Entomologia Experimentalis et Applicata 88: 7380, 1998. 1998 Kluwer Academic Publishers. Printed in the Netherlands.

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Probing and feeding characteristics of the greenhouse whitey in association with host-plant acceptance and whitey strains
H. Lei1,2, , W. F. Tjallingii1 & J. C. van Lenteren1
of Entomology, Wageningen Agricultural University, 6700 EH Wageningen, The Netherlands; of Biology, Beijing Normal University, Beijing 100875, P.R. China; Current address: Department of Ecology, Lund University, S-223 62 Lund, Sweden
2 Department 1 Department

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 whitey strain effects and their interactions on the probing and sap feeding of the greenhouse whitey, Trialeurodes vaporariorum (Westwood), have been investigated in this study using the DC-EPG (Electrical Penetration Graph) technique. Whiteies generally displayed fewer but longer probes on highly acceptable cucumber than on less acceptable tomato. Both whitey strains, the T(omato)-strain and the C(ucumber)-strain, showed a signicantly lower number of phloem phases on cucumber than on tomato. However, the duration of total phloem phases achieved by either of the whitey strains on these two host plants was not signicantly different. These data indicate that a more continuous phloem feeding has occurred on cucumber plants. Indeed, the percentage of phloem feeding time after the rst sustained phloem phase (longer than 15 min) was higher on cucumber for the C-strain whiteies. When comparing these two whitey strains, the T-strain whiteies probed less frequently but longer than the C-strain whiteies did on both host plants. Also, the T-strain whiteies displayed a longer duration of total phloem phases on tomato. An interaction between the whitey strain and plant effects was detected on a parameter, which showed that whiteies probed signicantly longer before reaching the rst phloem phase on the host plants that had been previously experienced. In conclusion, both plant species and whitey strains affect whiteys probing and feeding behaviour, though plant effects are much stronger.

Introduction The greenhouse whitey, Trialeurodes vaporariorum (Westwood) is a serious pest insect in temperate regions, causing damage to plants in greenhouses and open elds by feeding on plant assimilates and transmitting viruses. Sooty mould fungi which develop on whiteys excreted honeydew also cause economic loss by reducing the commercial values of products. Trialeurodes vaporariorum is a polyphagous insect, but large differences exist in its host-plant utilisation pattern, which can be expressed as a performance or acceptance ranking. The acceptance ranks of several host plants, based on the life history parameters of whiteies such as mortality and fecundity, has been established as follows: eggplant > gherkin > cucum-

ber > gerbera > melon > tomato > sweet pepper (van Lenteren & Noldus, 1990). The quality of the plant sap, the presence of secondary metabolites and certain leaf surface features are thought to contribute to this ranking (Noldus et al., 1986; van Vianen et al., 1988; van Lenteren & de Ponti, 1990). The acceptance ranks are not only inuenced by plant factors, but also by whitey strains (van Boxtel et al., 1978; Thomas, 1993), i.e., a whitey population that has been reared on a certain plant species for more than 50 generations. Transferring insects from a plant on which they have been reared for a long time to a new host plant species can result in changed performance. The cotton whitey has been observed to have a high mortality when transferred from cotton or sweet potato to cassava, although cassava is also an

