four species throughout development. I investigated whether the frequency of defences changed with instar. I found that the caterpillars employed up to seven different secondary defences throughout development. In one species the frequency of dropping and major
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thrashing increased in the late instars, and in a different species the frequency of regurgitation increased. I concluded that in some cases defence sound production accompanies other secondary defences that increase with the size of caterpillars during development. In Chapter Four I tested the hypothesis that the defensive whistle of the walnut sphinx caterpillar, Amorpha juglandis (Sphingidae: Sphinginae), functions to startle birds. I predicted that the birds would startle to the sounds, and habituate upon repeated exposure within a trial. Results showed that play-back recordings of the whistles elicited a startle response in captive red-winged blackbirds (Agelaius phoeniceus) and caused them to hesitate and/or flee from prey. I concluded that the whistles function as a startle display. Together, the experiments conducted within my thesis addressed important outstanding questions regarding the evolutionary origins of defence sounds in caterpillars, and their functions in predator-prey interactions.
... tymbals) 4,5,20 . Despite the diversity of defence sounds, their functions and the significance of their varied characteristics are poorly understood 6 . Sounds directed at predators are hypothesized to warn of a chemical or other defence (acoustic aposematism) 29,30 , advertize unprofitability, startle a predator (deimatic display) 29 , jam sonar signals 21,31,32 or mimic another dangerous species 22 . ...
... Signals directed at conspecifics or heterospecifics may function to warn kin, or recruit help. Disentangling these hypotheses has been the subject of considerable and ongoing debate 6 . The rich diversity of acoustic displays in Bombycoidea caterpillars reported here makes them excellent subjects to test hypotheses on the functions of acoustic defence signals, since the confounding variables associated with adult reproductive functions are out of the picture. ...
... We propose that in sonic caterpillars, some signals warn predators (acoustic aposematism), and others frighten them (startle displays). Acoustic aposematism typically occurs in species that use a chemical defence, and the sounds are predicted to precede or accompany chemical release to enhance the predator's association with the chemical 6,30,37 . Startle sounds on the other hand are predicted to be unexpected and intense, and not directly associated with a chemical defence 6 . ...
Caterpillars have long been used as models for studying animal defence. Their impressive armour, including flamboyant warning colours, poisonous spines, irritating sprays, and mimicry of plant parts, snakes and bird droppings, has been extensively documented. But research has mainly focused on visual and chemical displays. Here we show that some caterpillars also exhibit sonic displays. During simulated attacks, 45% of 38 genera and 33% of 61 species of silk and hawkmoth caterpillars (Bombycoidea) produced sounds. Sonic caterpillars are found in many distantly-related groups of Bombycoidea, and have evolved four distinct sound types- clicks, chirps, whistles and vocalizations. We propose that different sounds convey different messages, with some designed to warn of a chemical defence and others, to startle predators. This research underscores the importance of exploring acoustic communication in juvenile insects, and provides a model system to explore how different signals have evolved to frighten, warn or even trick predators.
... Bombycoidea caterpillar sounds are believed to function in defence against vertebrate predators. However, the specific effects that these and most other insect defence sounds have on predators remains poorly understood (Conner, 2014;Dookie et al., 2017). It has been recently proposed that different sound characteristics may communicate different meanings to predators (Bura et al., 2016). ...
... It is unlikely that these sounds function to warn of a chemical defence as A. floridensis lacks chemical-releasing spines or scoli, and regurgitation is not coupled to sound production. Compared with visual defensive ecology in insects, little is known about the functional significance of signal variation in defence sounds (Conner, 2014), and future studies should employ live predators and comparative analyses to test hypotheses (Bura et al., 2016;Dookie et al., 2017). ...
Insects have evolved a great diversity of sound-producing mechanisms largely attributable to their hardened exoskeleton, which can be rubbed, vibrated or tapped against different substrates to produce acoustic signals. However, sound production by forced air, while common in vertebrates, is poorly understood in insects. We report on a caterpillar that 'vocalizes' by forcing air into and out of its gut. When disturbed, larvae of the Nessus sphinx hawkmoth (Sphingidae:Amphion floridensis) produce sound trains comprising a stereotyped pattern of long (370 ms) followed by multiple short-duration (23 ms) units. Sounds are emitted from the oral cavity, as confirmed by close-up videos and comparing sound amplitudes at different body regions. Numerical models using measurements of the caterpillar foregut were constructed to test hypotheses explaining sound production. We propose that sound is generated by ring vortices created as air flows through the orifice between two foregut chambers (crop and oesophagus), a mechanism analogous to a whistling kettle. As air flows past the orifice, certain sound frequencies are amplified by a Helmholtz resonator effect of the oesophagus chamber. Long sound units occur during inflation, while short sound units occur during deflation. Several other insects have been reported to produce sounds by forced air, but the aeroacoustic mechanisms of such sounds remain elusive. Our results provide evidence for this mechanism by showing that caterpillars employ mechanisms similar to rocket engines to produce sounds.
... In birds, soft intraspecific communication has been associated with both aggression (Akçay, Tom, Campbell, & Beecher, 2011;Ballentine, Searcy, & Nowicki, 2008) and courtship (Dabelsteen et al., 1998;Reichard, Rice, Vanderbilt, & Ketterson, 2011), and there are multiple hypotheses regarding the role of 'quietness' per se, most notably the ability to convey private information while avoiding eavesdropping by unintended receivers (Dabelsteen et al., 1998;Nakano et al., 2014). These unintended receivers likely include conspecific rivals for mates, predators and acoustically orienting parasitoids (Conner, 2014;Dabelsteen et al., 1998;Searcy & Nowicki, 2006). Avian soft song is generally characterized as falling into one of two categories: a low-amplitude version of a species-typical, long-range song or a low-amplitude song that varies considerably in temporal characteristics from the typical long-range song (Anderson, Nowicki, & Searcy, 2007, Anderson, Searcy, Peters, & Nowicki, 2008Reichard et al., 2011). ...
... One extremely effective way to avoid acoustic eavesdroppers is to exercise adaptive silence (Conner, 2014). Males of many species of field cricket behave as satellite males, which forgo singing the loud, long-distance calling song and instead attempt to intercept females attracted to other calling males (Cade, 1975). ...
The study of low-amplitude or ‘soft’ songs and calls has largely been limited to organisms that produce multiple call types that fall neatly into a bimodal distribution with respect to amplitude. The soft vocalizations of many of these animals, including birds and mammals, have proven to be extremely difficult to collect data on due to difficulty in hearing and recording such songs in the wild, the lack of production of these sounds in captivity, and the difficulty in standardizing measurements of the amplitude produced by free-moving animals. Here I suggest we consistently expand the working definition of soft song to allow for the inclusion of insects and other organisms whose calls do not easily fit into a ‘high-amplitude’ versus ‘low-amplitude’ signal paradigm. For instance, some species of moths produce extremely quiet ultrasonic courtship songs without also producing a high-amplitude song, and field crickets sing courtship songs that contain both relatively loud and quiet elements within the same song. Soft-singing moths and crickets may not only prove more practical to work with, but may also provide answers to heretofore untestable hypotheses about the function and evolution of soft song.
... There are several facts strongly suggesting that moth ears evolved to detect echolocating bats: (1) the tuning of all moth ears to bat frequency range in spite of morphological differences (Fig. 1), (2) the positive correlation between how actively moths fly at night and their auditory sensitivity (ter Hofstede et al. 2008), (3) the absence of intraspecific acoustic communication in most moths (but see Sect. 4 below), (4) the evasive maneuvers and acoustic defenses elicited by bat sounds (Fullard 1998;Conner 2014; Greenfield 2014; see article in this volume by Pollack, G.S.), and (5) the correlation between bat predation pressure and moth hearing thresholds: Moths from Hawaii, with only one bat species, are tuned to the specific frequency of the sympatric bat (Fullard 2001). Moths that have escaped the predation by bats by being geographically isolated at remote islands without bats (Surlykke 1986;Fullard et al. 2007a) or, even more efficiently, by being temporally isolated by flying during the daytime or the winter time when no bats fly (Fullard et al. 1997;Rydell et al. 1997) show reduced hearing sensitivity. ...
... In contrast to the sound producing Arctiidae species and the geometrid beggar moth, where both species generally produce sound when hearing bat calls, only males produce sounds in the relatively rare examples of intense sound production in Noctuoidea, indicating that their sounds are for intraspecific communication. While ears in all Noctuoidea evolved once and are homologous, the wide diversity of sound-producing organs show that sound production has evolved independently several times (Conner 2014;Greenfield 2014). Noctuoidea ears are located on the metathorax, but sound-producing organs may be located in a variety of places and sound production mechanism may also vary for example males of the winter-flying species Rileyana (former Thecophora) fovea (Noctuidae) stridulate by scraping the modified hindleg against a bubble (fovea) on the hindwing (Surlykke and Gogala 1986). ...
Active echolocation enables bats to orient and hunt the night sky for insects. As a counter-measure against the severe predation pressure many nocturnal insects have evolved ears sensitive to ultrasonic bat calls. In moths bat-detection was the principal purpose of hearing, as evidenced by comparable hearing physiology with best sensitivity in the bat echolocation range, 20-60 kHz, across moths in spite of diverse ear morphology. Some eared moths subsequently developed sound-producing organs to warn/startle/jam attacking bats and/or to communicate intraspecifically with sound. Not only the sounds for interaction with bats, but also mating signals are within the frequency range where bats echolocate, indicating that sound communication developed after hearing by "sensory exploitation". Recent findings on moth sound communication reveal that close-range (~ a few cm) communication with low-intensity ultrasounds "whispered" by males during courtship is not uncommon, contrary to the general notion of moths predominantly being silent. Sexual sound communication in moths may apply to many eared moths, perhaps even a majority. The low intensities and high frequencies explain that this was overlooked, revealing a bias towards what humans can sense, when studying (acoustic) communication in animals.
... In comparison, male Asian corn borer moths (Ostrinia furnicalis) use very low intensity courtship songs of only 46 decibels with a range of just 1 cm, produced by male-specific scales on their forewings and the mesothorax (Nakano et al. 2008). Apparently, this very restrained acoustic communication behavior has evolved to form a private, close-vicinity communication channel between male and female moths as protection from interference of male competitors and potential eavesdropping predators (Conner, 2014). ...
