Abstract
Aposematic organisms warn predators of their unprofitability using a combination of defenses, including visual warning signals, startling sounds, noxious odors, or aversive tastes. Using multiple lines of defense can help prey avoid predators by stimulating multiple senses and/or by acting at different stages of predation. We tested the efficacy of three lines of defense (color, smell, taste) during the predation sequence of aposematic wood tiger moths (Arctia plantaginis) using blue tit (Cyanistes caeruleus) predators. Moths with two hindwing phenotypes (genotypes: WW/Wy = white, yy = yellow) were manipulated to have defense fluid with aversive smell (methoxypyrazines), body tissues with aversive taste (pyrrolizidine alkaloids) or both. In early predation stages, moth color and smell had additive effects on bird approach latency and dropping the prey, with the strongest effect for moths of the white morph with defense fluids. Pyrrolizidine alkaloid sequestration was detrimental in early attack stages, suggesting a trade-off between pyrrolizidine alkaloid sequestration and investment in other defenses. In addition, pyrrolizidine alkaloid taste alone did not deter bird predators. Birds could only effectively discriminate toxic moths from non-toxic moths when neck fluids containing methoxypyrazines were present, at which point they abandoned attack at the consumption stage. As a result, moths of the white morph with an aversive methoxypyrazine smell and moths in the treatment with both chemical defenses had the greatest chance of survival. We suggest that methoxypyrazines act as context setting signals for warning colors and as attention alerting or “go-slow” signals for distasteful toxins, thereby mediating the relationship between warning signal and toxicity. Furthermore, we found that moths that were heterozygous for hindwing coloration had more effective defense fluids compared to other genotypes in terms of delaying approach and reducing the latency to drop the moth, suggesting a genetic link between coloration and defense that could help to explain the color polymorphism. Conclusively, these results indicate that color, smell, and taste constitute a multimodal warning signal that impedes predator attack and improves prey survival. This work highlights the importance of understanding the separate roles of color, smell and taste through the predation sequence and also within-species variation in chemical defenses.
Highlights
Predation is one of the main threats to an organism’s survival
Rojas et al (2019) presented moths on a green background, while we presented moths against brown masonite (Supplementary Figure 1), which suggests that the white morph elicits longer approach hesitation even when presented against different colored backgrounds
Moth survival was highest for moths of the white morph with methoxypyrazine smell (Figure 7) and, despite the detrimental effects of pyrrolizidine alkaloid sequestration in terms of attack latency, drop latency, and kill latency, pyrrolizidine alkaloids did not negatively impact moth survival (Figure 7)
Summary
There are many different traits that have evolved to help organisms avoid predation and most organisms use more than one line of defense. In some cases, these multiple defenses can act simultaneously (Ruxton et al, 2018). Prey may evolve behaviors such as background choice (Sargent, 1966; Kang et al, 2012; Kjernsmo and Merilaita, 2012; Green et al, 2019) or body orientation (Kang et al, 2012; Rowland et al, 2020) and to have a color pattern that is camouflaged against their surroundings, all of which help avoid detection by predators (Stevens and Ruxton, 2018). Whether selection favors investment in primary and/or secondary defenses depends on the relative properties of those defenses such as their energetic cost and efficacy against predators (Broom et al, 2010)
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