Dispersal by Flight of Leafhoppers (Auchenorrhyncha: Homoptera)

Home , Arthaldeus, Cercopis vulnerata, Cicadulina, Corixidae, Doratura, Elymana

DISPERSAL BY FLIGHT OF LEAFHOPPERS (AUCHENORRHYNCHA: HOMOPTERA)

BY N. WALOFF

Departmentof Zoology and AppliedEntomology, ImperialCollege, London S. W.7.

INTRODUCTION In thelast fewyears a seriesof studieson thebionomics and ecologyof leafhoppers have been carriedout at theImperial College Field Station,Silwood Park,Berkshire. Results of a surveyof the speciesbreeding in acidic grasslandshave been reported(Waloff & Solomon 1973). Dispersal by flightof leafhoppersand the catchesin the aerial suction traps and in variousinterference traps, have also been studied.The interestin these problemsis two-fold,firstly, because dispersalto and frombreeding sites contributes to fluctuationsin the sizes of populations(see May 1971; Tay 1972; Solomon 1973) and, secondly,because many of these plant-suckinginsects are vectorsof plant diseases; transmittingviruses or mycoplasmato variousgraminaceous crops, clover, strawberries and otherplants (Slykhuis& Watson 1958; Watson & Sinha 1959; Raatikainen & Tinnila 1959; Maramorosch,Shikata & Granados 1968; Fewkes 1969; Nakasuji & Kiritani1970). Littleis knownabout thetimes of the year in whichthe leaf hoppers in Britaindisperse by flight,and theseaspects have been summarizedin thispaper. In thiscountry, leaf- hoppersare consideredpests of minorimportance only, but in partsof Europe,in North Americaand in tropicalcountries the effectsof transmittedplant diseases and of direct damage caused by leafhopperson cropsassume a highsignificance. Recently, the direct effectsof feeding,coupled withthe intenseoutbreaks of the delphacidSaccharosydne saccharivora(Westw.) on sugar cane throughoutthe Caribbean have been described (Metcalfe1971). Closely associatedwith dispersal by flightare the problemsof alary polymorphism, whichare both widespreadand diversifiedthroughout the Auchenorrhyncha.

METHODS Flight Dispersal by flightwas investigatedby recordingthe numbersof Auchenorrhyncha capturedin the aerial suctiontraps (Johnson 1950, 1957; Johnson& Taylor 1955; Taylor 1951, 1955, 1962). Traps IL and IV are permanentlysited east of Elm Ridge at Silwood,adjacent to one another,with trap II suspended1 2 m and trapIV 9*1m above groundlevel. Both are 46 cm in diameterand the inputof air is 71 m3/min.A third suctiontrap, 12 2 m above groundlevel and 65 m westof the other two, has beenoperated since 1969.It is referredto as the Rothamstedtrap (R.T.). Supplementarysuction-traps, 23 cm diameter,were also used in thisstudy. They were locatedon sitesof populationstudies on Psanimotettixconfines (Solomon 1973),Cicadella viridis(Tay 1972) and Stenocranusnminutus (May 1971). Anothersimilar trap which 705 706 Dispersalby flight of leafhoppers

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=$ Co 710 Dispersalby flight of leafhoppers segregatedthe catch into hourlysamples was erectedby traps II and IV in 1972. In addition,water traps and pots containinggrasses on whichthe flyinginsects landed weresuspended at 0l6, 1 2, 1 8 m above theground level within the area of study(Waloff & Solomon 1973).There were two watertraps and tensets of suspendedpots distributed throughthe 1-hafield. The catcheswere removed daily and preservedin 7000 alcohol forsorting and identi- ficationin winter.The data weresupplemented by catchesmade in 1962.Simultaneously, withsampling of the aerial populations,the seasonal abundanceof the acidic grassland species was recordedin the fieldand the methodsused are summarizedin Waloff& Solomon (1973). Flitting Flittingwas examinedin 1968,when ten sets,each of threepots withgrasses, which were periodicallyrenewed, were suspendedon poles at heightsof 0-6, 1 2 and 1-8 m above the groundlevel. The thirtypots wereexamined daily and any leafhoppersthat settledon themwere beaten on to a tray,collected and recorded.It can be seenin Table 2, thatas generationtime progressed, fewer insects settled on thehigher pots and more on the lowerones and thiscoincided with greater proportions of matureindividuals. Females were dissectedand the immatureones given the value of - 1, those with developingoocytes -2, and thosewith fully developed eggs -3 and spentfemales -4. The indicesof maturitybeing the averages of thesevalues. It maybe inferredfrom these data (Table 2) thatmature individuals tend to flit. Laboratorytests Some laboratorytests were made to see whetherthe leafhopperswould continueto flyon reachingmaturation. These werenot testsfor migratory abilities but theyhelped to distinguishbetween the femaleswhich retained flight ability throughout their lives fromthese that lost it withage. The insectswere gently shaken out of a tubeat a heightof 0l6 m intoa container1Il0 m longwith muslin sides and roof,a transparentwindow at one end and an open side at the releasingend. Some flewstraight to thewindow, others dropped on thefloor and hopped towardsit. This was repeatedfive times with each individualinsect. Secondly, the insects werereleased on to thefloor, one at a time,and gentlyprodded with a paintbrush, some onlyhopped, while the flyershopped and flitted.This was also repeatedfive times with each insect.The flyersand non-flyerswere then dissectedto ascertaintheir state of maturationand measurementsof their body length, the length of thefore and hindwings and of hindtibia (Table 7). Macrostelessexnotatus, Balclutha punctata retained powers offlight to death,whereas in otherspecies, e.g. Arthaldeus pascuellus, Streptanus sordidus, Euscelisplebejus, Diplocolenus abdorninalis, Elymana sulphurella, the older femaleswith abdomens distendedwith eggs, appeared to lose the abilityto flyand only hopped.