... Prey characteristics that result from selection via predation are most strongly shaped by the most common predators' hunting strategies and sensory modalities. For example, visually oriented predatory birds have driven changes in the ratio of dark to bright peppered moths in industrialised areas (Cook and Saccheri 2013) and acoustically oriented bats have most likely driven the evolution of 'acoustic crypsis' in advertising insects and frogs that suddenly stop calling when a bat approaches (Conner 2014). ...
Aim
The goal of this work was to investigate whether the community of avian nest predators shifts from nocturnal to diurnal with changes in latitude. This hypothesis was formulated 70 years ago, under the rationale that longer day length during the bird breeding season at high latitudes increases opportunities for visual predators. Based on other studies investigating the identity of nest predators, we also considered variation in the habitat and nest height.
Location
Global.
Time Period
1994–2020.
Major Taxa Studied
Birds and their nest predators.
Methods
We reviewed studies that report the results of nest monitoring by video or photograph camera and collected data on the identity of nest predators. We then used the activity pattern of the predator species as a proxy to estimate whether predation events were nocturnal or diurnal. We used multivariate logistic and ordinal regressions to investigate whether the probability that nest predators are nocturnal changes with latitude and habitat.
Results
We found that both habitat and latitude explain variation in the circadian type of nest predators. In open habitats, nest predation was more often due to diurnal predators at high latitudes and nocturnal predators near the equator. In forests, on the other hand, nocturnal predator activity patterns were more common closer to the poles.
Main Conclusions
Using meta‐analytical methods, we show that predator activity varies across habitats and latitude leading to markedly different consequences of predation for prey. These findings suggest that small‐scale environmental factors such as habitat type can strongly affect and even neutralise larger‐scale, ecological patterns. We speculate that day length might act along with other biotic and abiotic factors to shape the timing of nest predation in birds.
... All these clades have lost their stridulatory apparatuses (partially or entirely) and their ability to communicate by sounds. Evolution towards muteness is often related to the strength of predation (Conner, 2014;Zuk et al., 2006) as many predators are able to detect and localise singing males by sounds (contrary to silent females, which are susceptible to be detected by predators when they move to join a singing male, e.g., Hedrick & Dill, 1993;Sakaluk & Belwood, 1984). In an ancestral condition of acoustic communication, the loss of the acoustic apparatus and the conquest of the world of (relative) silence thus arose several times through Oecanthidae. ...
Fossils are valuable indicators of the evolutionary history of the clades to which they belong to, especially when they are incorporated as terminal taxa in a total-evidence phylog-eny. According to their state of preservation, fossils are often incompletely described for key morphological characters, such as genitalic structures. Here, the internal parts of the genitalia of a male fossil cricket from Cretaceous amber, †Picogryllus carentonensis Josse & Desutter-Grandcolas (Oecanthidae, Podoscirtinae), together with other key morphological characters (i.e., metanotal structures and tibial spurs), were reconstructed for the first time by 3D microtomography. Total-evidence phylogeny and dating combining morphological data (fossils and extant taxa), molecular data (extant taxa only) and time calibration (fossil dates) were performed to evaluate the tempo and mode of evolution of the cricket family Oecanthidae. Divergence time estimates were thus refined and the patterns of transformation for key morphological structures contrasted through the analysis of phylogenetic morphological partitions. Our results show that Oecanthidae date back to the Upper Jurassic (Oxfordian, around 162 Ma) and attest to the presence of the Podoscirtinae in Western Europe during the Lower Cretaceous. Morphological evolution may have been driven by the conquest of new resources (as shown by leg evolution in ancestral Oecanthidae) and/or the 'conquest of silence' (as shown by repetitive and definitive losses of acoustic structures). By contrast, genitalia evolution proved more diffuse.
... This behavior also exists in primates (Martí nez et al., 2022) and is often described as "eavesdropping behavior" (Magrath et al., 2015). In addition to the special warning sound, entering silence is also an anti-predatory strategy (Conner, 2013;Ibá ñez-Álamo et al., 2015). The sudden cessation of animal sounds can also indicate an approaching danger, which is common in animals such as frogs, cicadas, and crickets. ...
... This stressor response can be explained by the acoustic adaptation hypothesis and proposes that species exposed to noisy conditions adapt by modulating frequencies, altering diel patterns, or adjusting amplitude of their biological sounds (Barber et al., 2010). However, other species may employ acoustic crypsis as a stressor response to predators, as is an ultrasonic call (Conner, 2014;Geberzahn and Hultsch, 2004;Ruxton, 2009). Traditionally, crypsis refers to alterations in the appearance of a biological organism to deter predation, such as by changing color. ...
... 183 As previously mentioned, the second type of passive acoustic camouflage developed by earless moths consists in having much of the thorax covered by hairlike scales ( Figure 7A) acting as a stealth coating against bat biosonar. [184][185][186] As suggested by Hegel and Casey 186 and Lee and Moss, 187 such thoracic scales create a dense layer of elongated piliform elements, resembling the lightweight fibrous materials used in engineering as sound insulators. Their potential as ultrasound absorbers was explored in Hegel and Casey 186 by means of tomographic echo images, and an average of 67% absorption of the impinging ultrasound energy emerged. ...
Nature has engineered complex designs to achieve advanced properties and functionalities through millions of years of evolution. Many organisms have adapted to their living environments by producing extremely efficient materials and structures exhibiting optimized mechanical, thermal, and optical properties, which current technology is often unable to reproduce. These properties are often achieved using hierarchical structures spanning macro-, meso-, micro-, and nanoscales, widely observed in many natural materials like wood, bone, spider silk, and sponges. Thus far, bioinspired approaches have been successful in identifying optimized structures in terms of quasistatic mechanical properties, such as strength, toughness, and adhesion, but comparatively little work has been done as far as dynamic ones are concerned (e.g., vibration damping, noise insulation, sound amplification). In particular, relatively limited knowledge currently exists on how hierarchical structure can play a role in the optimization of natural structures, although concurrent length scales no doubt allow multiple frequency ranges to be addressed. Here, we review the main work that has been done to analyze structural optimization for dynamic mechanical properties, highlighting some common traits and strategies in different biological systems. We also discuss the relevance to bioinspired materials, in particular in the field of phononic crystals and metamaterials, and the potential of exploiting natural designs for technological applications.
... In turn, mimicry exploits the experience gathered by the receiver during interactions with an aposematic signaller, and it may (Müllerian mimicry) or not (Batesian mimicry) be Correspondence associated with unpalatability. Finally, startling sounds discourage the receiver from attempting predation for the short time the prey needs to evade the attack 6 and require no learning by the receiver. ...
Mimicry is one of the most fascinating phenomena in nature¹. Mimicry traits often reflect complex, finely tuned, and sometimes extravagant relationships among species and have evolved to deceive predators or prey. Indeed, mimicry has most often evolved to discourage predation: the ‘mimic’ exhibits phenotypic convergence towards a non-related ‘model’ organism which is inedible or harmful, so that a given predator, or ‘receiver’, will refrain from attacking or ingesting the mimic. Traditionally, mimicry is mainly evident and has been mainly studied in the visual domain. Here, we report experiments that document the first case of interspecific acoustic mimicry in a mammal and demonstrate that the distress calls the greater mouse-eared bat (Myotis myotis) broadcasts when handled imitate sounds of stinging bees or wasps to discourage the bat’s avian predators.
... As previously mentioned, the second type of passive acoustic camouflage developed by earless moths consists in having much of the thorax covered by hair-like scales ( Figure 10) acting as a stealth coating against bat biosonar [183][184][185]. As suggested by [184,186] such thoracic scales create a dense layer of elongated piliform elements, resembling the lightweight fibrous materials used in engineering as sound insulators. ...
Nature has engineered complex designs to achieve advanced properties and functionalities through evolution, over millions of years. Many organisms have adapted to their living environment producing extremely efficient materials and structures exhibiting optimized mechanical, thermal, optical properties, which current technology is often unable to reproduce. These properties are often achieved using hierarchical structures spanning macro, meso, micro and nanoscales, widely observed in many natural materials like wood, bone, spider silk and sponges. Thus far, bioinspired approaches have been successful in identifying optimized structures in terms of quasi-static mechanical properties, such as strength, toughness, adhesion, but comparatively little work has been done as far as dynamic ones are concerned (e.g. vibration damping, noise insulation, sound amplification, etc.). In particular, relatively limited knowledge currently exists on how hierarchical structure can play a role in the optimization of natural structures, although concurrent length scales no doubt allow to address multiple frequency ranges. Here, we review the main work that has been done in the field of structural optimization for dynamic mechanical properties, highlighting some common traits and strategies in different biological systems. We also discuss the relevance to bioinspired materials, in particular in the field of phononic crystals and metamaterials, and the potential of exploiting natural designs for technological applications.
... Noctuoidea moths possess homologous tympanal ears on both sides of the metathorax, which suggests that a common ancestor evolved ears once (Kawahara et al. 2019). In contrast, the diversity of sound-producing organs even within the same phylogenetic clade indicates that sound production has evolved independently several times (Conner 2014;Greenfield 2014). Sound-producing organs in moths that produce calling songs may be located in a variety of body parts, and the mechanisms may vary accordingly. ...
Coevolutionary adaptation leads to modifications of sensory physiology and behavioral responses of predators and prey. From the ecological point of view, insect hearing and acoustic behavior are an attractive study area for researchers in entomology, animal behavior, and neuroethology. Recent technical advances in sound-recording equipment and molecular techniques have contributed to understanding the evolution of acoustic communication, including sexual dialogue, intraspecific competition, and the interspecific arms race between predators (e.g., bats) and prey (e.g., moths). Singing male moths exploit ultrasound-induced freezing responses of potential female mates or unwelcome rival males to enhance mating success. Freezing responses to ultrasound by moths are originally an antipredator reaction to echolocating insectivorous bats. The aim of Chap. 5 is to provide a sensory-behavioral explanation of the freezing response of insects during predator–prey interaction.
... biosonar | acoustics | ultrasonic | moth scale | natural metamaterial N octurnal lepidoptera (moths) are under intense evolutionary pressure from echolocating bats, which has led to a host of bat avoidance strategies (7), including ultrasound sensitive hearing to detect and escape from foraging bats (8,9), and the production of ultrasonic clicks to confuse or warn attacking bats (10,11). Many moth species, however, do not possess ultrasound-sensitive ears and instead rely on other defense mechanisms. ...
Significance
Bats and moths are embroiled in an evolutionary arms race. Using ultrasonic biosonar, bats detect their insect prey, which in turn deploy diverse strategies to avoid predation. Here, we show that some moth species evolved wings covered with a canopy of scales that reduces ultrasonic echoes. Our empirical and mathematical analysis together show that moth wings exhibit key features of a desirable technological acoustic metamaterial. This work enriches our understanding of the structural and functional complexity of lepidopteran wings and reveals enticing new ways to design, using bioinspired metamaterial properties, high-performance acoustic panels and noise mitigation devices.
