Ultrasonic Hide’n’Seek: The Coevolutionary Relationship Between Bats and Moths
Evolutionary Biology| Jarod McTaggart
Moths and their predator, bats, have been locked in an evolutionary arms race for the past 50 million years, making their relationship and adaptations an area of active research. This review presents some of the most recent and exciting discoveries in the space of the moth-bat coevolutionary arms race. While studying this revolutionary race provides insight into the mechanisms behind coevolution, understanding the adaptations that have been developed also provides humans with tools for innovation and conservation.
Evolutionary Arms Race
Evolution, as proposed by Darwin, is defined as “descent with modification”, where populations change over time due to a complex combination of random chance and natural selection. Coevolution has been described as the evolution of two species, where one species’ adaptations are directly and reciprocally affected by the adaptations of the other [1]. While these relationships may be either mutualistic or antagonistic, this review will focus on antagonistic interactions, also known as a co-evolutionary arms race. In these co-evolutionary arms races, each species evolves mechanisms to improve its fitness at the expense of the other. Two key pressures that often drive these arms races are predation and evasion of predation, where predators and prey evolve in tandem, developing ways to counter the other's adaptations. Specifically, this review will highlight what is known about the co-evolutionary arms race between moths and their predator, bats – a relationship spanning millions of years. Moths are believed to have evolved ~300 million years ago during the late Carboniferous period [2], whereas bats appeared 52.5 million years ago [3]. Their co-evolutionary arms race has been studied in depth, with evidence for moth anti-predation adaptations and counters from bats [4]. Much of this research has been focused on echolocation/ultrasound, the primary sensory mode associated with bats that distinguishes them from other moth predators. This indicates that any anti-ultrasound adaptations present in moths have evolved directly in response to bat predation and echolocation.
Moth Anti-Predator Adaptations
Physiological Adaptations
While traditional ideas around camouflage are centred around visual mechanisms, moths have developed acoustic camouflage through structures that dampen and disrupt sonar. The most well-described are thoracic scales, where hair-like scales on the moth's thorax capture and absorb ultrasonic frequencies (20-160 kHz) [5]. These scales are very efficient, being considerably more effective than technical (man-made) fibrous porous absorbers with the same parameters. Furthermore, the scales’ location on the thorax is strategic, as it is the largest and thus most reflective part of the moth. Its multidirectional, broad frequency, and efficient sound absorption structures significantly reduce the detectability of the moth. Scales that act to dampen ultrasound are not confined to the thorax, with another study finding that scale structures on the wings of moths act as sound-absorbing metamaterials [5], [6]. The collection of scale structures works together to absorb a wide range of frequencies associated with bat echolocation while still maintaining aerodynamic requirements for flight.
Another more common physiological anti-bat adaptation found in moths is sound-detecting organs, or ‘ears’. These organs have evolved independently in Lepidoptera (moths and butterflies) at least 10 times, with ears being developed across the body plan of moths, including the head, thorax, abdomen, and wings [7]. However, not every group that has evolved ‘ears’ is sensitive to ultrasound, and there is evidence that these sound-detecting organs have evolved independently of bats, with many moth species producing ultrasound that is associated with mating [8]. This indicates that the ability for moths to hear did not arise as a defence mechanism for bats; instead it has been co-opted to serve a secondary purpose of bat detection. Unlike sound-dampening scales, ears alone do not directly reduce the predation of moths. However, the ability of eared moths to detect bats allows for the development of behavioural adaptations to avoid bat predation.
Behavioural Adaptations
A moth’s ability to detect if they are being pursued by a bat allows them to engage in evasive movements. Moths are able to determine the proximity of a bat, wherein low-intensity and infrequent ultrasound indicates that the bat is far, while high-intensity and frequent ultrasound indicates that the bat is close. Furthermore, since reflected sound needs to first travel back to the bat in order for the bat to detect the moth, moths are able to detect bats before they are detected themselves. Consequently, when low-intensity waves reach moths, they fly in the opposite direction; when moths detect high-intensity waves, they begin evasive manoeuvres, from erratic movements to diving [9]. These evasive movements have proved effective, with moths that initiated such movements being captured only 38% of the time, while moths that did not initiate evasive movements were captured in 98% of encounters [9]. The movements themselves are also important to the survival of the moth, with tighter escape angles (between 40-100°) and higher radial acceleration (the speed at which the moth gains velocity during turn) being associated with more successful evasions [9].
Ultrasonic Frequency Production in Moths
A particularly interesting adaptation that moths have developed to avoid bat predation is ultrasonic frequency production. In a recent study, over 20% of the 252 genera sampled were capable of producing ultrasonic frequencies, indicating that the ability to produce ultrasound is relatively widespread among moths [7]. Furthermore, it is likely that this ability evolved independently several times, as different lineages use different structures to produce these frequencies. Examples include tymbals on their thorax and modified genitals. It is important to note that not all examples of ultrasound production are linked to anti-bat adaptation, as moths are known to use ultrasound in mating [8]. While this ability is likely linked to the early development of ears in moths, it has, like ears, been co-opted in some cases to act as an anti-predation mechanism. There are three dominant theories as to the function of ultrasonic production in moths as an anti-bat mechanism: sonar jamming, aposematic signalling, and startling.
