THE RELATION BETWEEN AGE AND FLIGHT ACTIVITY IN THE MILKWEED BUG, ONCOPELTUS

Transcription

1 J. Exp. Bol. (5), a, - Wth 5 text-fgures Prnted n Great Brtan THE RELATN BETWEEN AGE AND FLGHT ACTVTY N THE MLKWEED BUG, ONCOPELTUS BY HUGH DNGLE Department of Zoology, Cambrdge* (Receved July ) NTRODUCTN Recent revews by Johnson (), Kennedy () and Southwood () have represented a change n outlook toward nsect mgraton. Prevously emphass had been placed on mass movements and orentaton of flghts; the subject from ths standpont has been revewed by Wllams (5 and 5) who was largely responsble for ts development and for demonstratng that mgraton was a wdespread phenomenon among nsects. Wllams defned mgraton as 'a contnued movement n a more or less defnte drecton, n whch both movement and drecton are under the control of the anmal concerned* (5), but the dffculty wth ths defnton s that such well-known mgrants as aphds and locusts are not ncluded. Mgraton flghts n these nsects may or may not be n a defnte drecton and are not under drect control snce both use the wnd as a transportng vehcle (Kennedy, ). Further, return movements of the same ndvduals, long consdered a fundamental aspect of mgratons (e.g. Allee et al. ) now must be consdered dubous for any nsect. But rather than abandon the term 'mgraton' altogether when consderng nsect movements, t seemed more reasonable to attempt a reassessment based on other than topographcal characterstcs. The new approach crystallzed by Johnson, Kennedy and Southwood consders mgraton n nsects a dstnct behavoural and physologcal syndrome essentally ndependent of specfc drectonal orentaton. Kennedy () defnes mgraton as ' persstent, straghtened out movement that s accompaned by and dependent upon the mantenance of an nternal nhbton of those 'vegetatve' reflexes that wll, eventually, arrest movement'. The straghtened-out movement, whch need have no drectonally adaptve sgnfcance, s a result of enhanced sensormotor functons, and the 'vegetatve' reflexes are those assocated wth growth, e.g. feedng and reproducton. The dstncton s no longer made between actve mgraton and passve dspersal by wnd snce large actve flers such as locusts are as much wnd-borne as such small weak flers as aphds (Kennedy, 5, ). To become wnd-borne any nsect must actvely rse above what Taylor (5) has called the 'boundary layer', the alttude, dfferent for each speces, above whch t no longer fully controls ts own orentaton. A further characterstc of mgratons s that they usually occur pre-reproductvely. The major dfference between mgratory and non-mgratory flghts s one of relatve thresholds, wth no sharp lne of demarcaton. Acceptance of Kennedy's defnton Present address: Department of Zoology, State Unversty of owa, owa Cty, owa, U.S.A.

2 HUGH DNGLE opens the way to the expermental analyss of the behavoural, physologcal, and ecologcal factors ntatng and controllng mgraton (Johnson, ; Southwood, ). The present paper concerns an attempt to study the above factors n the laboratory. For such a study needed an nsect whch would show a peak of flght actvty, obtaned convenently usng tethered flght, whch mght be consdered mgratory. Ths flght would presumably be a functon of age and deally would be characterzed by rather narrow lmts. The relaton of flght actvty to age could then be compared wth ts relaton to other varables mportant n connexon wth mgraton, such as physologcal development, reproductve actvty, and populaton parameters. The nsects consdered most lkely to exhbt a dstnct flght peak were the Hemptera and Coleoptera; these forms usually move about by walkng and fly only occasonally, and n these crcumstances a long flght could well be mgratory (Southwood & Johnson, 5; Southwood, ). Dptera whch have been popular nsects for studes of tethered flght usually move about by flyng anyway, thus ntroducng some ambguty. The nsect chosen for the present study was the 'large mlkweed bug' Oncopeltus fascatus (Dallas) (Heteroptera: Lygaedae). Oncopeltus has not been lsted as a mgrant, but certan consderatons ndcate that t probably s one. Southwood () has summarzed a consderable amount of nformaton concernng the relaton between the occurrence of mgraton n varous terrestral arthropods and the habtats n whch they are found. He gves extensve evdence that those frequentng 'temporary ' habtats such as annual and perennal plants of feld and wasteland are more apt to be mgrants than those of 'permanent' habtats such as woodland trees. On the crteron of habtat, snce t occurs on mlkweed {Asclepas sp.) whch s a perennal of open felds and roadsdes, one would predct that Oncopeltus would be a mgrant. Some feld observatons of mne (below) gve more drect evdence that t does n fact mgrate n the feld. Other Lygaedae closely smlar to Oncopeltus are known mgrants (Southwood, ). MATERALS AND METHODS The nsects used n the present study were all descended from a culture of Oncopeltus mantaned n the Sub-Department of Entomology at the Unversty of Cambrdge. They were rased at + C. at approxmately 5 % relatve humdty on a daly schedule of hr. of lght and hr. of darkness and were fed on dry mlkweed seeds every other day and gven water from soaked cotton wool. Dead ndvduals were removed daly, and f marked, ther age at death n days after the fnal moult was recorded. Daly checks were also made for newly emerged adults whch were then marked on the prothorax wth spots of quck-dryng pant. At every observaton of a partcular culture all ndvduals n the act of copulatng or egg-layng were noted. Loose cotton wool was suppled for egg-layng and proved satsfactory. For flght-testng, bugs were attached at the pronotum to a short stck by means of a small amount of paraffn wax. Onceflyng,they were clamped nto a rng stand about cm. above a black substrate wth a W. lght bulb about 5 cm. above them. The duratons of the frst fve successve flghts were recorded and summed to gve