... In comparison, male Asian corn borer moths (Ostrinia furnicalis) use very low intensity courtship songs of only 46 decibels with a range of just 1 cm, produced by male-specific scales on their forewings and the mesothorax (Nakano et al., 2008). Apparently, this very restrained acoustic communication behavior has evolved to form a private, close-vicinity communication channel between male and female moths as protection from interference of male competitors and potentially eavesdropping predators (Conner, 2014). ...
This article discusses the general aspects of insect communication, which can be broadly subdivided into auditory, visual, and chemical. The physical and conceptual basis is given for all three communication modalities, and prominent examples are listed for each category. Intra- as well as interspecific communication are discussed for each modality as well, with the former most prominently dealing with information transfer in sexual interactions between potential mating partners, whereas the latter is predominantly, but not exclusively, found in predator-prey relationships. The article closes with a fascinating look into case studies integrating different signaling modalities to obtain a more complete view on the various types of information transferred, and an outlook into what can and should be expected from future studies in this intriguing field.
... Many animals produce defensive sounds during predator-prey interactions (reviewed in Caro, 2005;Conner, 2014). Anitpredator defense is achieved through a diversity of mechanisms. ...
The observable diversity of antipredator defences across organisms demonstrates predation's impact on trait evolution. The functions of many traits that are presumed to have an antipredator function have never been directly tested. The spiny orb-weaving spider, Micrathena gracilis, for example, stridulates when grasped. While stridulation was first hypothesized to be an antipredator defence nearly 50 years ago, no data exist to support this hypothesis. To explore the form and function of M. gracilis stridulation, we first quantified the behavioural and acoustical properties of sound production. Next, using laboratory assays, we directly tested the effect of stridulation on survival with an avian predator – blue jays, Cyanocitta cristata. Finally, we conducted a large mark–recapture field study in which we compared the natural survival of experimentally manipulated adult female M. gracilis that could not stridulate (silenced) versus could stridulate (control). Stridulatory pulses produced broadband frequency spectra, consistent with acoustic antipredator defences in other taxa. We also observed stridulation by male M. gracilis for the first time. In staged laboratory interactions with captive blue jays, we found no differences in survival between silenced and control M. gracilis. Similarly, in our mark–recapture field study, we found no differences in survival estimates between silenced and control groups, nor an effect of stridulation rate. While M. gracilis stridulation closely resembles antipredator stridulation in other arthropods, our behavioural data do not yet provide solid support for an antipredator function in M. gracilis.
... These insects include tiger moths (Corcoran et al. 2010), hawkmoths (Barber and Kawahara 2013), and tiger beetles (Yager and Spangler 1997). Ultrasound-evoked sound production may have different specific antipredator functions, including aposematism or warning, mimicry, startle, and jamming bat sonar (Corcoran et al. 2009;Conner 2014). Responses of insects to bat echolocation sounds are not necessarily simplistic or predictable (Pollack 2015). ...
Insects have a diversity of hearing organs known to function in a variety of contexts, including reproduction, locating food, and defence. While the role of hearing in predator avoidance has been extensively researched over the past several decades, this research has focused on the detection of one type of predator- echolocating bats. Here we reassess the role of hearing in antipredator defence by considering how insects use their ears to detect and avoid the wide range of predators that consume them. To identify the types of sounds that could be relevant to insect prey, we first review the topic of hearing-mediated predator avoidance in vertebrates. Sounds used by vertebrate prey to assess predation risk include incidental sound cues (e.g. flight sounds, rustling vegetation, splashing) produced by an approaching predator or another escaping prey, as well as communication signals produced by a predator (e.g. echolocation calls, songs) or non-predator (e.g. alarm calls). We then review what is known, and what is not known, about such sounds made by the main predators and parasitoids of insects (i.e. birds, bats, terrestrial vertebrates, invertebrates) and how insects respond to them. Three key insights emerged from our review. First, there is a lack of information on how both vertebrate and insect prey use passive sound cues produced by predators to avoid being captured. Second, while there are numerous examples of vertebrate prey eavesdropping on the calls and songs of predators and non-predators to assess risk, there are currently no such examples for eared insect prey. Third, the hearing sensitivity of many insects, including those with ears considered to be dedicated to detecting bats or mates, overlaps with both sound cues and signals generated by non-bat predators. Sounds of particular relevance to insect prey include the flight sounds and calls of insectivorous birds, the flight sounds of insect predators and parasitoids, and rustling vegetation sounds of birds and terrestrial predators. We conclude that research on the role of insect hearing in predator avoidance has been disproportionally focused on bat-detection, and that acoustically-mediated responses to other predators may have been overlooked because the responses of prey may be subtle (e.g. ceasing activity, increasing vigilance). We recommend that researchers expand their testing of hearing-mediated risk assessment in insects by considering the wide range of sounds generated by predators, and the varied responses exhibited by prey to these sounds.
... Bark and ambrosia beetles live most of their lifetime inside plant tissue; therefore, sudden exposure to light means that the gallery has been compromised. The emission of sound could be used as a defensive strategy to deter predators as similar behaviours have been previously reported for other insects (Conner 2014;Masters 1979). It could also work as an alarm sound to inform conspecifics, like the vibrational signals produced by termites exposed to bright light after a predator has disturbed their nest (Kirchner et al. 1994). ...
Light-based stimuli elicited acoustic responses in male Hylesinus aculeatus Say (Curculionidae: Scolytinae: Hylesinina) instantaneously, with 100% reliability. Stridulations were elicited with a white light beam in a dark environment and recorded with an ultrasonic microphone. Acoustic responses were consistent, and, when compared with sounds produced under stressful conditions (i.e. physical stimulation), no significant differences were found. Hylesinus aculeatus possess an elytro-tergal stridulatory organ and acoustic communication is only present in males. This is also the first report of acoustic communication for this species. Instantaneous light-elicited acoustic communication has potential applications in the development of electronic traps and real-time acoustic detection and identification of beetles, border biosecurity, and noise-reduction in acoustic data collection.
... The second one is the adaptive silence of the non-aerial male lesser wax moth Achroia grisella that ceases its courtship song (Greenfield and Baker, 2003; Spangler, 1984). The last one is the clicking sounds of tiger moths (Noctuoidea: Erebidae) that function as acoustic aposematism, Batesian or Mü llerian mimicry, startle signals, or echolocation jamming (Conner, 2014; Conner and Corcoran, 2012; Miller and Surlykke, 2001). Hearing clearly offers a survival advantage; however, the auditory system comes with energetic and behavioural costs, and when it is no longer beneficial, such as in some moths that escape bat predation, it regresses (review: Miller and Surlykke, 2001). ...
The selection pressure from echolocating bats has driven the development of a diverse range of anti-bat strategies in insects. For instance, several studies have proposed that the wings of some moths absorb a large portion of the sound energy contained in a bat's ultrasonic cry; as a result, the bat receives a dampened echo, and the moth becomes invisible to the bat. To test the hypothesis that greater exposure to bat predation drives the development of higher ultrasound absorbance, we used a small reverberation chamber to measure the ultrasound absorbance of the wings of nocturnal (Bombycoidea: Saturniidae) and diurnal moths (Chalcosiinae: Zygaenoidea: Zygaenidae). The absorption factor of the nocturnal saturniids peaks significantly higher than the absorption factor of the diurnal chalcosiines. However, the wings of the chalcosiines absorb more ultrasound than the wings of some diurnal butterflies. Following a phylogenetic analysis on the character state of diurnality/ nocturnality in the Zygaenidae, we propose that diurnality in the Chalcosiinae is pleisiomorphic (retained); hence, the absorbance of their wings is probably not a vestigial trait from an ancestral, nocturnal form but an adaptation to bat activity that overlaps theirs. On a within-species level, females of the saturniids Argemma mittrei and Samia cynthia ricini have significantly higher absorption factors than the males. In the female S. c. ricini, the higher absorption factor corresponds to a detection distance by bats that is at best 20-30% shorter than that of the male.
... Insects exhibit a wide range of camouflage including many species that closely resemble leaves (Nentwig 1985;Schmidt 1990; Svenson and Whiting 2009;Conner 2014;Fabricant and Herberstein 2014;Pinheiro and Freitas 2014). At least five insect orders contain species with leaf-like mimesis, including Lepidoptera (butterflies and moths), Neuroptera (lacewings), Mantodea (mantises), Phasmatodea (walking sticks and leaf insects) and Orthoptera (grasshoppers, katydids and crickets) ( Fig. 1). ...
Insects have developed incredible means to avoid detection by predators. At least five insect orders have species that resemble leaves. Katydids (Orthoptera : Tettigoniidae) are the most diverse and wide-ranging of the leaf-like insects. At least 14 of the 20 extant katydid subfamilies contain species with leaf-like wings. Although it is undisputed that many katydids resemble leaves, methods for delineating the leaf-like from non-leaf-like forms have varied by author and in many cases are not explicitly stated. We provide a simple ratio method that can be used to differentiate the leaf-like and non-leaf-like forms. Geometric morphometrics were used to validate the ratio method. Leaf-like wings have been independently derived in at least 15 katydid lineages. Relative rates of speciation were found to be greater in the non-leaf-like forms, suggesting that leaf-like wings within Tettigoniidae are not a driver of diversification. Likewise, throughout Tettigoniidae, selection seems to be favouring the transition away from leaf-like wings. However, within the large Phaneropterinae subclade, relative speciation and transition rates between the leaf-like and non-leaf-like forms do not differ significantly.
... In the nocturnal Lepidoptera, sound signaling is invariably associated at some level with bats and their ultrasound echolocation signals (Greenfi eld 2014b ). Many species of noctuoid moths emit ultrasound signals that either jam bat echolocation systems or warn bats about the insect's chemical noxiousness (Conner 2014 ). In several species, these very same ultrasound signals serve as a close-range male courtship song (Simmons and Conner 1996 ). ...
