Sexual signaling under predation: attractive moths take the greater risks

Behavioral Ecology The official journal of the ISBE International Society for Behavioral Ecology Behavioral Ecology (2014), 25(2), 409–414. doi:10.1093/beheco/art128 Original Article Sexual signaling under predation: attractive moths take the greater risks Nils Cordes, Leif Engqvist, Tim Schmoll, and Klaus Reinhold Department of Evolutionary Biology, Bielefeld University, Morgenbreede 45, 33615 Bielefeld, Germany Individuals often have to balance the costs of risky behavior against the potential benefits they may gain from it. This trade-off is especially obvious in the interplay between natural and sexual selection because traits for mate attraction may attract predators as well. In the lesser wax moth Achroia grisella, ultrasonic sexual signaling comes with such a risk because calling for mates also attracts predatory bats. Attractive males should behave more cautiously than unattractive males under such circumstances, as they can expect more future mating opportunities and therefore have more to lose (the so-called asset protection principle). Contrary to these predictions, we found that pulse pair rate and peak amplitude, 2 song components attractive to females, correlated negatively with the duration of a silence response which is displayed when courtship song is experimentally overlayed with the search signal of a predator, the greater horseshoe bat. More attractive males thus recommence singing sooner than less attractive males. Although this is not in line with the asset protection principle, we discuss 3 different ways in which these distinct behavioral differences might be explained: 1) attractive males are in better condition and thus can more easily evade predators, 2) attractive signals are costly in terms of reduced life expectancy, and 3) risk-taking may in itself be a sexually selected trait and as such act as an honest signal of male quality. Key words: Achroia grisella, asset protection, attractiveness, consistent behavioral differences, risk-taking. Introduction In most species exhibiting elaborate courtship and sexual signaling, males that are conspicuous enough to attract females often are conspicuous enough to attract predators as well (Zuk and Kolluru 1998). Be it extravagant behavioral displays, bright colors, conspicuous odors, or attractive songs, sexual signaling often increases the risk of being eaten (Ryan et al. 1982; Magnhagen 1991; Acharya and McNeil 1998; Hedrick 2000; Kotiaho 2001), forcing individuals to trade current against future reproduction. Such is the case in males of the lesser wax moth Achroia grisella (Lepidoptera; Pyralidae) (Spangler 1984). Males gather in small leks on foliage or grass at night and attract females with ultrasonic songs. Females choose the individual with the most attractive song from the courting males for mating (Spangler et al. 1984; Jang and Greenfield 1996). Song attractiveness is determined by females based on 3 song traits: pulse pair rate, peak song amplitude, and the asynchrony of wing beat (Jang and Greenfield 1996, 1998). These courtship songs are, however, conspicuous also to echolocating predatory bats, informing them of the presence and position of the prey (Schnitzler and Ostwald 1983). The bat Rhinolophus ferrumequinum, for example, has been shown to attack live wax moths as well as loudspeakers broadcasting A. grisella courtship song (Alem et al. 2011). Male wax Address correspondence to N. Cordes. E-mail: . © The Author 2014. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: moths should therefore be selected to adjust their song in the presence of predators, for example, by ceasing acoustic signaling when they are aware of adjacent bats. Indeed, when signaling wax moths detect the search call of a predatory bat, they respond with a pause from singing (henceforth silence response) (Spangler 1984). Individuals differ repeatably in the length of this silence response, which may last from a few hundred milliseconds to over a minute (Greenfield and Baker 2003; Brunel-Pons et al. 2011; Cordes et al. 2013). There is evidence that males recommence singing sooner if under competition for females than if they sing alone (Brunel-Pons et al. 2011), suggesting that individual males can adjust their silence response to different social environments. The length of the silence response, however, can be considered a measure of risk-taking: Moths which start singing soon after the disturbance face greater risks of being detected by the bat than moths which remain silent for longer (Greenfield and Baker 2003). Taking a risk means jeopardizing one’s assets (Clark 1994). Often these assets can be an individual’s life or the chance for future reproduction. The amount of risks taken should therefore be higher for individuals with low compared with individuals with high residual reproductive value, a concept termed the “asset protection principle” (Clark 1994), which has found support in a number of species (Candolin 1998; Kemp 2002), including A. grisella (Lafaille et al. 2010). Wolf et al. (2007) showed that in theory such differences in asset protection could lead to the evolution of distinct Received 12 August 2013; revised 9 December 2013; accepted 19 December 2013; Advance Access publication 29 January 2014. Behavioral Ecology 410 Methods We used a laboratory population of A. grisella, a short-lived, social parasite of honey bees (Kunike 1930) and reared larvae from different families (i.e., full-sib offspring from 1 pair) at 3 different densities (1, 2, or 6 larvae per 30-ml plastic cup) with ad libitum food to examine the effect of larval density on song quality and correlated behaviors (see Cordes et al. 2013 for detailed information on study populations, rearing methods, and diet). On eclosion, adult moths were weighed, and body mass was measured to the nearest 0.01 mg with a Kern 770 scale (Kern & Sohn GmbH, Balingen, Germany). Experimental setup Adult moths were 24–48 h old when measurements started. Before acoustic measurements, we transferred all males individually into gauze cages (3 cm diameter, 5 cm height) and kept them in shelves covered with insulation foam. To prevent males from hearing the ultrasonic songs of other males during the experiment, we placed the gauze cages into insulated enclosures which opened only to the front. Achroia grisella males sing continuously throughout the night (scotophase). We therefore played back a recording of the search signal of the greater horseshoe bat R. ferrumequinum, a potential predator of A. grisella whose call specifically causes lesser wax moths to intermit their behavior (Greenfield and Weber 2000; Alem et al. 2011; Cordes et al. 2013), for 3 trials: at the onset of scotophase, again 1 h later and at the onset of the subsequent scotophase. For this, we used the software Avisoft RECORDER USGH (Avisoft Bioacoustics, Berlin, Germa (...truncated)