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Moth Tails Divert Bat Attack: Evolution of Acoustic Deflection

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Moth Tails Divert Bat Attack: Evolution of Acoustic Deflection Moth tails divert bat attack: Evolution of acoustic deflection Jesse R. Barbera,1, Brian C. Leavella, Adam L. Keenera, Jesse W. Breinholtb, Brad A. Chadwellc, Christopher J. W. McClurea,d, Geena M. Hillb, and Akito Y. Kawaharab,1 aDepartment of Biological Sciences, Boise State University, Boise, ID 83725; bFlorida Museum of Natural History, McGuire Center for Lepidoptera and Biodiversity, University of Florida, Gainesville, FL 32611; cDepartment of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, OH 44272; and dPeregrine Fund, Boise, ID 83709 Edited by May R. Berenbaum, University of Illinois at Urbana-Champaign, Urbana, IL, and approved January 28, 2015 (received for review November 15, 2014) Adaptations to divert the attacks of visually guided predators the individuals that were tested. Interactions took place under have evolved repeatedly in animals. Using high-speed infrared darkness in a sound-attenuated flight room. We recorded each videography, we show that luna moths (Actias luna) generate an engagement with infrared-sensitive high-speed cameras and ul- acoustic diversion with spinning hindwing tails to deflect echolo- trasonic microphones. To constrain the moths’ flight to a ∼1m2 cating bat attacks away from their body and toward these non- area surveyed by the high-speed cameras, we tethered luna moths essential appendages. We pit luna moths against big brown bats from the ceiling with a monofilament line. (Eptesicus fuscus) and demonstrate a survival advantage of ∼47% for moths with tails versus those that had their tails removed. The Results and Discussion benefit of hindwing tails is equivalent to the advantage conferred Bats captured 34.5% (number of moths presented; n = 87) of to moths by bat-detecting ears. Moth tails lured bat attacks to tailed luna moths, and 81.3% (n = 75) of moths without tails these wing regions during 55% of interactions between bats and were caught—a 46.8% survival advantage for hindwing tails (Fig. intact luna moths. We analyzed flight kinematics of moths with 1). Mixed-effects logistic regression revealed a moth without tails and without hindwing tails and suggest that tails have a minimal is 8.7 times [confidence interval (CI) = 2.1–35.3] more likely to role in flight performance. Using a robust phylogeny, we find that be captured than a moth with tails. During each foraging session, long spatulate tails have independently evolved four times in sa- we presented a bat with one intact luna moth, one luna moth turniid moths, further supporting the selective advantage of this with its tails ablated, and 1–2 pyralid moths as controls. Control anti-bat strategy. Diversionary tactics are perhaps more common moths were captured 97.5% (n = 136) of the time. The adult big than appreciated in predator–prey interactions. Our finding sug- brown bats (Eptesicus fuscus) used in these experiments are not gests that focusing on the sensory ecologies of key predators will sympatric with tailed saturniid moths and are thus naive to this reveal such countermeasures in prey. anti-bat strategy. Initial mixed-effects logistic regression analysis indicated that the number of nights bats hunted luna moths was antipredator defense | bat–moth interactions | Lepidoptera | Saturniidae not correlated with capture success (P = 0.42); bats did not learn to circumvent this defense over time. In addition, bats did not redators are under pressure to perform incapacitating initial alter their sonar cries with experience or prey type (Fig. S1). Pstrikes to thwart prey escape. It is thought that prey, in turn, To determine if moths with intact tails lured bat attacks, we have evolved conspicuous colors or markings to deflect predator determined where on the moths’ bodies the bats aimed their attack to less vulnerable body regions (1, 2). Eyespots are a well- known class of proposed deflection marks (3), which are found in Significance a variety of taxa, including Lepidoptera (3) and fishes (4), but only recently have experiments convincingly demonstrated that Bats and moths have been engaged in acoustic warfare these color patterns redirect predatory assault. Eyespots on ar- for more than 60 million y. Yet almost half of moth species tificial butterfly (5) and fish (4) prey draw strikes of avian and lack bat-detecting ears and still face intense bat predation. fish predators. Eyespots on the wing margins of woodland brown We hypothesized that the long tails of one group of seem- butterflies (Lopinga achine) lure the attacks of blue tits (Cya- ingly defenseless moths, saturniids, are an anti-bat strategy nistes caeruleus) (6). Brightly colored lizard tails also divert avian designed to divert bat attacks. Using high-speed infrared vid- predator attacks to this expendable body region (7). eography, we show that the spinning hindwing