3 Age and flght actvty n the mlkweed bug the total duratons whose means are plotted n Fg.. f a bug became flght-refractory after fewer than fve flghts, the total duraton was smply computed from the number of flghts obtaned. The expermental room was black walled and mantaned at a temperature of 5 + C. Flght was ntated n a bug by subjectng t to a standard sequence of procedures gven one after the other untl t flew. Each step was numbered to gve a relatve measure of threshold at whch flght began (Table ). The procedures and threshold values were as follows: () Bug lfted off substrate by stck attached to pronotum. () Stck clamped n rng stand and tapped frmly wth another stck. () Bug gven tarsal contact; ths suddenly removed and at the same tme a jet of ar drected at head. () Stck to whch bug attached held by expermenter and bug moved rapdly back and forth at arm's length fve tmes. (5) Bug allowed to walk 5 cm. then rapdly lfted off substrate and repeat (). () Wngs opened by expermenter (f stll unopened) and repeat (5). () Repeat (5). () Repeat (5). () Bug opens wngs to any of above, but never fles. () Bug never opens wngs wthout ad of expermenter. Thus f a bug faled to fly when subjected to (), (), or () above, but dd so the frst tme t was moved back and forth at arm's length, t would be assgned a flght threshold of. RESULTS Flght-duraton and age Mean flght-duraton as a functon of age n days after the fnal moult s shown plotted n Fg.. The szes and ranges of the samples from whch ths fgure was drawn are gven n Table. n both sexes a peak perod of maxmum length of flght occurs from to days, and n males a second peak occurs at -5 days. The peaks seem to represent real changes n flght actvty, for f the values at,, and days are compared wth ether the precedng (days, and ) or succeedng (days and 5) low flght values respectvely, the dfferences are found to be sgnfcant statstcally at the o-o level for a two-taled Mann-Whtney U test (Segel, 5). For males the fgures at and 5 days are lkewse dfferent from those at and 5 or and 5 days, ths tme at the - level. The occurrence of a peak of mean flght-duraton at - days s of specal nterest when the flght data are compared wth data for cutcle growth n Oncopeltus. Recently, Nevlle () has dscovered that nsect endocutcle s, n the adult, formed n pared lght and dark layers wth one par deposted daly untl the nsect s full grown; ths daly deposton occurs n many of the nsects so far examned ncludng Hemptera- Heteroptera (Nevlle, personal communcaton). Frozen sectons through the cutcle of Oncopeltus adults of dfferent ages ndcate daly deposton of pared zones wth cessaton of such growth at or days. Fg. s taken from a frozen secton through the hnd tba of an adult more than days old. t s not possble to dstngush whether there are nne or ten pared zones ether n the fgure or n the orgnal secton, Exp. Bol,

