The Coevolution of Bats and Moths: An Evolutionary Arms Race
Written by Ingrid Schoonover on December 6, 2021
The supporting presentation can be found at: Coevolution bats and moth [Presentation PDF]
The reciprocal adaptations observed in interacting species of moths and bats offer a great example for studying the process of coevolution in nature. The term coevolution refers to when two interaction species, such as parasite and host or predator and prey, evolve reciprocal adaptations in response to each other. These reciprocal counteradaptations fluctuate in populations of two interacting species over generations, this never-ending selection for one of the species to outmatch the other and gain the advantage is sometimes an arms race. An evolutionary arms race in the case of predator-prey interactions, describes the selective pressure for anti-predator behaviors to evolve in prey and the pressure for predators to evolve behaviors to catch prey. Moths belong to Lepidoptera, an order of insects that evolved 150 million years ago, long before the emergence of bats. Bats belong to the mammalian order Chiroptera, which evolved 60 to 95 million years ago, and while not all bats are insectivorous, many are, and they feed on moths as well as other insects. If moths and bats are indeed an example of coevolution, then the emergence of bats should have provided predation pressure that selects for bat-avoidance adaptations in moths, and the anti-predator behavior in moths should have selected for counter adaptions in bats.
Echolocation is a trait in bats that evolved once or possibly twice 50 million years ago as an adaption for nocturnal navigation and hunting; insectivorous bats use echolocation to detect, track, and assess prey. The way that echolocation works is by emitting pulses of ultrasonic sound (bats typically call in the 20 to 60 kHz range), and then the soundwave from the ultrasonic pulses bounce off objects and is received by the bat as an echo. There are two types of echolocation in insectivorous bats which differ in terms of the duration of sonar pulses and how they receive and interpret the information carries by the returning echo. In frequency-modulating or low duty cycling (LDC) echolocation the sonar pulses are short and timed between returning echoes, such that the distance to prey is determined by the timed separation between the sonar pulse and the echo. On the other hand, frequency-constant or high duty cycling (HDC) echolocation employs the use of longer duration sonar pulses, which results in an overlap between the calls and echoes. In this case the distance to the prey is determined by the difference between the frequency of the sonar pulse and the frequency of the echo, this phenomenon is termed to doppler shift effect and the difference in the frequency makes it possible for the bats to receive echoes while producing calls.
While echolocation was designed to provide information about prey to the bat predator, this trait has been exploited by moth prey to provide information about how far away the predatory bat is. Thus, many moths have convergently evolved sound-reception systems to be able to detect bat echolocation for the purpose of bat-avoidance. In fact, ear-like organs have evolved from the chordotonal organ at least six times in Lepidoptera in the following families: Sphingidae, Noctuidae, Oesandridae, Notodontidae, Geometridae, Uraniidae, Drepanidae, Pyralidae, and Crambidae. The most common sound reception system in Lepidoptera is the tympanal organ, which is a region of cuticle located on the thorax, abdomen, or wings, that forms a membrane and vibrates in response to sound waves. The tympanal organ contains two to four sensory cells that are specialized to detect the presence and intensity of ultrasonic sounds. The tympanic membrane also contains an inner air sac called the counter tympanic cavity, which is connected to the chordotonal organ which converts the vibrations into neural activity that tells the moth information about the position and movement of the bat. This sound-reception system is observed in the families Noctuidae, Geometridae, and Pyraloidae. On the other hand, the hawkmoths (Sphingoidae) have evolved a unique hearing system called the labial palp.
