Entomologia Experimentalis et Applicata88: 73–80, 1998.© 1998Kluwer Academic Publishers. Printed in the Netherlands.

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Probing and feeding characteristics of the greenhouse whitefly inassociation with host-plant acceptance and whitefly strains

H. Lei1,2,∗, W. F. Tjallingii1 & J. C. van Lenteren11Department of Entomology, Wageningen Agricultural University, 6700 EH Wageningen, The Netherlands;2Department of Biology, Beijing Normal University, Beijing 100875, P.R. China;∗Current address: Departmentof Ecology, Lund University, S-223 62 Lund, Sweden

Accepted: April 16, 1998

Key words: Trialeurodes vaporariorum, rearing history, host plants, acceptance ranks, probing, phloem feeding,electrical penetration graph, DC-EPG

Abstract

Host-plant and whitefly strain effects and their interactions on the probing and sap feeding of the greenhousewhitefly, Trialeurodes vaporariorum(Westwood), have been investigated in this study using the DC-EPG (Elec-trical Penetration Graph) technique. Whiteflies generally displayed fewer but longer probes on highly acceptablecucumber than on less acceptable tomato. Both whitefly strains, the T(omato)-strain and the C(ucumber)-strain,showed a significantly lower number of phloem phases on cucumber than on tomato. However, the durationof total phloem phases achieved by either of the whitefly strains on these two host plants was not significantlydifferent. These data indicate that a more continuous phloem feeding has occurred on cucumber plants. Indeed,the percentage of phloem feeding time after the first sustained phloem phase (longer than 15 min) was higher oncucumber for the C-strain whiteflies. When comparing these two whitefly strains, the T-strain whiteflies probed lessfrequently but longer than the C-strain whiteflies did on both host plants. Also, the T-strain whiteflies displayed alonger duration of total phloem phases on tomato. An interaction between the whitefly strain and plant effects wasdetected on a parameter, which showed that whiteflies probed significantly longer before reaching the first phloemphase on the host plants that had been previously experienced. In conclusion, both plant species and whitefly strainsaffect whitefly’s probing and feeding behaviour, though plant effects are much stronger.

Introduction

The greenhouse whitefly,Trialeurodes vaporariorum(Westwood) is a serious pest insect in temperate re-gions, causing damage to plants in greenhouses andopen fields by feeding on plant assimilates and trans-mitting viruses. Sooty mould fungi which developon whitefly’s excreted honeydew also cause economicloss by reducing the commercial values of products.Trialeurodes vaporariorumis a polyphagous insect,but large differences exist in its host-plant utilisationpattern, which can be expressed as a performance oracceptance ranking. The acceptance ranks of severalhost plants, based on the life history parameters ofwhiteflies such as mortality and fecundity, has beenestablished as follows: eggplant> gherkin> cucum-

ber> gerbera>melon> tomato> sweet pepper (vanLenteren & Noldus, 1990). The quality of the plantsap, the presence of secondary metabolites and certainleaf surface features are thought to contribute to thisranking (Noldus et al., 1986; van Vianen et al., 1988;van Lenteren & de Ponti, 1990).

The acceptance ranks are not only influenced byplant factors, but also by whitefly strains (van Boxtelet al., 1978; Thomas, 1993), i.e., a whitefly popula-tion that has been reared on a certain plant species formore than 50 generations. Transferring insects from aplant on which they have been reared for a long timeto a new host plant species can result in changed per-formance. The cotton whitefly has been observed tohave a high mortality when transferred from cotton orsweet potato to cassava, although cassava is also an

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acceptable host plant for certain strains of this species(Legg, 1996). It is uncertain whether this ‘strain effect’is reflected in the probing behaviour of whitefly.

