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 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 . 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 (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 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

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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 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 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. All combinations of amplitude ra- tios were calculated (e.g., amplitude of the signal at beginning [Beg] [Fig. 2A] to the midpoint of call [V2], and beginning to Vi6, etc.). Intersectional du- ration (s) was determined by measuring the dis- tance between 10 random sections. Dominant fre- quencies (frequencies that have the greatest amplitude [Broughton 1963]) were observed on sonograms and calculated from oscillograms. The variables of greatest interest (Table 1) were section duration, ratio of phase b to phase a du- Fig. 2. Enlargement of Fig. 1A. D. elimatus re- rations, pulse rate in phase b, intersectional dura- peated section of call showing pulse pattern. Time marker tion, and three amplitude ratios of pulse (i.e., ratio for both A and B is 0.03 s. A, beginning of phase a with between V|6 quantile point and beginning of call, markings where amplitude measurements made at be- V2 quantile to beginning of call, and % quantile to ginning (Beg), Vl6, and V& quantiles; B, group of pulses Vt quantile points). These ratios characterize re- of phase b. spectively, whether there are gradual or abrupt changes in amplitude at beginning of calls, mid- point amplitude differences, and whether the am- cages, in stock colonies, and in petri dishes on ta- plitude envelope was symmetrical. bletops. Means for data from these variables of greatest interest were calculated and because variances in- Results creased with the mean, data were log transformed to stabilize variance before repeated measures Males of all Dalbulus species produced common analysis of variance (Winer 1971). Species was the songs, courtship calls, rivalry calls, and distress calls. grouping factor and call per individual was the However, only courtship calls were recorded from repeated measure (trial factor). To compare means Dalbulus females using these methods. The num- within a variable, a Scott-Knott univariate, mean ber of repeated sections in a male common call of separation (Madden et al. 1982) was conducted a species is variable (e.g., D. elimatus emitted 1- whereby means were grouped into nonoverlap- 3 repeated sections [x — 1.5; SE = 0.13; n = 20], ping groups (P = 0.05). Then to compare the sim- whereas D. maidis emitted 1-11 repeated sections ilarities of calls of species using all the variables, a [x = 3.3; SE = 0.29; n = 20]). The number of multivariate, hierarchical cluster analysis of species phases within repeated sections is at most two (a using the single linkage method was performed on and b). D. elimatus, D. guevarai, D. longulus, and measured and calculated means (Dixon & Brown D. guzmani always emit phases a and b consecu- 1979). This clustering procedure, based on euclid- tively (Fig. 1 A-D and 3D), whereas D. tripsa- ean distances among variables, sequentially coides, D. gelbus, D. maidis, D. chiapensis, and grouped species based on their similarities with D. quinquenotatus may emit phase a only or phas- other species. es a and b (Fig. 1 E-J and 3 A-C). Approximately 100 observations of Dalbulus For section duration, intersectional duration, ra- courtship and, in some cases, copulation were con- tio of phase b to phase a durations, pulse rate in ducted in the glass recording chamber. Behavioral phase b, and amplitude ratios of pulses, there was observations were also made without acoustic sig- significant (P < 0.01) variation among species (Ta- nal recording while leafhoppers were in rearing ble 1). In all cases the variation within individuals 730 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 79, no. 4

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C D a 3000' 3000' 2000 - a / b 2000 " 1000" 1000 ' 40 1 i Fig. 3. Sonograms of Dalbulus spp. male common calls. Degree of darkening correlates with sound intensity. Frequency in hertz given on ordinate. Time in seconds given on abscissa. A, D. quinquenotatus; B, D. maidis; C, D. tripsacoides; D, D. guevarai. July 1986 HEADY ET AL.: Dalbulus ACOUSTIC AND MATING BEHAVIOR 731

Table 1. Male common call variables of Dalbulus spp.

