BR. J. ENT. NAT. HIST., 4: 1991 15 THE EFFECT OF LEAF AGE ON THE PERFORMANCE OF THE BIRCH APHID EUCERAPHIS BETULAE (KOCH) Gareth Edwards-Jones Edinburgh SchoolofAgriculture, 42 South OswaldRoad, Edinburgh EH92HH. Introduction Seasonalchangesintheabundanceoftree feedingaphids arewell known (Dixon, 1969;Wratten, 1974). Abundancetypicallypeaksinspring, decreasesinmidsummer and often rises again in the autumn. These patterns are probably caused by an interactionofseasonalvariationinthesuitabiUtyofleavesasafoodsourceanddensity- dependent population processes such as wing production and/or migration (Dixon, 1971). Although changes in leafwater content, leaftoughness and chemical defence concentration are well known (Feeny, 1970; Ayres & Maclean, 1987), it is the concentration of soluble nitrogen in the leaves which is beheved to be the most importantfactorindeterminingpatternsofabundanceinaphids(Mittler, 1958; Dixon, 1963, 1966, 1969). Theautumnalincreaseinaphidreproductiveswhichaccompanies the mobilization of nutrients in senescent leaves, supports this view. Euceraphisisalargeandactiveaphid, withallgenerations beingalate(possessing wings). The first (fundatrix) generation hatches from eggs in early spring, and gives rise to a series ofparthenogenetically reproducing generations during the summer. The sexual generation (oviparae) are produced in the autumn, these mate and lay theireggs, usuallyaroundthebaseofbudsandalongadjacenttwigs(Edwards-Jones unpublished observation). There are two British species in this genus; Euceraphis betulae (Koch), which is primarily associated with Betula pendula Roth, and E. punctipennis (Zett.) which is associated with B. pubescensEhrh (Blackman, 1977). This paper examines the effect of leaf age on the development and fecundity of the birch aphid Euceraphis betulae. Materials andmethods Six saplings ofBetulapendula Roth (approx. 1 m high) were planted into pots in early January. Three saplings were chosen at random at the beginning ofFebruary and were placed in a greenhouse at 20°C with a 16-h day-length in order to induce earlybud-burst, andthreewereleftoutsideinordertoallowbud-burstatthenormal time. On 2.iv.87 when the treatment sapHngs in the greenhouse had fully expanded leaves andthebuds ofthecontrolgroup were closeto bursting, all sixsaplings were movedintoaconstanttemperatureroomat 10 °C, 70*!7o relativehumidityanda 16-h day-length. Thesaplingswerewateredregularlyandmistsprayeddailywithdistilled water for the duration of the experiment. Leaves wereremoved fromeachtreeevery 14days between 21.iv.87 and 18.vi.87. These were analysed for toughness and soluble nitrogen content. Toughness was measured using a push-pull fruit tester, which estimated the force needed to push mm acircularmetalrodof5 diameterthroughtheleaflamina. Solublenitrogenwas measured by standard Kjeldhar method (van Emden & Bashford, 1969). Eggs of Euceraphis were collected in Silwood Park, Ascot during the last week of March 1987, and were kept in a refrigerator at 5 °C until the beginning of the experiment. On 13.iv.87, bywhichtimemostB.pendulainthefieldhadinfestations of Euceraphis, the eggs were removed from the refrigerator and left at room temperaturefor24h. Duringthistimethemajorityofeggshatched. Thenewlyhatched nymphswereintroducedonto thesaplings on 14.iv.87. Ten nymphswereplaced on 16 BR. J. ENT. NAT. HIST..4: 1991 eachsapling. Nymphs wereplaced individuallyonto terminal buds or leaves. Muslin bagslargeenough tocoverasingleleaf, andsecured aroundthesupportingtwigwere used to contain the aphids. Aphidswereobservedevery otherday, and the numberofoffspring produced per time interval was recorded. All second-generation nymphs were removed from their parent, and 56 were randomly allotted to one ofthe treatments and placed onto the relevant saplings as part of the second-generation experiment. As no nymphs