As phloem feeders, whiteflies need to probethrough the epidermis to the vascular bundles us-ing their stylets before they can start feeding on thephloem. Various invisible probing activities take placewhen the stylets are penetrating into the leaf tissue.The electrical penetration graph technique (EPG, DCsystem), developed to monitor the probing activitiesby aphids (Tjallingii, 1988), has also been used toinvestigate the probing activities by greenhouse white-flies (Janssen et al., 1989). The main advantage of thistechnique is that it allows visualisation and quantifica-tion of the invisible probing activities within the planttissue. The output EPG waveforms are determined bythe insect’s behaviour and by the stylet tip positionsin leaf tissue. The first EPG application to whiteflyadults yielded waveforms similar to aphids (Janssen etal., 1989). However, the waveforms from whitefly lar-vae appeared different than that from adults (Lei et al.,1996a). In adult EPGs, probing and non-probing canbe distinguished. Within probing, three main phasesare distinct: pathway phase (C and F waveform), re-flecting intercellular stylet penetration; xylem phase(G waveform), reflecting water ingestion; and phloemphase (E waveform), reflecting phloem feeding, in-cluding salivation and ingestion. Preliminary studiesregarding whitefly probing behaviour on plants of dif-ferent acceptance levels have shown that whitefliesprobe and feed less on the lowest-ranking host plant(sweet pepper) than on the highest-ranking host plant(cucumber) (Lei et al., 1996b). However, it is un-known whether this pattern would be maintained forthe host plants of less distinguishable acceptance lev-els and would be affected by the host-plant origin ofwhitefly.

This paper concerns the investigations into theprobing behaviour of the greenhouse whitefly, in asso-ciation with host plants of different acceptance levelsand with different whitefly strains.

Materials and methods

Plants and insects. Cucumber,Cucumis sativuscv.Lange Groene Giganta and tomato,Lycopersicon es-culentumcv. Moneymaker were grown in a glasshouseat 18–22◦C and L16:D8 photoperiod. Seedlings with3–5 true leaves were used in the experiments. Twowhitefly strains were used, one reared on tomato (cv.

Moneymaker) for about 8 years, referred to as T-strain, and another on cucumber (cv. Lange GroeneGiganta) for about 5 years, referred to as C-strain. Thewhitefly stock cultures were kept in separate cages inglasshouse compartments with the same climate con-ditions as above. Three-day-old females were used inthe experiments. Whitefly individuals were used once,but one plant was used for two EPG recordings.

EPG recording. The recording of EPGs was con-ducted using a DC system with an input resistance of109 Ohm (Tjallingii, 1988). Plant, whitefly, and ampli-fier were placed in a Faraday cage to shield the set-upfrom external electric noise sources. Before startingthe EPG recording, the whitefly was immobilised us-ing a vacuum device, and the white wax powder onthorax was cleaned off with a fine brush. Then, adroplet of conductive water-based silver paint was de-posited on the thorax. The whitefly was attached, withsilver paint, to a 2 cm length of gold wire of diam-eter 10µm, as this diameter has least influence onwhitefly’s probing behaviour (Lei et al., 1997). TheEPG signals were acquired (A/D conversion) by a PCand subsequently analysed withSTYLET 2.0software(Tjallingii & Mayoral, 1992). Recording was con-ducted for a total of 12 h for each treatment. About 20females were tested for each combination of the hostplant and whitefly strain.

EPG parameters. Numbers and mean duration of to-tal probes and phloem phases were used as generalparameters (Parameters 1–4, Tables 1 and 2). The se-quence of probing activities by each individual insectwas divided into two or three periods on the basisof the following key events: the first phloem phaseand the first phloem phase longer than 15 min. Theywere used as indicators of phloem finding and phloemacceptance, respectively. Therefore, to reflect the path-way factors affecting the phloem finding process, thetime needed to reach the 1st phloem phase and the 1stsustained phloem phase were measured, either fromthe start of an experiment or from the start of a probeduring which the event occurred (Parameters 5–8, Ta-bles 1 and 2). Moreover, the summed non-probingperiods (%) before the 1st phloem phase could reflectto what degree the pathway probing was interruptedeither by mesophyll factors or by surface factors (Pa-rameter 9, Tables 1 and 2). As the absolute durationof the total phloem phases (Parameter 4, Tables 1 and2) could be limited by the experimental time, we useda proportional phloem phase in the total time after the

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1st sustained phloem phase to reflect the continuity ofthe whitefly’s phloem feeding (Parameter 10, Tables1 and 2). The values of the general parameters (1–4)were calculated using all replicates, but the phloemphase related parameters (5–10) were based on theindividuals that showed any phloem phase. Finally,the percentage of whiteflies showing phloem phases(Parameter 11, Table 2) was calculated.