Tympanal organs for hearing in the far field have evolved on multiple occasions among insects and are currently found in seven orders. Many, if not most, cases of insect hearing probably originated as a means for detecting and avoiding predators. In particular, sensitivity to ultrasound appears to have coevolved with echolocation signaling by insectivorous bats. However, on an overall scale, hearing is relatively rare among insects in comparison with other modalities of perception, including detection of substrate vibration. Sound signaling in insects, which typically occurs in the context of mating communication, is rarer still and is known in only five orders. Phylogenetic analyses suggest that acoustic communication in the Lepidoptera and in the suborder Caelifera (grasshoppers) of the Orthoptera originated via a “sensory bias” mechanism. Hearing was ancestral and sound signaling by males subsequently arose on multiple, independent occasions. On the other hand, acoustic communication in the Cicadidae and in the suborder Ensifera (crickets, katydids) of the Orthoptera may have originated via coevolution between female perception and male signaling. The diversity of songs among acoustic insects may reflect genetic drift and reproductive character displacement. There is little evidence, however, that insect songs are adapted to specific physical environments. In one clade of acoustic insects, the diversification of song is associated with an unusually high rate of population differentiation and speciation, which may be facilitated by a genomic co-localization of loci influencing female response/preference and male signaling. The extent to which co-localization is a general factor in speciation remains to be explored.
... Motion-induced sound can act as a record of any biotic or abiotic movement, thus making it inherently informative (i.e. a cue). Nearly all animals possess the ability to detect this sound (Budelmann, 1989;Budelmann, 1992;Fay, 2009;Horch, 1971), and many may go to great lengths to mask their own locomotion-induced sounds (Conner, 2014;Graham, 1934;Roche et al., 1999). Conversely, however, many species have also developed remarkable ways to amplify and otherwise modulate these motion-induced sounds for communication (Bostwick, 2006;Clark and Prum, 2015;Darwin, 1871). ...
For centuries, naturalists have suggested that the tonal elements of pigeon wing sounds may be sonations (non-vocal acoustic signals) of alarm. However, spurious tonal sounds may be produced passively due to aeroelastic flutter in the flight feathers of almost all birds. Using mechanistic criteria emerging from recent work on sonations, we sought to: 1) identify characteristics of rock pigeon flight feathers that might be adapted for sound production rather than flight, and 2) provide evidence that this morphology is necessary for in vivo sound production and is sufficient to replicate in vivo sounds. Pigeons produce tonal sounds (700±50Hz) during the latter 2/3 of each downstroke during take-off. These tones are produced when a small region of long, curved barbs on the inner vane of the outermost primary feather (P10) aeroelastically flutters. Tones were silenced in live birds when we experimentally increased the stiffness of this region to prevent flutter. Isolated P10 feathers were sufficient to reproduce in vivo sounds when spun at the peak angular velocity of downstroke (53.9-60.3 rad s(-1)), but did not produce tones at average downstroke velocity (31.8 rad s(-1)), while P9 and P1 feathers never produced tones. P10 feathers had significantly lower coefficients of resultant aerodynamic force (CR) when spun at peak angular velocity than at average angular velocity, revealing that production of tonal sounds incurs an aerodynamic cost. P9 and P1 feathers did not show this difference in CR These mechanistic results suggest that the tonal sounds produced by P10 feathers are not incidental and may function in communication.
... By means of the same technique above, we examined the three moth species' hearing thresholds to 50 kHz pure tones with varied pulse duration. Duration of these pulses were 1,3,5,10,15,20,25,30,40 and 50 ms (0.1 ms rise/fall time), which cover the pulse duration of the approach phase echolocation calls emitted by the sympatric insectivorous LDC/HDC bats: P. abramus and M. macrodactylus, both of which emit short duration pulses, and R. ferrumequinum, which emits long duration pulses (Tian and Schnitzler, 1997;Funakoshi and Takeda, 1998;Koyanagi et al., 2003;Lee and Lee, 2005;Fujioka et al., 2011;Fenton et al., 2012;Luo et al., 2012;Mantani et al., 2012). Due to the fact that 1-5 ms duration pulses recorded at the sampling frequency of 192 kHz cannot be analyzed by fast Fourier transformation analysis with P1024 sampling points, sound intensity was measured as peak equivalent SPL in dB (dB peSPL) with reference to a known peak signal voltage from a sound calibrator (type 4231, 94 dB SPL, 1 kHz; Brüel and Kjaer) (Stapelles et al., 1982). ...
... The ecological context in which signalling occurs, however, has received relatively less attention and will be the focus of this article. We do not attempt a comprehensive review of all the factors that may affect signals and signalling, such as parasitoids and predation, which are covered in depth elsewhere (Lakes-Harlan and Lehmann this issue; Hedwig and Robert 2014;Conner 2014) or of all insect groups (lepidopteran communication is covered in depth in a recent review: Greenfield 2014) but focus on recent work on the role of habitat and co-existing signallers in shaping insect signal structures, signaller behaviour and receiver physiology (see Römer 2013, for a more comprehensive and general review of insect acoustic communication and noise). ...
The efficiency of long-distance acoustic signalling of insects in their natural habitat is constrained in several ways. Acoustic signals are not only subjected to changes imposed by the physical structure of the habitat such as attenuation and degradation but also to masking interference from co-occurring signals of other acoustically communicating species. Masking interference is likely to be a ubiquitous problem in multi-species assemblages, but successful communication in natural environments under noisy conditions suggests powerful strategies to deal with the detection and recognition of relevant signals. In this review we present recent work on the role of the habitat as a driving force in shaping insect signal structures. In the context of acoustic masking interference, we discuss the ecological niche concept and examine the role of acoustic resource partitioning in the temporal, spatial and spectral domains as sender strategies to counter masking. We then examine the efficacy of different receiver strategies: physiological mechanisms such as frequency tuning, spatial release from masking and gain control as useful strategies to counteract acoustic masking. We also review recent work on the effects of anthropogenic noise on insect acoustic communication and the importance of insect sounds as indicators of biodiversity and ecosystem health.
... Further information on strategies and evolution of bat-avoidance behaviors is available in several excellent reviews: e.g., Hoy 1992;Hoy and Robert 1996;Miller and Surlykke 2001;Conner and Corcoran 2011;Yager 2012;Conner 2014;cf. articles in this volume by Stumpner et al., Schul, Reinhold, Lakes-Harlan and Lehmann). ...
Ultrasound-driven avoidance responses have evolved repeatedly throughout the insecta as defenses against predation by echolocating bats. Although the auditory mechanics of ears and the properties of auditory receptor neurons have been studied in a number of groups, central neural processing of ultrasound stimuli has been examined in only a few cases. In this review, I summarize the neuronal basis for ultrasound detection and predator avoidance in crickets, tettigoniids, moths, and mantises, where central circuits have been studied most thoroughly. Several neuronal attributes, including steep intensity-response functions, high firing rates, and rapid spike conduction emerge as common themes of avoidance circuits. I discuss the functional consequences of these attributes, as well as the increasing complexity with which ultrasound stimuli are represented at successive levels of processing.
... One key factor contributing indirectly to individual fitness is the survival rate. In response to predation, animals have evolved a great variety of strategies to survive by avoiding to be killed by predators (Edmunds, 1990;Ruxton et al., 2004;Eisner et al., 2005;Ratcliffe and Nydam, 2008;Schmidt, 2009;Conner, 2014). These strategies have been classified into primary defences, protecting the animals from contact with a predator, e.g., by cryptic colouration and mimicry, and secondary defences, important after the contact with a predator (Robinson, 1969;Edmunds, 1974). ...
Caterpillars are attacked by a wide range of predators and parasitoids. Consequently they have evolved a plethora of defences to avoid, repel, or escape their enemies. To date, research has focused on antipredator strategies in the visual and chemical realms, but defences operating in the acoustic realm remain poorly understood. Here I review how caterpillars use sounds, vibrations, and silences to avoid predation. There are numerous reports of defensive hearing and vibration detection. Most notably, species from diverse taxa respond to low frequency (less than 1 kHz) airborne sounds by freezing, flicking, thrashing and dropping. Hearing is proposed to function in thwarting the attack of a flying insect predator or parasitoid. Other caterpillars eavesdrop on plant-borne vibrations generated by a hunting predator or parasitoid. In the majority of reports demonstrating behavioural responses to sounds and vibrations in caterpillars, the sensory receptors are unknown. Caterpillars also generate sounds and vibrations in the context of defence. Many species of Bombycoidea produce defence sounds by clicking, chirping, whistling, and vocalizing. These sounds are thought to be directed primarily at vertebrate predators and to function as aposematic signals, deimatic displays, or mimics of predator alarm calls. Other caterpillars generate solid-borne vibrations to recruit help or coordinate defences. Myrmecophilic larvae of Lycaenidae and Riodinidae butterflies use vibratory signals to attract and maintain relationships with ants that provide protection. Despite the growing body of literature on the subject of acoustic defences in caterpillars, there is still much to learn. First, while there are few confirmed reports of acoustic crypsis, remaining silent by ceasing activity is likely an important strategy for caterpillars to avoid detection. Second, further testing of caterpillars responding to low-frequency sounds and solid-borne vibrations should be conducted to gain a better appreciation of the ubiquity of ‘hearing’ across different taxa. Third, experiments should be conducted using natural enemies and on natural substrates to understand what acoustic signals and cues occur during predator-prey interactions. Finally, neurophysiological, anatomical, and behavioural studies are necessary to better understand how caterpillars sense their complex acoustic landscapes.
APPLICATION OF INSECT ACOUSTIC COMMUNICATION IN ECO FRIENDLY INSECT PEST MANAGEMENT
The use of acoustics in predator evasion is a widely reported phenomenon amongst invertebrate taxa, but the study of ultrasonic anti-predator acoustics is often limited to the prey of bats. Here, we describe the acoustic function and morphology of a unique stridulatory structure in the relict orthopteran Cyphoderris monstrosa (Ensifera, Hagloidea): the Ander's organ. This species is one of just eight remaining members of the family Prophalangopsidae, a group with a fossil record of over 90 extinct species widespread during the Jurassic. We reveal that the sound produced by this organ has the characteristics of a broadband ultrasonic anti-predator defence, with a peak frequency of 58±15.5 kHz and a bandwidth of 50 kHz (at 10 dB below peak). Evidence from sexual dimorphism, knowledge on hearing capabilities and assessment of local predators, suggest the signal likely targets ground-dwelling predators. Additionally, we reveal a previously undescribed series of cavities underneath the organ that likely function as a mechanism for ultrasound amplification. Morphological structures homologous in both appearance and anatomical location to the Ander's organ are observed to varying degrees in 4 of the 7 other extant members of this family, with the remaining 3 yet to be assessed. Therefore, we suggest that such structures may either be more widely present in this ancient family than previously assumed, or have evolved to serve a key function in the long-term survival of these few species, allowing them to outlive their extinct counterparts.