4 HUGH DNGLE but snce there are no more than nne or ten n a bug more than days old, the nsect evdently attans full growth at - days. Snce the peak flght-duraton occurs at the same tme (Fg. ), there s thus a remarkable correlaton between the growth and behavoural parameters. Long flghts evdently occur when an adult nsect reaches full maturty at least wth regard to the formaton of the endocutcle. Vrgn male* s Fg.. Days after fnal moult Mean flght-duraton n Oncopeltus as a functon of age n days after the fnal moult. Sold crcles and sold lne, males; open crcles and broken lne, females. n addton to the usual flght experments whch were run on bugs comng from cultures ncludng both sexes, 5 vrgn males at days and vrgn females at days also were tested. The respectve ages were chosen because they represented low ponts for the two sexes n the curves gven n Fg.. These expermental were kept separate from members of the opposte sex as soon as the fnal moult was complete. The -day vrgn females showed no sgnfcant dfference n performance from ther mated counterparts, but the -day vrgn males were strkngly dfferent (Fg. ). n fact -day vrgn malesflewlonger on the average than males at any other age, and the dfference between them and -day normal males was statstcally sgnfcant at the - level. The flght threshold was also generally lower n the vrgns (Table ). Reproductve actvty n males thus seems to have a decded nfluence on the tme course of the tendency to fly and to make long nghts. As each bug was tested the thresholds of each of ts flghts, n arbtrary unts as descrbed above, were recorded. The thresholds of the ntal nghts for each age are gven n Table. There s a general declne of flght threshold n both sexes as bugs become older wth no ndcaton that long-flyng bugs showed thresholds lower than those of others of the same age. Thresholds at - days, when flghts were of maxmum duraton, were thus hgher than for older ndvduals, whch showed consstently QW thresholds even when there were no long flghts. From the data for threshold and

5 Age and flght actvty n the mlkweed bug duraton there thus seem to be three knds of flghts: () long-duraton, hgh-threshold occurrng n both sexes at - days; () short-duraton, low-threshold occurrng n older ndvduals; and () long-duraton, low-threshold occurrng only n to 5-day males. Days after fnal moult Total* Table. Sample szes, ranges of flght-duraton, and number of flghts of dfferent ages used n flght tests Sample sze (vrgn) 5 (vrgn) (vrgn) (vrgn) Totals 5 Range Males - sec. - mn. sec. - mn sec - mn. sec. -5 nun- > ec - - mn. sec. sec- mn. sec. - mn. sec. -5 mn. sec. - mn. sec. - mn. sec. - mn. -5 mn. sec. sec- mn. sec - mn. sec. 5 sec- mn. sec Females mn. sec. - mn. 5 sec. - mn. sec. - mn. sec. - mn. 5 sec. - mn. 5 sec. - mn. sec. - mn. sec. - mn. sec. - mn. sec. - mn. sec. - mn. sec. - mn. sec. No. of bugs flyng 5 5 No. of nghts over 5 mn n respect of long-duraton flghts there was a further dfference between the sexes. n males f a long flght of more than mn. occurred n the fve test flghts, t was usually preceded by one or more short flghts of less than mn. Ths was not true of females. n the latter, long flghts when they occurred were more frequently the ntal flght of a seres. These dfferences are shown n Table and are statstcally sgnfcant (P < -5 usng x*)- For both sexes, n those anmals n whch long flghts occurred, 5 5 -

6 HUGH DNGLE the ntal flght f not of less than mn. was greater than mn. wth only two exceptons; these were males wth frst flghts of about and mn. respectvely. The pattern of actvty assocated wth long flghts s thus dfferent n the two sexes. Exocutcle Endocutcle Fg.. Drawng taken from cross-secton through the hnd tba of an Oncopeltus more than days old. Magnfcaton approxmately x. Age... Threshold 5 Total 5 Total Table. Threshold aganst age. n parentheses number at gven threshold flyng over 5 mn. () () () () () () () ( ( () () () () () () () (). ( () () ( 5 5 ( ( () d) () t^ () 5 ( d) Vrgn 5() Males Females ( () () () () (5) () () () 5 5 () ( ( () () Vrgn. 5 () () () 5 () 5 (: () ()

