Evolutionary escalation: the bat–moth arms race

Hofstede, Hannah M. ter; Ratcliffe, John M.

doi:10.1242/jeb.086686

Cited by 93 publications

(96 citation statements)

References 219 publications

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“…There is convincing evidence that low‐amplitude echolocation prevents detection by eared insects and that it evolved as an adaptation to prey hearing (Corcoran & Conner, ; Goerlitz et al., ; ter Hofstede & Ratcliffe, ). However, several species in the barbastelles’ sister taxon Corynorhinus (Howell, ; Lacki & Ladeur, ) and the closely related genus Plecotus (Dietz, von Helversen, & Nill, ; Waters & Jones, ) forage by gleaning prey from surfaces in cluttered habitats.…”

Section: Discussionmentioning

confidence: 99%

“…Yet, the bats’ echolocation has one major drawback: it is an active sensory mechanism (Nelson & MacIver, ) that – in contrast to ‘passive’ senses like vision or passive hearing – gives away the bat's presence. This characteristic and the substantial selection pressure posed by insectivorous echolocating bats led to the evolution of ultrasound‐sensitive ears and auditory‐evoked avoidance behaviours in at least six insect orders (ter Hofstede & Ratcliffe, ). Within the order of moths (Lepidoptera) alone, ears have evolved at least six times independently in direct response to the selection pressure by bats (Jacobs & Bastian, ; ter Hofstede & Ratcliffe, ).…”

Section: Introductionmentioning

confidence: 99%

“…Yet, the bats' echolocation has one major drawback: it is an active sensory mechanism (Nelson & MacIver, 2006) that -in contrast to 'passive' senses like vision or passive hearing -gives away the bat's presence. This characteristic and the substantial selection pressure posed by insectivorous echolocating bats led to the evolution of ultrasound-sensitive ears and auditory-evoked avoidance behaviours in at least six insect orders (ter Hofstede & Ratcliffe, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Continued source level reduction during attack in the low‐amplitude bat Barbastella barbastellus prevents moth evasive flight

Lewanzik

Goerlitz

2018

Functional Ecology

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Ears evolved independently in many insect taxa due to the selection pressure of echolocating bats. Eared moths perform evasive flight manoeuvres upon hearing approaching bats, thereby substantially increasing survival probability. Accordingly, eared moths constitute only a minor portion of many bats’ diets. In contrast, the barbastelle bat Barbastella barbastellus almost exclusively feeds on eared moths by emitting low‐amplitude stealth echolocation calls that are undetectable by distant moths. While closing in on the prey, however, the calls might become audible. We thus hypothesised that barbastelle bats lower the source level of their calls even further while closing in, such that the level at the moth's ear remains below the moth's hearing threshold and the moth fails to elicit its evasive manoeuvre. We tested these hypotheses by offering tethered moths to barbastelle bats in the wild and in captivity. We reconstructed the bats’ three‐dimensional flight paths based on time‐of‐arrival differences of the echolocation calls at four microphones, measured the received sound levels at the moth's position with an additional miniature microphone, and calculated call source levels. We show that barbastelle bats continuously reduced source level upon detecting a moth, thereby delaying the time and shortening the distance when the moth might detect the bat. The received level at the targeted moth never exceeded the moth's neuronal hearing threshold by more than 10 dB, which is likely sufficiently low to prevent moth evasive flight. Barbastelle bats emit low‐amplitude calls to counter moth hearing. Continued amplitude reduction during an attack extends the time before the prey becomes aware of the predator, if at all. In combination, these two strategies allowed barbastelle bats to access a food resource which is largely unavailable to competing species, thereby probably altering competition between sympatric predators. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13073/suppinfo is available for this article.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Continued source level reduction during attack in the low‐amplitude bat Barbastella barbastellus prevents moth evasive flight

Lewanzik

Goerlitz

2018

Functional Ecology

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“…We defined families Sphingidae, Noctuidae, Notodontidae, Geometridae and Pyralidae as eared moths, as they are known to have tympanate organs used for predator avoidance (ter Hofstede & Ratcliffe, ). We were unable to quantify abundance of prey items given variation in insect DNA degradation as it passes through a bats intestinal tract and differences in PCR amplification.…”

