Acoustic and Mating Behavior of Dalbulus Leaf hoppers (Homoptera: Cicadellidae) S. E. HEADY,1 L. R. NAULT,1 G. F. SHAMBAUGH,1 AND L. FAIRCHILD2 Ann. Entomol. Soc. Am. 79: 727-736 (1986) Downloaded from https://academic.oup.com/aesa/article-abstract/79/4/727/215293 by guest on 20 November 2018 ABSTRACT The acoustic repertoire and mating behavior of Dalbulus leafhoppers were studied in the laboratory. Acoustic signals were recorded via microphone and tape recorder, and analyzed sonographically and oscillographically. Male common calls of 10 Dalbulus spp. were compared using duration and rate measurements of call parts (sections, phases, and pulses), amplitude ratios of pulses, and dominant frequencies. Call types were characteristic based on repeated measures analysis of variance followed by Scott-Knott mean separation. Common calls had significant variations among species but no one acoustic variable uniquely identified a species. A multivariate hierarchical cluster analysis of calls partitioned Dalbulus species into three groups: 1) D. quinquenotatus DeLong & Nault and D. chiapensis Triple- horn & Nault; 2) D. longulus DeLong, D. guevarai DeLong, and D. elimatus (Ball); 3) D. maidis (DeLong & Wolcott), D. chariest Triplehorn & Nault, D. tripsacoides DeLong & Nault, D. gelbus DeLong, and D. guzmani DeLong & Nault. With the exception of D. guzmani, groupings of species based on male common calls are similar to groupings of species based on cladistic analysis of morphological characters. Beside common calls, Dal- bulus males produce courtship calls, copulatory calls, rivalry calls, and distress calls. Court- ship calls were recorded from Dalbulus females. The basic pattern of courtship and copu- lation for Dalbulus leafhoppers is described. KEY WORDS Dalbulus leafhoppers, mating, calls, phylogeny OSSIANNILSSON (1949) was first to discover acous- frequently heard were courtship calls emitted by tic communication among small Auchenorrhyn- both sexes before copulation and pairing calls pro- cha. With primitive equipment, he heard, record- duced during copulation. Rivalry calls are agres- ed, and analyzed the low-intensity sounds of 96 sive calls emitted by males during intrasexual ag- species of small Auchenorrhyncha. These sounds onistic encounters. Distress calls are produced by are produced by tymbal organs located in the first both sexes when alarmed. and, in some cases, the second abdominal segment. Acoustic signals are not only important in be- For many of the species, Ossiannilsson also noted havior studies but also in systematics, and have the courtship displays or patterns and mating be- been used as a taxonomic tool to separate species havior. Since Ossiannilsson's pioneering studies, the of cicadas (Alexander & Moore 1958), planthop- few acoustic and mating behavior studies of Au- pers (Booij 1982), and leafhoppers (Striibing 1970, chenorrhyncha have been summarized by Cla- 1976, 1983, Claridge & Reynolds 1973, Purcell & ridge (1983, 1985a,b). Loher 1976). Consequently, we examined in detail We describe the acoustic repertoire and the as- the male common calls of 10 of the 11 known sociated mating behavior of 10 Dalbulus leafhop- species (all but D. gramalotes Triplehorn & Nault), pers. We have adopted call categories, modified grouped species based on a cluster analysis of these by Alexander (1967), from terminology used by calls, and compared the resultant phenogram with Ossiannilsson (1949), who adapted Faber's (1929, previously proposed phylogenies of Dalbulus. 1932) classification of orthopteran sounds. Accord- ingly, we classify five types of acoustic signals as: 1) common song; 2) courtship calls; 3) pairing calls; Materials and Methods 4) rivalry calls; and 5) distress calls. The common Leafhoppers used in this study were taken from song or calling signal is produced by individuals laboratory colonies that had been established for when alone or in the presence of other insects not 1-4 years. Colonies were started from leafhoppers responding. Most of the calls Ossiannilsson (1949) collected from Zea and Tripsacum spp. from five heard were common songs that attract mates. Less Mexican states and Guatemala (Nault & Madden 1985, Triplehorn and Nault 1985). D. maidis I Dep. of Entomology, Ohio Agric. Res. & Dev. Center, The (DeLong & Wolcott), D. elimatus (Ball), D. gelbus Ohio State Univ., Wooster, OH 44691. DeLong, D. guevarai DeLong, D. longulus De- II Dep. of Zoology, The Ohio State Univ., Columbus, OH 43210. Long, D. quinquenotatus DeLong & Nault, and 727 728 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 79, no. 4 . _elim Downloaded from https://academic.oup.com/aesa/article-abstract/79/4/727/215293 by guest on 20 November 2018 Fig. 1. Oscillograms of male common calls of Dalbulus spp. Dark line at bottom of calls is time marker for 1 s. Amplitude of calls is only