RESULTS The seasonal incidenceof flying Auchenorrhyncha The seasonal incidenceof flightof leafhoppersand froghoppersis summarizedin Table 1. One hundredand fifteenspecies were identifiedin the catchesin the Silwood traps; threeCercopidae, fifty-eight Cicadellidae, twenty-nine plus Typhlocybinae,two Cixiidae and twenty-threeDelphacidae. This list constitutesone-third of the British speciesof Auchenorrhyncha. N. WALOFF 711 Table 2. Numbersof leafhopperssettling on grass in pots suspendedat differentheights and the indicesof maturityof thefemales in thesamples (1968) Date No. in Heightabove ground sample 1-8m 1-2m 0-6m 1-8m 1-2m 0-6m Proportionof sample Indexof maturity 16-31 May 17 0-88 0-12 000 1-3 - - 1-15June 42 0-67 0-21 0-12 1-7 1-5 16-30June 45 0-22 0-51 0-27 1.9 2-5 - 1-16July 36 0-14 0-28 0-58 1-8 2-0 2-7

The yearlycatches were small, the combined totals from traps II, IV and R.T. ranging betweena 1000and 1400in 1969to 1972.Generally, about one-halfof each annualcatch comprisedJavesella pellucida,Macrosteles sexnotatusand M. laevis only (Table 3). All are activeflyers, but not the most abundantlocal speciesand are vectorsof plant diseases.Javesella pellucida transmits the Europeanwheat striate mosaic virus(Watson & Sinha 1959) and the Macrostelesspp. carrythe 'astersyellow' mycoplasma. The proportionsin whichthe different families of Auchenorrhyncha formed the monthly catches in aerial traps are given in Table 4. As most delphacid species hibernateas nymphs,their adults were the firstto emergeand formedthe bulk of the catchin April and May. By June,the Cicadellidae,most of whichhibernated as eggs,were the most abundantboth in thefield and in theair, while the numbers of adultdelphacids declined. By mid-July,the second generationof adult delphacidsemerged and theirincidence in the aerial trapsrose. The second generationsof cicadellidadults tended to overlapwith thedelphacids, but whereasthe latter died out by theend of August,or in thefirst week of September,the cicadellidspersisted and some species continuedto emergeinto the adult stage into October. By Septemberand October the numbersof Typhlocybinae increasedand by November,only the Typhlocybinae and the occasionalcicadellids that hibernatedas adults(e.g. Balcluthapunctata, Mocydiopsis parvicauda) were caught in the aerial traps.

Table 3 (a). Numberof species and individualsof Auchenorrhyncha caught in suctiontraps II (1 2 m), IV (9 1 m), R.T. (12.2 m) at SilwoodPark 1970-71 Cercopidae Cicadellidae TyphlocybinaeCixiidae Delphacidae 1970 No. species 2 31 - 2 13 No. individuals 2 634 269 30 343 Totalcatch: 1276 1971 No. species 3 23 - 2 9 No. individuals 4 469 437 16 164 Total catch:1090

Table 3 (b). Proportionof totalannual catch made of Javesellapellucida Macrostelessexnotatus and M. laevis 1970 1971 No. 0 of catch No. 0 of catch J. pellucida 286 22 140 13 M. sexnotatus 344 27 278 26 M. laevis 82 8 90 9 Total 712 57 508 48 712 Dispersalby flight of leafhoppers Table 4. Totalmonthly catches of Auchenorrhyncha in aerial trapsII (1 2 m) and IV (9.1 m) at SilwoodPark, 1969-71 Month Total Percentageof totalcatch catch Cixiidae Cercopidae Delphacidae Cicadellidae Typhlocybinae Apr. 14 - - 1000 - - May 349 9 5 - 74-5 7-7 8-3 June 755 1-7 01 8-7 72-7 16-7 July 491 1P2 0 5 29-5 46 6 22-2 Aug. 507 0-6 0-2 35 9 48-5 14-8 Sept. 523 0 4 - 1-3 56 9 41-3 Oct. 311 - - - 12-2 87-8 Total for 3 years 2950 Percentagetotal for3 years 1.9 0.1 22-8 470 28-1

Patternsof flight (a) The two permanentlysited and adjacentsuction traps, one at 1 2 m, the otherat 9l1 m above groundlevel, probably distinguish between the more actively flying grassland speciesfrom the poorerflyers. The slopes of the lines of the logarithmsof the seasonal catches on the logarithmsof heightsof traps,provide an index of the abilityof the speciesto disperse.Examples of catchesof six commongrassland species are givenin Fig. I (a), fromwhich it maybe inferredthat although the numbers of flyingMacrosteles

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06 10 1 48 log Heightof aerial trap(m) FIG. 1. Differencesin dispersalpatterns of leafhoppers.(a) Grassland-dwellingspecies: 0, Macrostelessexnotatus; o, Javesellapellucida; A, Zygina scutellaris; I, Arthaldeuspas- cuel/us; *, Balciutha punctata; F, Psammotettixconfines. (b) Tree-living species: 0, Oncopsis spp.; o, Allygusspp.; A, Macropsis spp.; A, Idiocerusspp. N. WALOFF 713 sexnotatus,Javesella pellucida and Zyginascutellaris were greater than those of Psanimo- tettixconfines, individuals of thelatter species may have flowngreater distances and that withinthis group of insects,Arthaldeus pascuellus had thelowest power of dispersal.In contrastto thesespecies, the numbersof Balcluthapunctata were greater in the higher trap.This mayhave a bearingon itsbionomics, as thisgrassland species hibernates as an adult on pine treesand in the grasstussocks. (b) The patternsof flightwere differentin the grass-dwellingand the tree-dwelling Cicadellidae,which formed 10% ofthe catch of thisfamily. The catchesof thecicadellids in the two trapsin 1969-71 are shownin Fig. 1(b). Greaternumbers of the twenty-six speciesinhabiting ground vegetation were caught in the lowerthan in the highertrap, whereasthe reversewas trueof the seventeentree-living species, the exception being the grass-dwellingB. punctata.