7 Age and flght actvty n the mlkweed bug 5 The pattern of a long flght tself was, however, generally smlar n both. At onset and shortly thereafter flght was unsteady wth changes n wng-beat frequency and ampltude and often oscllatons of the abdomen presumably caused mechancally by the uneven wng-beats. After ths ntal perod the wngs settled down to a steady frequency and ampltude wth few changes; ths ' crusng' phase lasted untl shortly before the end of flght when another perod of unsteadness combned wth a general decrease n frequency and ampltude ensued. One could usually predct from the pattern of the wngbeats when a bug was about to cease flght. n spte of the general tendency to long flghts at - days, some ndvduals never flew. Some of these were tested repeatedly n the event of late development of flght readness, but no flght could be elcted. As a check on the general health of these ndvduals they were followed throughout the remander of lfe along wth those whch dd exhbt long flghts. The 'flghtless' bugs were no dfferent wth respect of length of lfe, general reproductve actvty, and n the case of females, frequency of egglayng. There s thus the possblty of a behavoural polymorphsm wth respect to flght actvty. Table. Comparson between the sexes of long flghts preceded and not preceded by flghts of less than mn. Preceded by Not flght of preceded by less than short mn. flght Males Females Flght-duraton and reproductve development n order to determne the relaton, f any, between flght-duraton and reproducton, three crtera of reproductve actvty were recorded: copulaton by males and by females and egg-layng by females, all as a functon of age. Two of these are shown plotted n Fg.. Egg-layng by females s frst observed at 5 days after becomng adult, rses to a maxmum at - days, and then declnes to a last recorded observaton at 55 days. As one would expect, copulatory actvty n males starts somewhat earler, but otherwse shows much the same pattern except for a few males copulatng at more than 55 days. The copulatory actvty of females gave essentally the same pcture. By comparng Fg. wth Fg. one can see that the declne of mean flght-duraton n females and the ntal declne n the males concdes wth the rse n reproductve actvty. The second flght-duraton peak of males occurs after reproductve actvty has begun to declne. At the peak of reproducton, - days, the flght-duraton curve for both sexes s at or near ts mnmum. As a result of the foregong, therefore, the - to -day flght-duraton peak for both sexes can be consdered pre-reproductve. The relaton of the male second peak to reproducton s less clear. Also, as descrbed above, males can be excted to much greater flght actvty by deprvng them of sexual partners. Whereas physologcally one can meanngfully speak of the flght-duraton peak as pre-reproductve, ecologcally t has greater meanng n terms of the 'reproductve

8 HUGH DNGLE value' of an ndvdual. Ths concept has been dscussed by Fsher (5) and Slobodkn () n terms of the worth of the ndvdual to the future growth of the populaton. Slobodkn defnes t as 'the dmnuton of future populaton ncrease produced by removng a sngle anmal of a gven age from a populaton...'. Reproductve value s a measure of senstvty to natural selecton; t follows logcally that peak reproductve value, snce t represents maxmum contrbuton to future populaton ncrease, also ndcates that perod of the lfe hstory at whch natural selecton exerts ts greatest nfluence. c A. Females - «- B. Males * «- * - s N UrrntlrNL A\ Days after fnal moult Fg.. Reproductve actvty n Oncopeltus as a functon of age n days after the fnal moult. Actvty s expressed as the percentage of those alve at a gven age observed ether copulatng (males) or egg-layng (females) on that day of age. The reproductve values (VJV ) for females, plotted n Fg., were determned by substtuton n the equaton _s = _ S y»x x+ where V x s the reproductve value at age x, V o s ths value at age o( = ), e s the base of natural logarthms, * s age n days, l x s the proporton of those alve at age o alve at age x, m x s the brth-rate expressed as the number of female eggs lad per female of age x (.e. durng the nterval x \ to x+%), and r s an expresson of the growth potental of a populaton usually referred to n the ecologcal lterature as ' the ntrnsc

9 Age and flght actvty n the mlkweed bug rate of (natural) ncrease' and s an nstantaneous rate (Slobodkn, ). The value of r s calculated by tral and error substtuton n the equaton = V o = a smple and rapd method of performng ths calculaton s outlned by Brch (). All the above concepts are dscussed by Slobodkn (). Oncopeltus S *a a. so Days after fnal moult Fg.. Reproductve values (VJV ) for Oncopeltus as a functon of age n days after the fnal moult. For explanaton and method of computaton, see text. The values for l x came drectly from the daly records of adult mortalty. t was estmated that 5 % of the eggs lad survved to become adult bugs; mortalty among eggs and nymphs could not be calculated precsely because of nsuffcent data, but the data avalable ndcated that t was certanly no more than 5 %. The fnal moult took place at days on the average so all adults were taken to be of that age at the completon of moultng. dd not have a drect estmate of m^ but dd record the number of females at varous ages observed layng eggs (Fg. ). Johansson (5) gves values of eggs per female per week from vrgn females; these gave an estmate of the number of eggs lad by a female durng her reproductve lfe. The curve for egg producton gven by Johansson shows a peak later than the peak of egg-layng actvty observed by me; but hs females were vrgn, and my observatons confrmed that egg-layng s delayed n vrgn females. Johansson also mantaned hs anmals on less than hr. of lght. By assumng that maxmum egg-layng actvty as expressed by number of females layng at age x (Fg. ) reflected maxmum number of eggs lad per female, estmates of m x for my anmals were obtaned. These estmates were then halved on the assumpton of a : sex rato and used n calculatng reproductve values for females. The value of r obtaned was - per day whch s smlar to