Insects have evolved a variety of traits that appear to be direct countermeasures to bat echolocation
. Insect defences
can be grouped into primary defences
to avoid detection
and secondary defences
that allow them to escape being captured after the bat has detected them. These defences
include auditory and non-auditory defences as wells as ultrasound in the form of tymbal clicks. Here, we review the non-auditory adaptations of insects, including anti-bat traits such as body size, morphological or acoustic crypsis
, interference
with the echolocation signal by some body appendages and scales
in moths, the detection of wind caused by bat wing beats, and increased detection capabilities through large eyes. Mechanisms for avoidance of detection by bats include shifting activity phases, temporally shifting their habitat
in response to bat activity, flightlessness
or swamping the predator, and confusing its detection system by occurring in aggregations, for example on leks. We discuss bat predation
and other factors that affect lek
size. Finally, we also consider whether these apparent anti-bat traits could have evolved for reasons other than bat predation, for example flightlessness in moths could have evolved for increased fecundity.
Internally coupled ears (ICEs) allow small animals, relatively to the wavelengths of sounds to be localized, to reliably determine the direction of a sound source. ICEs are found in a variety of taxa, but crickets have evolved the most complex arrangement of coupled ears; an acoustic tracheal system comprised of a large cross body trachea that connects two entry points for sound in the thorax with the leg trachea of both ears. The key structure that allows for the tuned directionality of the ear is a tracheal inflation (acoustic vesicle) in the midline of the cross body trachea holding a thin membrane (septum). Crickets are known to display a wide variety of acoustic tracheal morphologies, most importantly with respect to the presence of a single or double acoustic vesicle. However, the functional relevance of this variation is still not known. In this study, we investigated the peripheral directionality of three co-occurring, closely related cricket species of the subfamily Gryllinae. No support could be found for the hypothesis that a double vesicle should be regarded as an evolutionary innovation to increase (1) interaural directional cues, (2) the selectivity of the directional filter, or (3) provide a better match between the directional and sensitivity tuning. Nonetheless, by manipulating the double acoustic vesicle in the rainforest cricket P. podagrosus, selectively eliminating the sound transmitting pathways, we revealed that these pathways contribute almost equally to the total amount of IIDs, emphasizing their functional relevance in the system.
Casualties and impediments inflicted on consumers by defended prey, and vice versa, may be averted by vocalizations, postures, coloration, scents, and other warning, or so-called aposematic, displays. The existence of aposematic signals has challenged biologists who have sought plausible mechanisms for their evolution. Here, we elaborate on the rationale for the hypothesis that aposematic signals arise via concurrent reciprocal selection (CRS) enacted between inimical signal receivers and signal emitters, where signal emitters, e.g., defended prey, select against non-discriminating signal receivers, e.g., predators, and signal receivers select against unrecognized signal emitters. It is postulated that this mutual selective interaction culminates in the survival of discriminating signal receivers that avoid signal emitters, and recognized (distinctive) signal emitters that are avoided by signal receivers. A CRS hypothesis for the evolution of aposematism, therefore, maintains that distinctive features of prey arise in response to selection imposed by consumers, and that avoidances of those features by consumers arise in response to selection imposed by defended prey. We discuss the plausible inception of aposematism via CRS in light of related hypotheses, and describe points of concordance with previous observations and suggestions on the origin of aposematism. Aposematism arising via CRS is not contingent upon the relatedness of signallers, aversions acquired by learning, or other conditions postulated for some other evolutionary hypotheses. CRS is a credible alternative hypothesis for the evolution of warning signals in diverse consumer-prey interactions.
Bats and insects provide a model system for integrating our understanding of predator-prey ecology, animal behavior and neurophysiology. Previous field studies of bat-insect interactions have been limited by the technological challenges involved with studying nocturnal, volant animals that use ultrasound and engage in battles that frequently last a fraction of a second. We overcame these challenges using a robust field methodology that included multiple infrared cameras calibrated for three-dimensional reconstruction of bat and moth flight trajectories and four ultrasonic microphones that provided a spatial component to audio recordings. Our objectives were to document bat-moth interactions in a natural setting and to test the effectiveness of a unique prey defense - sonar jamming. We tested the effect of sonar jamming by comparing the results of interactions between bats and Grote's tiger moth, Bertholdia trigona, with their sound-producing organs either intact or ablated. Jamming was highly effective, with bats capturing more than 10 times as many silenced moths as clicking moths. Moths frequently combined their acoustic defense with two separate evasive maneuvers: flying away from the bat and diving. Diving decreased bat capture success for both clicking and silenced moths, while flying away did not. The diving showed a strong directional component, a first for insect defensive maneuvers. We discuss the timing of B. trigona defensive maneuvers - which differs from that of other moths - in the context of moth auditory neuroethology. Studying bat-insect interactions in their natural environment provides valuable information that complements work conducted in more controlled settings.
While the evasive responses of many flying acoustic insects to aerial-hawking bats are duly recognized and studied, the responses of non-aerial insects to gleaning bats are generally overlooked. It has been assumed that acoustic insects are deaf to these predators because gleaning bat echolocation calls are typically low in amplitude, brief (1–3 ms) and very high in frequency (>60 kHz). We tested this assumption in a series of playback experiments with a moth (Achroia grisella) that uses hearing in both predator evasion and mating. We report that ultrasound pulses ≥78 dB peSPL (peak equivalent sound pressure level) and ≥1 ms in duration inhibit stationary males from broadcasting their own ultrasonic advertisement calls, provided that the pulsed stimuli are delivered at a repetition rate ≤30/s. Further analyses suggest that inhibition by pulsed ultrasound comprises two processes performed serially. First, a startle response with a latency <50 ms is elicited by a single pulse ≥1 ms duration. Here, a male misses broadcasting several calls over a 50–100 ms interval. Secondly, the startle may be extended as a silence response lasting several to many seconds if subsequent pulses occur at a rate ≤30/s. Call inhibition cannot represent a simple response to acoustic power because of the inverse interaction between pulse duration and rate. On the other hand, the temporal and energy characteristics of inhibitory stimuli match those of gleaning bat echolocation calls, and we infer that inhibition is a specialized defensive behavior by which calling males may avoid detection by eavesdropping bats.
This study examines the behavioural responses to ultrasound in 52 species from the family Cicindelidae using both tethered flight and non-flight assays. Tethered flying tiger beetles respond to trains of bat-like ultrasonic pulses with a short-latency, multi-component behaviour. There was no variation in the nature of the behavioural responses regardless of geographical distribution or phylogenetic position. Lowest mean behavioural thresholds lie predominantly between 30 and 45 kHz. Sensitivity, however, varies widely, and several species do not respond at all in these assays. The lowest thresholds for responders are most often between 70 and 80 dB SPL. Almost all subgenera of North American tiger beetles in the genus Cicindela have at least some species with low-threshold acoustic behaviour. The single exception is the large subgenus Cicindela where all species are completely unresponsive or have very high thresholds. There was little relationship between habitat and responsiveness to ultrasound, but there is a strong correlation with seasonal activity – species with adults active in the spring and autumn (all in the subgenus Cicindela) do not show ultrasound-triggered behaviour whereas summer-active species generally do. Superimposing these data on a current phylogeny of the North American tiger beetles suggests that acoustic behaviour (and hearing) is a shared primitive trait among the taxa examined here and that there have been at least five independent losses of this character.
1.
Many arctiid and ctenuchid moths produce clicking sounds in response to the ultrasonic cries of bats. Clicks were recorded from the two arctiid moth speciesArctia caja, the garden tiger, andPhragmatobia fuliginosa, the ruby tiger. The threshold for eliciting clicks was around 60 to 75 dB pe SPL in both species.A. caja produced single clicks, andP. fuliginosa bursts of clicks. The maximum intensity of the clicks was 90 to 94 dB pe SPL at 5 cm forA. caja and 85 dB pe SPL at 5 cm forP. fuliginosa. The clicks contain most energy in the frequency range from 40 to 80 kHz (Figs. 2, 3).
2.
Pipistrelle bats (Pipistrellus pipistrellus) were trained to sit on a platform and discriminate the difference in range,d, to two targets. The minimum d the bats could discriminate with more than 75% success rate was 1.5 cm.
3.
The targets had built-in electrostatic loudspeakers through which different sounds could be played back to the bat. Playback of arctiid moth clicks from both targets did not disturb the bat's discrimination accuracy. The success rate did not decrease at anyd, and the minimum d in the presence of clicks was 1 cm.
4.
The clicks played from both loudspeakers did not influence the acoustic behavior or discrimination behavior of the bats in any obvious way. In all trials the bats went through a period with long (3 ms) slowly repeated (12–15 pulses/s) cries, a period with shorter cries and increased PRR (20 pulses/s) in which the decision seemed to be made, and finally a period with very short cries (0.5 ms) repeated at rates of up to 150 pulses/s (Figs. 4 and 5). The cries were FM sweeps from 120 kHz to 55 kHz with a second harmonic, which was strongest in the short cries.
5.
The bats' response to the playback of different sounds, such as noise and recorded bat cries, from either the left or right loudspeaker, suggested that the bats reacted to clicks as if they were noise. The playback of sounds from only one speaker at a time decreased the bats' success rate, since the bats were attracted to the sounds (Figs. 6 and 7).
6.
A secretion from the cervical glands ofA. caja, which contains choline ester, was given to a bat if it crawled towards a clicking target. Both bats tested in this way learned to associate the clicks with a noxious reward and avoided the clicks after just one or two trials (Fig. 8).
7.
These results suggest that the function of the garden tiger and ruby tiger clicks in nature is to warn the bat of the moth's distastefulness, and not to jam the bat's sonar system.
Coevolutionary arms races between predators and prey can lead to a diverse range of foraging and defense strategies, such as countermeasures between nocturnal insects and echolocating bats. Here, we show how the fine structure of wing scales may help moths by slightly increasing sound absorbance at frequencies typically used in bat echolocation. Using four widespread species of moths and butterflies, we found that moth scales are composed of honeycomb-like hollows similar to sound-absorbing material, but these were absent from butterfly scales. Micro-reverberation chamber experiments revealed that moth wings were more absorbent at the frequencies emitted by many echolocating bats (40-60 kHz) than butterfly wings. Furthermore, moth wings lost absorbance at these frequencies when scales were removed, which suggests that some moths have evolved stealth tactics to reduce their conspicuousness to echolocating bats. Although the benefits to moths are relatively small in terms of reducing their target strengths, scales may nonetheless confer survival advantages by reducing the detection distances of moths by bats by 5-6%.
