Behavioural changes in aposematic Heliconius melpomene butterflies in response to their predatory bird calls

Prey-predator interactions have resulted in the evolution of many
anti-predatory traits. One of them is the ability of prey to listen to
predators and avoid them. Although prey anti-predatory behavioural
responses to predator auditory cues are well described in a wide range of
taxa, studies on whether butterflies change their behaviours in response
to their predatory calls are lacking. Heliconius butterflies are
unpalatable and form Müllerian mimicry rings as morphological defence
strategies against their avian predators. Like many other butterflies in
the Nymphalidae family, some Heliconius butterflies possess auditory
organs, which are hypothesized to assist with predator detection. Here we
test whether Heliconius melpomene changes their behaviour in response to
their predatory bird calls by observing the behaviour of male and female
H. m. plessini exposed to calls of Heliconius avian predators:
rufous-tailed jacamar, migratory Eastern kingbird, and resident tropical
kingbird. We also exposed them to the calls of the toco toucan, a
frugivorous bird as a control bird call, and an amplified greenhouse
background noise as a noise control. We found that individuals changed
their behaviour in response to Jacamar calls only. Males increased their
walking and fluttering behaviour, while females did not change their
behaviour during the playback of the jacamar call. Intersexual behaviours
like courtship, copulation, and abdomen lifting did not change in response
to bird calls. Our findings suggest that despite having primary predatory
defences like toxicity and being in a mimicry ring, H. m. plessini
butterflies changed their behaviour in response to predator calls.
Furthermore, this response was predator-specific, as H. m.
plesseni did not respond to either the Eastern kingbird or the tropic
kingbird calls. This suggests that Heliconius butterflies may be able to
differentiate predatory calls, and potentially the birds associated with
those calls.

猎物与捕食者的相互作用推动了诸多反捕食性状（anti-predatory traits）的演化。其中之一便是猎物感知捕食者并躲避其追击的能力。尽管学界已在众多分类单元（taxa）中对猎物针对捕食者听觉线索的反捕食行为反应开展了充分研究，但关于蝴蝶是否会因捕食者鸣叫声改变行为的相关研究仍较为匮乏。
釉蛱蝶（Heliconius）不可食用，且会形成缪氏拟态环（Müllerian mimicry rings）作为对抗鸟类捕食者（avian predators）的形态防御策略。与蛱蝶科（Nymphalidae）的多数类群类似，部分釉蛱蝶拥有听觉器官（auditory organs），该器官被认为可辅助其侦测捕食者。
本研究以红带袖蝶（Heliconius melpomene）的plessini亚种（H. m. plessini）为实验对象，通过向雌雄个体播放其鸟类捕食者的鸣叫声——棕尾鶲鴷（rufous-tailed jacamar）、迁徙性东部必胜鸟（migratory Eastern kingbird）以及居留性热带必胜鸟（resident tropical kingbird）的鸣叫声，探究其是否会因捕食者鸣叫声调整行为。此外，本研究还设置了两类对照：一是以果实为食的巨嘴鸟（toco toucan）的鸣叫声作为鸟类对照，二是经放大的温室背景噪音作为噪音对照。
研究结果显示，仅在播放棕尾鶲鴷的鸣叫声时，蝴蝶个体才会改变行为：雄性个体的行走与振翅行为显著增加，而雌性个体行为无明显变化。求偶、交配、抬腹等雌雄间行为均未因鸟类鸣叫声发生改变。
本研究发现，尽管红带袖蝶plessini亚种已具备毒性等基础捕食防御策略，且处于缪氏拟态环中，但其仍会针对捕食者鸣叫声调整自身行为。且该反应具有捕食者特异性——该亚种并未对东部必胜鸟或热带必胜鸟的鸣叫声产生行为响应。这表明釉蛱蝶或可区分不同的捕食者鸣叫声，以及这些鸣叫声对应的鸟类类群。