Statistics. Statistical tests were carried out using thesoftware packageSTATGRAPHICS 7.0(ManugisticsInc. and Statistical Graphics Corp.). A two-way analy-sis of variance (ANOVA), followed by the Tukey–Kramer multiple comparison of means, was adopted totest the whitefly strain effect, the plant effect, and theirinteractions. Before running the ANOVA, square root,logarithmic and arcsine transformations were appliedto the data concerning the number, duration, and per-centage of the probing activities, respectively. To testthe efficiency of these transformations, the Scheffé-Box and Kolmogorov-Smirnov methods were used toexamine the variance homogeneity and the data nor-mality, which are important assumptions for ANOVA.Among the 10 parameters, Scheffé-Box method re-vealed that the F value for Parameter 10 in Table 2(F = 8.59) was bigger than the critical value (F =5.95) at 0.05 significance level and thus concludedthat the variates of this parameter have heterogeneousvariances. The P values of both Parameters 4 and 10in Table 2 calculated from the Kolmogorov-Smirnovmethod were 3.77E-6 and 0.025, respectively, andthus concluded that the variates of these parametersdo not fit to a normal distribution. Therefore, in thefurther analysis, non-parametric Kruskal–Wallis andMann–Whitney U tests were applied to these data.

Results

Two-way ANOVA. ANOVA analysis was conductedfor Parameters 1–3 and 5–9, and the results gener-ated from this analysis are presented in Table 1. Bothwhitefly strain and plant effects were significant forthe number and duration of total probes (Parameters 1and 2). All other parameters showed only significantplant effects. Note that for the time to the first phloemphase in a probe (Parameter 6), in addition to a strongplant effect, a significant interaction between whiteflystrain and plant effects was also detected (P=0.042).In general, the host plants had a much stronger influ-ence on the probing and feeding activities of whiteflies

than the whitefly strains and the interactions betweenthe two.

Host-plant effects. On cucumber, the whiteflies hadsignificantly fewer but longer probes and a lower num-ber of phloem phases (Parameters 1–3, Table 2), buta longer time was needed to reach the first phloemphase, both from the start of an experiment as wellas from the beginning of the probe concerned (Para-meters 5–6, Table 2). Also, the time needed to achievea sustained phloem feeding was longer on cucumberthan on tomato (Parameters 7–8, Table 2). The meanduration of total phloem phases (Parameter 4, Table 2)was not significantly different between cucumber andtomato for both whitefly strains. Moreover, a signif-icantly lower percentage of non-probing time beforethe first phloem phase (Parameter 9, Table 2) wasfound on cucumber than on tomato. Also, the percent-age of time spent in the phloem after the first sustainedphloem phase in the experiment (Parameter 10, Ta-ble 2) was higher on cucumber than on tomato for theC-strain whiteflies, but not significantly so (Kruskal–Wallis, P<0.001; Mann–Whitney U, P=0.362). Incontrast, the percentage of whiteflies that showed anyphloem phase within one EPG recording period (12 h)(Parameter 11, Table 2) was lower on cucumber thanon tomato.

Whitefly strain effects. Significant whitefly strain ef-fects were detected in the number of probes (P=0.005)and the mean duration of total probes (P=0.008) inthe ANOVA (Parameters 1–2, Table 1). When testedeither on tomato or on cucumber, the T-strain white-flies probed fewer times but for longer periods thanthe C-strain whiteflies did (Table 2). The T-strainwhiteflies showed a significantly longer duration oftotal phloem phases than the C-strain whiteflies ontomato (Kruskal–Wallis, P=0.061; Mann-Whitney U,P=0.047) but not on cucumber (Parameter 4, Ta-ble 2). Similarly, the T-strain whiteflies showed asignificantly higher percentage of phloem feeding timeafter the first sustained phloem phase than the C-strain whiteflies on tomato (Kruskal–Wallis, P<0.001;Mann–Whitney U, P=0.001) but not on cucumber(Parameter 10, Table 2).