The tiger moth Bertholdia trigona is the only animal in nature known to defend itself by jamming the sonar of its predators - bats. In this study we analyzed the three-dimensional flight paths and echolocation behavior of big brown bats (Eptesicus fuscus) attacking B. trigona in a flight room over seven consecutive nights to determine the acoustic mechanism of the sonar-jamming defense. Three mechanisms have been proposed: (1) the phantom echo hypothesis, which states that bats misinterpret moth clicks as echoes; (2) the ranging interference hypothesis, which states that moth clicks degrade the bats' precision in determining target distance; and (3) the masking hypothesis, which states that moth clicks mask the moth echoes entirely, making the moth temporarily invisible. On nights one and two of the experiment, the bats appeared startled by the clicks; however, on nights three through seven, the bats frequently missed their prey by a distance predicted by the ranging interference hypothesis (∼15-20 cm). Three-dimensional simulations show that bats did not avoid phantom targets, and the bats' ability to track clicking prey contradicts the predictions of the masking hypothesis. The moth clicks also forced the bats to reverse their stereotyped pattern of echolocation emissions during attack, even while bats continued pursuit of the moths. This likely further hinders the bats' ability to track prey. These results have implications for the evolution of sonar jamming in tiger moths, and we suggest evolutionary pathways by which sonar jamming may have evolved from other tiger moth defense mechanisms.
Although the use of distinct colors to indicate unprofitability to predators (i.e. aposematism) is commonly thought of as an adaptation, our knowledge of its macroevolutionary effects is limited. Because aposematism is expected to decrease attacks by predators, we hypothesized that aposematic lineages should be larger on average than their non-aposematic sister groups because of the decreased probability of extinction and/or increased probability of speciation (i.e. increased diversification). The results of our sister-group analysis are consistent with the hypothesis that the evolution of aposematism is accompanied by increased diversification of lineages, with the aposematic focal group having more species in 11 of 14 pairs of sister groups. Despite the apparent advantages of reduced predation risk on diversification rates, the evolution of aposematism is relatively rare and reversions to a cryptic state are not uncommon. In addition to the difficulties in evolving a trait that initially decreases the survivorship of prey among naive predators, we discuss other factors that may limit the apparent prevalence and success of aposematism. It is hoped that the results of our analysis will encourage further analyses of the phylogenetic relationships among aposematic groups and their relatives, and of the evolutionary time scales over which the benefits of aposematism are the greatest to lineages with this condition.
Many animals bear colors and patterns to reduce the risk of predation from visually hunting predators, including warning colors, camouflage, and mimicry. In addition, various species possess paired circular features often called "eyespots," which may intimidate or startle predators preventing or postponing an attack. Most explanations for how eyespots work assert that they mimic the eyes of the predators own enemies. However, recent work has indicated that spots may reduce the risk of predation based purely on how conspicuous they are to a predator's visual system. Here, we use a field technique involving artificial prey marked with stimuli of various shapes, numbers, and sizes, presented to avian predators in the field, to distinguish between the eye mimicry and conspicuousness theories. In 3 experiments, we find that the features which make effective antipredator wing markings are large size and higher numbers of spots. Stimuli with circles survived no better than those marked with other conspicuous shapes such as bars, and changing the spatial construction of the spots to increase the level of eye mimicry had no effect on the protective value of the spots. These experiments support other recent work indicating that conspicuousness, and not eye mimicry, is important in promoting avoidance behavior in predators and that eyespots on real animals need not necessarily, as most accounts claim, mimic the eyes of other animals. Copyright 2008, Oxford University Press.
The night sky is the venue of an ancient acoustic battle between echolocating bats and their insect prey. Many tiger moths (Lepidoptera: Arctiidae) answer the attack calls of bats with a barrage of high frequency clicks. Some moth species use these clicks for acoustic aposematism and mimicry, and others for sonar jamming, however, most of the work on these defensive functions has been done on individual moth species. We here analyze the diversity of structure in tiger moth sounds from 26 species collected at three locations in North and South America. A principal components analysis of the anti-bat tiger moth sounds reveals that they vary markedly along three axes: (1) frequency, (2) duty cycle (sound production per unit time) and frequency modulation, and (3) modulation cycle (clicks produced during flexion and relaxation of the sound producing tymbal) structure. Tiger moth species appear to cluster into two distinct groups: one with low duty cycle and few clicks per modulation cycle that supports an acoustic aposematism function, and a second with high duty cycle and many clicks per modulation cycle that is consistent with a sonar jamming function. This is the first evidence from a community-level analysis to support multiple functions for tiger moth sounds. We also provide evidence supporting an evolutionary history for the development of these strategies. Furthermore, cross-correlation and spectrogram correlation measurements failed to support a “phantom echo” mechanism underlying sonar jamming, and instead point towards echo interference [Current Zoology 56 (3): 358–369, 2010].
Moths Battling Bats
Many night-flying insects hear the sonar sounds of attacking bats and take evasive action. Among moths, evasive flight is often accompanied by the production of ultrasonic sounds. Three functions of these sounds have been proposed: to startle the bat, to warn of distastefulness, or to “jam” the bat's sonar system. Corcoran et al. (p. 325 ) studied a species of tiger moth ( Bertholdia trigona ) that emits a particularly dense series of ultrasonic clicks and the interception behavior of big brown bats ( Eptesicus fuscus ) presented with silenced or sound-producing tethered moths. If the moth sounds evoke startle, naïve bats should initially break off their attacks, but then the bats should habituate to the sounds and complete subsequent attacks. In contrast, if the moth sounds have a warning effect, naïve bats should initially complete their attacks on sound-emitting moths, discover that the moths are distasteful, and refuse to capture them in future trials. Most of the bats in the tests reliably caught the silenced moths but avoided completing attacks on sound-producing moths, with no evidence of increasing or decreasing probability of capture from the first to the last trial, which suggests that the moths effectively jammed the bats' sonar.
The book discusses the diversity of mechanisms by which prey can avoid or survive attacks by predators, both from ecological and evolutionary perspectives. There is a particular focus on sensory mechanisms by which prey can avoid being detected, avoid being identified, signal (perhaps sometimes dishonestly) to predators that they are defended or unpalatable. The book is divided into three sections. The first considers detection avoidance through, for example, background matching, disruptive patterning, countershading and counterillumination, or transparency and reflective silvering. The second section considers avoiding or surviving an attack if detection and identification by the predator has already taken place (i.e., secondary defences). The key mechanism of this section is aposematism: signals that warn the predator that a particular prey type is defended. One particularly interesting aspect of this is the sharing of the same signal by more than one defended species (the phenomenon of Mullerian mimicry). The final section considers deception of predators. This may involve an undefended prey mimicking a defended species (Batesian mimicry), or signals that deflect predator’s attention or signals that startle predators. The book provides the first comprehensive survey of adaptive coloration in a predator-prey context in thirty years.
Signals used to attract mates are often conspicuous to predators and parasites, and their evolution via sexual selection is expected to be opposed by viability selection. Many secondary sexual traits may represent a compromise between attractiveness and avoidance of detection. Although such signal exploitation appears to be widespread, most examples come from species that use acoustic or olfactory mating signals, and relatively few cases of visual signal exploitation can be substantiated. Because males are usually the signaling sex, they are more at risk from predators or parasitoids that locate prey or hosts by sexual signals; this differential selection on the two sexes can affect the intensity of sexual selection on male ornamental traits. The notable exception to male signaling and female attraction occurs in pheromone-producing insects, particularly lepidopterans, which show an opposite pattern of female odor production. Exploitation of such sex pheromones is relatively rare. We discuss reasons for the reversal in sex roles in these species and its implications for signal exploitation. Changes in signals that appear to be adaptations to avoid predation include the use of different signal modalities, changes in signaling behavior, loss of signals, and alteration of signal characteristics such as pitch. Selection pressure from signal exploiters could lead to the production of a novel signal and thus facilitate speciation. Relatively little work has been done on adaptations on the part of the exploiting species, but such adaptations could indirectly influence the mating system of the predator or parasitoid. Signal exploitation is also expected to be a fruitful source of examples of coevolution. Finally, plants emit attractants analogous to secondary sex characters in animals, and may also be vulnerable to signal exploitation.
The aim of this chapter is to review the evidence that organisms have adaptations that have been selected because they confer difficulty of detection by enemies (principally predators and parasites) that primarily detect their prey using sensory systems other than vision. That is, I will review the empirical evidence for non-visual crypsis and explore how our understanding of visual crypsis can be expanded to non-visual sensory systems. The review is arranged in terms of different sensory modalities.
Have you ever wondered how stealth planes achieve "invisibility," how sunken ships are found, or how fishermen track schools of fish in vast expanses of ocean? Radar and sonar echolocation-a simple matter of sending, receiving, and processing signals. Weaving history with simple science, Mark Denny deftly reveals the world of radar and sonar to the curious reader, technology buff, and expert alike. He begins with an early history of the Chain Home radar system used during World War II and then provides accessible and engaging explanations of the physics that make signal processing possible. Basic diagrams and formulas show how electromagnetic and sound waves are transmitted, received, and converted into images, allowing you to literally see in the dark. A section on bioacoustic echolocation, with a focus on the superior sonar systems of bats and whales and a discussion of the advanced technology of next-generation airborne signal processors, opens the imagination to fascinating possibilities for the future. © 2007 The Johns Hopkins University Press. All rights reserved.
In response to tactile stimulation and to ultrasonic pulses such as those of attacking bats, many moths of the family Arctiidae produce ultrasonic clicks. To test the hypothesis that these clicks are aposematic sounds, warning bats of unpalatable prey, African moths of these two families were captured at lights, assayed for clicking responses to tactile and ultrasonic stimulation and placed, together with moths of similar body sizes and other families captured at the same time, in a small cage with sympatric Tadarida pumila bats. Arctiid fragments were sought among the insect remains (mostly moth wings) dropped by free-foraging Hipposideros caffer bats. There were no arctiid wings among them, and the captive bats ate a significantly larger proportion of control moths than arctiids. There were no significant differences by species or sex in the arctiids' clicking responses to either stimulus or in their palatability to bats. Since the arctiids did click in response to bat-like stimuli and were clearly less palatable to the bats than the control moths, we conclude that the sounds of these moths can act as aposematic sounds.