Jamming involves the production of a loud clicking at the same ultrasonic frequency used by bats. Ultrasound as a jamming mechanism is thought to have evolved independently at least six times in moths [7]. The dominant theory as to how ultrasound jamming works is the ranging interference hypothesis, which states that moth clicks decrease the precision in determining target distance, leading to inaccurate strikes and more successful evasions by moths [10]. In a recent study [11], the ultrasonic clicks of a hawkmoth (Cechenena minor) were compared to the calls of its predator, free-flying horseshoe bats (Rhinolophus osgoodi). The spectral signature of both moth clicks and bat-feeding buzzes occupied the same frequency range, as indicated in the red circle in Figure 1b. Furthermore, there was a temporal relationship between the calls: the moth began producing ultrasonic clicks as soon as feeding buzzes were detected, indicating that the bat was locating its target (Figure 1b). This behaviour is consistent with the hypothesis of jamming, as both the spectral and temporal elements of moth clicks align with that of the bats: moths begin clicking at the same frequency and time as when bats begin to locate them.
Figure 1: Examples of echolocation calls of the bat Rhinolophus osgoodi and anti-bat ultrasonic clicks of Cechenena minor (a) and Creatonotos transiens (b). Examples of acoustic interactions between the clicking moths and echolocating bats: (c) C. minor emitted anti-bat clicks immediately after the end of the bat-feeding buzz, (d) C. transiens emitted clicks before the emergence of the bat-feeding buzzes. Adapted from Hu et al. (2023) [11].
Aposematic signalling is another anti-predator mechanism used by moths. Aposematism is a strategy of prey animals to warn potential predators that they have an anti-predator defence [12], which is unpalatability in the case of moths. When a predator attacks an aposematic individual, they encounter the defence and get punished, prompting the predator to learn to avoid that species in the future. This has been tested a number of times; one example is the tiger moth (Creatonotos transiens) [11], which were tested in the same study as hawkmoths. It was found that temporally, as soon as the moth detected bat calls (not just feeding buzzes), it would begin clicking. The spectral analysis revealed no frequency overlap (Figure 1d, red line indicating max frequency achieved by C. transiens compared to calls of R. osgoodi), indicating this was not jamming. When C. transiens was tested for palatability, it was found the species was highly unpatentable, with no bat consuming the entire moth, confirming that it is an honest signal of unpalatability.
New research has indicated that while much of the known ultrasonic production in moths was thought to be active, within micro-Lepidoptera, there are widespread specialised structures on the wings that passively produce ultrasonic frequencies [13]. These structures are present in almost all (10/12) microlepidopteran superfamilies; however, they are not present in the majority of species. These microstructures are not thought to be linked to mating as species that display these structures have not developed ears and thus do not hear the frequencies produced. This is an incredibly interesting discovery as these structures not only developed directly for anti-bat purposes (unlike the origins of other ultrasound production mechanisms), but also act as a passive deterrent to bat predation. It is believed that these structures are a form of passive jamming. Further research on palatability is required to prove the jamming hypothesis or explore a secondary reason for these microstructures.
Bat Adaptations
Bats rely on ultrasound to find prey; however, moths can hide from predators using their environment to camouflage acoustically. New evidence suggests that bats are able to use leaves as specular reflectors to detect acoustically hidden prey [14]. By flying in at oblique angles, bats can detect prey on leaves, where they would usually be acoustically camouflaged due to the different reflective properties of leaves and the angle of sonic reflection. In addition to using leaves as reflective mediums, bats also use water to amplify signals from prey. Due to the multiple reflections of the sound waves off prey and the water, bats can easily locate prey items when hunting above bodies of water [15]. Bats utilise their environment to counter moth behaviour, with Daubenton’s bats (Myotis daubentonii) choosing to hunt within 30cm above ponds [16]. The bat benefits from reflectance; however, it also exploits moths' evasive behaviour, particularly diving. In this case, moths dive and fall into the water, becoming trapped by the surface tension, at which point the bats are able to locate and skim the moth from the surface of the water. Further, it was determined that environmental factors such as the stillness of the lake and floating debris influence the lake choice, with still and clear lakes providing less disturbance, making it easier to locate submerged moths [17].