were producedbyindividuals feedingon thematureleaves, onlynymphs produced on the young buds were utilized in the second-generation experiment. Second-generation aphidsweremonitored inasimilar fashion tothoseofthe firstgeneration. All third- generation nymphs were removed from the saplings, but not utilized in any further experiments. Theexperimentterminated on 20.vi.87 with thedeath ofthe last second- generation aphid. Results Thelevelofsolublenitrogenwasgreaterinyoungleavesthanoldoneverysampling date(Fig. la). Leaftoughnessincreasedthroughout theexperiment in both treatments (Fig. lb), and was greater in old leaves than young on all dates prior to 18.vi.87, when the two measurements converged. e...^ O) 6 ^^^^^ -a ^^^"-^ F 6 -Q c Q---- "D 0) 4 - ao> Z.t; 3 - » n 2 - 3 o (/> 1 1 1 7thMay 21May Date 7thMay 21May Date Yo—unge—Birch Old..QB.i.r.c.h Fig. 1. ChangesintheattributesofyoungandmatureleavesofBetulapendula,(a)meansoluble nitrogen content and (b) leaf toughness. Bars are standard errors. BR. J. ENT. NAT. HIST., 4: 1991 17 The differences in leaf quality between treatments were reflected in the aphid's performance (Table 1). No first-generation nymphs survived to adulthood on the matureleaves, andonlytwosecondgenerationnymphsreachedmaturity.Thesurvival of nymphs was significantly greater on young leaves where approximately 50% of individuals reached maturity (two by two contingency table; generation 1, Yates' corrected x^=10.5, P<0.01; generation 2, Yates' corrected x^=6.48, P<0.05). The development time ofindividuals on old leaves was also longer than those on young foliage, and the average fecundity was lower. Table 1. Survival,developmentandfecundityoffirstandsecondgenerationEuceraphisbetulae on young and mature foliage ofBetulapendula. Figures in parentheses are standard errors. Young leaves Old leaves Generation: 1st 2nd 1st 2nd Initial population size 30 26 30 30 Proportion alive after 7 days 0.77 0.73 0.03 0.27 Proportion surviving to adulthood 0.50 0.38 — 0.07 Mean time to adulthood (days) 12.4 22.4 25 (0.98) (0.49) — Mean duration as mature pre-reproductive (days) 1.82 3.167 2 (0.12) (1.45) — Mean adult life time (days) 15.3 10.4 12 (2.95) (2.125) Total number offspring 226 37 — 7 Mean number nymphs per adult 15.06 3.7 3.5 (4.89) (2.09) Therewerealsosubstantialdifferencesinperformancebetweengenerations. Second- generation nymphs did sUghtly better on mature foliage than first generation ones, however, the opposite was true on young foliage. Two of the three measures of performance tested showed significant differences between generations on young foliage, these were fecundity (Kruskalls-WalHs statistic= 14.52, P<0.001) and developmenttime(T=8.26, DF=23,P<0.001). However, therewerenostatistically significant differences in survival to maturity (two bytwo contingencytable, Yates' Discussion The effect offood quality on the population dynamics ofthis aphid is dramatic. The increasing leaf toughness probably renders the leaf cuticle more difficult to penetrate, andthereducedlevelsofsolublenitrogenintheunderlyingtissues, which isimportant forproteinproduction, slowsaphidgrowthandreproduction. Individuals hatchinglaterintheyear, whenmostleavesaremature, are facedwithanincreasingly difficult task of accessing ever diminishing resources, and consequently have very little chance of attaining maturity. It is easy to see how selection acts to maintain hatching in the early spring. AlthoughadultEuceraphisarelargeandmaybeabletofeedonmatureleavesand twigs(Gauge, 1989; Stroyan, 1977), theabilityoffirst-generationnymphsto feedon matureleavesappearstobelimited. However, nymphsoflatergenerationsmust feed successfullyonmatureleavesinordertoallowthespeciestosurviveuntiltheautumn. Itisnotclearhowtheselaterhatchingnymphsovercomethedifficultiesoffeedingon nutritionally poor substrates. There may be some physiological or