Research Article |
Corresponding author: Klaus-Gerhard Heller ( heller.volleth@t-online.de ) Academic editor: Fernando Montealegre-Z
© 2018 Klaus-Gerhard Heller, Olga Korsunovskaya, Bruno Massa, Ionuț Ștefan Iorgu.
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:
Heller K-G, Korsunovskaya O, Massa B, Iorgu IȘ (2018) High-speed duetting – latency times of the female acoustic response within the bush-cricket genera Leptophyes and Andreiniimon (Orthoptera, Phaneropteridae). ZooKeys 750: 45-58. https://doi.org/10.3897/zookeys.750.23874
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To find a mate, male and female bush-crickets of the family Phaneropteridae typically engage in duets. The male sings and the female responds. For mutual recognition, the amplitude pattern of the male song and the species-specific timing of the female response have been shown to be very important. In the seven studied species, belonging to the genera Leptophyes and Andreiniimon, these duets are extremely fast and nearly completely in the ultrasonic range. The females produce very short sounds by fast closing movements of the tegmina. They respond with species-specific delays of 20 to 150 ms after the beginning of the male song. The different latency times are probably not important for species recognition, since in sympatric species they are quite similar.
Phaneropterinae , katydid, female acoustic signals, duet, stridulatory movement
In bush-cricket (katydid) species of the family Phaneropteridae (or subfamily Phaneropterinae, depending on author) not only the males produce songs, but typically the females respond acoustically to these signals (for a review, see
At the end of the last century, three groups of scientists studied simultaneously and independently this communication system (
In the present paper we focus on the genus Leptophyes Fieber, 1853 and the monotypic genus Andreiniimon Capra, 1937. Both genera are closely related to Isophya (
The female response behaviour was studied in the laboratory using virgin females, collected as nymphs (or from a laboratory culture, only some L. punctatissima females). We studied the following species (number of females studied in brackets): Andreiniimon nuptialis (3), Leptophyes albovittata (4), L. punctatissima (6), L. discoidalis (1), L. laticauda (5), L. lisae (4), L. sicula (1). The duets were recorded – mostly in the evening – using a Racal store 4-D tape recorder (Racal Electronics plc, Weybridge, United Kingdom) and modified tape-recorder Yupiter 202-Stereo (Komunist Works, Kiev, USSR/Ukraine), with microphones Brüel & Kjær 4133 and 4135 (B&K, Nærum, Denmark; frequency response flat up to 40 and 70/100 kHz respectively; distance to microphone 50 to 100 mm). Leptophyes discoidalis was recorded using a digital audio recorder EDIROL R-09HR (Roland Corporation US, Los Angeles, USA; frequency response flat 20 Hz – 40 kHz; sampling rate 96 kHz). Wing movements were registered by an opto-electronic device (
Song — Latency time: interval between beginning of male song/song model to beginning of female response. Calling song: song produced by an isolated male. Syllable: the sound produced by one complete up (opening) and down (closing) stroke of the wing. Echeme: a first-order assemblage of syllables. Impulse: a simple, undivided, transient train of sound waves (here: the highly damped sound impulse arising as the impact of one tooth of a stridulatory file).
Measurements of body and spermatophore mass follow
The females of all species studied here (Leptophyes punctatissima (Bosc, 1792), L. albovittata (Kollar, 1833), L. laticauda (Frivaldszky, 1868), L. discoidalis (Frivaldszky, 1868), L. lisae Heller & Willemse, 1989, L. sicula Kleukers, Odé & Fontana, 2010, Andreiniimon nuptialis (Karny, 1918)) responded to male songs with very short signals consisting of one to three loud impulses and occasionally of some more soft ones. Rarely, up to five loud impulses were observed. In all species studied in this respect, the loud impulses were produced by a closing movement of the tegmina. The peak of the carrier frequency of the females’ responses was mostly similar to that of the males, with the notable exception of A. nuptialis (Table
Peak frequencies of male and female song and body and spermatophore mass in European Leptophyes and Andreiniimon species.
Species | Male (kHz) | Source | Female (kHz) | Source | Body mass male/female (mg) | Spermato-phore mass (% male body mass; n) | Source |
L. punctatissima | 40 | F | 40 | F | 172/302 | 5.8; 2 | B |
L. albovittata | 50–57 | C, G, H | 67 | D | 124/255 | 6.3; 9 | B |
L. laticauda | 20–23 | C, D | 22 | D | 423/668 | 24.6; 21 | B |
L. discoidalis | 32–35 | A, E | 35 | A | – | – | – |
L. lisae | 27(–30) | C, D | 30 | D | 177/297 | 4.5; 6 | B |
L. sicula | 29 | A | 30 | A | 203/354 | – | A |
A. nuptialis | 61 | C, D | 44 | D | 354/494 | 9.8; 2 | B |
Specimens studied: 5 females, GREAT BRITAIN: laboratory culture, 1 ix–31 x 1983, leg. C. Hartley; 1 female, GERMANY: Nürnberg (49°27'N, 11°3'E), 1 x–31 xii 1987, leg. K. Reinhold.
The male calling song consists of single, short syllables presented at intervals of several seconds. The acoustical response behaviour of the female was studied intensively by
Latency times of the female response. The times refer to the beginning of the male song with temperature in European Leptophyes species and Andreiniimon nuptialis. Open symbols: L. punctatissima from
Oscillograms of male-female-duets. Stridulatory movement of female Leptophyes and Andreiniimon together with male-female duet (sound A, D, E, G, I) or male-female duet, sound only (B, C, F, H). Oscillograms of stridulatory movement and song [synchronous registration of left tegmen movement and sound (upper line: upward deflection represents opening, downward closing; lower line: sound)]. A–C female reaction to model of male song D female reaction to heterospecific male song (see text) E–I female reaction to conspecific male song. Female responses in box highlighted in red, proposed trigger point marked with red arrow.