Bats have also evolved a defence against moth ultrasonic production, specifically against sonar jamming moths. Big brown bats (Eptesicus fuscus) have been observed lengthening the duty cycle of their terminal feeding buzzes to compensate for moth ultrasound jamming [18]. This allows for the bat terminal buzz to outlast the moth response click, circumnavigating the jamming and leading to higher capture rates. Another example of bats adapting their call structure to compensate for moth behavioural adaptations is ‘whispering’ bats [19]. Townend’s big-eared bat (Corynorhinus townsendii) is one such species that displays this behaviour, producing calls that are quieter than other bat species' calls, at approximately 93.6 dB compared to the average 138-226 dB of other bats [20]. Notably, this volume is below the known threshold of moth species, making the calls undetectable, and not initiating anti-bat behaviours in prey. However, this reduces the radius in which they can detect prey, creating a tradeoff between wide detection and stealth. This tradeoff may also explain why ‘whispering’ behaviour is not widespread.
Another strategy is for bats to use acoustic cues made by prey rather than feeding buzzes to capture them [21]. At least five species have been observed using prey acoustic cues instead of their own ultrasonic sonar. While these strategies are limited by the fact that they are not as precise, have far less range than sonar, and do not work well with fast-moving prey, they are a response to moth behavioural strategies.
Discussion
Recently, several studies have focused on leveraging moth responses to ultrasonic stimuli. The dominant use of this technology would be in the agricultural sector, where ultrasonic emitters would be deployed to repel pest moth species [22], [23]. Should this technology prove effective, it could potentially decrease the reliance on pesticides for managing certain moth pests, thereby positively impacting the surrounding ecological communities [24]. While this is not a silver bullet, as not all moths are capable of hearing ultrasound, it has shown potential for effectively repelling eared moths from crops.
Humans may also take inspiration from these adaptations, with sound-dampening scales providing a biological example of soundproofing/noise dissipation. Sound pollution is a significant problem in contemporary times, with negative ecological and human impacts [25]. Any technology that is able to dissipate anthropogenic sound may prove helpful, especially for industries that produce harmful levels of sound or in cases where legislative sound limits are implemented. Furthermore, the development of soundproofing materials has the potential to benefit other sectors, such as the music or acoustics industries. The demonstration that moth scales are metamaterials capable of absorbing a wide range of sound frequencies allows for further research into how similar artificial structures may be developed.
Both bats and moths have essential ecological roles, each group providing ecosystem services that are beneficial to humans (Box 1). For instance, bats are a biological pest control measure, providing insect pest control in agricultural and forestry industries [26-28]. Moths also offer ecosystem services, such as a food source for various organisms that we eat, night pollinators, and even bioindicators [29]. Therefore, it is important to understand the relationships and pressures they have on each other and the rest of the environment.
Conclusion
Moths and bats are locked in a co-evolutionary arms race, each evolving unique and interesting adaptations to counter the other's strategies. In the ~50 million years since the emergence of bats, moths have developed a diverse range of anti-predator adaptations to evade capture by bats. Most of these strategies are related to ultrasound and sonar of bats, ranging from acoustic crypsis through behaviour and physiological adaptations, like sound absorbing scales. Moths utilise pre-existing hearing structures to increase their detection of bats and develop bat-avoidant behaviour. Ultrasound production is used actively for aposematic signalling, as well as passively for sonar jamming. Bats have countered a number of these adaptations with their own, mainly behavioural adaptations that work to detect moths despite their defensive behaviours. Their altered acoustic behaviour either increases the duty cycle of feeding buzzes, utilises whispers, or entirely shifts to using prey auditory cues instead of sonar. Bats also use the environment around them to circumvent evasive moth behaviours, using reflective surfaces to detect acoustically camouflaged moths and exploiting avoidant behaviour. This evolutionary relationship between predator and prey has led to a number of adaptations, illustrating how species develop in response to each other. By understanding these adaptations, we can develop new technologies with biological innovation or leverage behaviour for biosecurity. Both bats and moths are incredibly important to human existence. Understanding their biological and evolutionary relationships allows for continued conservation of these vital groups.
The concept of ecosystem services is a framework for understanding how species and ecosystems provide for humans, and it underscores the importance of biodiversity to human life. Ecosystem services are categorised as the following:
1) Provisioning services, eg. food/fiber production, biocontrol and habitat indicators.
2) Regulating services, eg. nutrient cycling, pollination/seed dispersal and water flow/treatment.
3) Supporting services, eg. habitat creation, oxygen production and soil formation.
4) Cultural services, eg. heritage, knowledge systems and spirituality.
Box 1: Explanation of ecosystem services as well as examples of the types of services both moths and bats may provide [30].
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Jarod is a Masters student researching the behavioural effects that ultrasonic devices to be used in agricultural systems have on native bats and pest moth species. He is passionate about conservation in New Zealand, wanting to contribute to the protection of our native species. Jarod also holds a BA in Communications/Media, Film and Television, with experience in the film/advertising industry and a hobby for making films. One day, hoping to use these skill sets in tandem to communicate science and make research more broadly available and accessible.