EFFECTS OF WEATHER ON FLIGHT

To see whetherflight, as measuredby the daily catches in thesuction traps was influenced byweather, multiple correlation analyses were made on thenumbers ofJavesellapellucida, Macrostelessexnotatus and Arthaldeuspascuell/is with the independentvariables which comprisedthe mean and maximumdaily temperatures, hours of sunshine,average wind speed,day of flight(day I beingthe firstday of catch),the 'indexof abundance'which was measuredby the numbersof adultsin thefield samples and the 'indexof maturity'. From theseanalyses it maybe seen thatmost of thevalues of R are significant(Table 5). However,the values of R2 indicatethat much of the variance is stillnot accountedfor by the independentvariables. Temperaturestimulated flight in all the threespecies (indicated by positivecorrela- tions) and higherwind speeds inhibitedit as is indicatedby negativecorrelations. No significanteffects of thehours of sunshine,nor of abundancein thefield and of the day of flightwere obtained. It is also probablethat insufficiency of data accountfor the two non-significantcorrelations with the 'index of maturity',since the inhibitingeffects of maturationon flightwere seen in laboratorytests on Javesellapellucida and Arthaldeus pascuellus.Moreover, Nuorteva (1962) notedthat the mass migratoryflight of Javesella pellucidais commonlythe firstflight of immatureadults. Lewis & Taylor (1965) showedthat althoughMacrosteles sexnotatus fly throughout theday, its peak offlight is between17.00-19.00 hours G.M.T. At Silwoodthe mean tem- peraturebetween these hours on the days of flightwas 17.50 C, butthere was no correlation betweenvariations around this mean and the numbersof Macrostelesin traps. The thresholdof daily mean temperatureon thedays of flight was above 14?C and that ofthe maximum at or above 200 C. Furthermore,in thisspecies there was littleflight at wind speeds above 6&2m s- . In Javesellapellucida, flight occurred when the mean daily and maximumtemperatures were at or above 15? and 20? C respectively.Winds above 4 2-4 6 m s -' appeared to have an inhibitingeffect. In thethree species examined, the hours of sunshinehad littleinfluence, as obtainedby May (1971) withStenocranus minutes, where temperatures above 15? C and windspeeds below 7 7 rns-' low sunshinehours favoured flight. By contrast,flight in Cicadella viridiswas positivelycorrelated with hours of sunshine and negativelywith a decreasein hoursof rainfall(Tay 1972). 714 Dispersalby flight of leafhoppers

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LIFE HISTORIES AND TIME OF DISPERSAL Johnson(1969) considersthat there are threeclasses of migrationin insects:(1) emigra- tion withoutreturn, usually by relativelyshort-lived adults; (2) emigrationand return by the same individualswithin a season; and (3) emigrationto hibernationand aestiva- tion sitesand returnby the same individualsafter imaginal diapause.

Table 6. Voltinism,hibernation stage and timeof dispersalby flight Hibernation stage Timeof dispersalby flight Species Univoltinespp. Egg Mainlyimmature adults Philaenusspumarius (Cerc.*) Neophilaenuslineatus (Cerc.*) Cercopis vulnerata(Cerc.*) Cicadella viridis(C) Graphocephalacoccinea (C) Doratura stylata (C) Diplocolenusabdominalis (C) Deltocephalus coronifer(C) Graphocraerusventralis (C) Elymana sulphurella(C) Conomelusanceps (D) Adult Pre-hibernationflight Mocydiopsisparvicauda (C) Stenocranusminutus (D) Pre-and post-hibernationflight Baicluthapunctata (C) Bivoltinespp. Egg (a) In 1stgeneration only Errastunusocellaris (C) Egg (b) In 1stgeneration with very Jassarguspseudocellaris (C) small proportionin 2nd Arthaldeuspascuellus (C) Streptanussordidus (C) Laodelphax elegantulus(D) Nymph (c) In both1st and 2nd Psammotettixconfines (C) generations Cicadula persimilis(C) Macrostelessexnotatus (C) M. laevis (C) \M.viridigriseus (C) Euscelisplebejus (C) Javesellapellucida (D) Muirodelphaxexiguus (D) Paraliburniadalei (D) Xanthodelphaxstramineus (D) Polyvoltinespp. Nymphand adult Flightin successivegenerations Zyginascutellaris (T) * Cerc,Cercopidae; C, Cicadellidae;D, Delphacidae;T, Typhlocybinae. The majorityof Auchenorrhynchaexamined appeared to fall into class 1. However, someindividuals of thecicadellid Bal/lutha punctata hibernate on pine treesand in grass tussocksand may returnto the originalbreeding sites, therefore, this speciesfalls into class 3. Most of the grasslandspecies studied were either univoltine or bivoltineand the only certainpolyvoltine species encountered was the typhlocybid,Zygina scutellaris. The incidenceof dispersalby flightwithin the life cycles is summarizedin Table 6 and in Figs. 2-5. 716 Dispersalby flight of leafhoppers

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D 718 Dispersalby flight of leafhoppers Migratoryflight in leafhoppersoccurs when the females are teneraland stillimmature (Lawson, Chamberlain& York 1951; Nuortova 1962; Johnson1965, 1966, 1969). It is possible,however, that some of the leafhopper species, for instance Macrosteles sexnotatus, continueto flyactively between successive ovipositions, whereas others, e.g. Arthaldeus pascuellus,Elymana sulphurella, become less activeon maturation(see below). Balclutha punctatahas a pre-and a post-hibernationflight and remainscompletely immature, with thread-likeovarioles, from the time of its emergencein late summeror autumnuntil the followingspring. On the otherhand, Mocydiopsis parvicauda, which has onlyone flight period,preceding the imaginaldiapause, may begin to maturein autumn,i.e. its oocytes beginto grow.However, they do not reachfull size and theovaries regress to thethread- likecondition in the winter. In thebivoltine species, and in Delphacidae in particular,the proportions of theflying individualsin the two annual generationsare closelylinked with alary polymorphism, i.e. withthe proportionsof populationsthat are brachypterous. It was also ofinterest that some of the more actively flying species were capable ofmass exodusfrom their breeding sites. Thus Balcluthapunctata which formed a largebreeding colonyin 'thestudy area' (Waloff& Solomon 1973),emigrated on reachingits adult stage in 1969. Similarly,Macrosteles laevis which colonized a disturbedsite in 'the studyarea' in 1968 and formeda largebreeding colony for four generations, took offfrom this site whenit became overgrownby densevegetation.

ALARY POLYMORPHISM IN LEAFHOPPERS Alary polymorphismis widespreadin Auchenorrhyncha,but whereasit is frequentin speciesliving in grassesor otherlow vegetation,so far,only the macropterousforms of tree-livingleafhoppers have been encounteredin Britain. The femaleflyers and non-flyersare subdividedinto five groups, but it is emphasized thatthe abilityto flyis not necessarilysynonymous with that to migrate.

