Research Article |
Corresponding author: Takashi Kuriwada ( t.kuriwada@gmail.com ) Academic editor: Ming Kai Tan
© 2024 Takashi Kuriwada.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kuriwada T (2024) Mating behavior and three types of mating songs of the sandy beach-dwelling ground cricket Dianemobius csikii (Grylloidea, Trigonidiidae, Nemobiinae). Journal of Orthoptera Research 33(2): 249-254. https://doi.org/10.3897/jor.33.108536
|
This study aimed to investigate the mating behavior of the sandy beach-dwelling ground cricket, Dianemobius csikii (Bolívar, 1901) (Orthoptera, Grylloidea, Trigonidiidae, Nemobiinae). The calling songs of males were recorded, and the temporal structures of the songs were analyzed. Subsequently, the courtship song and mating behavior of cricket pairs were observed. The calling song consisted only of monotonous chirps, while the courtship song consisted of similar chirps and ticks consisting of a single pulse. Dianemobius csikii exhibited a relatively longer courtship duration than other cricket species. The female stayed with the male for approximately 25 min while the male emitted the courtship song. The male then changed to the trill song, which is a continuous song, just before copulation. Copulation occurred within 10–40 s of the male emitting the trill song. The courtship behavior differs from that of other well-studied cricket species, such as Gryllinae. The findings of this study provide insight into the mating behaviors of crickets.
calling song, courtship song, Orthoptera, sexual selection, Trigonidiidae
In many animal species, males produce signals for mating (
In crickets for several well-studied species, especially for Gryllinae, males produce three types of acoustic signals: calling, courtship, and aggressive songs (
The bulk of research on the acoustic communication of crickets has focused on Gryllinae, with few studies other cricket groups. However, several species of Trigonidiidae, which includes more than 700 species and inhabits diverse environments (
The sandy beach-dwelling ground cricket Dianemobius csikii (Bolívar, 1901) is mainly distributed along the sandy beaches of Japan, Korea, and China (
This study measured the temporal structures of the calling and courtship songs of D. csikii and examined the relationship between the structures of the courtship song and the copulation success of males. Furthermore, the male of D. csikii was observed emitting another type of song—a trill song—just before copulation that differed from their calling and courtship songs. The details of these results of the analyses of the songs along with observations of mating behavior of the cricket are reported here.
Insect collection and rearing—Nymphs of D. csikii were collected from a sandy beach in Minamisatsuma city, Kagoshima Prefecture, Japan (31.4413°N, 130.2832°E), between late July and early August 2020. A total of 58 crickets were reared in a container (42 × 24 × 25 cm) at 27 ± 1°C under photoperiods of 15 h of light to 9 h of darkness (light cycle: 04:00 to 19:00). The crickets were given egg cartons for shelter, soil in a 200 mL plastic cup, guinea pig food (Marmot selection; Yeaster Co., Ltd., Hyogo, Japan), and cat food (Purina One Metabolic Energy Control; Purina, Kobe, Japan) provided ad libitum. Furthermore, the soil was sprinkled with water every 2–3 days to provide the crickets with a source of water and a site suitable for oviposition. The individuals used in this experiment were the third-generation progeny of the crickets originally collected from the beach. The final instar nymphs were reared individually in plastic containers (diameter = 6.0 cm; height = 3.0 cm), and the cups were checked daily for newly emerged adults. Adult crickets were kept in identical individual cups until the experiment began.
Recording of the calling song.—Using an uncompressed digital IC recorder with a 44.1 kHz sampling rate and a 16-bit dynamic range, the male calling song was recorded one to two days before the observation of mating behavior (RR-XS455; Panasonic, Osaka, Japan). The recordings were saved as WAV files. Each male container (6 cm diameter, 3 cm high) was placed with the IC recorder in a two-ply corrugated fiberboard box (inner side: 23 × 17 × 17 cm, outer side: 28 × 23 × 23 cm) that was physically, visually, and acoustically isolated from other cricket containers. All recordings were made at temperatures of 27 ± 1°C from 19:00 to 04:00, which corresponds to the dark period. Using Audacity v2.0.5 software (Dominic Mazzoni, Mountain View, CA, USA), seven components of the calling song were analyzed: time spent calling at night, chirp duration, chirp interval length, dominant frequency of the chirp, pulse duration, pulse interval length, and the number of pulses per chirp (Fig.
Observation of mating behavior.—Unmated males and females 8–14 d after their final molt were used for the observations. A focal male was placed in a plastic container (diameter = 12 cm, height = 19.0 cm), an unmated female was added to the container after 1 min, and the mating behavior of the pair was observed for 40 min. This process was repeated until 40 pairs had been observed . All experiments were started between 16:00 and 18:20 under fluorescent light. The timing fluctuated between 40 min and 3 h before the dark cycle, when crickets are usually active (
Statistical analyses.—To examine the effect of the temporal structure of courtship songs on copulation success, a generalized linear model with binomial error and logit link was implemented using R 4.1.2 (
Temporal structure of the three song types.—The median time spent calling at night was 5.40 min (25–75% quantiles: 0–125.8 min, N = 40). The calling song of D. csikii comprised only chirps (Fig.
Sound spectrogram (A) and oscillograms (B and C) of trill song of Dianemobius csikii. The oscillogram in C is an expansion of the time axis in B. Once the courtship song changed to the trill song, the trill song was continuously emitted until copulation began. Dotted lines B to C show the approximate corresponding times.