Interactions between plant and whitefly strain effects.Among the EPG parameters shown in Table 1, onlythe time to the 1st phloem phase in a probe (Parame-ter 6) showed a significant interaction between plantand whitefly strain effects in the ANOVA. On tomato,

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Table 1. Results of two-way ANOVA for EPG parameters concerning whitefly strains (T-, C-strain), host-plants(tomato, cucumber), and their interactions. P values smaller than 0.05 are marked in bold face. Abbreviations: d.f.degree of freedom; SS, sum of squares; P, significance level; E, phloem phase; sustained E, phloem phase longer than15 min; dash line, data violating ANOVA assumptions not shown

Whitefly strain Plant Strain× plant Residual

d.f. 1 1 1 78

1. Number of probes SS 32.691 85.002 2.331 305.982

P 0.005 <0.001 0.452

d.f. 1 1 1 78

2. Duration of total probes SS 0.047 0.065 0.001 0.492

P 0.008 0.002 0.852

d.f. 1 1 1 61

3. Number of phloem phases (E) SS 0.074 67.211 0.022 68.442

P 0.8 <0.001 0.891

d.f. – – – –

4. Duration of total phloem phases (E) SS – – – –

P – – – –

d.f. 1 1 1 76

5. Time to the 1st E in experiment SS 0.098 2.201 0.091 9.621

P 0.392 <0.001 0.408

d.f. 1 1 1 65

6. Time to the 1st E in probe SS 0.056 1.941 0.301 4.481

P 0.382 <0.001 0.042d.f. 1 1 1 75

7. Time to the 1st sustained E in experiment SS 0.048 0.874 0.076 9.933

P 0.558 0.012 0.459

d.f. 1 1 1 60

8. Time to the 1st sustained E in probe SS 0.003 2.122 0.112

P 0.825 <0.001 0.151

d.f. 1 1 1 76

9. Percentage of non-probe before the 1st E SS 0.0431 0.601 0.018 3.051

P 0.305 <0.001 0.507

d.f. – – – –

10. Percentage of phloem period after the SS – – – –

1st sustained E P – – – –

the T-strain whiteflies spent more time in the path-way probing which led to phloem feeding than theC-strain whiteflies did. Similarly, the C-strain white-flies showed a longer pathway phase before reachingthe phloem phase when tested on cucumber than theT-strain whiteflies (Figure 1). Although no signifi-cant differences were found, some other parametersshowed a similar trend on average, such as the time tothe 1st sustained phloem phase in an experiment and ina probe (Parameters 7–8, Table 2) and the proportionalphloem feeding time after the 1st sustained phloemphase (Parameter 10, Table 2).

Discussion and conclusions

Effects of host-plant tissue factors on acceptanceranks. The process of host-plant selection by white-flies consists of a series of consecutive events startingwith the first labial contact with the plant surface,followed by the stylet penetration through successivetissue layers between the epidermis and the phloemsieve elements and, ultimately, by phloem sap feeding.Continuous phloem sap feeding can be regarded as ac-ceptance of a host plant. However, before feeding onthe phloem sap, many factors can play different rolesin the initiation, maintenance, and cessation of eachsubsequent event in this process and thus contribute to

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Table 2. Means and standard errors of EPG parameters in association with two host-plant species (cucumber and tomato) and twowhitefly strains (T-strain and C-strain). Different letters in the same row indicate significance derived from Tukey–Kramer method.E, phloem phase; sustained E, phloem phase longer than 15 min. The significance test for Parameter 4 and 10 was carried out usingKruskal-Wallis and Mann–Whitney U methods