Males of both the lesser wax moth, Achroia grisella (F.) and the bush katydid (Insara covilleae Rehn and Habard), call mates with high-frequency sound audible to insectivorous bats. Both insects cease acoustical mate calling when they hear the cries of either an approaching bat or a similar artificially-produced sound. But, the lesser wax moth sometimes continues to call by producing pheromone, but not sound. Both insects resume acoustical calling either soon after a bat has passed or after the artificial sound is removed.
In the last decade, research on the previously dormant field of camouflage has advanced rapidly, with numerous studies challenging traditional concepts, investigating previously untested theories and incorporating a greater appreciation of the visual and cognitive systems of the observer. Using studies of both real animals and artificial systems, this book synthesises the current state of play in camouflage research and understanding. It introduces the different types of camouflage and how they work, including background matching, disruptive coloration and obliterative shading. It also demonstrates the methodologies used to study them and discusses how camouflage relates to other subjects, particularly with regard to what it can tell us about visual perception. The mixture of primary research and reviews shows students and researchers where the field currently stands and where exciting and important problems remain to be solved, illustrating how the study of camouflage is likely to progress in the future.
Coevolution is the accumulation of reciprocal adaptations that phylogenetically distant species undergo as a result of their
interactions over evolutionary time. Although the classic definition of coevolution requires highly specialized, one-to-one
relationships between the participants (e.g., the proboscises of bees and the corollas of orchids, Darwin 1862), today we recognize coevolutionary relationships in a global perspective that does not involve localized interactions (Thompson 1994). Predator-prey relation-ships have formed the basis for many coevolutionary studies, most using the morphology or behavior
of the organisms involved to examine the presence of reciprocal adaptations (e.g., the defenses of cladocerans, Dodson 1998; Riessen and Sprules 1990). Coevolutionary processes between predators and prey can be difficult to observe because of the multiple functions that
most animal structures serve, and it can be difficult to determine which parts of an organism’s phenotype have been subjected
to the specific changes induced by coevolutionary effects (e.g., are the horns of male deer directed against predators or
other males?). Vertebrates, in particular, present special problems in the study of coevolution because of their rela-tively
long life span and the complexities of their interactions with other organisms, both predators and competitors.
We used the responses of four trained captive big brown bats (Eptisicus fuscus) to the clicks of arctiid moths to test the hypothesis that predators learn their responses to preys' defensive displays. Bats were trained to fly to a platform where they sometimes received a mealworm reward. On about 5% of the occasions on which bats came within 0.5 m of the platform, they were randomly presented with one of three acoustic stimuli, including recorded clicks of an arctiid moth, synthetic clicks (white noise temporally matched to arctiid clicks), or tape noise. It took less than three trials for the bats to habituate to the arctiid clicks and longer for them to cease responding to the other stimuli. In less than eight pairings of arctiid clicks and a noxious food reward, two of the bats learned to associate moth clicks with a bad taste. Our data support the hypothesis by showing that although unexpected clicks startle inexperienced bats, they may also warn experienced bats of bad-tasting prey.
Seventeen of the 24 species of Nearctic Arctiidae which we examined produced sounds under a variety of tactile and acoustic stimuli. Seven of 14 sound-producing species tested emitted their sounds in response to the hunting cries of insectivorous bats or simulations thereof. The sounds were generated by the buckling action of the microtymbal band (=striated band) on the surface of the modified thoracic metepisternum (=tymbal). Sound production is not dependent on the presence of microtymbals as four species of Callarctia possessed nonstriated, functional tymbals. In contrast, other species possessed striated, apparently nonfunctional tymbals.The sounds of the arctiids we studied were predominantly ultrasonic (> 20 kHz) and relatively faint (< 85 dB at 2 cm) compared with other insect sounds.The acoustic parameters of the arctiids surveyed revealed extremely high levels of variability in the sounds. Smaller species generally emit higher pulse repetition rates and more intense signals than larger ones. The ...
Many arctiid moths emit trains of ultrasonic clicks upon tactile stimulation and when exposed to trains of ultrasonic pulses like those emitted by bats. We observed the responses of captive big brown bats (Eptesicus fuscus) and free-foraging red bats (Lasiurus borealis) to arctiid moths and similar-sized moths of other families, and the responses of free-flying moths to trains of ultrasonic pulses like those of bats. Both the big brown bats and the red bats ate significantly fewer arctiids than were available to them, but the captive bats were more likely to kill arctiids than were the free-flying ones. The captive bats ate fewer of the arctiids they killed than moths of other families. Muted arctiid moths were caught by the red bats more than intact conspecifics but usually were dropped without being eaten. Free-flying arctiid moths changed their flight paths less in response to trains of ultrasonic pulses than did moths of other families similarly capable of hearing these signals. These results suggest that arctiid moths use their clicks and chemical defenses to protect them from the bats that prey upon them, and that these clicks are aposematic signals that warn bats of unpalatable prey.
We observed the echolocation and hunting behaviour of Lasiurus borealis and Lasiurus cinereus from May to August of 1989, 1990, and 1991 to assess the role of feeding buzzes in the behaviour of echolocating bats attacking airborne prey. Feeding buzzes consist of short echolocation pulses produced at a rapid rate just before contact between a flying bat and its prey. The hypothesis that the duration of the feeding buzz reflects the size of the attacked prey was not supported by the data. The mean lengths of silent periods between the end of the feeding buzz and the next echolocation call were significantly longer after successful attacks than after unsuccessful attacks. There was, however, no threshold value unambiguously separating successful from unsuccessful attacks in either species. The responses of bats to tossed pebbles and to some insects indicated that during some feeding buzzes L. borealis and L. cinereus judged the nature and range of prey being attacked. Attacks by free-flying L. borealis on muted arctiid moths (Hypoprepia fucosa), combined with the rejection of these moths as food by captive bats, suggest that in this setting the clicks of these moths are aposematic signals, warning the bats of the moths' bad taste.
Analysis of the clicks produced by some arctiid moths shows that their acoustic characteristics (power spectra and frequency–time structures) are remarkably similar to those of frequency-modulated echolocation calls produced by many bats as they close with their prey. We suspect that the clicks are initially processed as echoes by the auditory systems of these bats and function by interfering with information processing by the bat.
Signals used to attract mates are often conspicuous to predators and parasites, and their evolution via sexual selection is expected to be opposed bg viability selection. Many secondary sexual trails may represent a compromise between attractiveness and avoidance of detection. Although such signal exploitation appears to be widespread, most examples come from species that use acoustic or olfactory mating signals, and relatively few cases of visual signal exploitation can be substantiated. Because males are usually the signaling sex, they are more at risk from predators or parasitoids that locate prey or hosts by sexual signals; this differential selection on the two sexes can affect the intensity of sexual selection on male ornamental traits. The notable exception to mab signaling and female attraction occurs in pheromone-producing insects, particularly lepidopterans, which show an opposite pattern of female odor production. Exploitation of such sex pheromones is relatively rare We discuss reasons for the reversal in sex roles in these species and its implications for signal exploitation. Changes in signals that appear to be adaptations to avoid predation include the use of different signal modalities, changes in signaling behavior, loss of signals, and alteration of signal characteristics such as Pitch. Selection pressure from signal exploiters could lend to the production of a novel signal and thus facilitate speciation. Relatively little work has been done an adaptations on the part of the exploiting species, but such adaptations could indirectly influence the mating system of the predator or parasitoid. Signal exploitation is also expected to be a fruitful source of examples of coevolution. Finally, plants emit attractants analogous to secondary sex characters in animals, and may also be vulnerable to signal exploitation.
The exoskeletal morphology, muscular organization, and innervation patterns of the tymbals of seven sound-producing species of tiger moths (Arctiidae) were compared with the undifferentiated episterna of two silent species. At least three muscles are involved in sound production: the tymbal muscle, pv2, and the accessory muscles, pvl and/or pv6. All of the tymbal muscles are innervated by the IIIN2a branch of the metathoracic leg nerve, which contains two axons larger than the others. Backfills of the tymbal branch of the IIIN2a reveal a medial sensory neuropil and a population of five ipsilateral motor neurons whose somata are clustered into three groups along the anterior edge of the metathoracic ganglion. The dendritic arborizations of the motor neurons extend to the ganglionic midline but are separate from one part of the auditory neuropil observed in other noctuoids. The study concludes that the arctiid tymbal reveals only minor modifications (e.g., cuticle thinning) of the episterna of silent moths and represents a primitive form of the tymbal compared to those of the Cicadidae.
1. Lepidoptera belonging to several different families bear eyespot patterns on their wings, often with a very strong resemblance to the vertebrate eye. These have been derived from different morphological structures in different groups, and their evolution is therefore convergent within the order. 2. A study of two individual hand-reared Yellow Buntings has shown that the pursuit of flying insect prey is fully released at the bird's first encounter with a flying butterfly, but that the orientation of the attack is modified by experience. 3. Eyespot patterns are associated with displays which exhibit them. In the case of a Nymphalid butterfly, Nymphalis io, an experiment has shown that the display releases escape responses from Yellow Buntings, and that the major part of this effect is due to the four ocelli on the upper surface of the fore- and hind wings. Experiments with other species of insects suggest that other factors contributing include the bright field of colour surrounding the eyespots, the rhythmic movements of the display, and the rustling noise which accompanies it. The bird's responses to this display waned rapidly in the majority of individuals, but some birds became conditioned to avoid the butterflies altogether. 4. Experiments with models showed that circular patterns presented suddenly to feeding birds (Chaffinches, Yellow Buntings and Great Tits) release escape responses more effectively than do non-circular patterns of the same area and perimeter. An increase in the perimeter of the models, achieved by the use of three concentric circles of the same area as the single circle, increased its releasing value. A flat, eye-like pattern which was so shaded and distorted as to appear three-dimensional was more effective than a similar flat pattern which was not shaded, and hence was more bright. Large models were more effective than similar small ones. Waning was again rapid. The differential responsiveness to circular and non-circular patterns is inborn in the case of Great Tits and Chaffinches. 5. An experiment with mealworms artifically ornamented with small eye-like spots at their extremities has shown that such markings, placed on a prey-object, tend to direct to themselves the attack of Yellow Buntings. The waning of the element of disturbed orientation in the responses is slow, and may not be significant. 6. The deflection and intimidation effects are discussed. The origin of the predator's responses to deflection marks is not known, but it is suggested that intimidating eyespots act by mimicking the eyes of the large avian predators preying on the small insectivorous passerines which are among their natural enemies. It has been shown that many small passerines possess inborn responses to their predators, and it is probable that these are "parasitised" by the eyespot patterns of insects. Eyespot patterns must be regarded as wholly distinct from pseudaposematic colouration. The effect of experience on small passerines, either of the predator-model or of an ocellated imitator, is most usually the reverse of that sustained by a predator encountering the model or mimic in a true case of Batesian or Mullerian mimicry, and the restrictions on the population size of a pseudaposematic insect relative to its model do not apply to insects utilising the inborn responses of their predators.