Mean | SD | CV | N | |
---|---|---|---|---|
Calling song | ||||
Chirp duration (s) | 0.59 | 0.056 | 0.095 | 26 |
Interval length (s) | 0.33 | 0.081 | 0.240 | 26 |
Dominant frequency (kHz) | 6.99 | 0.260 | 0.037 | 26 |
Pulse duration (ms) | 5.45 | 0.817 | 0.150 | 26 |
Pulse interval (ms) | 3.51 | 0.904 | 0.258 | 26 |
No. pulse/chirp | 65.04 | 13.07 | 0.201 | 26 |
Courtship song | ||||
Chirp duration (s) | 0.56 | 0.17 | 0.30 | 40 |
Interval length (s) | 0.14 | 0.024 | 0.16 | 40 |
Dominant frequency (kHz) | 6.87 | 0.32 | 0.046 | 40 |
No. chirps† | 17.92 | 22.19 | 1.24 | 40 |
Pulse duration (ms) | 6.01 | 0.162 | 0.027 | 40 |
Pulse interval (ms) | 4.05 | 0.105 | 0.026 | 40 |
No. pulse/chirp | 66.15 | 26.24 | 0.40 | 40 |
No. ticks‡ | 6.78 | 3.30 | 0.49 | 40 |
Tick duration (ms) | 9.21 | 4.32 | 0.47 | 40 |
Tick interval (s) | 0.19 | 0.11 | 0.58 | 40 |
Trill song | ||||
Dominant frequency (kHz) | 6.50 | 0.20 | 0.031 | 9 |
Effect of the temporal structure of the courtship song on copulation success. Results were obtained using generalized linear model testing.
Explanatory variable | t-value | P-value |
---|---|---|
Chirp duration | 0.41 | 0.68 |
Interval length | 0.39 | 0.70 |
Dominant frequency | 0.55 | 0.59 |
No. chirps† | 1.04 | 0.31 |
No. ticks‡ | 0.47 | 0.64 |
Pulse duration | 0.59 | 0.56 |
Pulse interval | 1.42 | 0.17 |
No. pulse/chirp | 1.22 | 0.23 |
Tick duration | 0.61 | 0.55 |
Tick interval | 0.12 | 0.91 |
Mating behavior.—The mating behavior of the crickets began when a female approached a male. When the female body parts, including the antennae, touched the male, the male emitted a courtship song. The male continued to emit the courtship song for approximately 25 min without interruption, while the female remained nearby. Subsequently, the courtship song changed to the trill song. Approximately 10–40 sec after the change, the female mounted the male, and copulation occurred. Copulation lasted approximately 3 min. In 5 of 40 cases, the experiment was terminated 40 min after the courtship song began and before the cricket switched to the trill song. In these cases, no copulation was observed; however, the females remained near the males for the duration of the observation. Only one male successfully copulated without producing the trill song. Furthermore, 33 of the 34 males that emitted the trill song succeeded in copulation. In the one failed case, the female mounted the male, but the male spermatophore was not attached to the female genitalia, and the female ate the spermatophore. Figs
Mating behavior of Dianemobius csikii. A. Male emitting the calling song. B. When a part of the female body touches that of the male, the male emits the courtship song. The female stays by the male during the courtship song. All males (40 individuals) emitted a courtship song when approached by a female. C. Approximately 25 min after the male begins to produce the courtship song, most males (34/40 = 85%) switched to the trill song. Only one male (1/34 = 2.9%) copulated without production of the trill song. D. The female mounts and copulates with the male approximately 20 s after the beginning of the trill song. All females (34 individuals) mounted the male when the male emitted the trill song (although only one male failed to pass the spermatophore). E. When copulation ended, the female dismounts and leaves the male. Illustrations by Yu Hirayama.
Histogram of mating behavior parameters of Dianemobius csikii. A. Latency to courtship, B. courtship duration (i.e., time from start of courtship song to change to trill song), C. latency to copulation (i.e., time between trill song and copulation), and D. copulation duration. The white bar indicates no copulation within 40 min (B).
In orthopteran insects, males produce multiple songs (calling, courtship, and aggressive songs), each used as a different behavioral signal (
The production of mating songs in crickets requires high energetic expenditure (
The likely function of the trill song identified in the present study is to induce female mounting for mating because almost all pairs copulated within 40 s after males switched to the trill song. In contrast, the function of the courtship song may be to allow the female to assess the quality of the male, as the male emits the courtship song for approximately 25 min while the female stays nearby. Most of the pairs had a courtship song lasting approximately 25 min. However, some pairs (12.5%) did not change to the trill song after 40 min, and copulation did not occur. Identifying the factors that lead to the change in the song, such as micro-movements or female chemical cues, is an important area for future research.
Specific environments may cause the evolution of novel song types and mating behaviors. For example, owing to the abundance of acoustically orienting parasitoids, two new male morphs have been observed in the Hawaiian populations of the Pacific field cricket Teleogryllus oceanicus (Le Guillou, 1841) producing a novel purring song (
The data used for this study are available from the corresponding author on request.
All experimental procedures in this study were conducted in accordance with the guidelines for the use of animals in research in Kagoshima University.
I would like to thank Yu Hirayama (Kagoshima University) for the illustrations in Fig.