Group1: macropterousspecies, in whichfemales retain ability to flythroughout their lives The abilityto flywas testedas describedand by theincidence of individualsin suction traps,e.g. Macrostelessexnotatus and M. laevis.Some speciesof the genusMacrosteles are veryactive flyersand the long-rangemigrations of M. fascifrons(Stal) in North America, have been extensivelystudied and linked with synopticmeteorology (see Johnson1969; Chiykowski& Chapman 1965; Medler 1962; Miller & De Lyzer 1960; Westdal,Barrett & Richardson1961; Wallis 1962). However,even this activelyflying specieshas short-wingedforms in isolatedpopulations (Beirne 1956; Severin1940). A few,relatively short-winged males of M. sexnotatuswere encounteredin the field samplesat Silwood in 1970.They were different from the usual forms,in havingshorter bodies as well as wings,and wereonly recognized as M. sexnotatusafter examination of theirgenitalia and sternalapodemes. Equal numbersof males and femalesof M. sexnotatusand M. laeviswere caught in the suctiontraps.

Group2: macropterousspecies in whichflight ability greatly diminishes, or is lost with maturationand age Numerousspecies fall into this group, e.g. Elymanasulphurella, Diplocolenus abdomin- alis, Cicadellaviridis and themacropterous forms of thedelphacid Javesella pellucida. In thesespecies flight tends to be inhibitedby maturation. N. WALOFF 719 Group3: speciesthat can be distinguishedinto macropterous and sub-macropterousforms All individualsof this group are capable of flight,but at Silwood,only the macropterousforms have been caughtin thesuction traps and are presumedto be themigratory forms.One specieswithin this group is the delphacid,Stenocranus minutus (May 1971). Muller(1957, 1958, 1960) foundthat when its larvaewere subjected to a shorterphoto- periodthan normally experienced, different morphological forms were produced and it is probablethat differencesin day lengthand in otherenvironmental conditions may be criticalin the productionof submacroptersand macropters.However, macropterous individualsfound by May (1971) have not been previouslyencountered or described.

Table 7. Means and ratiosoffore- and hind-winglengths of flyers and non- flyers

Mean wing Significanceof comparison length(mm)t Ratio of means No. and sex (F) (H) (F)/(H) t P

Errastunusocellaris 15?? Non-flyers 3 00 2-50 1P20 (F)t 5 749 179? Flyers 3 49 3-17 1-10 (H) 7-553 34&& Non-flyers 2-94 2-31 1-27 (F) 0.898 n.s. 5&& Flyers 3-16 2-84 1-11 (H) 4-257 Arthaldeuspascuellhs 10S Non-flyers 3 40 2-58 1-32 (F) 1-168 n.s. 8?? Flyers 3 54 3 03 1I18 (H) 3.195 * 15&S Non-flyers 2-97 2-34 1-27 (F) 3.359 * 15&S Flyers 3-23 2-91 111 (H) 6-715 Psammotettixconfines 1st generation 4?? Non-flyers 3-52 3-02 1-17 (F) 0-603 n.s. 21S? Flyers 3-60 3 03 1-19 (H) 0-119 n.s. 2nd generation 14?? Non-flyers 3-51 2-84 1P24 (F) 0-327 n.s. 15?? Flyers 3-53 3 00 1418 (H) 1P833 n.s. 10&& Non-flyers 3 49 2-72 1-28 (F) 0-235 n.s. 18&d Flyers 3-47 3 00 1P16 (H) 2-778 * *, P<0.05; ***, P<0-001; n.s., not significant. t F, Fore-wing; H, hind-wing.

At 250 C tetheredand suspendedmacropters flew on averagefor 1200 s and submacroptersfor 240 s. Macropterousforms of S. minutusare slightlysmaller than submacropters but have longerwings and differin coloration.In submacropterousforms the fore-wings are 2 25-2 5 timesas long as the abdomen,but in macroptersthey are 2 5-2 75 as long; thelength of thehind-wings in submacroptersis 1 5-2 0 and in macropters2 25-2 5 that of theabdomen. The black markingsin themacropters are moreextensive and theblack stripeson the fore-wingsmore prominent. Moreover the apical cells are moreextended and the wingtips morepointed in macroptersthan in submacropters. The assumptionthat macroptersare the migratoryforms was substantiatedby May (1971) not onlyby trap catches,but also by observationson a localized populationon Dactylisglomerata L. In 1969,macropters formed 52.5% ofthe total population before theflight period and in 1970,4822%. After the flight period these percentages fell to 19 4 and 17-9,respectively. At 20? C and 16 h of light,crowded nymphs produced high proportions of macropters on wiltingDactylis and equally high proportionsof sub-macropterson green and succulentgrass. However, isolated nymphs reared on wiltingand succulentDactylis gave 720 Dispersalby flight of leafhoppers rise to submacropters(May 1971). It is thereforepossible, that the leafhopperswere affectedby the conditionof the plant,and also by crowding. A differenttype of macropteryand submacropteryhas been encounteredby Rose (1972b) in Cicadulinaspp. (Cicadellidae). In C. mbila (Naude), C. s-toreyiChina and C. parazeae Ghauri,the winglengths in the two formsremained more or less constant, but the individualswere eithershort-bodied or long-bodied.Tethered and suspended long-bodiedindividuals flew for 8-15 s, or not at all, theshort-bodied Cicadulina flew for an average of 500 s. Most of the testswere made on males, to avoid confusionwith elongationof thebody on maturationin thefemales. Field experimentsand observations also consistentlypointed to theexistence of two rangesof distancesflown by Cicadulina. Rose's resultsindicate also thatflight ability in thethree Cicadulina spp. is inherited,the progenyof non-flyersbeing mostlynon-flyers while those of the long-flyers,mainly flyers. No experimentshave been made on the grasslandcicadellid, Balclutha punctata, but immatureadults, collected in the fieldprior to winterdiapause, showeda considerable variationin theirwing lengths and weresubdivided into short-and long-wingedindividuals. This variation,however, is not associatedwith the colour polymorphismwhich exists,in thisspecies, since the long-and the short-wingedforms have been seen in both the greenand the brownindividuals. In a sense,Group 2 and Group 3 intergrade,since in Group2 femalesalteration in the proportionsof thebody to winglengths occur on maturation,when the abdomenis full of eggsit extendswell beyondthe wingtips and flightis inhibited. Group4: speciesin whichthe ability tofly is linkedwith the alteration in theratio of lengths of thefore- to hind-wing Errastunusocellaris and Arthaldeuspascuellus fall withinthis group.In both species the maturefemales lose theirflight ability, but some cannotfly, even when immature. Errastunusocellaris provides a particularlygood exampleof such dimorphism, the greater proportionof its populationsconsisting of non-flyersand the highproportion of flyers beingfemale. The sex ratioof E. ocellariscaught in suctiontraps between 1967 and 1970 was 1 ( :25 W.Measurements of thetotal body length,the fore-and hind-wingand hind tibia weremade on the flyersand non-flyersof E. ocellaris,Arthaldeus pascuellus and of Psammotettixconfines, which was originallysuspected of belongingto this group.The most relevantdifferences were foundin the lengthsof the fore-wingsand hind-wings (Table 7). In Errastanusocellaris females, there was a differencebetween the lengths of thefore- and hind-wingsof flyersand hoppers.The ratio of the two winglengths in flyersbeing 1 10 and thatin non-flyers1-20. In themales, there was no differencein thelengths of the fore-wingsof thetwo groups,but a significantdifference in thehind-wings. The ratiosof thelengths in theflyers being 1 11 and in non-flyers1 27. The low numberof flying males measuredreflects their scarcity.Arthaldeus pascuellus was similar,but in contrastto Errastanusocellaris, most individuals were capable of flight,and non-flyerswere rare. In Psammotettixconfines, variations in the wing-lengthsbetween the flyingand non- flyingimmature individuals were not significant,suggesting that physiologicalfactors may determinewhether an individualis a flyeror a non-flyer. Group5: speciesexhibiting clear alarypolymorphism In the brachypterousforms of thesespecies, both pairs of wingsare reducedand the skeletalstructure of the thoraxand the dimensionsof the flightmuscles are modified. N. WALOFF 721 A distinctionbetween the brachypterous and macropterousforms of the same species is foundin manyDelphacidae, whilethe normallyshort-winged Doratura stylata and Ulopa reticulate(F.), in whichthe hind wingsare normallyabsent, provide examples withinthe Cicadellidae. The incidenceof brachyptersand macroptersin severalspecies of Delphacidae, is givenin Table 8. In thehabitat studied, the great bulk ofJavesella pellucida were macropterous and of the 2063 individualsexamined throughout the six generationsbetween 1969 and 1971,76% of the femalesand 7500 of the males werelong winged,the greater Table 8. The incidenceof macropterousand brachypterousforms in field samplestaken at SilwoodPark

