New Data on Vibrational Calling Signals of Fulgoroidea (Homoptera: Auchenorrhyncha) from the Asian Part of Palaearctic with New Records of Three Species of Cixiidae
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Russian Entomol. J. 25(4): 307–322 © RUSSIAN ENTOMOLOGICAL JOURNAL, 2016 New data on vibrational calling signals of Fulgoroidea (Homoptera: Auchenorrhyncha) from the Asian part of Palaearctic with new records of three species of Cixiidae Íîâûå äàííûå î âèáðàöèîííûõ ïðèçûâíûõ ñèãíàëàõ Fulgoroidea (Homoptera: Auchenorrhyncha) èç àçèàòñêîé ÷àñòè Ïàëåàðêòèêè è íîâûå íàõîäêè òðåõ âèäîâ Cixiidae D.Yu. Tishechkin Ä.Þ. Òèøå÷êèí Department of Entomology, Faculty of Biology, M.V. Lomonosov Moscow State University, Vorobyevy Gory, Moscow 119234, Russia. E- mail: [email protected] Кафедра энтомологии Биологического факультета Московского государственного университета имени М.В. Ломоносова, Воробьёвы Горы, Москва 119234, Россия. KEY WORDS: Homoptera, Auchenorrhyncha, Fulgoroidea, Cixiidae, Dictyopharidae, Meenoplidae, Caliscel- idae, vibrational communication, vibrational signals, new records. КЛЮЧЕВЫЕ СЛОВА: Homoptera, Auchenorrhyncha, Fulgoroidea, Cixiidae, Dictyopharidae, Meenoplidae, Caliscelidae, вибрационная коммуникация, вибрационные сигналы, новые находки. ABSTRACT. Calling signals of three species of Introduction Delphacidae (Kelisiinae and Delphacinae), 13 species of Cixiidae, one species of Meenoplidae, two species of Delphacinae (Homoptera: Auchenorrhyncha: Del- Dictyopharidae (Dictyopharinae and Orgeriinae), and phacidae) were the first objects of Fulgoroidea bioa- two species of Caliscelidae from the Asian part of coustics. Nilaparvata lugens (Stål, 1854) was the first Palaearctic are described and illustrated by oscillo- species not only of Delphacinae, but also of all small grams and sonograms. Species of Cixiidae, Meenopl- Auchenorrhyncha for which was proved conclusively, idae, and Dictyopharidae produce simple calling sig- that its acoustic signals transmit via substrate i.e. leaves nals consisting of uniform short pulses; in Delphacidae and stems of host plants [Ichikawa, Ishii, 1974]. Inves- and Caliscelidae signals have much more complex tem- tigation of signals of Javesella Fennah, 1963, Muelleri- poral and frequency pattern. Signal recordings of Cixius anella Wagner, 1963, Ribautodelphax Wagner, 1963, sibiricus, C. granulatus, and Reptalus narynensis were Chloriona Fieber, 1866, and species from some other made far outside their known ranges; for these species genera showed that the calling signals in this subfamily drawings of male genitalia of specimens from new for the most part are rather complex phrases consisting localities are given. of several different elements [de Vrijer, 1984, 1986; Booij, 1982; den Bieman, 1986, 1987; Strübing, Rollen- РЕЗЮМЕ. Описаны призывные сигналы 3 видов hagen, 1988; de Winter, Rollenhagen, 1990; Gillham, Delphacidae (Kelisiinae и Delphacinae), 13 видов de Vrijer, 1995]. Cixiidae, 1 вида Meenoplidae, 2 видов Dictyopharidae Information on signals of other Fulgoroidea in those (Dictyopharinae и Orgeriinae) и 2 видов Caliscelidae years was very scarce. Description of vibrational sig- из азиатской части Палеарктики, приведены их ос- nals and mating behaviour of Dictyophara europaea циллограммы и сонограммы. Представители (Linnaeus, 1767) (Homoptera: Dictyopharidae) was Cixiidae, Meenoplidae и Dictyopharidae издают сиг- published by Strübing [1977]. Vibrational signals and налы со сравнительно простым временным рисун- mating behaviour in a number of peculiar species of ком, состоящие из коротких однотипных пульсов; cave-dwelling Cixiidae (Homoptera) were described by сигналы Delphacidae и Caliscelidae имеют гораздо Hoch and co-authors [Howarth et al., 1990; Hoch, более сложную временную и частотную структуру. Howarth, 1993; Hoch, Wessel, 2006]. In species from Записи сигналов Cixius sibiricus, C. granulatus и both families signals consist of short simple uniform Reptalus narynensis были сделаны в точках, лежа- pulses, which can be grouped into single succession щих за пределами их известных ареалов; для этих (syllable) either arranged in several trains of equal or видов приведены рисунки гениталий самцов из но- different duration. Thus, their temporal pattern is much вых местонахождений. more simple, than in Delphacidae. In Cixiidae, this 308 D.Yu. Tishechkin phenomenon seemed to be the part of general reduction to Lower Volga Region, Central Asia, South Siberia and the trends usually occurring in cave-dwelling organisms. Russian Far East. On the one hand, this made it impossible Later, three papers on vibrational signals of Fulgoroi- to study mating behaviour including female reply signals, dea from Russia and adjacent territories were published but on the other, it allowed to obtain signal recordings of [Tishechkin, 1997, 1998, 2003]. The number of families some