The evolution of this bat-specialized hearing system in moths is termed the syntonic frequency hypothesis, which states that eared moths have the greatest adaptive benefit when their most sensitive hearing frequency matches the peak frequency of sympatric bat echolocation. The adaptive benefit for moths to hear bats comes from the survival advantage of having increased time to escape, since the moth is able to detect the bat from further away. Support for the syntonic frequency hypothesis comes from the fact that moths with ears have hearing that is specialized to detect bat calls in the frequency of 20 to 60 kHz, and that eared moths are 40% less likely to be eaten by bats than artificially deafened moths. Additionally, there are 3 traits of moth hearing that provide support for this hypothesis. First, sound-receptive systems in moths are insensitive to constant ambient sounds and only sensitive to pulses of high-intensity ultrasound. Secondly, the auditory sensitivity threshold of eared moths appears adapted to the specific calling frequency of the bat species they coexist with. Moths that live in a diverse community of bats with a wide range of hunting calls have ears specialized to hear a wise range of frequencies, whereas moths that live in a community with a low diversity of bats have a narrower hearing frequency. For example, the Hawaiian moth only shares its range with one bat species (Lasiurus cinereus semotus), and it’s hearing frequency is very narrow to only detect the echolocation of this one bat species. Third, secondarily diurnal moth species are deaf or have reduced hearing, and moths that live in areas without endemic bats have thickened tympanal membranes and neural regression resulting in less sensitive hearing or complete deafness. All of this evidence supports the idea that hearing in moths is specialized for the purpose of detecting and avoiding bats.
A counteradaptation exists in some bat species, termed the allotonic frequency hypothesis, which states that bats can maximize the adaptive benefit of their echolocation by calling at very high or very low frequencies that are beyond the hearing range of moth prey, thus allowing the bats to hunt without being detected by calling at an inaudible frequency. Analysis of echolocation call frequency and bat diet has revealed a correlation between the call frequency and the proportion of moths that make up a bat’s diet; the relationship between the frequency of moth consumption and call frequency (kHz) is parabolic, with bat species that call above 60 kHz and below 20 kHz consuming the greatest proportion of moths. In fact, one study found that bats that produce low frequency calls (below 12 kHz) consume 80% moths versus species that call at normal frequencies (20-60 kHz) have a diet that is 5-20% moth. For examples of low frequency calling as an adaption for catching moth prey, there is the spotted bat (Euderma maculatum) with 10 kHz calls and the bulldog bat (Tadarida teniotis) with 11-12 kHz calls. Fecal analysis has confirmed that both species consume more moth prey than would be predicted by moth abundance, which confirms that these moth-specialists avoid detection by moths using low-frequency echolocation and are thus more successful at catching them. Alternatively, the Percival’s trident bat (Cloeotis percivali) provides an example of how high-frequency echolocation can be equally effective, this moth-specialist produces calls above 200 kHz to avoid being detected by moths.
Most bats produce loud high-intensity echolocation calls because they are able to detect prey from further away, but this also means that eared prey can detect the bat from a further distance as well. This has led some bats to evolve quiet low-intensity echolocation, which allows the bats to get closer to eared moths before being detected, giving the moth less time to escape, and thus by using the element of surprise they have a greater chance of catching their moth prey. The significance of this adaptation is shown when comparing two sympatric bat species that both produce calls around 30 kHz, but which differ in terms of the sound intensity of their calls. The insect generalist bat species Nyctalus leisleri uses loud high-frequency echolocation, which is detected by moths when the bats are 30 meters away giving them plenty of time to escape. On the other hand, the moth-specialist species Barbastella barbastellus uses quieter low-intensity echolocation, which is only detected by the moths when the bats are 4 meters away, giving the moths less time to escape.
Random flight behavior is unpredictable in nature and thus difficult for bats to track, so for moths that evolve evasive flight behaviors this can provide a survival advantage during attack by a bat. This has led to the evolution of several evasive flight behaviors in moths, including spiraling, diving, looping, and abrupt changes in flight path. Moths with the most evasive flight behavior escape more often from bats, and the moths that fail to show escape patterns are those that are most likely to be caught. Earless moth species are most likely to display continuous erratic flight, and they are also less likely to fly and more likely to fly close to the ground. Eared moth species will only initiate their erratic flight behavior in response to sounds. For example, pyralid moths will dive to the ground when they hear a bat, whereas noctuids and geometrids will maneuver away from the source of ultrasonic bat calls. Additionally, a study that compared moth activity in the presence and absence of an auditory bat call recording found that moths decrease their flight activity in the presence of bat calls.