Specimen studied: 1 female, GREECE: N. Drama, valley of river Nestos, above Paranestion, (41°17'N, 24°29'E), 5 m, 17 vi 1984, leg. v. Helversen; 3 males, 3 females, RUSSIA, Kursk distr.: Centralno-Chernozemny reserve (51°09'N, 36°26'E), 10–13 viii 1985, leg. O. Korsunovskaya.
The male calling song consists of single, short syllables presented at intervals of several seconds. The acoustic response behaviour of the female was first studied by
Specimens studied: 1 male, 1 female, ITALY: Medeazza near Trieste (45°55'N, 13°25'E), 1–10 vii 1995, leg. v. Helversen; 1 male, 1 female, MONTENEGRO: Petrovac (42°12'N, 18°56'E), 9 vi 2017, leg. M. Heller; 3 females, MONTENEGRO: Lovcen pass above Kotor (42°24'N, 18°45'E), 4 vi 2017, leg. M. and K.-G. Heller; 1 male, MONTENEGRO: Zabljak (42°19'N, 16°9'30"E), 8 vi 2017, leg. M. Heller.
The male calling song of L. laticauda is more variable and the song units (see below) are produced in a much faster rhythm (
Specimens studied: 1 male, 1 female, ROMANIA: Telciu (47°24'N, 24°23'E), 7 vii 2017, leg. I. Ș. Iorgu.
In contrast to all other European Leptophyes species, the male calling song consists not of single syllables (or very short echemes), but of a series of six up to 30 syllables (
Specimens studied: 1 male, 1 female, GREECE: N. Korinthia, southeast of Korinth (37°50'N, 23°2'E), 1–30 iv 1984, leg. E. Blümm; 1 male, 3 females, GREECE: Chios, 2 km west of Mesta (38°16'N, 25°54'E), 24 v 1995, leg. K.-G. Heller.
The male calling song consists of single syllables, but these syllables are much longer (ca. 150 ms at 20 °C;
Specimens studied: 1 male, 1 female, ITALY: Sicily, 1–31 viii 2015, leg. Bruno Massa.
The male calling song consists of relatively long (
Specimens studied: 1 male, 1 female, FYR MACEDONIA: 10 km w Miravci, Vardar near Demir Kabija (41°24 N, 22°9'E), 21 vi 1984, leg. D. and O. v. Helversen; 2 males, 2 females, GREECE: N. Ilia, Peloponnesos, valley of river Erimanthos, 6 km east of Koumanis (37°48'N, 21°47'E), 1–30 vi 1997, leg. K.-G. Heller.
The male calling song consists of single, very short syllables presented at intervals of several seconds. The female response occurred only about 20 ms later (see also
The females of Andreiniimon and all six Leptophyes species studied here responded acoustically to the male calling song with very short signals, consisting of a few sound impulses only, produced by a closing movement of the tegmina (Fig.
Five species are grouped together with reaction times shorter than 60 ms. The fastest species, with a latency of about 20 ms or lower, was Andreiniimon nuptialis. It is thus the species with the fastest known duet in insects world-wide (see
The last two species, L. lisae and L. sicula, have longer latency times than the five discussed above. Both are morphologically most similar to each other and then to L. punctatissima, but none occurs sympatrically with any other according to present knowledge. Otherwise, the three species would present a nice example of the importance of latency times. Males of L. punctatissima will certainly not accept the slow L. lisae females (see
Why do the females use such short latency times? If the male phonotactically approaches a responding female, he may prefer the nearest one. The sound needs three milliseconds to travel one metre, so by answering rapidly a female can get an advantage. In L. punctatissima the males even did not walk towards a female whose response they received later than 55 ms and with an intensity lower than 50 dB SPL. Successful duetting started only at distances lower than four metres (
In species in which the females respond to song models which differ from the species-specific song pattern, artificial signals nevertheless contain the information necessary for species recognition and for triggering the female acoustic response. The females of some Leptophyes species do not seem to be very selective concerning species recognition. They responded to signals much shorter and much longer than the song (see above,
Of course, more studies are necessary to understand the differences in the female response behaviours between the species. There is, however, no evidence that the mating behaviour affects the acoustical response (see Table
So neither sexual selection (as far as the known differences in mating behaviour are concerned) nor species recognition play an easily understandable role for the evolution of female latency times. In both contexts male calling songs are probably more important. However, for the coexistence of different species ecological adaptations should not be underestimated. Leptophyes punctatissima and L. albopunctata, for example, occur sympatrically, but not syntopically over large parts of Europe (
We are indebted to Dr. J. C. Hartley of Nottingham University and Dr. J. Rheinlaender for providing some animals of L. punctatissima, to Drs. G. and A. Lehmann for help in organising the transport of L. sicula and to E. Blümm, M. Heller, Drs. D. and O. v. Helversen and Dr. K. Reinhold for collecting specimens. Dr. Holger Braun and Dr. Thorin Jonsson gave helpful comments to a previous version of the manuscript. Some investigations were supported by the Russian Science Foundation (14–50–00029 – Scientific basis of the national biobank – depository of the living Systems).