74 acceptable host plant for certain strains of this species (Legg, 1996). It is uncertain whether this strain effect is reected in the probing behaviour of whitey. As phloem feeders, whiteies need to probe through the epidermis to the vascular bundles using their stylets before they can start feeding on the phloem. Various invisible probing activities take place when the stylets are penetrating into the leaf tissue. The electrical penetration graph technique (EPG, DC system), developed to monitor the probing activities by aphids (Tjallingii, 1988), has also been used to investigate the probing activities by greenhouse whiteies (Janssen et al., 1989). The main advantage of this technique is that it allows visualisation and quantication of the invisible probing activities within the plant tissue. The output EPG waveforms are determined by the insects behaviour and by the stylet tip positions in leaf tissue. The rst EPG application to whitey adults yielded waveforms similar to aphids (Janssen et al., 1989). However, the waveforms from whitey larvae appeared different than that from adults (Lei et al., 1996a). In adult EPGs, probing and non-probing can be distinguished. Within probing, three main phases are distinct: pathway phase (C and F waveform), reecting intercellular stylet penetration; xylem phase (G waveform), reecting water ingestion; and phloem phase (E waveform), reecting phloem feeding, including salivation and ingestion. Preliminary studies regarding whitey probing behaviour on plants of different acceptance levels have shown that whiteies probe 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 unknown whether this pattern would be maintained for the host plants of less distinguishable acceptance levels and would be affected by the host-plant origin of whitey. This paper concerns the investigations into the probing behaviour of the greenhouse whitey, in association with host plants of different acceptance levels and with different whitey strains. Moneymaker) for about 8 years, referred to as Tstrain, and another on cucumber (cv. Lange Groene Giganta) for about 5 years, referred to as C-strain. The whitey stock cultures were kept in separate cages in glasshouse compartments with the same climate conditions as above. Three-day-old females were used in the experiments. Whitey individuals were used once, but one plant was used for two EPG recordings. EPG recording. The recording of EPGs was conducted using a DC system with an input resistance of 109 Ohm (Tjallingii, 1988). Plant, whitey, and amplier were placed in a Faraday cage to shield the set-up from external electric noise sources. Before starting the EPG recording, the whitey was immobilised using a vacuum device, and the white wax powder on thorax was cleaned off with a ne brush. Then, a droplet of conductive water-based silver paint was deposited on the thorax. The whitey was attached, with silver paint, to a 2 cm length of gold wire of diameter 10 m, as this diameter has least inuence on whiteys probing behaviour (Lei et al., 1997). The EPG signals were acquired (A/D conversion) by a PC and subsequently analysed with STYLET 2.0 software (Tjallingii & Mayoral, 1992). Recording was conducted for a total of 12 h for each treatment. About 20 females were tested for each combination of the host plant and whitey strain. EPG parameters. Numbers and mean duration of total probes and phloem phases were used as general parameters (Parameters 14, Tables 1 and 2). The sequence of probing activities by each individual insect was divided into two or three periods on the basis of the following key events: the rst phloem phase and the rst phloem phase longer than 15 min. They were used as indicators of phloem nding and phloem acceptance, respectively. Therefore, to reect the pathway factors affecting the phloem nding process, the time needed to reach the 1st phloem phase and the 1st sustained phloem phase were measured, either from the start of an experiment or from the start of a probe during which the event occurred (Parameters 58, Tables 1 and 2). Moreover, the summed non-probing periods (%) before the 1st phloem phase could reect to what degree the pathway probing was interrupted either by mesophyll factors or by surface factors (Parameter 9, Tables 1 and 2). As the absolute duration of the total phloem phases (Parameter 4, Tables 1 and 2) could be limited by the experimental time, we used a proportional phloem phase in the total time after the

Materials and methods Plants and insects. Cucumber, Cucumis sativus cv. Lange Groene Giganta and tomato, Lycopersicon esculentum cv. Moneymaker were grown in a glasshouse at 1822 C and L16:D8 photoperiod. Seedlings with 35 true leaves were used in the experiments. Two whitey strains were used, one reared on tomato (cv.