Phase b: f-V II 1 Section Pulse rate Intersectional Amplitude ratios of pulses in phase a a Dalbulus spp. durations (s) phase a in phase b durations (s) 6 0 durations (s)fc ViffBeg VfeiBeg %:'/4 quinquenotatus 0.152D 1.403C 3.775B 3.592C 0.708B chiapensis 0.084E 0.691D 3.524B 4.024C 0.873B maidis 0.193C 0.953D 5.344A 14.594A 0.856B gelbus 0.125D 0.423D 2.656C 15.562A 1.844A tripsacoides 0.279B 2.612B 2.114C 15.760A 2.425A charlesi 0.222C 2.261B 1.276C 8.547B 2.234A

guzmani 0.277B 0.521C _d 1.117C 1.844C 15.594A 1.900A Downloaded from https://academic.oup.com/aesa/article-abstract/79/4/727/215293 by guest on 20 November 2018 longulus 1.232A 1.463A 64.333B 9.598A 7.391A 12.641A 1.229B guevarai 1.207A 1.517A 61.000B 14.950A 8.818A 9.448B 1.055B climatus 1.061A 1.045B 95.333A 7.870A 4.054C 15.604 A 1.080B

Means followed by the same letter within a column are not significantly different (P = 0.05) based on Scott-Knott cluster analysis of log-transformed data. Means based on 16 observations per species except for intersectional duration, which is based on 10. " Section duration is composed of phases a and b for D. guzmani, D. longulus, D. guevarai, and D. elimatus and phase a for other species. b Only four species consistently had phase b and, thus, could be compared. c Beg, beginning of phase a. d Pulse groups not segregated, so pulse rate undeterminable.

(repeated measures) of a species was not signifi- calls partitioned Dalbulus species into three main cant, nor was the interaction of repeated measures groups (Fig. 4). D. quinquenotatus and D. chia- and species significant (P > 0.20). Based on Scott- pensis composed the first group of the phenogram Knott separations (Table 1), D. elimatus, D. gue- at an amalgamation distance of 0.366. D. longulus, varai, and D. longulus had significantly longer re- D. guevarai, and D. elimatus composed the sec- peating sections than the other species, and D. ond group at an amalgamation distance of 1.916. chiapensis had the shortest. Of the four species The remaining species joined together and formed that always emitted phases a and b consecutively, a third group at 1.946. These three groups joined the duration of phase b of D. longulus and of D. with one another based on their similarities. guevarai calls was ca. 1.5-fold longer than phase Dominant frequency for pulses of all male Dal- a. D. elimatus produced phases a and b of about bulus spp. was ca. 1,000 Hz and, therefore, was equal duration. D. guzmani phase a duration was not used to differentiate species. From sonograms about twice as long as phase b duration (Table 1; (Fig. 3 and 5), a dominant frequency band was Fig. ID). Although no significant differences were apparent with overtone and undertone bands. Fre- noted in phase a pulse rate, three species could be quency bands are down-slurred (Alexander 1967) compared for phase b pulse rate. D. elimatus had among most of the Dalbulus spp. Up-slurring at the fastest pulse rate of phase b followed by D. the end of calls was characteristic only for D. char- guevarai and D. longulus, which were not signif- lesi and D. tripsacoides (Fig. 3C). Most Dalbulus icantly different from one another. Those species calls onomatopoetically would be termed croak- with the longest section duration were also those like; however, those of D. elimatus, D. guevarai, species with the longest intersectional duration and D. longulus are more tonelike due to the (Table 1). D. chiapensis, D. maidis, and D. gelbus greater length of the repeating section and nar- had the shortest intersectional duration. rower band width. The amplitude envelope was characterized by Temperature affected the duration of the re- amplitude ratios of pulses within phase a (Fig. 2A). peated section significantly (P < 0.05). With each Based on Scott-Knott separations, D. maidis, D. degree increase in temperature between 22 and longulus, and D. guevarai had the most abrupt 28°C, the total section duration decreased 0.03 s. changes in amplitude from the beginning of phase Adjusting section duration means for temperature a to the first Vl6 quantile point (Table 1). The pulse had no effect on the Scott-Knott mean separation. amplitudes of most species gradually increased No other acoustic parameter was affected by tem- from the beginning to the Vi6 quantile point. D. perature. Dalbulus leafhoppers did not produce quinquenotatus and D. chiapensis had the least calls below 17°C or above 32°C. increase in amplitude at the Vfe quantile compared Although courtship variations existed among with beginning of phase a. Although there was no species, there was an observable basic pattern of significant difference among %:lA amplitude ratios Dalbulus leafhopper courtship. Dalbulus leafhop- of D. gelbus, D. tripsacoides, D. charlesi, and D. pers will mate any time day or night ca. 30 h after guzmani, all these species were significantly dif- adult eclosion. No male was heard producing calls ferent from the other six species. For the remain- before that time. When a male produced common ing six species, there were no significant differ- calls (Fig. 3B), nearby receptive females would ences between them for %:V4 amplitude ratios. respond with courtship calls that were much lower The multivariate hierarchical cluster analysis of in frequency (300-500 Hz) than male calls and 732 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 79, no. 4