Some bats will change their echolocation strategy as a counter adaption to evasive flight, one way is by changing the frequency of their calls in response to erratic movements. For example, the eastern red bat (Lasiurus borealis) which specializes on moths, will produce a long “feeding buzz” at a low frequency sonar, and will also dive to the ground to catch moths. This special type of feeding buzz termed Buzz II is seen in three bat families: Vespertilionidae, Molossidae, and Rhinolophidae. Buzz II refers to a drop in frequency at the end of hunting calls that is used to broaden the reach of the bat’s sonar beam, and hypothetically allows for quicker tracking system that could be beneficial to bats when tracking erratic movements.
Sound defense is another anti-bat adaptation observed in moths to reduce predation, with 21% of moth genera capable of producing ultrasonic noise in response to bat echolocation. It is significant to note that this behavior has evolved independently multiple times in bats and can be produced in one of three ways: tymbal organ, abdominal stridulation, or percussive wing beating. Sound production via the tymbal organ occurs when the surface of the tymbal buckles due to muscle contractions, the muscle contractions produce ultrasonic clicking noises at contraction and relaxation. This method of sound production is common in the tiger moths (Arctinnae). The sphinx or hawk moths (Sphingidae) have a unique type of sound production called abdominal stridulation, in response to auditory playbacks of bat attack sounds they will rub together modified scales on genital valves to produce ultrasonic sounds. Percussive wing beating is seen in some members of the Pyralidae and Noctuidae families, such as the Australian whistling moth (Hecatesia thyridion), in this method of sound production an ultrasonic noise is produced during the wing upbeat as the wings hit together.
There are two adaptive functions for sound production in moths: sonar jamming and acoustic aposematism. These two functions can appear independently or in conjunction for moth species capable of noise production. Sonar jamming works because the ultrasonic sound production disrupts the prey-tracking ability of bat echolocation and provides the moth with more time to escape. Alternatively, sound production can be a form of acoustic aposematism, meaning that the ultrasonic clicks serve as a warning to the bats that signals that the moth is unpalatable due to chemical defense. This unique form of aposematism makes sense considering that moths and bats are nocturnal, and low visibility would make visual signaling ineffective, but acoustic signaling overcomes this problem. For example, the dogbane tiger moth Cycnia tenera and the milkweed tiger moth Euchaetes egle are both unpalatable due to compounds sequestered from plants during their caterpillar stage, and both species produce clicks when they detect a bat to discourage being eaten. Additional support for acoustic aposematism is widespread in the tiger moth family Arctiinae, with tiger moth species that emerge in the summer during peak bat activity can produce defensive sounds, but the tiger moth species that emerge during the spring or other times when bats are less active do not have the ability to produce sounds. Interestingly, the adaptive benefit of acoustic aposematism in moths has also led to the volution of Batesian mimics, with some palatable non-toxic species producing ultrasonic clicks as a way of conferring the benefits of sound defense without the costs of producing toxic defense chemicals.
Some bat species will change their hunting strategy in response to hearing sonar-jamming ultrasonic clicks, usually elongating the duration of their echolocation calls and the interval between pulses to diminish the disruptive effects of the moth’s clicking. Bats will also avoid unpalatable moths (as signaled by ultrasonic clicks), with wild and captive bats being less likely to eat arctiid moths versus non-arctiid moths, and the northern long-eared bat (Myotis septentrionalis) drops 75% of clicking dogbane tiger moths (Cycnia tenera) without harming them.
Since bats are nocturnal hunters, some moth species have modified their activity period to reduce overlap with periods of bat activity, and thus decrease their risk of predation. For example, the Ghost swift moth (Hepialus humuli) will only fly for 30 minutes at dusk, and flies close to cluttered spaces to avoid bats. But bats in turn can also modify their activity period to increase overlap with periods of moth activity. The bat species Eptesicus nilssonii specializes on the ghost swift moth, and thus emerges before dark and uses vision to find its prey.