10 HUGH DNGLE estmates of r for other nsects of smlar generaton tme all of whch approxmate to o- per day (Evans & Smth, 5). The reproductve values calculated for the Oncopeltus females n ths study are shown plotted as a functon of age n Fg.. The peak value occurs -5 days after completon of the fnal moult. The flght peak n both sexes, - days, occurs pror to the tme of maxmum reproducton, but at a perod when the reproductve value s stll better than 5 % of maxmum. Snce the long flghts do occur durng a perod of hgh reproductve values, they must have been subject to strong favourable selecton. That such flghts are stll not oblgatory, however, s ndcated by the fact that some bugs never dsplayed them. Several plots of reproductve value were calculated usng somewhat dfferent assumptons from those made n calculatng Fg.. For nstance, t was assumed that there was no mortalty among eggs and nymphs, that all adults were age o at the completon of the fnal moult, and that values of r were hgher or lower. The curves obtaned were of slghtly altered shape and the actual values were, of course, not the same as n Fg., but the peak reproductve value always occurred at - days. Assumptons concernng brth rate remaned the same. Aphs fabae ' ' ' Age (day) Fg. 5. Reproductve values for Aphs fabae as a functon of age n days from brth. For comparson wth those calculated for Oncopeltus, reproductve values were also calculated for the alate alencolae of Aphs fabae. The data for these calculatons were taken from Cockban () usng the values gven for flown nsects. The fnal moult occurs -5 days after brth (Kennedy & Booth, 5), and the mortalty curve of Cockban was extrapolated back 5 days, on the assumpton of a 5-day larval perod, to reach an estmate of larval mortalty whch was thus taken to be 5 %. The resultant curve of reproductve value s shown n Fg. 5. The mgraton flght of A. fabae usually occurs wthn the frst hr. after thefnalmoult (Cockban, ) whch means that t vrtually concdes wth peak reproductve value. Ths close correlaton s a reflexon of the burst of larval deposton mmedately followng a flght and ndcates that the aphd s maxmally senstve to selecton at tme of flght. A. fabae s thus relatvely more senstve to selecton at ts flght peak than s Oncopeltus.

11 Age and flght actvty n the mlkweed bug DSCUSSN The queston that must frst be asked wth regard to the earler flght-duraton peak of Oncopeltus s: does ths peak n fact represent mgraton? beleve that t does for the followng reasons. Frst, the long flghts occurrng durng that perod are of a much greater order of magntude than flghts whch usually occur. The latter are of less than mn. duraton, whereas the former may last over an hour; a tenfold ncrease at the peak would not be an unreasonable estmate of the dfference. The long flghts certanly represent persstent movement, one of Kennedy's crtera for mgraton (see above). Secondly, the pattern of an ndvdual prolonged flght s suggestve of mgraton. ntally t was uneven, but later settled nto a 'crusng' phase; ths pattern s smlar to that observed by Kennedy & Booth ( a) n aphd mgrants n a flght chamber. The crusng ndcates that the flght, had t been n nature, would probably have been straghtened out. Thrdly, the flght peak occurs pre-reproductvely durng a lmted tme n the lfe hstory (ths s somewhat less clear for males because of the second flght peak, see below), and most mgraton flghts areprereproductve (Johnson, ). Fourthly, Oncopeltus would be expected to be a mgrant because t s a denzen of a 'temporary habtat' (Southwood, ). And, ffthly, have some evdence of actve dspersal, at least, n the feld. Oncopeltus tends to congregate n groups of -5 ndvduals up to and ncludng the ffth nstar. About a week to days after the fnal moult, however, the bugs dsappear from the aggregate. Soon after the last ffth nstars have moulted, there are no nsects left at the ste. f the flght-duraton peak n Oncopeltus does represent mgraton, then the present results support Johnson's (, ) thess that mgraton n nsects s a postteneral phenomenon. The method of countng cutcular growth rngs dscovered by Nevlle () provdes a precse, objectve, morphologcal determnaton of the teneral perod; the major flght effort of Oncopeltus, at - days after the fnal moult, occurs just at the tme when deposton of cutcular layers ceases. Kennedy (5) has already noted that mgraton of locusts develops as the cutcle hardens; Taylor (5) dscusses the teneral perod n aphds defnng t manly by behavoural crtera, whle Bursell () correlates ths perod wth feedng and muscular growth n the tsetse fly (Glossna). n both aphds and tsetse flght actvty ncreases n post-teneral or ' non-teneral' adults. n all these cases, however, exact means of dentfyng tenerals are lackng wth the result that some ambguty s ntroduced. Ths ambguty s elmnated by the use of daly growth rngs, and for most nsects post-teneral mgraton must mean mgraton occurrng shortly after the cessaton of cutcular deposton. t s also usually pre-reproductve. The data for flght thresholds n Oncopeltus (Table ) at frst seem paradoxcal, for the lowest thresholds do not occur at the tme of peak flght-duraton. n terms of the bugs' behavour n the feld, however, the fact that flght threshold at presumed mgraton s at least moderately hgh nsures that flght wll take place only under favourable condtonson a warm sunny day, for example, nstead of a cold rany one. Mortalty whch mght result from a long flght under adverse weather condtons would thus be avoded. The fact that many more Heteroptera mgrate durng the day than at nght (Southwood, ) may also be a reflexon of relatvely hgh flght-