Dalbulus phylogeny Cluster tree based on based on morphology Dalbulus common calls

quinquenotatus chiapensis maidis gramalotes chariest tripsacoides Downloaded from https://academic.oup.com/aesa/article-abstract/79/4/727/215293 by guest on 20 November 2018 gelbus guzmani longulus el i mat us guevarai

amalgamation distance Fig. 4. Proposed phylogeny (cladogram) of Dalbulus spp. (Triplehorn & Nault 1985) at left and matched at right with cluster tree (phenogram) based on measured and calculated means given in Table 1. Species ordered on the basis of euclidean distances among them. Euclidean distance = square root of the sum of the squared differences between species for each of the variables. Amalgamation distance is the euclidean distance between species in a cluster. sounded like a rumble (Fig. 5A). Structure of male walk away. The male may try to join genitalia courtship calls resembled the structure of common again, and if allowed, the pair then orients end to calls but as more were produced in courtship, they end. Once in copula, a few calls are emitted (Fig. became shorter in duration and had a faster rep- 5C) and these may accompany dorsoventral puls- etition rate than common calls. Male courtship calls ing of the connected abdomens. Copulation pro- also have more phase b type sections as courtship ceeds until one member of the pair breaks away. progresses. As courtship began, the male and the Dalbulus males of at least four species are polyg- female alternated calls with one another. The fe- ynous. Dalbulus females do not mate a second time, male stopped walking, and the male flew or walked unless the first copulation has been interrupted. around her. When the male moved within 2-3 cm Another type of call produced by Dalbulus males of the female, the rate of alternating calls in- was the rivalry call (Fig. 5D) used in the context creased. As courtship continued, the male "danced" of intrasexual competition, usually among conspe- around her, calling continually. The dance was cifics. But interspecific pairs of males confined to- characterized by jerky running movements. The gether (e.g., D. elimatus and D. tripsacoides) in male may touch the body of the female, particu- the glass recording chamber also produced rivalry larly her abdomen or front tibia, with his head, calls. Two males will both emit rivalry calls par- abdomen, or legs. He may also "buzz" his wings ticularly if both are unmated and there is a female and produce another type of sound (Fig. 5B) that present. In this situation, one male eventually be- sounds like "snoring." Eventually, the male would comes quiet, and the other male will begin to court move his body parallel to hers and open his geni- the female. During one experiment, while a pair talia and move his abdomen to hers. If he was not was in copula, the other male began rivalry calls facing the same direction as the female, he some- and continued calling until the pair ended copu- times would attempt to join his genitalia to her lation. The unmated male then unsuccessfully at- head, but eventually he would turn around. An tempted courtship with the now mated and un- unreceptive female would extend her hind leg and receptive female. kick the male away, and if the male did not im- Finally, all male Dalbulus spp. produce short mediately begin to call again, the female would bursts of sound, typically of <45 ms durations.