T-whitefly strain C-Whitefly strain

Cucumber Tomato Cucumber Tomato

N = 20 N = 19 N = 23 N = 20

1. Number of probes 29.2± 3.0 a 50.0± 4.5 b 43.0± 6.1 ab 79.3± 9.6 c

2. Duration of total probes (min) 603.0± 18.3 c 528.6± 20.6 b 539.0± 19.5 bc 478.7± 20.2 a

3. Number of phloem phases (E) 1.3± 0.2 a 9.7± 1.8 b 1.4± 0.3 a 9.9± 1.5 b

4. Duration of total phloem phases (E) (min) 226.8± 52.3 ab 258.3± 29.4 a 184.6± 39.1 ab 162.8± 22.8 b

5. Time to the 1st E in experiment (min) 364.9± 55.0 ab 168.4± 27.0 a 443.8± 49.4 b 185.3± 27.5 a

6. Time to the 1st E in probe (min) 34.9± 5.2 b 23.2± 4.1 a 41.9± 6.0 b 16.1± 3.0 a

7. Time to the 1st sustained E in experiment (min) 389.2± 55.1 a 292.4± 52.8 ab 454.2± 50.8 a 248.4± 33.6 b

8. Time to the 1st sustained E in probe (min) 35.3± 6.0 b 18.0± 2.6 a 43.5± 6.2 b 15.4± 1.9 a

9. Percentage of non-probe before the 1st E 24.0± 3.2 a 35.3± 4.4 bc 31.0± 3.7 ab 43.9± 4.1 c

10. Percentage of phloem period after the 46.5± 9.5 ab 58.5± 3.4 a 49.7± 9.1 ab 32.8± 3.8 b

1st sustained E

11. Percentage of whiteflies showing sustained 70 95 65 95

phloem phase

Figure 1. Graphic expression of an interaction between the planteffect and the whitefly strain effect. The data points are the meansof log (time to 1st phloem phase (E) in a probe (seconds), with 95%confidence interval.

the total acceptance rank. A critical selection of pa-rameters to evaluate the acceptance ranks is thereforeimportant. In our selection of parameters (numbered1–11 in Tables 1 and 2), we used two key events,(1) the first phloem phase and (2) the first phloemphase that is sustained for more than 15 min. Onsuitable host plants, the first phloem phase is usuallysustained already. These two key events divide theprobing process into two or three natural parts, de-

pending on whether the first phloem phase is longerthan 15 min. Before the first key event, i.e., the firstphloem phase, pathway activities are predominant, asreflected by the Parameters 5–9 in Table 2. These pa-rameters have been thought to reflect the host-plantrecognition as well as the phloem finding process inwhich factors from epidermis, mesophyll, and non-transport tissue in the vascular bundle are involved.After the first key event, specific phloem propertiesplay a predominant role which may lead to acceptanceof the sap as a food source. In a few observationswhere concurrent EPG and honeydew recordings wereconducted, we found that whitefly did not excrete anyhoneydew droplets when the phloem phase was in pe-riods shorter than 15 min. Thus, we took a periodlonger than 15 min as a criterion for the sustainedingestion, in other words phloem acceptance, whichcan also be regarded as the first sign of host-plant ac-ceptance. A host plant is considered to be of higheracceptance rank when the phloem feeding is morecontinuous (Parameter 10, Tables 1 and 2).

Chemical and physical properties of plant tissuecan greatly affect each element of the probing process.As some of the apical sensilla on a whitefly’s labium,in contrast to aphids, are chemosensilla (Walker &Gordth, 1989), the non-probing duration may be in-fluenced by the surface semiochemicals (van Lenteren& Noldus, 1990). For the duration of the stylet path-

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way phase, factors in the superficial tissue layers seemvery important. Different pathway probing time maybe caused by stimulating or deterring effects of somechemicals in the tissue. This result could relate tothe presence of a large number of pre-cibarial andcibarial chemosensilla in whiteflies (Wensler & Fil-shie, 1969; Hunter et al., 1996). Whiteflies may usethese chemoreceptors to taste intercellular plant flu-ids, as these homopterans, in contrast to aphids, mostlikely do not sample cells intracellularly (Tjallingii,1988; Janssen et al., 1989; Lei et al., 1996a). Whenthe pathway phase exerts an analogous influence onthe whitefly’s probing, the phloem phase, especiallythe sustained phloem ingestion, becomes importantfor ranking a host-plant acceptance level. Usually, thehigher the acceptance ranks the longer the phloemingestion andvice versa.