tails of luna Deflection coloration is unlikely to be an effective strategy moths lure echolocating bat attacks to these nonessential against echolocating bats, as these predators have scotopic vision appendages in over half of bat–moth interactions. Further we and poor visual acuity unsuited for prey localization and dis- show that long hindwing tails have independently evolved crimination (8). Most bats rely on echoes from their sonar cries multiple times in saturniid moths. This finding expands our to image prey and other objects in their environment—they live knowledge of antipredator deflection strategies, the limi- in an auditory world (9). Thus, we would expect a deflection tations of bat sonar, and the extent of a long-standing evolu- strategy, effective against bats, to present diversionary acoustic tionary arms race. signatures to these hearing specialists. Weeks (10) proposed that saturniid hindwing tails might serve to divert bat attacks from Author contributions: J.R.B. and A.Y.K. designed research; J.R.B., B.C.L., A.L.K., J.W.B., G.M.H., and A.Y.K. performed research; J.R.B., B.C.L., A.L.K., J.W.B., B.A.C., C.J.W.M., essential body parts. We hypothesized that saturniid tails, spin- G.M.H., and A.Y.K. analyzed data; and J.R.B. wrote the paper. ning behind a flying moth (Movie S1) and reflecting sonar calls, The authors declare no conflict of interest. serve as either a highly contrasting component of the primary This article is a PNAS Direct Submission. echoic target or as an alternative target. We predicted that bats Data deposition: The data reported in this paper have been deposited in the Dryad Data would aim their attacks at moth tails, instead of the wings or Repository, datadryad.org (accession no. 0vn84). body, during a substantial percentage of interactions. To test this 1To whom correspondence may be addressed. Email: [email protected] or prediction, we pit eight big brown bats against luna moths with [email protected]. and without hindwing tails. To control for handling, we restrained This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. each moth similarly and removed tails from approximately half of 1073/pnas.1421926112/-/DCSupplemental. 2812–2816 | PNAS | March 3, 2015 | vol. 112 | no. 9 www.pnas.org/cgi/doi/10.1073/pnas.1421926112 Downloaded by guest on September 25, 2021 evidence indicates bats that emit FM sonar might do so, using information either within a single echo (14) or across an echo strobe group (15, 16). Regardless, the FM bats in these experi- ments were lured to the echoes of spinning tails. To understand the historical pattern of tail evolution, we measured tail lengths of 113 saturniid moth species and con- structed a phylogeny using maximum likelihood (ML) and Bayesian approaches. Trees from both analyses provided very similar results that are largely congruent (Fig. 2 and Fig. S3). Our Fig. 1. Luna moth tails lure echolocating bat attacks. (A) Percentage of results demonstrate four independent origins of long (>30 mm) moths captured during interactions with big brown bats (E. fuscus). Error hindwing tails with modified spatulate tips in the Saturniidae. bars are binomial 95% CIs. Brackets show P values for comparisons using Tails evolved in the well-supported Actias + Argema + Graellsia mixed-effects logistic regression. (B) Movie frames of a bat biting and re- clade, Copiopteryx, Eudaemonia, and Coscinocera, which are moving the tail of a luna moth (A. luna). placed in disparate tribes and two different saturniid subfamilies. Evidence for a single origin of tails is strongly rejected statistically < strikes. We did so by reviewing three different high-speed camera (SH test, P 0.0001). Examination of the tailed moth clades angles of the interactions. Bats aimed at tails in 55.2% (n = 87) of appears to show tail length increases from tailless or ancestrally interactions with intact moths (Movie S2), slightly more often than shorter tails. Tail length might be increasing under selection from they aimed at the moth’s body (44.8%, n = 87; binomial test, P = bats to move the echoic target created by spinning tails further 0.05; Movie S3). Visual deflection marks are also usually found on from the body and forewings. Although a phylogenetic study with ’ increased sampling focusing on these tailed clades is needed to the posterior of prey animals, which likely draws the predators = attack away from the escape trajectory (1–7). In fact, bats were support this conclusion, we note forewing damage in 8% (n 87) of bat–luna moth interactions. It would be informative to look rarely successful at capturing moths when they aimed at tails broadly across the Saturniidae and assess both the rates of damage (4.2%, n = 48) but showed similar capture success to moths with to critical flight infrastructure (17) and bat capture rates of moths tails removed when they targeted the body (71.8%, n = 39; bi- with longer (e.g., Copiopteryx, >100 mm) and shorter (e.g., Arsenura, nomial test, P = 0.07).
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