12 HUGH DNGLE thresholds at the tme of mgraton. Southwood found durng extensve trappng operatons that Lygaedae were restrcted to durnal catches. As for the short-duraton, low-threshold flghts whch are common to both sexes, they may be consdered to represent trval nghts or 'flts' (Southwood,, ) whch n the feld are short flghts to change feedng ste or to search for a sexual partner. The long-duraton, low-threshold flghts whch occur only n older males do not ft as well the concept of a post-teneral mgraton flght. They are not pre-reproductve, although some mgratons are nter-reproductve (Kennedy, ; Schneder, ), and these may fall nto that category. n. fact t s probably most reasonable to suggest that there are, n males, two types of mgraton. The frst s the 'typcal' post-teneral, pre-reproductve flght whch s characterstc also of females and whch occurs when threshold s relatvely hgh. The second type occurrng n older ndvduals, snce ts threshold s low, may be an 'exploson' from trval flttng actvty nto mgraton proper. The general pattern of flght n males n whch long flghts are apt to be preceded by short flghts (Table ) s further suggestve of ths. A possble trgger could be deprvaton of responsve sexual partners. Vrgn males (Fg. ) exhbted low-threshold, long-duraton nghts at an age when mated males were short-flyng. f the declne of sexual actvty n older males (Fg. ) s a reflexon of lack of female responsveness rather than of male senlty (expermental anmals dd come from cultures of smlar aged ndvduals), then the long flghts of old males are the product of events smlar to those resultng n long flghts of vrgns. Makng such a second mgraton flght ncreases the probablty of fndng females elsewhere wth whch to mate. Johnson () has ndcated that male mgraton s more varable nterspecfcally, and for Oncopeltus ths seems to be true ntraspecfcally as well. t appears that n Oncopeltus the male s the more moble sex wth the advantage of beng able to adapt moblty to dfferent envronmental condtons. Snce the 'typcal' long-duraton flght, n males and females, occurs pre-reproductvely, t s worthwhle to examne what ths means ecologcally as well as behavourally and physologcally. Reproductve value, VJV, snce t takes nto account fecundty, mortalty, and the tme course of reproducton, s the most meanngful ecologcal parameter. Maxmum reproductve value represents the tme of maxmum senstvty to natural selecton. The fact that the flght peak occurs at a tme when reproductve value s hgh (Fg. ) ndcates that there s strong selecton favourng t. The maxmum VJV s reached shortly after the flght peak, so at ths tme the bugs wll have ther greatest potental wth respect to future populaton growth. One of the theores appearng often n the lterature concernng the functon of nsect mgraton s that t s a means of allevatng populaton pressure or, n other words, that mgrants are refugees. n vew of the correlaton between hgh reproductve value and long flghts ths explanaton seems unlkely, for one would not expect refugees to have a hgh VJV. Settlers, on the other hand, would be expected to have hgh values, or they would have lttle worth as colonzers. Mgratng Oncopeltus females, then, are presumably settlers, and by mplcaton, so are males mgratng at the same tme. The foregong lne of reasonng supports the contenton that mgraton s an evolved adaptaton rather than a reacton to current adversty (Johnson, ). Further one would predct that mgraton flghts n other nsects would occur when reproductve value was hgh.