morphological variation between generations, for example, in stylet length. The aggregation of 18 BR. J. ENT. NAT. HIST.,4: 1991 Euceraphis in midsummer onto leaves of better quality (Wratten, 1974), combined with the natural variation in leafand treequalitywillcertainlyserve to reduce some of the difficulties. Theslightlygreatersuccessofsecond-generation aphids in feedingon mature leaves, suggeststhatsomeadaptivemechanismmayindeedbeinplace, henceallowingnymphs oflater generations to feed successfully. Ifsuch an adaptation existed, it could well be traded off against increased fecundity in the first generation. Ovariole number is known to vary between aphid generations. In Euceraphis the first generation possessten ovarioles, and subsequentgenerationseight (Leatheretal., 1988). This alonewill lead todifferences in fecundity between generations. However, the difference in fecundity between first- and second-generation nymphs on young leaves seems toogreat tobeexplained totallybydifferencesin ovariolenumbers. The observed differences areprobablydueto acombination ofreducedovariolenumber, andthe fact that second-generationaphids fedon apoorerdiet than thoseinthe first generation. Dixon (1976) reportsthat nymphsofthesycamoreaphid(Drepanosiphum platanoidis Schr.) feeding on newly burst buds were heavier and more fecund than those feeding on foliage which had burst their buds only 7 days earlier. This serves todemonstratetheimportanceofsmallchangesinfoodqualitytoaphidpopulations. References Ayres, M. P. & Maclean, S. F. 1987. Development ofbirch leaves and the growth energetics of Epirrita autumnata (Geometridae). Ecology 68: 558-568. Blackman, R. L. 1977. The existence of two species of Euceraphis (Homoptera: Aphididae) on birch in Western Europe, and a key to European and North American species ofthe genus. Syst. Ent. 2: 1-8. Dixon,A. F. G. 1963. Reproductiveactivityofthesycamoreaphid,Drepanosiphumplatanoidis (Schr.) (Hemiptera: Aphididae). J. AnimalEcol. 32: 33-48. Dixon, A. F. G. 1966. Theeffect ofpopulation densityand nutritivestatus ofthe host on the summerreproductiveactivityofthe sycamoreaphidDrepanosiphumplatanoidis(Schr.). J. AnimalEcol. 35: 105-112. Dixon, A. F. G. 1969. Quality and availabilityof food for a sycamore aphid population. In: Animalpopulationsinrelationtotheirfoodresources. Ed. A. Watson, Symposium No. 10. British Ecological Society, pp. 271-287, Blackwell Scientific Publications, Oxford. Dixon, A. F. G. 1971. The role ofintra-specific mechanisms and predation in regulating the numbers of the lime aphid, Eucallipterus tiliae (L.). Oecologia Berl8: 179-193. Dixon,A.F.G. 1976.Timingofegghatchandviabilityofthesycamoreaphid,Drepanosiphumplata- noidis(Schr.),atbudburstofsycamore,AcerpseudoplatanusL.J. AnimalEcol. 45:593-603. van Emden, H. F. & Bashford, M. 1969. A comparison of the reproduction of Brevicoryne brassicaeandMyzuspersicaeinrelationtosolublenitrogenconcentrationandleafage(leaf position)intheBrusselssproutplant.Entomologia, ExperimentalisetApplicata12: 351-364. Feeny, P. 1970. Seasonalchangesinoak leaftanninsand nutrientsasacauseofspringfeeding by winter moth caterpillars. Ecology 51: 565-581. Gange, A. C. G. 1985 Overwintering in thebirch aphid, Euceraphispunctipennis. Br. J. Ent. Nat. Hist. 2: 181-183. Leather, S. R., etal. 1988. Variation in ovariole number within the Aphidoidea. J. Nat. Hist. 22: 381-393. Mittler, T. 1958. Studies on the feeding and nutrition of Tuberolachnus salignus Gmelin (Homoptera: Aphididae). II. Thenitrogenandsugarcompositionofingestedphloemsap and exuded honeydew. J. Exp. Biol. 35: 74-84. Stroyan, H. L. G. 1977. HomopteraAphidoideaChaitophoridaeandCallaphididae. Handbk Ident. Insects 2 (4a). London, Royal Entomological Society. Wratten, S. D. 1974. AggregationinthebirchaphidEuceraphispunctipennis(Zett)in relation to food quality. J. AnimalEcol. 43: 191-198.