Species Year Generation ?? I' br* m* br m Javesella 1969 1 84 198 167 267 pellucida 2 20 106 17 154 1970 1 66 195 30 222 2 5 153 3 136 1971 1 47 56 43 74 2 4 4 2 10 Laodelphax 1969 1 188 0 151 0 elegantulus 2 56 1 56 1 1970 1 443 0 308 0 2 58 0 53 1 1971 1 103 0 58 0 2 13 0 12 0 Muirodelphax 1969 1 155 0 136 0 exiguus 2 170 0 256 0 1970 1 129 1 107 0 2 70 0 67 0 1971 1 105 0 104 0 2 18 0 2 0 Ribautodelphax 1969 1 35 0 12 0 angulosus 2 21 1 32 0 1970 1 55 0 44 0 2 - _ _ _ 1971 1 5 0 4 0 Paraliburnia 1969 1 148 0 175 0 dale 2 219 0 140 0 1970 1 128 1 93 0 2 74 1 47 0 1971 1 16 0 9 0 2 17 0 10 0 Dicranotropis 1969 - 36 1 15 0 hamata 1970 - 15 0 19 0 1971 - 34 1 46 0 1972 - 99 2 59 1 Ciomorphus 1969 - 13 0 20 3 albomarginatus 1970 - 8 1 9 0 Xanthodelphax 1969 - 2 0 5 0 stramineus 1970 - 1 0 3 2 * br,brachypterous; m, macropterous. 722 Dispersalbyflight of leafhoppers proportionsof macroptersin both sexes occurringin the second generationof each year.In the otherspecies (Table 8), brachypterousforms predominated and out of the 1502 individualsof Laodelphaxelegantulus examined, 0.1% of the femalesand 0.300 of the males were long winged.A higherincidence of macropterousforms was seen in Dicranotropishamata, Criomorphusalbomarginatus and in the locally rare species Xanthodelphaxstramnineus. Macropteryoccurred in Doraturastylata, a monovoltinespecies collected in the study area for 5 years.The numbersof adults fromsimilar samples were 45 in 1967, 87 in 1968,214 in 1969,1037 in 1970and 233 in 1971,indicating fluctuation in abundanceby a factorof twenty-three.The sample of 1037 in 1970, contained535 femalesand 502 males. No macropterousmales wereseen, but 25 (4.70 %) of the femaleshad long wings

LL - :00 062 4 * i

208

1-83 13- 15 19-21 23-29 1-5 May June 1970 FicG. 6. Delayed maturationin macroptersof Javesellapellucida (Delphacidae). Propor- tions of samples of a fieldpopulation withmature brachypterous (c) and macropterous(o) females. thatextended beyond the abdomen. The macropterscaught in thesuction traps were also females.As thisspecies was concentratedin a relativelysmall area and, as in 1970,its nymphswere abundant, the effectsof densityon productionof macropterscannot be dismissed.Comparable effectsof crowdingon productionof long-wingedforms of Delphacodesstriatella (Fallen) and otherleafhoppers have been describedby Kisimoto (1965). In some cicadellidspecies macroptery is veryrare and, none has been encounteredin Ulopa retictilata,where normally the hind wingsare absent. However,in 732 adults dissectedbetween 1969 and 1972,there were two fullywinged females. Le Quesne (1965) statesthat in the only otherspecies of thisgenus in Britain,i.e. in U. triviaGermar, a singlemacropterous individual has been reportedby Duffield(1963). In additionto the structuraldifferences between the macroptersand brachypters,the femalesof the two formsdiffer in theirreproductive physiology. In macroptersthe preovipositionperiod is prolonged,and fecunditymay be reduced.In fieldpopulations of Javes~ellapellucida and Doraturastylata the brachypterousfemales mature long before the macropterousones (Figs. 6 and 7). May (1971) has shown thatthe macroptersof Stenocranusminutes lay fewereggs than the submacropterskept under comparable conditions.Similarly, Kisimoto (1965) foundthat the preovipositionperiod was prolonged and fecundityreduced in the macroptersof Delph1acodesstriatella, Nilaparvata lugensStall and Sagata furciferaHorvath. N. WALOFF 723

o 0 0

D 08 0 E Q) E06 6 _-

cC04 04/ } 2

LL 0*2 -

w it i/ I ! I~~~~~~~~~~~~~~~~~~~~I ! 22 29 6 13 20 27 3 10 17 June JUlY August 1970 FIG. 7. Delayedmaturation in macroptersof Doratura stylata (Cicadellidae).Proportions of samplesof a fieldpopulation with mature brachypterous (@) and macropterous(o) females.