Moths have also evolved several morphological adaptations that help them reduce their risk of being caught by bats. Some of these adaptations include sound absorbing wings, large body size, and long hindwing tails. Recent research into the structure of scales on moth wings such as for the tiger moth has revealed that moths have a honeycomb-like structure on the scales of their wings that absorb sounds between 50 to 60 kHz, by absorbing echolocating calls instead of deflecting them back towards the bat’s moths are able to reduce their acoustic image, and thus reduces the distance that moths can be spotted by bats. The sound-absorption nature of moth wings confers a survival advantage by making more difficult for bats to detect moths via echolocation. The fact that these types of scales are not seen in butterflies (which are diurnal and not in contact with bats) reinforces the idea that this is a specific adaptation for bat-avoidance in moths. Furthermore, the experimental removal of these scales in moths resulted in decreased sound absorption. Large body size in some moth species may be an additional adaptation for avoiding predation by bats, because insectivorous bats are generally small and limited by mouth gape size, thus are physiologically unable to fit large moths into their moths. Finally, the long hindwing tails seen in the Saturniidae family are likely another adaptation in moths that has been selected for by bat predation. The hindwing tails spin behind the moth in flight, acting as a lure, and reflects sonar calls making the tail the primary echolocation target. This lure encourages the bat to attack the moth further away from their body which increases their chances of survival and escape during attack by bats. Support for this idea comes from experimental data: with experimental elongation of hindwing tails increase moth escape from bats by 25%; and in the case of the luna moth (Actias luna) versus the big brown bat, moths that had their tails removed were 8.7 times more likely to be captured by a bat in comparison to moths with intact tails.
The emergence of bats selected for behaviors and traits in moths that allowed them to avoid detection and capture by bats, which in turn selected for counteradaptations in bats to increase their detection and capture of moths. There is more selective pressure on moth prey than there is on the predator bat because the cost of death (for the moth) is a greater selective pressure than the cost of a missed meal (for the bat). This dynamic, combined with the fact that bats also tend to eat other prey besides moths has led to there being more anti-predator defense adaptions in moths than there are predatory counter offenses in bats. In summary, anti-bat adaptions by moths include: (1) sound-detection systems (syntonic frequency hypothesis), (2) evasive flight behaviors, (3) defensive sound production (acoustic aposematism and sonar jamming), (4) changes in activity pattern, and (5) morphological adaptations. Counter-adaptions by bats include: (1) allotonic frequency hypothesis, (2) quiet calling, (3) ability to change call frequency during approach of prey (Buzz II), and (4) changes in activity pattern.
Bogdanowicz, Wieslaw & Fenton, M. & Daleszczyk, Katarzyna. (1999). The relationships between echolocation calls, morphology and diet in insectivorous bats. Journal of Zoology. 247. 381 - 393. 10.1111/j.1469-7998.1999.tb01001.x.
Diebold, Clarice & Salles, A., and Moss, Cynthia. (2020). Adaptive Echolocation and Flight Behaviors in Bats Can Inspire Technology Innovations for Sonar Tracking and Interception. Sensors, 20(10), 2958; https://doi.org/10.3390/s20102958.
Ratcliffe, John M., "Evolutionary Escalation: The Bat–Moth Arms Race" (2016). Dartmouth Scholarship. 2336. https://digitalcommons.dartmouth.edu/facoa/2336
Waters, Dean. (2003). Bats and moths: what is there left to learn? Physiological Entomology, 28, 237-250.
Barber, Jesse & Kawahara, Akito. (2021). Anti-Bat Ultrasound Production in Moths is Globally and Phylogenetically Widespread. BioRxiv. https://doi.org/10.1101/2021.09.20.460855
Rydell, J., Jones, G., & Waters, D. (1995). Echolocating Bats and Hearing Moths: Who Are the Winners? Oikos, 73(3), 419–424. https://doi.org/10.2307/3545970
Zeng, Jinyao et al. (2011). Moth Wing Scales Slightly Increase the Absorbance of Bat Echolocation Calls. PLoSONE, 6(11): e27190. Doi:10.1371/journal.pone.0027190.