Shaking Youngsters and Shaken Adults: Female Beetles Eavesdrop on Larval Seed Vibrations to Make Egg-Laying Decisions

Egg-laying decisions are critical for insects, and particularly those competing for limited resources. Sensory information used by females to mediate egg-laying decisions has been reported to be primarily chemical, but the role of vibration has received little attention. We tested the hypothesis that vibrational cues produced by feeding larvae occupying a seed influences egg-laying decisions amongst female cowpea beetles. This hypothesis is supported by three lines of evidence using two strains of the cowpea beetle (Callosobruchus maculatus), an Indian strain with choosy females and aggressively competing larvae and a Brazilian strain with less choosy females and larvae exhibiting an “accommodating” type of competition. First, in free-choice bioassays of seed selection, choosy Indian females selected control seeds (free of eggs, larvae, or egg-laying marker) over seeds with live larvae (free of eggs and egg-laying marker), but did not discriminate between control seeds and those with dead larvae. In contrast, less choosy Brazilian females showed no preference for seeds containing live or dead larvae over controls. Second, laser-doppler vibrometer recordings confirmed that larvae feeding inside seeds generate vibrations that are available to the female during egg-laying decisions. Third, during dichotomous choice experiments where artificial vibrations approximating those produced by feeding larvae were played back during seed selection, Indian females preferred immobile control seeds over vibrating seeds, but Brazilian females showed no preference. These results support the hypothesis that females use larval vibrations in their egg-laying decisions; whether these vibrations are passive cues exploited by the female, or active signals that ‘steer’ the behaviour of the female is unknown. We propose that vibration cues and signals could be important for host selection in insects, particularly those laying on substrates where visual or chemical cues may be unreliable. This seems to be the case with females of the cowpea beetle since visual cues are not important and chemical egg-marking does not last more than two weeks, allowing vibration cues to improve discrimination of egg-laying substrate particularly by choosy females.

产卵决策对于昆虫，尤其是那些在有限资源中竞争的昆虫而言至关重要。已有研究表明，雌性昆虫用于调控产卵决策的感官信息主要来自化学信号，但振动信号的作用却鲜有关注。我们验证了这一假说：寄居于种子内的取食幼虫所产生的振动线索，会影响雌性豇豆象（Callosobruchus maculatus）的产卵决策。该假说通过三项实验证据得到了支持：我们使用了两种豇豆象品系——印度品系（雌性挑剔、幼虫具有竞争性掠夺行为）与巴西品系（雌性选择偏好较弱、幼虫竞争模式为‘互助型’）。其一，在自由选择的种子选择生物测定实验中，挑剔的印度品系雌性会选择无卵、无幼虫且无产卵标记的对照种子，而非带有活幼虫（无卵与产卵标记）的种子；但它们无法区分对照种子与带有死幼虫的种子。与之相对，选择偏好较弱的巴西品系雌性并不会对带有活/死幼虫的种子与对照种子表现出偏好。其二，激光多普勒振动计（laser-doppler vibrometer）的记录证实，种子内取食的幼虫会产生振动信号，且雌性在产卵决策过程中能够感知到这类振动。其三，在二分选择实验中，当播放模拟幼虫取食产生的人工振动信号时，印度品系雌性更倾向于选择静止的对照种子，而非带有振动的种子；但巴西品系雌性并未表现出此类偏好。上述研究结果支持‘雌性豇豆象会利用幼虫振动信号进行产卵决策’这一假说；但目前尚不清楚这类振动是雌性利用的被动线索，还是能够‘引导’雌性行为的主动信号。我们提出，振动线索与信号可能对于昆虫的寄主选择具有重要意义，尤其是那些将卵产在视觉或化学线索可能不可靠的基质上的昆虫。对于豇豆象雌性而言，这一情况确实存在：它们的视觉线索并不重要，且化学产卵标记的持续时间不超过两周，因此振动线索能够帮助挑剔的雌性更好地辨别产卵基质。