Section: Methodsmentioning

confidence: 99%

Illuminating prey selection in an insectivorous bat community exposed to artificial light at night

Cravens

Brown

Divoll

et al. 2017

Journal of Applied Ecology

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Light pollution has been increasing around the globe and threatens to disturb natural rhythms of wildlife species. Artificial light impacts the behaviour of insectivorous bats in numerous ways, including foraging behaviour, which may in turn lead to altered prey selection. In a manipulative field experiment, we collected faecal samples from six species of insectivorous bats in naturally dark and artificially lit conditions, and identified prey items using molecular methods to investigate effects of light pollution on prey selection. Proportional differences in identified prey were not consistent and appeared to be species specific. Red bats, little brown bats and grey bats exhibited expected increases in moths at lit sites. Beetle‐specialist big brown bats had a sizeable increase in beetle consumption around lights, while tri‐coloured bats and evening bats showed little change in moth consumption between experimental conditions. Dietary overlap was high between experimental conditions within each species, and dietary breadth only changed significantly between experimental conditions in one species, the little brown bat. Policy implications. Our results, building on others, demonstrate that bat–insect interactions may be more nuanced than the common assertion that moth consumption increases around lights. They highlight the need for a greater mechanistic understanding of bat–light interactions to predict which species will be most affected by light pollution. Given differences in bat and insect communities, we advocate biologists, land stewards and civil planners work collaboratively to determine lighting solutions that minimize changes in foraging behaviour of species in the local bat community. Such efforts may allow stakeholders to more effectively craft management strategies to minimize unnatural shifts in prey selection caused by artificial lights.

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“…Echolocating bats and eared moths are an ideal study system to address this question. Both groups interact in an evolutionary predator-prey arms race (Ter Hofstede & Ratcliffe, 2016;Rydell, Jones, & Waters, 1995;Waters, 2003). Many insectivorous bats have a broad, overlapping diet consisting of many different species of moths and other nocturnal insects (Anthony & Kunz, 1977;Bogdanowicz, Fenton, & Daleszczyk, 1999;Findley & Black, 1983;Gordon et al, 2019), which they hunt by echolocation in mid-air (Denzinger & Schnitzler, 2013;Fenton, Portfors, Rautenbach, & Waterman, 1998).…”

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confidence: 99%

Species‐specific strategies increase unpredictability of escape flight in eared moths

Hügel

Goerlitz

2019

Functional Ecology

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Many prey species overlap in time and space and are hunted by the same predators. A common anti‐predator behaviour is using evasive manoeuvres to escape an attacking predator. The escape‐tactic diversity hypothesis postulates that species‐specific differences in evasive behaviour will increase the overall unpredictability experienced by predators within a predator–prey community. Evolutionary, escape‐tactic diversity would be driven by the enhanced predator protection for each prey individual in the community. However, escape‐tactic diversity could also be a functional consequence of morphological differences that correlate with evasive capabilities. Echolocating bats and eared moths are a textbook example of predator–prey interactions. Moths exhibit evasive flight with diverse tactics; however, the variability of their evasive flight within and between species and individuals has never been quantified systematically. In addition, moth species show variation in size, which correlates with their flight capability. We recorded flight strength during tethered flight of eight sympatric moth species in response to the same level of simulated bat predation. Our method allowed us to record kinematic parameters that are correlated with evasive flight in a controlled way to investigate species‐specific differences in escape tactics. We show species‐specific and size‐independent differences in both overall flight strength and change of flight strength over time, supporting the escape‐tactic diversity hypothesis for eared moths. Additionally, we show strong interindividual differences in evasive flight within some species. This diversity in escape tactic between eared moths increases the overall unpredictability of evasive flight experienced by bat predators, likely providing increased protection against predatory bats for the single individual.

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Evolutionary escalation: the bat–moth arms race

Cited by 93 publications

References 219 publications

Continued source level reduction during attack in the low‐amplitude bat Barbastella barbastellus prevents moth evasive flight

Continued source level reduction during attack in the low‐amplitude bat Barbastella barbastellus prevents moth evasive flight

Illuminating prey selection in an insectivorous bat community exposed to artificial light at night

Species‐specific strategies increase unpredictability of escape flight in eared moths

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