The results of this study demonstrate that cucum-ber is more readily accepted as a host plant thantomato, based on a number of EPG parameters. Theseparameters include: fewer probing times (Parameter1, Table 2), longer total probing duration (Parameter2, Table 2), shorter non-probing time before the firstphloem phase (Parameter 9, Table 2), fewer numberof phloem phases (Parameter 3, Table 2) but almostequal total duration on two host plants, and more per-sistent phloem feeding after the 1st phloem phase inthe C-strain whiteflies (Parameter 10, Table 2). Thesedifferences were also observed in host-plant rankingfor aphids (Webster et al., 1993; Cole, 1994; Cail-laud et al., 1995). However, the time to the first orthe first sustained phloem phase in an experiment orin a probe (Parameters 5–8, Table 2), complicates thispoint, due to the paradox that whiteflies actually spentlonger time in the pathway probing and thus causeda postponement of subsequent phloem phases on cu-cumber. This postponement may decrease the numberof whiteflies that reached the phloem phase in theexperimental time (Parameter 11, Table 2), togetherwith other possible factors such as the impedimentof whitefly’s free movement caused by wiring. Thisimpediment may be more serious on cucumber leavesthan tomato leaves due to different morphological leaffeatures. No further experiment was carried out toclarify what factors were involved. Usually, such anegative effect can be overcome by using the sameplant species or varieties as control. The percentage ofwhiteflies that reached the phloem phase (Parameter11, Table 2) can be enhanced by prolonging the dura-tion of the experiment (Lei et al., 1997). The fact of alonger total pathway in high-ranking cucumber is con-

trary to the results of some aphid studies where moreacceptable host-plants were shown to cause shorterpathway probing (Givovich & Niemeyer, 1995, andreferences therein). This might be related to a white-fly’s characteristic pathway probing (e.g., very fewpotential drops; clearly distinguishable subpatterns ofC waveform). We can speculate that some stimulantspresent in cucumber tissue have been detected duringthe occurrence of the C waveform of a whitefly andresult in a prolonged intercellular exploration whichmay give the whitefly a better chance to contact asieve element. Apparently, more comparative studiesare greatly needed to confirm this point. Alternatively,one may consider that the overall acceptance rank ofa host plant, as indicated by the insects’ performance,does not necessarily reflect the acceptance at all tissuelevels in the plant. Consequently, this overall accep-tance may be inconsistent with some phases of theprobing process.

The question arises whether physical factors couldhave caused this prolonged pathway phase. Anatomi-cal differences between the two host plants, especiallythe distance to the phloem, could account for this.Therefore, we measured the distance to the phloem inthe tertiary veins (the preferred probing sites) and itis indeed larger in cucumber than in tomato (Table 3).However, the proportional increase in distance is muchlower than that in the pathway probing time prior to thefirst phloem phase in a probe (Table 3). Therefore, thedifferences in distance cannot explain this phenom-enon completely. An involvement of chemical factorscan certainly not be excluded.

Whitefly strain effects and their interactive role inhost-plant acceptance.Differences in performancebetween strains of whitefly have been shown by otherauthors. Van Lenteren et al. (1989) reported thata Hungarian strain of the greenhouse whitefly per-formed much better on sweet pepper, which is gen-erally a poor host plant for whiteflies, than a Dutchwhitefly strain. In our study, two parameters (Parame-ters 1–2; Table 1) showed significant whitefly straineffects. The T-strain whiteflies exhibited fewer probesand longer total probing time than the C-strain oneson cucumber as well as on tomato. Within the to-tal probing time, only the figures of the total phloemphases (Parameter 4, Table 2) showed the same ten-dency, thus forming the principal contribution. Infact, on tomato plants, the T-strain whiteflies had asignificantly longer phloem phase than the C-strainwhiteflies, but no significance was observed on cu-

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Table 3. Proportional increment (%) in cucumber (Cucumis sativus) phloem distance fromlower epidermis, in comparison with the increased whitefly pathway time before the 1stphloem phase and 1st sustained phloem phase in the probe concerned (Parameters 6 and 8in Table 2)

Tomato Cucumber % increment in cucumber

Phloem distance (µm) 97 108 11

Time to 1st E in probe (min)

T-strain 23 35 52

C-strain 16 42 163

Time to 1st sustained e in probe

T-strain 18 35 94

C-strain 15 44 193

cumber plants. Other parameters, such as those relatedto the two key events (Parameters 5–10, Table 2)showed no clear strain differences. In the course oftheir rearing history, a certain selection ‘pressure’ hasbeen effective on the insects. On the other hand, along-time association with a host-plant species mayresult in behavioural modifications, known as ‘host-plant induction’ (Bernays & Weiss, 1996). The adultstested in our experiments were reared on their strainhost plants and had no previous experience on anyother plants. So, the resulting effect could be partlygenetic and partly phenotypic. Our experiments do notallow the separation of these two components.