Fig. 5. Sonograms of D. maidis calls. Same scales as in Fig. 3. A, male and female courtship calls early in courtship; B, gradual progression into snoring call by male; C, male copulatory calls; D, male rivalry calls; E, male distress ticks; F, male distress grunts. July 1986 HEADY ET AL.: Dalbulus ACOUSTIC AND MATING BEHAVIOR 733

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These bursts are unpatterned, irregularly emitted, rations (Table 1). Three species, D. longulus, D. and are likely to be distress or alarm calls. They guevarai, and D. elimatus, do not differ from one may be onomatopoetically termed ticking (Fig. 5E) another but do differ from other Dalbulus species or squawklike (Fig. 5F). Distress calls are pro- in male common call repeating sections and inter- duced by solitary males and by males in the pres- sectional durations (Table 1). These three species ence of other leaf hoppers. When males penetrated are allopatric and consequently are not likely to the paranlm of the recording chamber with their hybridize (Triplehorn & Nault 1985). Thus, selec- mouthparts and had difficulty withdrawing their tive pressures for behavioral isolating mechanisms stylets, they often produced distress calls. (e.g., calls) are absent. D. maidis and D. elimatus are sympatric in Mexico, and their calls probably serve as species-isolating mechanisms. Although no Downloaded from https://academic.oup.com/aesa/article-abstract/79/4/727/215293 by guest on 20 November 2018 Discussion D. elimatus and D. guevarai hybrids have been We have studied 10 of the 11 known Dalbulus found in the field, male D. elimatus will mate spp. and have determined that all produce sound. with female D. guevarai and produce viable off- Based on our cluster analysis, Dalbulus common spring (F,) in the laboratory (S.E.H., unpublished calls were divided into three major groups and data). Of species in the elimatus group, D. lon- these groups are similar to the three monophyletic gulus and D. guevarai are more acoustically sim- groups derived from external morphology (Fig. 4) ilar to each other (Table 1; Fig. 1) than either is (Triplehorn & Nault 1985). D. quinquenotatus and to D. elimatus. Despite the similarities of D. lon- D. chiapensis contain the most morphological ple- gulus and D. guevarai calls, no laboratory hybrids siomorphies. D. maidis, D. gramalotes, D. char- have been produced between these species. D. lesi, D. tripsacoides, and D. gelbus form the sec- quinquenotatus and D. chiapensis are morpholog- ond group, which is designated the maidis group. ically and acoustically similar but are allopatri- D. guzmani, D. longulus, D. guevarai, and D. eli- cally distributed. They too will court, copulate, matus form the third group, designated the eli- and produce viable offspring (F,) infrequently in matus group, which has the most derived mor- the laboratory when male D. quinquenotatus are phological characters. Evidence from isoenzymes crossed with female D. chiapensis. No other in- (B. W. Triplehorn, G.F.S., and L.R.N., unpub- terspecific matings have been successful among lished data), oviposition behavior (Heady et al. other Dalbulus spp. combinations (S.E.H. & B. W. 1985), and egg microfilaments (Heady & Nault Triplehorn, unpublished data). Thus, common calls 1984) further supports these relationships. The may act as isolating mechanisms. phenogram produced from data from male com- The amplitude envelope, or shape of the call, mon calls of Dalbulus (Fig. 4), like isoenzyme was important for differentiating Dalbulus at least analysis, failed to place D. guzmani in the eli- into groups. While the common calls of the eli- matus group. Morphologically, D. guzmani re- matus group, particularly D. guevarai, are similar sembles species in the elimatus group because it (Fig. 3D) to that of lineolatus Brulle always has phase b, but in other acoustic variables, (Michelsen et al. 1982), the pulse structures of calls such as section and intersectional duration, it is of other Dalbulus species are very different from most similar to those species of the maidis group. those of other Cicadellidae (see references in Cla- Shaw et al. (1974) did not find the common songs ridge [1983, 1985a,b]). of Empoasca spp. to be species specific and, thus, Unlike many insect species that produce sounds postulated that common calls are probably not dependent on temperature, we found only section species-isolating mechanisms. They suggested that duration of Dalbulus to be affected by tempera- the courtship call of Empoasca may be the isola- ture. A number of call variables of Muellerianella tor. Claridge & Howse (1968) and M. F. Claridge (Booij 1982) and Javesella (de Vrijer 1984) are & G. A. Nixon (personal communication) deter- affected by temperature changes. Claridge (1985b) mined that common songs and courtship calls of did not find much effect of temperature on Nila- Oncopsis are species specific. In another study, parvata lugens (Stal), which, like Dalbulus, comes Fleming (1971) determined that the calls of allo- from a tropical region. patric species were not clearly different. In Rivalry calls were first recognized by Ossian- contrast, Striibing & Hasse (1975) found differ- nilsson (1949) in the Auchenorrhyncha, but he ences in calls of allopatric Javesella found them only in a single species, Achorotile species. Whether differences are detected among albosignata (Dahlberg). Rivalry calls since have species by researchers in part depends on methods been identified in Oncopsis (Claridge & Howse used, analysis techniques, and even the number of 1968) and N. lugens (Ichikawa 1982). Male rivalry species examined. calling may be induced by keeping virgin males In our study of Dalbulus common calls, we found together for several days before female introduc- that no one particular measured acoustic variable tion (Ichikawa 1982). In our studies, Dalbulus vir- uniquely identified all species. However, 8 of the gin males that were kept together for several days 10 species produce species-specific common calls also produced male rivalry calls. that are characterized by unique combinations of Distress sounds of Dalbulus (Fig. 5 E and F) are repeating section durations and intersectional du- similar to the ticking sounds of Agallia constricta July 1986 HEADY ET AL.: Dalbulus ACOUSTIC AND MATING BEHAVIOR 735

