Hindwings are unnecessary for flight but essential for execution of normal evasive flight in Lepidoptera

Jantzen, Benjamin C.; Eisner, Thomas

doi:10.1073/pnas.0807223105

Cited by 110 publications

(99 citation statements)

References 21 publications

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“…Although a phylogenetic study with increased sampling focusing on these tailed clades is needed to support this conclusion, we note forewing damage in 8% (n = 87) of bat-luna moth interactions. It would be informative to look broadly across the Saturniidae and assess both the rates of damage to critical flight infrastructure (17) and bat capture rates of moths with longer (e.g., Copiopteryx, >100 mm) and shorter (e.g., Arsenura, <10 mm) tails than luna moths (average 37.5 mm).…”

Section: Resultsmentioning

confidence: 99%

Moth tails divert bat attack: Evolution of acoustic deflection

Barber

Leavell

Keener

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Adaptations to divert the attacks of visually guided predators have evolved repeatedly in animals. Using high-speed infrared videography, we show that luna moths (Actias luna) generate an acoustic diversion with spinning hindwing tails to deflect echolocating bat attacks away from their body and toward these nonessential appendages. We pit luna moths against big brown bats (Eptesicus fuscus) and demonstrate a survival advantage of ∼47% for moths with tails versus those that had their tails removed. The benefit of hindwing tails is equivalent to the advantage conferred to moths by bat-detecting ears. Moth tails lured bat attacks to these wing regions during 55% of interactions between bats and intact luna moths. We analyzed flight kinematics of moths with and without hindwing tails and suggest that tails have a minimal role in flight performance. Using a robust phylogeny, we find that long spatulate tails have independently evolved four times in saturniid moths, further supporting the selective advantage of this anti-bat strategy. Diversionary tactics are perhaps more common than appreciated in predator-prey interactions. Our finding suggests that focusing on the sensory ecologies of key predators will reveal such countermeasures in prey.antipredator defense | bat-moth interactions | Lepidoptera | Saturniidae P redators are under pressure to perform incapacitating initial strikes to thwart prey escape. It is thought that prey, in turn, have evolved conspicuous colors or markings to deflect predator attack to less vulnerable body regions (1, 2). Eyespots are a wellknown class of proposed deflection marks (3), which are found in a variety of taxa, including Lepidoptera (3) and fishes (4), but only recently have experiments convincingly demonstrated that these color patterns redirect predatory assault. Eyespots on artificial butterfly (5) and fish (4) prey draw strikes of avian and fish predators. Eyespots on the wing margins of woodland brown butterflies (Lopinga achine) lure the attacks of blue tits (Cyanistes caeruleus) (6). Brightly colored lizard tails also divert avian predator attacks to this expendable body region (7).Deflection coloration is unlikely to be an effective strategy against echolocating bats, as these predators have scotopic vision and poor visual acuity unsuited for prey localization and discrimination (8). Most bats rely on echoes from their sonar cries to image prey and other objects in their environment-they live in an auditory world (9). Thus, we would expect a deflection strategy, effective against bats, to present diversionary acoustic signatures to these hearing specialists. Weeks (10) proposed that saturniid hindwing tails might serve to divert bat attacks from essential body parts. We hypothesized that saturniid tails, spinning behind a flying moth (Movie S1) and reflecting sonar calls, serve as either a highly contrasting component of the primary echoic target or as an alternative target. We predicted that bats would aim their attacks at moth tails, instead of the wings or body, durin...

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Section: Resultsmentioning

confidence: 99%

Moth tails divert bat attack: Evolution of acoustic deflection

Barber

Leavell

Keener

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Several studies have quantified the escape performance of flying insects but this behavior is usually motivated by artificial or atypical stimuli (e.g. Yager and May, 1990;Srygley and Kingsolver, 2000;Almbro and Kullberg, 2008;Jantzen and Eisner, 2008;Combes et al, 2010), or rarely by a trained predator in pursuit (Srygley and Dudley, 1993). The flight performance of a predator and prey each flying alone under laboratory conditions has been compared (McLachlan et al, 2003), and the flight paths of predators and their prey have been reconstructed to assess interception strategy (Olberg et al, 2000;Ghose et al, 2006;Ghose et al, 2009) but studies of the simultaneous flight mechanics of both participants during natural predatory encounters are virtually non-existent.…”

Section: Introductionmentioning

confidence: 99%

Linking biomechanics and ecology through predator–prey interactions: flight performance of dragonflies and their prey