13 Age and flght actvty n the mlkweed bug Ths predcton s borne out n the case of Aphs fabae (Fg. 5) n whch peak flght and peak reproductve value occur vrtually smultaneously. The mgraton flght s thus subject to maxmum selecton. A reflexon of ths strong selecton s the fact that the flght of alate alencolae s n normal condtons a necessary prerequste for settlng and deposton of young (Kennedy, 5; Kennedy & Booth, ). The producton of wnged ndvduals s facultatve and n ths respect so s mgraton, but the wnged forms themselves must normally fly. The relatvely greater senstvty to selecton at the flght peak of A. fabae when compared wth Oncopeltus s thus reflected n the tendency of vrtually all ndvduals tofly. There s lttle varablty n the occurrence of mgraton. n Oncopeltus, on the other hand, flght peak and reproductve value do not concde exactly, and the flght s not oblgatory. Some of the ndvduals tested never flew, suggestng, snce these were as long-lved and as reproductvely actve as flers, a behavoural polymorphsm whch s undoubtedly of adaptve advantage. Bugs takng part n mgraton would assure the dspersal of the speces to new stuatons whle sedentary ndvduals would mantan a centre of dspersal n a currently sutable habtat. Johnson () and Southwood () have ponted out that factors whch produce morphometrc dfferences n mgrants mght also be expected to produce behavoural dfferences. There are a few nstances where other nsects have been studed wth respect to age and flght. Regert (), for example, studed three North Amercan grasshoppers and found that long flghts n both sexes took place mostly between and days. Females of all three speces flew longer than males ndcatng that, n contrast to Oncopeltus, they are the more moble sex. n the Douglas fr beetle, Dendroctonus, on the other hand, the males seem the more actve (Atkns, 5). Both sexes of ths wood-borng beetle flew pror to gallery-constructon, but once constructon began females ceased flght whle some males stll flew. After approxmately 5 days n the galleres there was a second perod durng whch a relatvely small proporton of both sexes flew. Wllams, Barness & Sawyer () studed the flght of Drosophla funebrs females and correlated t wth the amount of glycogen present n the body. Perods of hgh flght actvty, as measured by duraton and wng-beat frequency, and hgh glycogen concentraton both occurred between and 5 days. Varous changes n bochemstry have also been correlated wth flght maturaton n certan other nsects; the subject has been revewed by Rocksten (5). n Oncopeltus the flght peak s correlated wth the completon of developmental changes n the form of deposton of cutcular growth rngs, and there are no doubt bochemcal changes as well. But the crucal queston s stll, as Wllams et al. ponted out so long ago (): what s the bass, presumably n part at least hormonal, for the developmental changes ncludng flght? The demonstraton by Haskell & Moorhouse () that the hormone ecdysone affects central and perpheral nervous actvty s perhaps a start toward an answer to the behavoural sde of that queston. SUMMARY. The mean flght-duraton, n tethered flght, of the 'large mlkweed bug', Oncopeltus fascatus (Dallas), was measured as a functon of age n days after the fnal moult.

14 HUGH DNGLE. n both sexes a peak of flght occurs at - days. n males there s a second flght peak at -5 days, whereas there s no second peak n females.. Vrgn males tested at days, a tme when mated males were short-flyng, flew longer than bugs at any other age. Thrty-day-old vrgn females were not sgnfcantly dfferent from mated females of the same age.. When long flghts occurred n males they were n general preceded by one or more nghts of less than mn. Ths was not true for females, and the dfference between the sexes was statstcally sgnfcant. 5. The results n, and, above ndcate two, and possbly three, dfferences between the sexes. Males and females should thus be studed separately wth respect to flght actvty.. Some ndvduals never flew. These were as long-lved and as reproductvely actve as those whch dd, ndcatng the possblty of a behavoural polymorphsm.. The ntal peak of mean flght-duraton for both sexes occurs when the daly deposton of pared cutcular growth rngs ceases. Maxmum flght thus seems to occur at the end of the teneral perod.. The threshold for flght declnes wth age. There are thus three types of flght: long-duraton, hgh-threshold; short-duraton, low-threshold; and (n males only) long-duraton, low-threshold.. The ntal flght peak s pre-reproductve and occurs at a tme when reproductve value, a measure of the expected contrbuton of an ndvdual to future populaton growth and hence of senstvty to selecton, s hgh. Long-flyng bugs are evdently colonzers, and a mgraton s an evolved adaptaton, not a response to current adversty.. t s concluded that the long-duraton, hgh-threshold flghts represent mgraton and the short-duraton, low-threshold nghts represent non-mgratory 'flts'. Ths study was supported by a Postdoctoral Fellowshp from the U.S. Natonal Scence Foundaton. am grateful to Dr J. S. Kennedy for sponsorshp, dscusson, and crtcsm; to Dr L. B. Slobodkn for valuable advce and comment; to Prof. V. B. Wgglesworth for facltes; and to Geraldne Dngle for crtcsm and typng. Dr A. C. Nevlle kndly prepared the secton from whch Fg. s taken. REFERENCES AHR, W. C, EMEHSON, A. E., PARK, O. ( PARK, T. & SCHMDT, K. P. (). Prncples of Anmal Ecology. Phladelpha: Saunders. ATKNS, M. D. (5). A study of the flght of the Douglas fr beetle, Dendroctonus pseudottugae Hopk. (Coleoptera: Scolytdae).. Flght preparaton and response. Canad. Ent., -. BRCH, L. C. (). The ntrnsc rate of natural ncrease of an nsect populaton. J. Anxm. Ecol., 5-. BURSELL, E. (). Post-teneral development of the thoracc musculature n tsetse fles. Proc. R. Ent. Soc. Land. A,, -. COCKBAN, A. J. (). Vablty and fecundty of alate alencolae of Aphs fabae Scop, after nghts to exhauston. J. Exp. Bwl., -. EVANS, F. C. & SMTH, F. E. (5). The ntrnsc rate of natural ncrease for the human louse Pedculus humanus L. Am. Naturalst,, -. FSHER, R. A. (5). The Genetcal Theory of Natural Selecton. New York: Dover. HASKELL, P. T. & MOORHOUSB, J. E. (). A blood-borne factor nfluencng the actvty of the central nervous system of the desert locust. Nature. Lond, 5-.