species not available for laboratory studies. and subfamilies studied increased significantly; calling Signal recordings of three species of Cixiidae were signals of Derbidae, Issidae, Caliscelidae (Caliscelinae made far outside their known ranges. For these species and Ommatidiotinae), Tropiduchidae, Kelisiinae (Del- drawings of male genitalia are given to illustrate our phacidae) and Orgeriinae (Dictyopharidae) were described interpretations of these forms and to provide new data for the first time. Surprisingly, it was found that simple on the variability of penis shape. calling signals consisting of uniform short pulses are not the exception but rather the rule in Fulgoroidea. Only in Material and methods Delphacidae and Caliscelidae calling signals are com- plex, sometimes very long and variable phrases. Planthopper vibrational signals were recorded by Similarity of signal temporal pattern in different spe- means of portable recording equipment consisting of a cies of Fulgoroidea is not a rare case. First, in congeneric piezocrystal gramophone cartridge GZP-311 connected species calling signals sometimes are almost indistin- to the microphone input of a minidisk recorder Sony guishable. Three species from the genus Cedusa Fowler, Walkman MZ-NH900 or a cassette recorder Elektronika- 1904 (Derbidae) and two closely related species of Rep- 302-1 (before 2005) via a custom-made matching ampli- talus Emeljanov, 1971 (Cixiidae) can be mentioned as fier. For recording a twig of host plant about 10–15 cm in examples [Tishechkin, 2008; Emelyanov, Tishechkin, length was attached to the cartridge by a rubber ring so 2012]. Second, species from different genera of Delpha- that the cartridge needle touched the stem slightly. Then cidae quite often produce similar signals; in fact, signals a nylon cage containing a male leafhopper was put on the of a considerable part of species studied can be attributed twig. After a time, the male usually sat on the twig and to one of several main types. Third, simple trains of started singing. All recording were made by the author. pulses typical for many Cixiidae, Issidae and Dic- Signal analysis was performed on a PC fitted with an tyopharidae occasionally are similar even in species from analog/digital converter L-305 (L-Card Ltd., Russia). different families. Anyway, in all cases the similarity of Oscillograms and sonograms of signals were produced signal pattern occurs in acoustically isolated species with TurboLab 4.2 and Cool Edit Pro 2.1 software. occupying different communication cannels i.e. in allo- For elements of signal temporal pattern the following patric forms, in species dwelling in different plant com- terms are used. Pulse is a brief elementary fragment of munities, etc. [Tishechkin, 2008]. signal (or succession of sine waves) with rapid increase Recently, several new papers on vibrational signals and subsequent decrease of amplitude, i.e. separated of Fulgoroidea were published. from similar fragments by amplitude minimums. Short Comprehensive study of vibrational communication fragments with more or less constant temporal pattern of Metcalfa pruinosa (Say, 1830) (Homoptera: Flatidae) usually repeated with regular intervals and consisting of provided first data on signals of Flatidae [Virant-Do- uniform or different pulses are referred to as syllables. berlet, Žežlina, 2007]. It was found that the signals of Any more or less prolonged signal with complex pattern this species consist of uniform short pulses as in most (e.g. succession of similar or different syllables, combi- other fulgoroid families. It is particularly remarkable nation of several syllables and succession of pulses, etc.) that this species has nocturnal acoustic activity in con- is referred to as a phrase. Repetition period of pulses or trast to most other small Auchenorrhyncha. syllables is an interval from the beginning of one syllable Detailed investigation of mating behaviour of Hyal- (pulse) to the beginning of the next one. esthes obsoletus Signoret, 1865 (Cixiidae) was per- Specimens studied are deposited in the collection of formed by Mazzoni et al. [2010]. the Zoological Museum of M.V. Lomonosov Moscow Data on vibrational signals of three species of Cixi- State University, digital signal recordings will be de- idae were published by Hoch and co-authors [Hoch et posited in the Museum in the near future. al., 2011, 2013; Kunz et al., 2014]. Although the num- ber of studied species increased only slightly, extensive study of their biology and mating behaviour is of great Results interest. In particular, it was shown that one species, Apartus michalki (Wagner, 1948) has the only rather Family Delphacidae short peak of the mating activity in the evening [Kunz et Subfamily Kelisiinae al., 2014]. Another species studied, Celebenna thoma- 1. Kelisia ribauti Wagner, 1938 rosa Hoch et Wessel, 2011 belongs