75 1st sustained phloem phase to reect the continuity of the whiteys phloem feeding (Parameter 10, Tables 1 and 2). The values of the general parameters (14) were calculated using all replicates, but the phloem phase related parameters (510) were based on the individuals that showed any phloem phase. Finally, the percentage of whiteies showing phloem phases (Parameter 11, Table 2) was calculated. Statistics. Statistical tests were carried out using the software package STATGRAPHICS 7.0 (Manugistics Inc. and Statistical Graphics Corp.). A two-way analysis of variance (ANOVA), followed by the Tukey Kramer multiple comparison of means, was adopted to test the whitey strain effect, the plant effect, and their interactions. Before running the ANOVA, square root, logarithmic and arcsine transformations were applied to the data concerning the number, duration, and percentage of the probing activities, respectively. To test the efciency of these transformations, the ScheffBox and Kolmogorov-Smirnov methods were used to examine the variance homogeneity and the data normality, which are important assumptions for ANOVA. Among the 10 parameters, Scheff-Box method revealed 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 signicance level and thus concluded that the variates of this parameter have heterogeneous variances. The P values of both Parameters 4 and 10 in Table 2 calculated from the Kolmogorov-Smirnov method were 3.77E-6 and 0.025, respectively, and thus concluded that the variates of these parameters do not t to a normal distribution. Therefore, in the further analysis, non-parametric KruskalWallis and MannWhitney U tests were applied to these data. than the whitey strains and the interactions between the two. Host-plant effects. On cucumber, the whiteies had signicantly fewer but longer probes and a lower number of phloem phases (Parameters 13, Table 2), but a longer time was needed to reach the rst phloem phase, both from the start of an experiment as well as from the beginning of the probe concerned (Parameters 56, Table 2). Also, the time needed to achieve a sustained phloem feeding was longer on cucumber than on tomato (Parameters 78, Table 2). The mean duration of total phloem phases (Parameter 4, Table 2) was not signicantly different between cucumber and tomato for both whitey strains. Moreover, a significantly lower percentage of non-probing time before the rst phloem phase (Parameter 9, Table 2) was found on cucumber than on tomato. Also, the percentage of time spent in the phloem after the rst sustained phloem phase in the experiment (Parameter 10, Table 2) was higher on cucumber than on tomato for the C-strain whiteies, but not signicantly so (Kruskal Wallis, P<0.001; MannWhitney U, P=0.362). In contrast, the percentage of whiteies that showed any phloem phase within one EPG recording period (12 h) (Parameter 11, Table 2) was lower on cucumber than on tomato. Whitey strain effects. Signicant whitey strain effects were detected in the number of probes (P=0.005) and the mean duration of total probes (P=0.008) in the ANOVA (Parameters 12, Table 1). When tested either on tomato or on cucumber, the T-strain whiteies probed fewer times but for longer periods than the C-strain whiteies did (Table 2). The T-strain whiteies showed a signicantly longer duration of total phloem phases than the C-strain whiteies on tomato (KruskalWallis, P=0.061; Mann-Whitney U, P=0.047) but not on cucumber (Parameter 4, Table 2). Similarly, the T-strain whiteies showed a signicantly higher percentage of phloem feeding time after the rst sustained phloem phase than the Cstrain whiteies on tomato (KruskalWallis, P<0.001; MannWhitney U, P=0.001) but not on cucumber (Parameter 10, Table 2). Interactions between plant and whitey strain effects. Among the EPG parameters shown in Table 1, only the time to the 1st phloem phase in a probe (Parameter 6) showed a signicant interaction between plant and whitey strain effects in the ANOVA. On tomato,

Results Two-way ANOVA. ANOVA analysis was conducted for Parameters 13 and 59, and the results generated from this analysis are presented in Table 1. Both whitey strain and plant effects were signicant for the number and duration of total probes (Parameters 1 and 2). All other parameters showed only signicant plant effects. Note that for the time to the rst phloem phase in a probe (Parameter 6), in addition to a strong plant effect, a signicant interaction between whitey strain and plant effects was also detected (P=0.042). In general, the host plants had a much stronger inuence on the probing and feeding activities of whiteies

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Table 1. Results of two-way ANOVA for EPG parameters concerning whitey 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, signicance level; E, phloem phase; sustained E, phloem phase longer than 15 min; dash line, data violating ANOVA assumptions not shown Whitey strain d.f. SS P d.f. SS P d.f. SS P d.f. SS P d.f. SS P d.f. SS P d.f. SS P d.f. SS P d.f. SS P d.f. SS P 1 32.691 0.005 1 0.047 0.008 1 0.074 0.8 1 0.098 0.392 1 0.056 0.382 1 0.048 0.558 1 0.003 0.825 1 0.0431 0.305 Plant 1 85.002 <0.001 1 0.065 0.002 1 67.211 <0.001 1 2.201 <0.001 1 1.941 <0.001 1 0.874 0.012 1 2.122 <0.001 1 0.601 <0.001 Strain plant 1 2.331 0.452 1 0.001 0.852 1 0.022 0.891 1 0.091 0.408 1 0.301 0.042 1 0.076 0.459 1 0.112 0.151 1 0.018 0.507 Residual 78 305.982 78 0.492 61 68.442 76 9.621 65 4.481 75 9.933 60

1. Number of probes

2. Duration of total probes

3. Number of phloem phases (E)

4. Duration of total phloem phases (E)

5. Time to the 1st E in experiment

6. Time to the 1st E in probe

7. Time to the 1st sustained E in experiment

8. Time to the 1st sustained E in probe

9. Percentage of non-probe before the 1st E

76 3.051

10. Percentage of phloem period after the 1st sustained E

the T-strain whiteies spent more time in the pathway probing which led to phloem feeding than the C-strain whiteies did. Similarly, the C-strain whiteies showed a longer pathway phase before reaching the phloem phase when tested on cucumber than the T-strain whiteies (Figure 1). Although no signicant differences were found, some other parameters showed a similar trend on average, such as the time to the 1st sustained phloem phase in an experiment and in a probe (Parameters 78, Table 2) and the proportional phloem feeding time after the 1st sustained phloem phase (Parameter 10, Table 2).

