Pea leafminer Liriomyza huidobrensis (Diptera: Agromyzidae) uses vibrational duets for efficient sexual communication

Abstract

The pea leafminer (Liriomyza huidobrensis) is a notorious pest of vegetables and ornamental plants worldwide. Despite a large number of studies on its biology and ecology, the courtship behavior and sexual communication of this species remain unclear. Here, we studied vibrational communication in the sexual interaction of the pea leafminer. On host plant leaves, females and males behaviorally displayed the bobbing-quivering alternation, which finally led to copulation. Moreover, records of laser vibrometry revealed three-signal duets underlying the behavioral alternation. Sexually mature males spontaneously emitted calls (MCs) to initiate the duets. The females rapidly responded to MCs by emitting replies (FRs) that are longer in duration. The FRs further triggered male replies (MRs) in their search for potential partners. Leafminer-produced vibrational signals convey efficient information to partners and generate pair formation on stretched substrates, such as plant leaves and nylon mesh, but cannot elicit responses on dense substrates, such as glass and plastic. Vibrational playbacks of both MCs and FRs can elicit replies in females and males, respectively. This study completely characterizes substrate-borne vibrational duets in a dipteran insect. The discovery of vibrational sex signals in the pea leafminer provides new insights for the development of novel approaches to control the pest and its relative species.

Keywords: Liriomyza; biotremology; courtship behavior; vibrational communication.

Figure 1

Premating behavior and vibrational signals on bean leaves. (A) Ethogram of premating behavior constructed based on the first‐order transition of behaviors. The size of the boxes representing each behavior is proportional to the relative frequency of occurrence of a particular behavioral pattern. The color of the boxes represents female (red) or male (black) behavioral elements. Behavioral transitions are depicted as arrows when they occur significantly more often than predicted by chance. The arrow size indicates the degree of possibility in transition. (B) Frames of a video and a vibrational oscillogram of vibration of behavior before, during and after a behavioral duet. Each clip of vibrational signals is shown in a 1 s time frame.

Figure 2

Mating behavior and three‐signal duets on nylon mesh. (A) Oscillograms of mating behavior of paired adult leafminers recorded on a nylon mesh. Six repetitions are shown below at higher resolution. M: pulses produced by males. F: pulses produced by females. (B) A representative duet. Male calls (MC) generated by male body flickering: male call, female response (FR) generated by female bobbing: female reply, male response (MR) generated by male quivering: male reply. (C) Oscillogram (at bottom), spectrogram (at top left), and instantaneous amplitude spectrum (at right) of each signal in a duet.

Figure 3

Male‐manipulated experiment. (A) Percentages of signaling males in the 2‐day‐old or 0‐day‐old groups. (B) Percentages of signaling females paired with 2‐day‐old, 0‐day‐old, or immobilized 2‐day‐old males.

Figure 4

Female‐manipulated experiment. (A) Percentages of signaling females in 2‐day‐old or 0‐day‐old groups. (B) Percentages of signaling males paired with 2‐day‐old, 0‐day‐old, or immobilized 2‐day‐old females.

Figure 5

Substrate‐manipulated experiment. (A) Percentages of signaling females paired with males on five substrates. (B) Measured amplitudes of two elements of male calls (MCs) on five substrates. Different letters show significant differences between amplitudes after Kruskal–Wallis test followed by Dunn's multiple comparison.

Figure 6

Playback experiment. (A) Oscillogram of female responses (FRs) of a responsive female replying to male call (MC) playbacks. (B) Oscillogram of male responses (MRs) of a responsive male replying to FR playbacks.