15 Age and flght actvty n the mlkweed bug JOHANSSON, A. S. (5). Relaton of nutrton to endocrne reproductve functons n the mlkweed bug Oncopeltus fascatus (Dallas) (Heteroptera: Lygaedae). Ny«Mag. Zool., -. JOHNSON, C. G. (). A bass for a general system of nsect mgraton and dspersal by flght. Nature, Lond.,, -5. JOHNSON, C. G. (). Physologcal factors n nsect mgraton by flght. Nature, Lond.,, -. KENNEDY, J. S. (5). The mgraton of the desert locust (Schstocerca gregana Forsk.).. The behavour of swarms.. A theory of long range mgratons. Phl. Trans. B, 5, -. KENNEDY, J. S. (). The expermental analyss of aphd behavour and ts bearng on current theores of nstnct. Proc. th nt. Congr. Ent., Montreal, 5, a, -. KENNEDY, J. S. (). A turnng pont n the study of nsect mgraton. Nature, Lond.,, 5-. KENNEDY, J. S. & BOOTH, C. O. (5). Methods of maw rearng and nvestgatng the host relatons of Aphufabae Scopol. Ann. Appl. Bol., 5-. KENNEDY, J. S. & BOOTH, C. O. ( a). Free flght of aphds n the laboratory. J. Exp. Bol., -5. KENNEDY, J. S. & BOOTH, C. O. (). Coordnaton of successve actvtes n an aphd. The effect of flght on the settlng responses. J. Exp. Bol., 5-. NEVLLE, A. C. (). Daly growth layers n locust rubber-lke cutcle nfluenced by an external rhythm. J. ns. Physol., -. REGERT, P. W. (). Flght of grasshoppers n the laboratory. Nature, Lond.,,. RocKSTEtN, M. (5). Metachemogeness-postemergence bochemcal maturaton n nsects. Srmthson. Msc. Coll., -. SCHNEDER, F. (). Dspersal and mgraton. Arm. Rev. Entomol., -. SEGEL, S. (5). Nonparametrc Statstcs for the Behavoral Scences. New York: John Wley and Sons. SLOBODKN, L. B. (). Populaton and Communty Ecology. New York: Holt, Rnehart and Wnston. SOUTHWOOD, T. R. E. (). The flght actvty of Heteroptera. Trans. R. Ent. Soc. Lond. a, -. SOUTHWOOD, T. R. E. (). Mgraton of terrestral arthropods n relaton to habtat. Bol. Rev., -. SOUTHWOOD, T. R. E. & JOHNSON, C. G. (5). Some records of nsect flght actvty n May, 5, wth partcular reference to the massed flght of Coleoptera and Heteroptera from concealng habtats. Ent. Mon. Mag., -. TAYLOR, L. R. (5). Temperature relatons of teneral development and behavour n Aphs fabae Scop. J. Exp. Bol., -. TAYLOR, L. R. (5). Aphd dspersal and durnal perodcty. Proc. Lnn. Soc. Lond., -. WLLAMS, C. B. (5). nsect mgraton. Ann. Rev. Entomol. a, -. WLLAMS, C. B. (5). nsect Mgraton. London: Collns. WLLAMS, C. M., BARNESS, L. A. & SAWYER, W. H. (). The utlzaton of glycogen by fles durng flght and some aspects of the physologcal ageng of Drosophla. Bol. Bull., Woods Hole,, ^.