Discussion and conclusions Effects of host-plant tissue factors on acceptance ranks. The process of host-plant selection by whiteies consists of a series of consecutive events starting with the rst labial contact with the plant surface, followed by the stylet penetration through successive tissue layers between the epidermis and the phloem sieve elements and, ultimately, by phloem sap feeding. Continuous phloem sap feeding can be regarded as acceptance of a host plant. However, before feeding on the phloem sap, many factors can play different roles in the initiation, maintenance, and cessation of each subsequent 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 two whitey strains (T-strain and C-strain). Different letters in the same row indicate signicance derived from TukeyKramer method. E, phloem phase; sustained E, phloem phase longer than 15 min. The signicance test for Parameter 4 and 10 was carried out using Kruskal-Wallis and MannWhitney U methods T-whitey strain Cucumber N = 20 1. Number of probes 2. Duration of total probes (min) 3. Number of phloem phases (E) 4. Duration of total phloem phases (E) (min) 5. Time to the 1st E in experiment (min) 6. Time to the 1st E in probe (min) 7. Time to the 1st sustained E in experiment (min) 8. Time to the 1st sustained E in probe (min) 9. Percentage of non-probe before the 1st E 10. Percentage of phloem period after the 1st sustained E 11. Percentage of whiteies showing sustained phloem phase 29.2 3.0 603.0 18.3 1.3 0.2 226.8 52.3 364.9 55.0 34.9 5.2 389.2 55.1 35.3 6.0 24.0 3.2 46.5 9.5 70 a c a ab ab b a b a ab C-Whitey strain Cucumber Tomato N = 23 N = 20 b b b a a a ab a bc a 43.0 6.1 539.0 19.5 1.4 0.3 184.6 39.1 443.8 49.4 41.9 6.0 454.2 50.8 43.5 6.2 31.0 3.7 49.7 9.1 65 ab bc a ab b b a b ab ab 79.3 9.6 478.7 20.2 9.9 1.5 162.8 22.8 185.3 27.5 16.1 3.0 248.4 33.6 15.4 1.9 43.9 4.1 32.8 3.8 95 c a b b a a b a c b

Tomato N = 19 50.0 4.5 528.6 20.6 9.7 1.8 258.3 29.4 168.4 27.0 23.2 4.1 292.4 52.8 18.0 2.6 35.3 4.4 58.5 3.4 95

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

the total acceptance rank. A critical selection of parameters to evaluate the acceptance ranks is therefore important. In our selection of parameters (numbered 111 in Tables 1 and 2), we used two key events, (1) the rst phloem phase and (2) the rst phloem phase that is sustained for more than 15 min. On suitable host plants, the rst phloem phase is usually sustained already. These two key events divide the probing process into two or three natural parts, de-

pending on whether the rst phloem phase is longer than 15 min. Before the rst key event, i.e., the rst phloem phase, pathway activities are predominant, as reected by the Parameters 59 in Table 2. These parameters have been thought to reect the host-plant recognition as well as the phloem nding process in which factors from epidermis, mesophyll, and nontransport tissue in the vascular bundle are involved. After the rst key event, specic phloem properties play a predominant role which may lead to acceptance of the sap as a food source. In a few observations where concurrent EPG and honeydew recordings were conducted, we found that whitey did not excrete any honeydew droplets when the phloem phase was in periods shorter than 15 min. Thus, we took a period longer than 15 min as a criterion for the sustained ingestion, in other words phloem acceptance, which can also be regarded as the rst sign of host-plant acceptance. A host plant is considered to be of higher acceptance rank when the phloem feeding is more continuous (Parameter 10, Tables 1 and 2). Chemical and physical properties of plant tissue can greatly affect each element of the probing process. As some of the apical sensilla on a whiteys labium, in contrast to aphids, are chemosensilla (Walker & Gordth, 1989), the non-probing duration may be inuenced by the surface semiochemicals (van Lenteren & Noldus, 1990). For the duration of the stylet path-