SEX RATIOS OF SPECIES IN SUCTION TRAPS Sex ratiosof some speciescaught in suctiontraps are givenin Table 9, wherethe size of R.T. is not adjustedto thatof the two adjacenttraps. In Auchenorrhynchathere is a considerablevariation in the proportionsof the two sexes that fly.In manyspecies of Cicadellidae,e.g. Macrostelessexnotatus, M. laevis, Balcluthapunctata, Arthaldeus pascuellus, Mocydiopsis parvicatida, in the threespecies of Cicadulinastudied by Rose (1972a, b), and in the delphacidsJal'esella pellucida and Stenocranusminutes, the two sexesfly in approximatelyequal proportions.These species includesome of mostactive flyers and probablymigrants, i.e. thosethat regularly occur in largernumbers in the aerial suctiontraps. In Cixiuspilosus and in Psammotettixconfines there was a consistentexcess of flying males in all thetraps. The reversewas trueof the cicadellidStreptanus Sordidus and the typhlocybidZygina scutellaris, where the femalesappear to be the moreactive sex and are caught in largernumbers. In Errastunusocellaris only a low proportionof the populationsare flyers,but therewas a greatexcess of flyingfemales over males, the numberscaught in trapsbetween 1967 and 1970 being5 d: 126 W. In thenormally brachypterous cicadellid species Doratura stylata and Ulopareticulata theonly macropterous individuals, capable offlight were all female.In 1970,in Doratura, 25/535females collected in thefield population were macropterous. In Ulopa,of the 517 individualsexamined between 1969 and 1972,two femaleswere fully macropterous.

Table 9. Sex ratio (5: ?) in total seasonal catches of some species of Auchenorrhynchacaught in suctiontraps at SilwoodPark 1969-71 Heightabove ground 1-2m 91 m 12-2m Species Trap II Trap IV R.T. Total Arthaldeuspascuellus 1:1 3 1:0-7 1:1 1 1:1 1 Balcluthapunctata 1:1-4 1:0-8 1:1 1:1 0 Mocydiopsisparvicaiuda 1:P14 1:1 1:0 5 1:1-2 Cixius pilosus 1:0-7 1:0-4 1:0-3 1:0 5 Psammotettixconfines 1:0-6 1:0-4 1:0-3 1:0 5 Streptanussordidus 1:1-4 1:3-6 1:4 1:1 9 Zygina scutellaris 1:1 5 1:1 5 1:1-6 1:1 5 724 Dispersalby flight of leafhoppers

FLIGHT OF PARASITIZED LEAFHOPPERS Lewis & Taylor(1965) have shownthat the vast majorityof Auchenorrhynchaare day flyers.They also pointout, that the synchronization of life cycles and distributionof many small parasiticHymenoptera with their hosts is assistedby flightactivity in daytime, when theyare subjectto the same distributiveprocesses. However, this associationis evencloser, since parasitized individuals were not uncommonin theaerial suctiontraps,

Table 10. Numberof parasitized Javesella pellucida (Delphacidae) caught in suctiontraps at SilwoodPark Metresabove No. parasitizedby Percentage Year Generation ground No. examined StrepsipteraDryinidae Pipancu- parasitized lidae 1960 1 1-2 371 10 3 - 3.5 2 1P2 85 - - - 0 1962 1 1-2 318 12 9 - 6-6 1968 1 1-2 104 10 1 1 115 2 1-2 34 - - - 0 1 91 34 - - - 0 2 91 19 - - - 0 1969 1 1-2 51 4 - - 7-8 2 1P2 75 1 - - 1-3 1 91 13 - - - 0 2 91 33 2 - - 6-1 1 12-2 12 1 - - 8-3 2 12-2 16 - - - 0 1970 1 1-2 101 4 - 1 4-9 2 1-2 42 - - - 0 1 91 50 2 1 - 6-0 2 91 32 1 - - 3-1 1 12-2 37 1 - - 2-7 2 12-2 15 - - - 0 1971 1 1-2 33 2 - - 6-1 2 1P2 28 - - - 0 1 91 18 2 - - 11*1 2 91 14 - - - 0 1 12-2 8 - - - 0 2 12-2 3 - - -- 0 evenat 12-2m. The mostcommon parasites of the nymphal and adultstages of Auchenor- rhynchaare thestrepsipteran Elenchtus tenuicornis (Kirby) on Delphacidae,many species of Dryinidae(Hymenoptera) on Delphacidae and Cicadellidae and species of Pipun- culidae (Diptera) on delphacids,cicadellids, cercopids and cixiids. Parasitizedindividuals were readily detected in thetrap catches, since the Strepsiptera and Dryinidaeprotrude from their hosts and all threesets of parasitestend to give rise to 'intersexes'. The incidenceof parasitizedindividuals of Javesellapellucida in the trap catches is givenin Table 10. Catchesin- 1960 and 1962,i.e. in theyears prior to thisstudy, are also included.It is probablethat the recordedincidence of the Strepsipterais accurate,but thatof the Dryinidaeand Pipunculidaeis an underestimate,since it is difficultto detect N. WALOFF 725 youngparasitic larvae in the leafhopperspreserved in alcohol. The percentageof the flyingJavesella of thefirst generation parasitized by Elenchuswas 4-2,that by Dryinidae 1 2 and thatby Pipunculidae0-2. In laboratorytests, the macropterous delphacids parasitized by Strepsipteraflew until the males of Elenchuspupated and the femaleswere almost fully grown, delphacids and cicadellidsparasitized by Dryinidaeand Pipunculidaeflew actively when the internal parasiteswere small, but lost theirflight ability when the parasiticlarvae reachedtheir fullsize.