Male Teleogryllus
oceanicus prefer to call from refuges and from these protected sites produce signals that contain more trill elements than produced by males calling without the protection of refuges. We tested the vulnerability of male crickets to predation from two species of gleaning bats, Nyctophilus
major and N.
geoffroyi. Crickets called from the floor of darkened fly-ways where bats preyed on calling rather than silent males. Both species of bat used passive listening to locate their prey rather than echolocation. Those crickets calling from refuges avoided predation. By counting the number of passes each bat made over paired speakers emitting different digitized songs, we tested the bat's preference for different call elements or the total number of sound elements in the song per unit time. When the total number of sound elements of each signal was balanced, bats preferred trills to chirps, and when call length differed, bats preferred those signals with more total sound elements. We discuss the possibility that predation by bats is a form of counter-selection on calling in T.
oceanicus.
Myopophyllum speciosum is a pseudophylline katydid (Tettigoniidae) from the neotropics that generates unusually high ultrasonic frequencies as the dominant carrier in its calling song. Male calls average only 148 ms duration and are given at long intervals: 8.7 s. Pairing is completed with vibrational signals, generated at closer range by body oscillation (tremulation). Two distinctive vibrational motor patterns, short and long, are produced by both sexes. Physical parameters of the sound and vibratory signals of this species are described. The relatively high‐Q carrier frequency (mean = 81 kHz) varies between males over a range of 20 kHz but does not predict a singer's body size. Short tremulations are much more intense than long as measured by acceleration. Descriptions of the songs of three other pseudophylline species with unusually high principal carriers (65–105 kHz) are also presented.
Eavesdropping by predatory bats offers the most plausible selective explanation for the features of M. speciosum's signal system. This hypothesis is supported by the species' sexually dimorphic defensive spination: males, the sound‐signalling sex, have metafemoral spines of greater size and distinctive orientation. Evidence for eavesdropping and for alternative hypotheses is assessed. Other neotropical tettigoniids in rainforest understorey also employ elaborate vibratory signals (species of Choeroparnops, Schedocentrus, Docidocercus, Copiphora ) and some show a trend to reduce or even to eliminate their use of airborne sound. Some rainforest tettigoniids may have replaced acoustic with vibrational signalling as a response to bat eavesdropping.
Two independent methods of comparison, serial homology and phylogenetic character mapping, are employed to investigate the
evolutionary origin of the noctuoid moth (Noctuoidea) ear sensory organ. First, neurobiotin and Janus green B staining techniques
are used to describe a novel mesothoracic chordotonal organ in the hawkmoth, Manduca sexta, which is shown to be serially homologous to the noctuoid metathoracic tympanal organ. This chordotonal organ comprises a
proximal scolopidial region with three bipolar sensory cells, and a long flexible strand (composed of attachment cells) that
connects peripherally to an unspecialized membrane ventral to the axillary cord of the fore-wing. Homology to the tympanal
chordotonal organ in the Noctuoidea is proposed from anatomical comparisons of the meso- and metathoracic nerve branches and
their corresponding peripheral attachment sites. Second, the general structure (noting sensory cell numbers, gross anatomy,
and location of peripheral attachment sites) of both meso- and metathoracic organs is surveyed in 23 species representing
seven superfamilies of the Lepidoptera. The structure of the wing-hinge chordotonal organ in both thoracic segments was found
to be remarkably conserved in all superfamilies of the Macrolepidoptera examined except the Noctuoidea, where fewer than three
cells occur in the metathoracic ear (one cell in representatives of the Notodontidae and two cells in those of other families
examined), and at the mesothoracic wing-hinge (two cells) in the Notodontidae only. By mapping cell numbers onto current phylogenies
of the Macrolepidoptera, we demonstrate that the three-celled wing-hinge chordotonal organ, believed to be a wing proprioceptor,
represents the plesiomorphic state from which the tympanal organ in the Noctuoidea evolved. This ’trend toward simplicity’
in the noctuoid ear contrasts an apparent ’trend toward complexity’ in several other insect hearing organs where atympanate
homologues have been studied. The advantages to having fewer rather than more cells in the moth ear, which functions primarily
to detect the echolocation calls of bats, is discussed.
Adult tiger moths exhibit a wide range of palatabilities to the insectivorous big brown bat Eptesicus fuscus. Much of this variation is due to plant allelochemics ingested and sequestered from their larval food. By using a comparative approach involving 15 species from six tribes and two subfamilies of the Arctiidae we have shown that tiger moths feeding on cardiac glycoside-containing plants often contain highly effective natural feeding deterrents. Feeding on pyrrolizidine alkaloid-containing plants is also an effective deterrent to predation by bats but less so than feeding on plants rich in cardiac glycosides. Moths feeding on plants containing iridoid glycosides and/or moths likely to contain biogenic amines were the least deterrent. By manipulating the diet of several tiger moth species we were able to adjust their degree of palatability and link it to the levels of cardiac glycosides or pyrrolizidine alkaloids in their food. We argue that intense selective pressure provided by vertebrate predators including bats has driven the tiger moths to sequester more and more potent deterrents against them and to acquire a suite of morphology characteristics and behaviors that advertise their noxious taste.
Two big brown bats (Eptesicus fuscus) were trained to report the presence or absence of a virtual sonar target. The bats' sensitivity to transient masking was investigated by adding 5 ms pulses of white noise delayed from 0 to 16 ms relative to the target echo. When signal and masker occurred simultaneously, the bats required a signal energy to noise spectrum level ratio of 35 dB for 50% probability of detection. When the masker was delayed by 2 ms or more there was no significant masking and echo energy could be reduced by 30 dB for the same probability of detection. The average duration of the most energetic sonar signal of each trial was measured to be 1.7 ms and 2.4 ms for the two bats, but a simple relation between detection performance and pulse duration was not found.
In a different experiment the masking noise pulses coincided with the echo, and the duration of the masker was varied from 2 to 37.5 ms. The duration of the masker had little or no effect on the probability of detection.
The findings are consistent with an aural integration time constant of about 2 ms, which is comparable to the duration of the cries. This is an order of magnitude less than found in backward masking experiments with humans and may be an adaptation to the special constraints of echolocation. The short time of sensitivity to masking may indicate that the broad band clicks of arctiid moths produced as a countermeasure to bat predation are unlikely to function by masking the echo of the moth.
Sound-producing moths have evolved a range of mechanisms to emit loud conspicuous ultrasounds directed toward mates, competitors and predators. We recently discovered a novel mechanism of sound production, i.e., stridulation of specialized scales on the wing and thorax, in the Asian corn borer moth, Ostrinia furnacalis, the male of which produces ultrasonic courtship songs in close proximity to a female (<2 cm). The signal is very quiet, being exclusively adapted for private communication. A quiet signal is advantageous in that it prevents eavesdropping by competitors and/or predators. We argue that communication via quiet ultrasound, which has not been reported previously, is probably common in moths and other insects.
Ecology Letters (2010) 13: 744–753
Many animals use bright colouration to advertise their toxicity to predators. It is now well established that both toxicity and colouration are often variable within prey populations, yet it is an open question whether or not brighter signals should be used by the more toxic members of the population. We therefore describe a model in which signal honesty can easily be explained. We assumed that prey toxicity is environmentally conferred and variable between individuals, and that signalling bears a cost through attracting the attention of predators. A key assumption is that predators know the mean toxicity associated with each signalling level, so that the probability of attack for each signal value declines as mean toxicity associated with that signal increases. The probability of death given attack for each individual, however, declines with the precise value of its own toxicity, and prey must evolve the optimal level of signal to match the toxicity level that they acquire from their environments. At the start of our simulations there is no signalling system, as neither prey nor predators have biases that favour signal diversification. Over evolutionary time, however, a positive correlation emerges between signal strength and the mean toxicity associated with each signal level. When stability is reached, predators change their behaviour so that they now tend to avoid prey that signal conspicuously. In addition to predicting within-species signal reliability, our model can explain the initial evolution of aposematic displays without the need to assume special biases in predators.
Neotropical katydids (Orthoptera: Tettigoniidae) are preyed on by gleaning bats, which are known to use male calling songs to locate them. At least one katydid species has been reported to stop singing in response to bat echolocation calls. To investigate the relationship between this behavioural defence and ecological and sensory factors, we surveyed calling song characteristics, song cessation in response to the echolocation calls of a sympatric gleaning bat (Trachops cirrhosus), and T-cell responses (an auditory interneuron sensitive to ultrasound) in five katydid species from Panamá. The two katydid species that stopped singing in response to bat calls (Balboa tibialis and Ischnomela gracilis, Pseudophyllinae) also had the highest T-cell spike number and rate in response to these stimuli. The third pseudophylline species (Docidocercus gigliotosi) did not reliably cease singing and had low T-cell spiking activity. Neoconocephalus affinis (Copiphorinae) produced continuous calling song, possibly preventing males from hearing the bat during singing, and did not show a behavioural response despite high T-cell activity in response to bat calls. Steirodon rufolineatum (Phaneropterinae) did not cease singing and differed in T-cell activity compared to the other species. T-cell function might not be conserved in katydids, and evidence for this idea is discussed.
Theories of aposematism often focus on the idea that warning displays evolve because they work as effective signals to predators. Here, we argue that aposematism may instead evolve because, by enhancing protection, it enables animals to become more exposed and thereby gain resource-gathering benefits, for example, through a wider foraging niche. Frequency-dependent barriers (caused by enhanced conspicuousness relative to other prey and low levels of predator education) are generally assumed to make the evolution of aposematism particularly challenging. Using a deterministic, evolutionary model we show that aposematic display could evolve relatively easily if it enabled prey to move more freely around their environments, or become exposed in some other manner that provides fitness benefits unrelated to predation risk. Furthermore, the model shows that the traits of aposematic conspicuousness and behavior which lead to raised exposure positively affect each other, so that the optimal level of both tends to increase when the traits exist together, compared to when they exist in isolation. We discuss the ecological and evolutionary consequences of aposematism. One conclusion is that aposematism could be a key evolutionary innovation, because by widening habitat use it may promote adaptive radiation as a byproduct of enhanced ecological opportunity.