Van Duzee and Agalliopsis novella (Say) (Shaw 84-CRCR-1-1370) appropriated to the Ohio Agric. Res. 1976) and the disturbance sounds of Empoasca and Dev. Center, The Ohio State Univ. This is Journal fabae Harris (Vargo 1973, Shaw et al. 1974, Shaw Article No. 167-85. 1976). Whether distress sounds are communicated interspecifically or intraspecin'cally or both is un- known. References Cited The male and female behavior of alternating Alexander, R. D. 1967. Acoustical communication in calls with one another during courtship has been . Annu. Rev. Entomol. 12: 495-526. reported for leafhoppers and (Shaw Alexander, R. D. & T. E. Moore. 1958. Studies on et al. 1974, Shaw 1976, Ichikawa 1979, Saxena & the acoustical behaviour of seventeen-year cicadas Kumar 1984). However, it is not characteristic of (Homoptera: Cicadellidae: Magicidada). Ohio J. Sci. Downloaded from https://academic.oup.com/aesa/article-abstract/79/4/727/215293 by guest on 20 November 2018 all Auchenorrhyncha, as cicada females are mute 58: 107-127. Booij, C. J. H. 1982. Biosystematics of the Muelleri- (Claridge 1985b). Dalbulus female courtship calls anella complex (Homoptera, ), interspe- appear similar to the "cooing" sounds of Amrasca cific and geographic variation in acoustic behaviour. devastans (Distant) (Saxena & Kumar 1984) but Z. Tierpsychol. 58: 31-52. are much less patterned than those of Empoasca Broughton, W. B. 1963. Method in bioacoustic ter- (Shaw et al. 1974), A. constricta, and A. novella minology, pp. 3-24. In R. G. Busnel [ed.], Acoustic (Shaw 1976). Like A. novella (Shaw 1976), Dal- behavior of . Elsevier, New York. bulus males produce buzzing by wing vibration Claridge, M. F. 1983. Acoustic signals and species and a "snoring" sound before copulation that may problems in the Auchenorrhyncha, pp. 11-20. In W. be similar to sounds made by A. devastans (Saxena J. Knight, N. C. Pant, T. S. Robertson & M. R. Wilson [eds.], Proceedings 1st International Workshop on & Kumar 1984). During copulation by Dalbulus, Leafhoppers and Planthoppers of Economic Impor- calls are produced and although we are not certain tance. Commonwealth Inst. Entomol., London. which sex is producing the call, we believe the 1985a. Acoustic signals in the Homoptera: behavior, male is responsible. The male's movements affect , and evolution. Annu. Rev. Entomol. 30: the characteristics of the call, whereas female wing 297-317. or other body movements during calls do not affect 1985b. Acoustic behaviour of leafhoppers and plant- the call. hoppers: species problems and speciation, pp. 103- During copulation, Dalbulus leafhoppers move 125. In L. R. Nault & J. G. Rodriguez [eds.], The their abdomens dorsoventrally. This abdominal leafhoppers and planthoppers. Wiley, New York. Claridge, M. F. & P. E. Howse. 1968. Songs of some pulsing may indicate sperm transfer, but as West- British Oncopsis species (: Cicadellidae). Eberhard (1984) suggested, it may not entail sperm Proc. R. Entomol. Soc. London Ser. A 43: 57-61. transfer but rather serve to stimulate females to Claridge, M. F. & W. J. Reynolds. 