DISCUSSION Dispersal by flightof insectsis an integralpart of theirpopulation dynamics (Johnson 1969). Wherethe exodus by flightfrom the breedingsite is relatedto density,as in the broom psyllid,Arytaina sparti (Guerin-Meneville)(Watmough 1968; Dempster1968) and in the broommirid, Orthotylus virescens (Douglas & Scott; Waloff& Bakker1963), densitymust be consideredalong with the other processes that not only alter, but regulate populationsof insects. In Auchenorrhyncha,widespread and diversifieddispersal by flightis closely linked with alary polymorphism.Frequently populations of the same species are composed of macropterousindividuals capable of colonizingnew areas and of brachyptersthat re- producewithin the original breeding sites. Thus, not only parts of ontogeny of individuals are 'set aside' fordispersal, but thereis functionaldifferentiation between members of populations.This is a typeof divisionof labourin whichthere is no apparentco-operation betweenthe morphsand alary polymorphismin the leafhoppersis probablyakin to, thoughless highlyevolved than, that in the Aphididae. Lewis & Taylor(1965) have shownthat most of theHemiptera and Auchenorrhyncha are day-flyers.In theiranalysis of aerial samples of morethan a quarterof a millionday- flyinginsects, Auchenorrhyncha comprised no morethan 0.900. By comparison,Aphi- didae comprised32% and Phoridae3000 of the total.The smallnumber of leafhoppers in theaerial traps was notdue to scarcity,since they are abundantin grasslands,reaching up to a 100-200/M2 (Whittaker1969; Morris 1971; Waloff& Solomon 1973). Perhaps this apparentscarcity reflects both the high proportionof brachypterousindividuals or of macroptersand submacroptersthat do not migrate.It is possible that the low numbersof leafhopperscaught in the aerial trapsin Britainare also relatedto weather conditions,since there are indicationsthat the dailycatches are affectedby temperature (Table 5). Moreover,the weather in theBritish Isles, in mostof the years, enables grass to remainturgid even in thesummer months, whereas, there is evidencethat in some species of leafhoppers,the highincidence of migratoryforms is associatedwith the wiltingor dryingstate of theirfood plants.Thus, Rose (1972b) foundgreater numbers of short- bodied migratoryforms of threespecies of Cicadulinain perennialgrasses than in irri- gated Kikuyugrass. Similarly, Kisimoto (1965) considersthat the seasonal fluctuations in the numbersof macroptersof Nilaparvatalugens within field populations, are related not onlyto crowding,photoperiod and otherenvironmental conditions, but also to the stageof growthof itsfood plant.In N. lugens,the greatest numbers of migrantsoccurred in the autumngenerations and it may be relevantthat in the presentobservations, the proportionsof macropterousJai'esella pellucida were consistently greater in the second generations(Table 8). AlthoughNuortova (1962) points out, that the mass migratory flightof thisspecies is commonlythe firstflight after emergence and thatit takes place 726 Dispersalby flight of leafhoppers irrespectiveof thecondition of the food plant,he is probablyreferring to thethresholds of stimulifor 'take off'and notto the developmentalthresholds that may be responsible for the productionof the two morphs. May (1971) in experimentson Stenocranus minutes,suggested that the productionof the macropterous,migratory forms was associatedwith the interaction of densityof nymphswith the state of grass on whichthey were reared. In many species of the Aphididae,besides density-inducedinterference whichseems to be primarilyresponsible for the switchfrom aptera to alate production, manyother factors including the state of the host plant may enhance this process (Hughes 1963; Lees 1966,Way 1968,van Emden et al. 1969). The relativelylow numbersof Auchenorrhynchain the air in thiscountry is a local phenomenon,since vast numbersof these vectorsof plant diseases (e.g. Macrosteles fascifronsStal, Curcilifertenellus (Baker) and Empoascafabae (Harris) are known to migrateover long distancesin NorthAmerica. These long-rangemovements, which have been correlatedwith synoptic meteorology have been discussedby Johnson(1969) and De Long (1971). Moreover,migrations of leafhoppers may occur at differentaltitudes and Glick (1939) foundthem at almostevery height from 61 to 4267 m. One-thirdof all the species of BritishAuchenorrhyncha were caughtin the Silwood traps, but numbersof tree-dwellerswere low. This supportsSouthwood (1962) who suggeststhat migration occurs most often amongst insects that occupy more temporary habitats.Also, up to 50?' of theannual catches included only Macrostelessexnotatus, M. laevis and Javesellapellucida, although locally they were not the most abundant leafhoppersin the field.The catchesin aerial trapsmay be relatedto the considerable powerof dispersalof theseleafhoppers, which readily arrive to colonizefield crops. Most leafhoppersmigrated while they were still immature and did not retrunto their originalhabitat. Johnson (1969) and Dingle (1972) emphasizethat the developmentof thereproductive system is minimizedwhile that of theflight system is maximizedduring migratoryflight. In most speciesexamined readiness to flywas inhibitedby maturation.Whether the abilityto disperseby flightis also associatedwith autolysis of flightmuscles as in Sitona (Jackson1933) and in Corixidae(Young 1965a,b) is not known.In thebivoltine species dispersalby flight may occur equally in bothgenerations, or witha smallerproportion or absence in the second generation. Dispersalby flightin leafhoppersis dependenton alarypolymorphism which is widespread amongstspecies livingin groundvegetation, but not in tree dwellers.Clearly definedmacroptery and brachypteryexists in many Delphacidae and among the cica- dellidsexamined in Doraturastylata and Ulopa reticulate.Brachyptery is a synonymfor the numerousmorphological changes that accompanythe shorteningof wing length, since thereare simultaneousalterations in the skeletalstructure of the thorax,and in flightmuscles and physiologicalchanges which find expressionin higherfecundity (Kisimoto 1965; May 1971). Much has been said about the evolutionof migrationand of the behaviouraland physiologicalprocesses that accompany dispersal by flight(Kennedy 1961; Southwood 1962; Johnson1969), but it is arguablethat the evolutionof brachypterousmorphs in the Pterygotais as strikingand musthave been subjectto greatselective pressure. In Auchenorrhyncha,differentiation between flyers, including the migratoryforms and non-flyers,has been achievedby a varietyof means.Various degreesof alarypoly- morphismare widespreadthroughout the Insecta, particularly in the qualitatively different formsin locusts (e.g. Uvarov 1961). Among the Hemiptera,long-winged 'good' and N. WALOFF 727 'poor' flyersin the milkweedbug, Oncopeltusfasciatus (Dallas) have been identifiedby Dingle (1965, 1966, 1968), who relatedthe proportionsin populationsof these be- haviouralmorphs to photoperiodism.Similarly Shaw (1967, 1968) demonstrateddiffer- encesin flightperformance and evenabsence of flight in thealatae of Aphisfabae(Scop.). It is probable that the same phenomenonexists in leafhoppers,e.g. in Psammotettix confines.Moreover, there are membersof species whichare usuallylong-winged with some individualsthat have extra long wingsin proportionto theirbody length,i.e. submacroptersand macropters.All can fly,but the submacroptersfor shorter distances. Submacropterymay be achieved in two ways, i.e. by shorteningthe wing lengthin proportionto the body length,as in Stenocranus-minutes (May 1971), or by increasing the body length,the winglength in the two morphsremaining relatively constant, as in the Cicadulinaspecies (Rose 1972b).The same alterationsin the proportionsof wingto body lengthalso occurs in ontogenyof femaleadults of manyspecies, e.g. Arthaldeus pascuellus,Elymana sulphurella, Diplocolenus abdomninalis where in immaturefemales the wingsextend beyond the abdomen,and matureones the distendedabdomens project beyondthe wings. It seemsprobable that maturation does not onlyinhibit flight physio- logically,but thatmature females also becomeless 'flight-worthy'mechanically. Thereare otherspecies of leafhoppers which do not showfully developed brachyptery, the forewings of non-flyersbeing only slightly shorter than in flyersbut the hind-wings showinga muchgreater reduction in length.The ratio of lengthsof the fore-and hind- wingsin Errastunusocellaris determines whether the individuals are able to fly,or onlyto hop (Table 7). A similardifferentiation in lengths of the fore-and hind-wingsoccurs in Arthaldeuspascuellus, but whereas non-flyersform the bulk of fieldpopulations or Errastunus,they are relativelyrare in Arthaldeus. In manyspecies the sexes flewin approximatelyequal numbers,but in those where macropteryis rare,as in Doraturastylata and Ulopa reticulate,the only individuals seen withfully developed wings, were all females.It is not difficultto visualizewhy an excess of long-wingedfemales are producedwhen macropteryis rare,but the excess of flying males over femalesof Cixius pilosus and of Psammotettixconfines (Table 9), needs a furtherexplanation. Den Boer (1968) formulateda conceptof stabilizationof animalspecies by phenotypic variation,later he (Den Boer 1970)applied thisconcept to thedifferentiation of carabid populationsinto alary morphs. Whether alary polymorphism in leafhoppers is genetically fixedis not known.Rose (1972b) considersinheritance of flightability in the Cicadullina spp. suggestingthat progeny of non-flyersare mostlynon-flyers, those of flyersmainly flyers.Wigglesworth (1962) presenteda hypothesisthat 'all charactersare the product of chromosomeconstitution and thattherefore in a verybroad senseall of themare of geneticorigin'. He emphasizedthat although the changes such as those betweenbrachy- pteryand macropteryof some speciesmay be ofgenetic origin, they may also be subject to environmentalinfluences. Differentiationof insectpopulations into 'good', 'poor' and non-flyerssuggests that the switch-mechanismsinvolved are labile, and that selectivepressure must have been operatingin oppositedirections producing the more sedentarybrachypters and more active migratorymacropters in the same populations,i.e. by 'spreadingof risk' (Den Boer 1968). Finally,the factthat parasitizedleafhoppers are activethroughout at least a part of theirflight period is interesting,since in colonizationof new breedingsites the host populationswill transfersome of theirregulatory mechanisms with them. This may be 728 Dispersalby flight of leafhoppers fairlywidespread and has been recordedin Miridae that live on broom (Waloff& Bakker1963).