Host-plant induced changes on the whitefly’s per-formance have been previously reported. Enkegaard(1993) examined the performance of two cotton white-fly (Bemisia tabaci(Gennadius)) strains (poinsettiastrain and tobacco strain) on poinsettia plants and dis-covered that the poinsettia-strain whiteflies had longerlongevity and higher fecundity than the tobacco-strainwhiteflies. In our experiments, the only parameter thatshowed significant interactive effects in the ANOVAwas the time to the first phloem phase in a probe(Parameter 6, Table 1). This time was longer on cu-cumber than on tomato, as shown in plant effects, butthis effect was not independent. Instead, the white-fly strains interacted so that the ranking of the strainson tomato, according to the values of this parameter,was the reverse of that on cucumber (Figure 1). Actu-ally, some other parameters (Parameters 7, 8 and 10,Table 2) showed the same non-significant tendency.This interactive effect indicates that a previous expe-rience can cause the insects to spend a longer time onpathway probing. This might be a favourable strategyfor whiteflies to find the phloem vessel by exploring

the tissue more extensively. Besides the prolongedpathway probing, previous experience also resulted inmore persistent phloem feeding after the 1st phloemphase (Parameter 10, Table 2).

In conclusion, the probing and feeding profile ofwhiteflies is mainly determined by plant factors at alltissue levels. Long-time rearing of whiteflies on a sin-gle host-plant species can form a certain strain withits own probing characteristics. The host-plant ori-gin of whiteflies should be taken into account whenperforming EPG tests on different host plants.

Acknowledgements

This study was part of the co-operative research pro-gram between Wageningen Agricultural University(WAU), the Netherlands and Beijing Normal Univer-sity, P.R. China. The senior author was financiallysupported by the Dutch Royal Academy of Sciences(KNAW), the Dutch Ministry of Agriculture & Fish-eries and WAU.

References

Bernays, E. A. & M. R. Weiss, 1996. Induced food preferencesin caterpillars: the need to identify mechanisms. EntomologiaExperimentalis et Applicata 78: 1–8.

Boxtel, W. van, J. Woets & J. C. van Lenteren, 1978. Determina-tion of host plant quality of eggplant (Solanum melongenaL.),cucumber (Cucumis sativusL.), tomato (Lycopersicon esculen-tum L.) and paprika (Capsicum annuumL.) for the greenhousewhitefly (Trialeurodes vaporariorum(Westwood)) (Homoptera:Aleyrodidae). Medeldelingen van de Faculteit Landbouwweten-schappen Rijksuniversiteit Gent, 43/2, 397–408.

Caillaud, C. M., J. S. Pierre, B. Chaubet & J. P. Di Pietro, 1995.Analysis of wheat resistance to the cereal aphidSitobion ave-naeusing electrical penetration graphs and flow charts combined

80

with correspondence analysis. Entomologia Experimentalis etApplicata 75: 9–18.

Cole, R. A., 1994. Locating a resistance mechanism to the cab-bage aphid in two wild Brassicas. Entomologia Experimentaliset Applicata 71: 23–31.

Enkegaard, A., 1993. The poinsettia strain of the cotton whitefly,Bemisia tabaci(Homoptera: Aleyrodidae), biological and de-mographic parameters on poinsettia (Euphorbia pulcherrima) inrelation to temperature. Bulletin of Entomological Research 83:535–546.

Givovich, A. & H. M. Niemeyer, 1995. Comparison of the effecthydroxamic acids from wheat on five species of cereal aphids.Entomologia Experimentalis et Applicata 74: 115–119.

Hunter, W. B., E. Hiebert, S. E. Webb, J. E. Polston & J. H.Tsai, 1996. Precibarial and cibarial chemosensilla in the white-fly, Bemisia tabaci(Gennadius) (Homoptera: Aleyrodidae). In-ternational Journal of Insect Morphology & Embryology 25:295–304.

Janssen, J. A. M., W. F. Tjallingii & J. C. van Lenteren, 1989.Electrical recording and ultrastructure of stylet penetration by thegreenhouse whitefly. Entomologia Experimentalis et Applicata52: 69–81.

Legg, J. P., 1996. Host-associated strains within Ugandan popula-tions of the whiteflyBemisia tabaci(Genn.), (Hom., Aleyrodi-dae). Journal of Applied Entomology 120: 523–527.