1973. Male court- continue courtship and facilitate copulation. ship songs and sibling species in the Oncopsis flavi- Like other small Auchenorrhyncha, we believe collis species group (Hemiptera: Cicadellidae). J. that Dalbulus communicate with one another by Entomol. Ser. B Taxon. 42: 29-39. acoustic signals via the substrate (Ichikawa & Ishii Claridge, M. F., J. Den Hollander & J. C. Morgan. 1974, Ichikawa et al. 1975, Ichikawa 1976, 1979). 1985. Variation in courtship signals and hybridiza- tion between geographically definable populations of Subsequent to these studies, we used a phonograph the rice brown planthopper, Nilvaparvata lugens cartridge (Claridge 1985a,b) to record substrate (Stal). Biol. J. Linn. Soc. 24: 35-49. signals in D. maidis, D. elimatus, and D. quin- D'Arcy, C. J. & L. R. Nault. 1982. Insect transmission quenotatus. An analysis of these substrate record- of plant viruses, mycoplasmalike and rickettsialike ed signals revealed that they are virtually identical organisms. Plant. Dis. 66: 99-104. with the airborne recorded signals we report here. de Vrijer, P. 1984. Variability in calling signals of Cicadas respond to airborne signals via a tympa- the planthopper Javesella pellucida (Homoptera: num, an organ unknown in the small Auchenor- Delphacidae) in relation to temperature and conse- rhyncha (Claridge 1985b). Until the organs of quences for species recognition during distant com- acoustic reception in the small Auchenorrhyncha munication. Neth. J. Zool. 34: 388-407. are identified, the relative importance of substrate Dixon, W. J. & M. B. Brown [eds.]. 1979. Biomed- ical computer programs P-series. Univ. of California, versus airborne acoustic signals will remain in Berkeley. question. Faber, A. 1929. Die Lautausserungen der Orthopte- ren. I. Z. Morphol. Okol. Tiere 13: 745-803. 1932. Die Lautausserungen der Orthopteren. II. Z. Acknowledgment Morphol. Okol. Tiere 26: 1-93. Fleming, C. A. 1971. A new species of cicada from We thank Randy Fetcenko (Bruel and Kjaer), Ross rock fans in southern Wellington, with a review of Brazee and Rex Alvey (Agricultural Engineering, ARS- three species with similar songs and habitat. N.Z. J. USDA), Mike Claridge (University College, Cardiff), and Sci. 14: 443-479. The Borror Bioacoustic Laboratory (OSU) for advice, Heady, S. E. & L. R. Nault. 1984. Leafhopper egg assistance, and equipment usage. We also thank Larry microfilaments (Homoptera: Cicadellidae). Ann. Madden for statistical assistance. Salaries and research Entomol. Soc. Am. 77: 610-615. support provided by State and Federal funds (especially Heady, S. E., L. V. Madden & L. R. Nault. 1985. USDA Competitive Grants No. 81-CRCR-1-0646 and Oviposition behavior of Dalbulus leafhoppers (Ho- 736 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 79, no. 4