comparable within calls of a species. A, D. elimatus; B, D. guevarai; C, D. longulus; D, D. guzmani; E, D. gelbus; F, D. tripsacoides; G, D. charlesi; H, D. maidis; I, D. chiapensis; and J, D. quinquenotatus. Abbreviations of species names given at end of calls. Calls are made of repeated sections with one section given in A-C; two repeated sections given in D, F, G, and J; three given in E and H; and four given in I. Repeated sections consist of one or two phases designated a and b. Intersection is the time between sections. D. charlesi Triplehorn & Nault were laboratory A thermometer was inserted into the glass tube reared exclusively on maize ('Aristogold Bantam from the top end and temperatures were 22-28°C Evergreen'). D. tripsacoides DeLong & Nault, D. during recording. If leafhoppers were to be ob- guzmani DeLong & Nault, and D. chiapensis Tri- served for >1 h, then a piece (1 by 2 cm) of maize plehorn & Nault were reared on maize and Trip- leaf was inserted for leafhopper feeding. The glass sacum spp. Stock leaf hoppers were reared in cages recording chamber was housed in two plywood (D'Arcy & Nault 1982) at 26-28°C and a photo- and foam soundproof boxes. One side of the box period of 12:12 (L:D) in an insect rearing room. was covered with foam and had a magnifying glass Virgin leafhoppers were obtained either by sepa- (1.6 x) inserted in a hole so that leafhopper behav- rating fourth or fifth instars into individual plexi- ior could be observed while recording. A micro- glass tube cages (30.5 cm height by 8 cm diam) scope lamp was positioned to light the recording over one small potted maize plant or by collect- chamber. ing adults from stock cages immediately after adult Leafhopper acoustic signals were analyzed eclosion. Unmated adult leafhoppers, 5-7 days old, sonographically on a Kay Elemetric Sonagraph were observed and acoustically recorded as well (Model 7029A), using both wide (300 Hz) and nar- as mated adults taken directly from stock colonies. row (45 Hz) band analysis. The frequency filter Leafhoppers were placed singly or multiply in was set at FL-1. Oscillograms of calls were made a glass cylinder (7 cm height by 4.6 cm diam) with by a pen and ink polygraph (Grass Model 7, DC the bottom end closed with stretched paranlm and driver amplifier). Because the polygraph could not the top end closed with a microphone fitted with respond quickly enough to frequencies >ca. 70 a foam collar. To dampen possible substrate vibra- Hz, the tape speed was slowed to lower the fre- tions, the cylinder was placed on a foam mat 5 cm quency. The slowest tape speed of the Nagra tape thick. We recorded leafhopper acoustic signals on recorder was our recording speed (i.e., 19 cm/s). magnetic tape (3M 250) with either a Uher 4000 Thus, signals were rerecorded on a Sangamo tape Report L tape recorder (40 Hz-20 kHz) and a recorder (Model 3562) at 152 cm/s (FM carrier Uher M514 dynamic microphone or with a Nagra 108 kHz, Flat response DC to 20 kHz) via filtering E tape recorder (30 Hz-20 kHz) and a condenser (Krohn-Hite variable filter 335R) at 300 Hz high microphone, preamplifer, power supply (Bruel and pass. The signals were then played back from the Kjaer 4130, 2642, 2810), and a DC amplifier Sangamo at 4.8 cm/s (FM carrier 3.375 kHz, Flat (Dana 3640). The latter equipment was used for response DC to 625 Hz) and rerecorded onto the the majority of recordings. Headphones were used Nagra tape recorder at 19 cm/s. Additional anal- to listen while recording. Most recordings were yses of signals were made using a storage oscillo- made at distances <3 cm from the calling insect. scope fitted with a camera (Tektronix 549, C-27). All recordings were made at 19 cm/s tape speed. Call terminology used herein is consistent with July 1986 HEADY ET AL.: Dalbulus ACOUSTIC AND MATING BEHAVIOR 729 Claridge et al. (1985). Calls are made of repeated sections and each section consists of phases. For example, D. elimatus calls have repeated sections that always consist of two phases (phases a and b) (Fig. 1A); in contrast, D. quinquenotatus calls have repeated sections with one phase (phase a) (Fig. 1J) or sometimes two phases (phases a and b) (Fig. 3A). Phases consist of groups of pulses (Fig. 2) and are designated by differences in pulse pattern. Oscillograms from 20 calls for each species were used to measure mean number of repeated sec- Downloaded from https://academic.oup.com/aesa/article-abstract/79/4/727/215293 by guest on 20 November 2018 tions per call. Oscillograms of four consecutive re- peated sections per individual leafhopper and four individuals per species were used to measure du- ration of call sections and phases (a and b), ratios of pulses in phases, and amplitude levels in phase a. Phase a was divided into 16 equal intervals and amplitudes measured (mm) at each of these Vi6 time intervals.