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.

中文翻译：

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通过捕食序列的多模态防御

Aposematic 生物使用多种防御措施警告捕食者它们的无利可图，包括视觉警告信号、惊人的声音、有害气味或厌恶的味道。使用多道防线可以通过刺激多种感官和/或在捕食的不同阶段采取行动来帮助猎物避开捕食者。我们使用蓝山雀（Cyanistes caeruleus）捕食者测试了三道防线（颜色、气味、味道）在捕食木虎蛾（Arctia plantaginis）的过程中的功效。对具有两种后翅表型（基因型：WW/Wy=白色，yy=黄色）的飞蛾进行操作，使其具有具有厌恶气味的防御液（甲氧基吡嗪）、具有厌恶味道的身体组织（吡咯里西啶生物碱）或两者兼而有之。在早期捕食阶段，飞蛾的颜色和气味对鸟类接近潜伏期和掉落猎物有累加作用，对带有防御液的白色变种飞蛾的效果最强。吡咯里西啶生物碱螯合在早期攻击阶段是有害的，这表明吡咯里西啶生物碱螯合和其他防御投资之间的权衡。此外，单独的吡咯里西啶生物碱味道并不能阻止鸟类捕食者。鸟类只有在含有甲氧基吡嗪的颈部液体存在时才能有效区分有毒飞蛾和无毒飞蛾，此时它们在食用阶段放弃攻击。因此，具有令人厌恶的甲氧基吡嗪气味的白色变种飞蛾和接受两种化学防御的飞蛾生存的机会最大。我们建议甲氧基吡嗪作为警告颜色的上下文设置信号，以及作为令人反感的毒素的注意警报或“减速”信号，从而调节警告信号和毒性之间的关系。此外，我们发现后翅着色杂合的飞蛾与其他基因型相比，在延迟接近和减少飞蛾潜伏期方面具有更有效的防御液，这表明着色和防御之间的遗传联系可以帮助解释颜色多态性。总之，这些结果表明颜色、气味和味道构成了一种多模式警告信号，可以阻止捕食者的攻击并提高猎物的生存率。这项工作强调了通过捕食序列以及化学防御中的物种内变异来理解颜色、气味和味道的不同作用的重要性。我们发现，与其他基因型相比，后翅着色杂合的飞蛾在延迟接近和减少飞蛾掉落的潜伏期方面具有更有效的防御液，这表明着色和防御之间存在遗传联系，这有助于解释颜色多态性。总之，这些结果表明颜色、气味和味道构成了一种多模式警告信号，可以阻止捕食者的攻击并提高猎物的生存率。这项工作强调了通过捕食序列以及化学防御中的物种内变异来理解颜色、气味和味道的不同作用的重要性。我们发现，与其他基因型相比，后翅着色杂合的飞蛾在延迟接近和减少飞蛾掉落的潜伏期方面具有更有效的防御液，这表明着色和防御之间存在遗传联系，这有助于解释颜色多态性。总之，这些结果表明颜色、气味和味道构成了一种多模式警告信号，可以阻止捕食者的攻击并提高猎物的生存率。这项工作强调了通过捕食序列以及化学防御中的物种内变异来理解颜色、气味和味道的不同作用的重要性。表明着色和防御之间的遗传联系可能有助于解释颜色多态性。总之，这些结果表明颜色、气味和味道构成了一种多模式警告信号，可以阻止捕食者的攻击并提高猎物的生存率。这项工作强调了通过捕食序列以及化学防御中的物种内变异来理解颜色、气味和味道的不同作用的重要性。表明着色和防御之间的遗传联系可能有助于解释颜色多态性。总之，这些结果表明颜色、气味和味道构成了一种多模式警告信号，可以阻止捕食者的攻击并提高猎物的生存率。这项工作强调了通过捕食序列以及化学防御中的物种内变异来理解颜色、气味和味道的不同作用的重要性。