Lei, H., W. F. Tjallingii, J. C. van Lenteren & R. M. Xu, 1996a.Stylet penetration by larvae of the greenhouse whitefly on cu-cumber. Entomologia Experimentalis et Applicata 79: 77–84.

Lei, H., W. F. Tjallingii & J. C. van Lenteren, 1996b. Recordingof electrical penetration graphs and honeydew excretion by thegreenhouse whitefly. In: D. Gerling & R. T. Mayer (eds), Bemisia1995: Taxonomy, Biology, Damage, Control and Management.Intercept Ltd, Andover, Hants, UK, pp. 53–68.

Lei, H., W. F. Tjallingii & J. C. van Lenteren, 1997. Effect of teth-ering during EPG recorded probing by adults of the greenhousewhitefly. Journal of Applied Entomology 121: 211–217.

Lenteren, J. C. van, A. van Vianen, I. Hatala-Zseller & C. S. Budai,1989. The parasite-host relationship betweenEncarsia formosaGahan (Hymenoptera, Aphelinidae) andTrialeurodes vaporari-orum (Westwood) (Homoptera, Aleyrodidae) XXIX. Suitabilityof two cultivars of sweet pepper,Capsicum annuumL. for twodifferent strains of whiteflies. Journal of Applied Entomology108: 113–130.

Lenteren, J. C. van & L. P. J. J. Noldus, 1990. Whitefly-plant re-lationships: behavioral and ecological aspects of whitefly-plantrelationships. In: D. Gerling (ed.), Whiteflies: Bionomics, Peststatus and Management. Intercept, Andover, Hants, pp. 47–89.

Lenteren, J. C. van & O. M. B. de Ponti, 1990. Plant-leaf morphol-ogy, host plant resistance and biological control. Proceedings of7th International Symposium of Insect-Plant Relationships, 3–8June 1989, Budapest, Hungary. Sympia Biologia Hungarica 39:365–386.

Noldus, L. P. J. J., R. M. Xu & J. C. van Lenteren, 1986. Theparasite-host relationship betweenEncarsia formosaGahan (Hy-menoptera, Aphelinidae) andTrialeurodes vaporariorum(West-wood) (Homoptera, Aleyrodidae) XIX. Feeding site selection bythe greenhouse whitefly. Journal of Applied Entomology 101:492–507.

Thomas, D. C., 1993. Host plant adaptation in the glasshousewhitefly. PhD thesis, Wageningen Agricultural University, TheNetherlands.

Tjallingii, W. F., 1988. Electrical recording of stylet penetration ac-tivities. In: A. K. Minks & P. Harrewijn (eds.), Aphids: TheirBiology, Natural Enemies and Control, Vol.2B, Elsevier SciencePublishers B.V. Amsterdam, pp. 95–108.

Tjallingii, W. F. & A. Mayoral, 1992. Criteria for host acceptanceby aphids. In: S. B. J. Menken, J. H. Visser, P. Harrewijn (eds.),Proceeding 8th Int. Symp. Insect-Plant Relationships, KluwerAcademic Publishers Dordrecht, The Netherlands, pp. 280–282.

Vianen, A. van, R. M. Xu & J. C. van Lenteren, 1988. Theparasite-host relationship betweenEncarsia formosaGahan (Hy-menoptera: Aphelinidae) andTrialeurodes vaporariorum(West-wood) (Homoptera: Aleyrodidae). XXVII. Feeding-site selec-tion by the greenhouse whitefly on different host-plant species.Journal of Applied Entomology 105: 149–153.

Walker, G. P. & G. Gordh, 1989. The occurence of apical labial sen-silla in the Aleyrodidae and evidence for a contact chemosensoryfunction. Entomologia Experimentalis et Applicata 51: 215–224.

Webster, J. A., D. R. Porter, C. A. Baker & D. W. Mornhinweg,1993. Resistance to russian wheat aphid (Homoptera: Aphidi-dae) in barley: effects on aphid feeding. Journal of EconomicEntomology 86: 1603–1608.

Wensler, R. J. D. & B. K. Filshie, 1969. Gustatory sense organs inthe food canal of aphids. Journal of Morphology 129: 473–492.