ACKNOWLEDGMENTS My sincerethanks are due to Miss Sandra McCarthywho has carefullysorted out the Auchenorrhynchafrom the dailycatches in aerial trapsand who identifiedsome of the species of Delphacidae and to Martin Cooper who identifiedthe leafhoppersin the earlystages of thiswork. I am also gratefulto Dr Y. Y. May and Dr E. B. Tay forallow- ing me to quote fromtheir theses. Special thanksare due to the AgriculturalResearch Council fora grant,which made thiswork possible.

SUMMARY (1) One-thirdof the total of Britishspecies of Auchenorrhynchahave been identified in aerial trapsat Silwood. (2) The numbersof leafhoppersin annual catchesin trapsare small comparedwith those of otherinsects and about halfof themare composedof Macrostelessexnotatus, M. laevisand Javesellapellucida, which are knownvectors of plantdiseases. (3) Patternsof dispersalhave beenexamined in severalspecies and relatedto voltinism and to the seasonal incidenceof adults. (4) Ten per cent of the Cicadellidae in aerial traps were tree-dwellers;this may be relatedto permanencyof theirhabitats. Also, tree-dwellersoccurred in greaternumbers in higherthan lowertraps, whereas the reversewas trueof the grasslandspecies. This indicatesdifferences in dispersalpatterns of leafhoppersfrom different habitats. (5) Many species show alary polymorphism.(a) Some exhibitextreme brachyptery and macroptery,the long-winged, migratory females showing delayed maturation. (b) In anothergroup, ability to flywas linkedwith the ratio of lengthsof fore-and hind-wings. Flyersand non-flyerswere distinguishedby laboratorytests. (c) In a thirdgroup all individualswere macropterous,but some had extra long wings and were the only morphscaught in aerial traps. (6) Most, or all speciesdispersed when they were immature.In manyspecies males and femalesdispersed in equal numbers.In thosewhere macroptery was rare,the long- wingedindividuals were all females.In a few species greaternumbers of males than femaleswere caught in aerial traps. (7) Parasitizedleafhoppers dispersed by flight, at leastwhile the internal parasitic larvae were still small. Thus in invadingand colonizingnew breedingsites, some regulatory mechanismsof leafhopperpopulations were transmitted together with the host species.

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(Received2 January1973)