Combes

Rundle

Iwasaki

et al. 2012

Journal of Experimental Biology

136

141

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SummaryAerial predation is a highly complex, three-dimensional flight behavior that affects the individual fitness and population dynamics of both predator and prey. Most studies of predation adopt either an ecological approach in which capture or survival rates are quantified, or a biomechanical approach in which the physical interaction is studied in detail. In the present study, we show that combining these two approaches provides insight into the interaction between hunting dragonflies (Libellula cyanea) and their prey (Drosophila melanogaster) that neither type of study can provide on its own. We performed >2500 predation trials on nine dragonflies housed in an outdoor artificial habitat to identify sources of variability in capture success, and analyzed simultaneous predator-prey flight kinematics from 50 high-speed videos. The ecological approach revealed that capture success is affected by light intensity in some individuals but that prey density explains most of the variability in success rate. The biomechanical approach revealed that fruit flies rarely respond to approaching dragonflies with evasive maneuvers, and are rarely successful when they do. However, flies perform random turns during flight, whose characteristics differ between individuals, and these routine, erratic turns are responsible for more failed predation attempts than evasive maneuvers. By combining the two approaches, we were able to determine that the flies pursued by dragonflies when prey density is low fly more erratically, and that dragonflies are less successful at capturing them. This highlights the importance of considering the behavior of both participants, as well as their biomechanics and ecology, in developing a more integrative understanding of organismal interactions.

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“…Many studies have used wing wear to estimate relative insect age (Mueller and Wolf-Mueller, 1993;Kemp, 2000;Burkhard et al, 2002;Richards, 2003;Inoue and Endo, 2006;Peixoto and Benson, 2008). Wing wear has consequences, which include increased wingbeat frequency (Hargrove, 1975;Kingsolver, 1999;Hedenstrom et al, 2001), changed flight speed (Fischer and Kutsch, 2002), changed flight performance (Haas and Cartar, 2008;Jantzen and Eisner, 2008;Combes et al, 2010), changed foraging behaviour (Higginson and Barnard, 2004;Foster and Cartar, 2011) and increased risk of mortality (Cartar, 1992).…”

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confidence: 99%

What causes wing wear in foraging bumble bees?

Foster

Cartar

2011

Journal of Experimental Biology

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Organisms undergo wear and tear of their bodies as they age, as illustrated by tooth erosion, hearing loss, appendage loss and ovipositor wear (reviewed by Finch, 1990;Lalonde and Mangel, 1994). An example common to many flying insects is wing wear. Insects have no mechanism to repair damage to their wings; therefore, as an insect ages and continues to use its wings, the amount of wing wear is cumulative and progressive (Alcock, 1996;Eltz et al., 1999;Hayes and Wall, 1999;Burkhard et al., 2002;Higginson and Barnard, 2004;Lopez-Uribe et al., 2008). Many studies have used wing wear to estimate relative insect age (Mueller and Wolf-Mueller, 1993;Kemp, 2000;Burkhard et al., 2002;Richards, 2003;Inoue and Endo, 2006;Peixoto and Benson, 2008). Wing wear has consequences, which include increased wingbeat frequency (Hargrove, 1975;Kingsolver, 1999;Hedenstrom et al., 2001), changed flight speed (Fischer and Kutsch, 2002), changed flight performance (Haas and Cartar, 2008;Jantzen and Eisner, 2008;Combes et al., 2010), changed foraging behaviour (Higginson and Barnard, 2004;Foster and Cartar, 2011) and increased risk of mortality (Cartar, 1992).Many eusocial insects, particularly bees and wasps, rely on their wings to defend their nest from predators (Breed et al., 1990;Kastberger et al., 2009), maintain colony temperature and assure proper larval development (Heinrich, 1979a;O'Donnell and Foster, 2001), and acquire food for themselves and their colony (Heinrich, 1979a). Providing protection, care and food for the colony's young are the ways in which a non-reproductive forager increases its inclusive fitness. Therefore, wing wear may have important consequences for both individual and colony fitness.Risk of mortality in worker bumble bees (Bombus spp.) increases with age (Brian, 1952;Garofalo, 1978;Rodd et al., 1980;Goldblatt and Fell, 1987;Smeets and Duchateau, 2003), as it does in honey bees (Apis mellifera) (Dukas, 2008). Wing wear has been speculated to lead to an increased risk of mortality in honey bee drones (Rueppell et al., 2005) and tsetse flies (Glossina morsitans) (Allsopp, 1985). Bumble bees that either were wing-clipped or had high naturally occurring amounts of wear died earlier than did those with more pristine wings (Cartar, 1992). An increase in mortality risk with wing wear could result from a number of factors, all of which are supported only by speculation: decreased manoeuvrability, making it more difficult for a bee to escape from predators or severe weather conditions (Rodd et al., 1980), increased energy expenditure (Cartar, 1992) (but see Hedenstrom et al., 2001) and/or increased wingbeat frequency, which matters if the number of wingbeats is limited over a lifespan (Higginson and Gilbert, 2004). Regardless of how wing wear is linked with lifespan, the causes of wing wear have yet to be formally investigated in any insect.Wing wear is associated with male intra-sexual competition (Alcock, 1996), mating attempts (Ragland and Sohal, 1973), failed predator attacks (Robbins, 1981) and foraging activity...

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Hindwings are unnecessary for flight but essential for execution of normal evasive flight in Lepidoptera

Cited by 110 publications

References 21 publications

Moth tails divert bat attack: Evolution of acoustic deflection

Moth tails divert bat attack: Evolution of acoustic deflection

Linking biomechanics and ecology through predator–prey interactions: flight performance of dragonflies and their prey

What causes wing wear in foraging bumble bees?

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