moptera: Cicadellidae). Ann. Entomol. Soc. Am. 78: per, Amarasca devastans. Physiol. Entomol. 9: 77- 723-727. 86. Ichikawa, T. 1976. Mutual communication by sub- Shaw, K. 1976. Sounds and associated behavior of strate vibration in the mating behaviour of planthop- Agallia constricta and Agalliopsis novella (Homop- pers (Homoptera: Delphacidae). Appl. Entomol. Zool. tera: Auchenorrhyncha: Cicadellidae). J. Kans. Ento- 11: 8-23. mol. Soc. 49: 1-17. 1979. Studies on the mating behaviour of four species Shaw, K. C, A. Vargo & O. V. Carlson. 1974. Sounds of auchenorrhynchous Homoptera which attack the and associated behavior of some species of Empoasca rice plant. Mem. Fac. Agric. Kagawa Univ. 34: 1- (Homoptera: Cicadellidae). J. Kans. Entomol. Soc. 60. 47: 284-307. 1982. Density-related changes in male-male compet- Striibing, H. 1970. Zur Artberechtigung von Euscelis itive behaviour in the rice brown planthopper, Ni- alsius Ribaut Gegenuber Euscelis plebejus Fall. (Ho- Downloaded from https://academic.oup.com/aesa/article-abstract/79/4/727/215293 by guest on 20 November 2018 laparvata lugens (Stal) (Homoptera: Delphacidae). moptera-Cicadina). Ein Beitrag zur Neuen Syste- Appl. Entomol. Zool. 17: 439-452. matik. Zool. Beitr. 16: 441-478. Ichikawa, T. & S. Ishii. 1974. Mating signal of the 1976. Euscelis ormaderensis Remane 1968. 1. Sai- brown planthopper Nilaparvata lugens (Stal) (Ho- sonformenbildung und akustische Signalgebung. Sit- moptera: Delphacidae): vibration of the substrate. zungber. Ges. Naturforsch. Freunde Berlin 16: 151- Appl. Entomol. Zool. 9: 196-198. 160. Ichikawa, T., M. Sakuma & S. Ishii. 1975. Substrate 1983. Die Bedeutung des Kommunikationssignals fur vibrations: mating signal of three species of plant- die Diagnose von Eusce/is-Arten (Homoptera-Cica- hoppers which attack the rice plant. Appl. Entomol. dina). Zool. Jahrb. Physiol. 87: 343-351. Zool. 10: 162-171. Striibing, H. & A. Hasse. 1975. Ein Beitrag zur neuen Madden, L. V., J. K. Knoke & R. Louie. 1982. Con- Systematik—demonstriert am Beispiel zweier Jave- siderations for the use of multiple comparisons pro- sella-Arten (Homoptera-Cicadina: Delphacidae). cedures in phytopathological investigations. Phyto- Zool. Beitr. 21: 517-543. pathology 72: 1015-1017. Triplehorn, B. W. & L. R. Nault. 1985. Phylogenetic Michelsen, A., F. Fink, M. Cogala & D. Traue. 1982. classification of the genus Dalbulus (Homoptera: Plants as transmission channels for insect vibrational Cicadellidae), and notes on the phylogeny of the songs. Behav. Ecol. Sociobiol. 11: 269-281. Macrostelini. Ann. Entomol. Soc. Am. 78: 291-315. Nault, L. R. & L. V. Madden. 1985. Ecological strat- Vargo, A. 1973. Intraspecin'c communication of Em- egies of Dalbulus leafhoppers. Ecol. Entomol. 10: poasca fabae and Empoasca obtusa (Homoptera: 57-63. Cicadellidae): a comparative analysis. Ph.D. disser- Ossiannilsson, F. 1949. Insect drummers. A study on tation, Iowa State Univ., Ames. the morphology and function of the sound-produc- West-Eberhard, M. J. 1984. Sexual selection, com- ing organ of Swedish Homoptera Auchenorrhyncha petitive communication and species-specific signals with notes on their sound-production. Opusc. Ento- in insects, pp. 283-324. In T. Lewis [ed.], Insect com- mol. Suppl. 10: 1-145. munication. Academic, London. Purcell, A. H. & W. Loher. 1976. Acoustical and Winer, B. J. 1971. Statistical principles in experi- mating behavior of two taxa in the Macrosteles fas- mental design, 2nd ed. McGraw-Hill, New York. cifrons species complex. Ann. Entomol. Soc. Am. 69: 513-518. Received for publication 20 September 1985; accept- Saxena, K. N. & H. Kumar. 1984. Acoustic com- ed 16 April 1986. munication in the sexual behaviour of the leafhop-