78 way phase, factors in the supercial tissue layers seem very important. Different pathway probing time may be caused by stimulating or deterring effects of some chemicals in the tissue. This result could relate to the presence of a large number of pre-cibarial and cibarial chemosensilla in whiteies (Wensler & Filshie, 1969; Hunter et al., 1996). Whiteies may use these chemoreceptors to taste intercellular plant uids, as these homopterans, in contrast to aphids, most likely do not sample cells intracellularly (Tjallingii, 1988; Janssen et al., 1989; Lei et al., 1996a). When the pathway phase exerts an analogous inuence on the whiteys probing, the phloem phase, especially the sustained phloem ingestion, becomes important for ranking a host-plant acceptance level. Usually, the higher the acceptance ranks the longer the phloem ingestion and vice versa. The results of this study demonstrate that cucumber is more readily accepted as a host plant than tomato, based on a number of EPG parameters. These parameters include: fewer probing times (Parameter 1, Table 2), longer total probing duration (Parameter 2, Table 2), shorter non-probing time before the rst phloem phase (Parameter 9, Table 2), fewer number of phloem phases (Parameter 3, Table 2) but almost equal total duration on two host plants, and more persistent phloem feeding after the 1st phloem phase in the C-strain whiteies (Parameter 10, Table 2). These differences were also observed in host-plant ranking for aphids (Webster et al., 1993; Cole, 1994; Caillaud et al., 1995). However, the time to the rst or the rst sustained phloem phase in an experiment or in a probe (Parameters 58, Table 2), complicates this point, due to the paradox that whiteies actually spent longer time in the pathway probing and thus caused a postponement of subsequent phloem phases on cucumber. This postponement may decrease the number of whiteies that reached the phloem phase in the experimental time (Parameter 11, Table 2), together with other possible factors such as the impediment of whiteys free movement caused by wiring. This impediment may be more serious on cucumber leaves than tomato leaves due to different morphological leaf features. No further experiment was carried out to clarify what factors were involved. Usually, such a negative effect can be overcome by using the same plant species or varieties as control. The percentage of whiteies that reached the phloem phase (Parameter 11, Table 2) can be enhanced by prolonging the duration of the experiment (Lei et al., 1997). The fact of a longer total pathway in high-ranking cucumber is contrary to the results of some aphid studies where more acceptable host-plants were shown to cause shorter pathway probing (Givovich & Niemeyer, 1995, and references therein). This might be related to a whiteys characteristic pathway probing (e.g., very few potential drops; clearly distinguishable subpatterns of C waveform). We can speculate that some stimulants present in cucumber tissue have been detected during the occurrence of the C waveform of a whitey and result in a prolonged intercellular exploration which may give the whitey a better chance to contact a sieve element. Apparently, more comparative studies are greatly needed to conrm this point. Alternatively, one may consider that the overall acceptance rank of a host plant, as indicated by the insects performance, does not necessarily reect the acceptance at all tissue levels in the plant. Consequently, this overall acceptance may be inconsistent with some phases of the probing process. The question arises whether physical factors could have caused this prolonged pathway phase. Anatomical differences between the two host plants, especially the distance to the phloem, could account for this. Therefore, we measured the distance to the phloem in the tertiary veins (the preferred probing sites) and it is indeed larger in cucumber than in tomato (Table 3). However, the proportional increase in distance is much lower than that in the pathway probing time prior to the rst phloem phase in a probe (Table 3). Therefore, the differences in distance cannot explain this phenomenon completely. An involvement of chemical factors can certainly not be excluded. Whitey strain effects and their interactive role in host-plant acceptance. Differences in performance between strains of whitey have been shown by other authors. Van Lenteren et al. (1989) reported that a Hungarian strain of the greenhouse whitey performed much better on sweet pepper, which is generally a poor host plant for whiteies, than a Dutch whitey strain. In our study, two parameters (Parameters 12; Table 1) showed signicant whitey strain effects. The T-strain whiteies exhibited fewer probes and longer total probing time than the C-strain ones on cucumber as well as on tomato. Within the total probing time, only the gures of the total phloem phases (Parameter 4, Table 2) showed the same tendency, thus forming the principal contribution. In fact, on tomato plants, the T-strain whiteies had a signicantly longer phloem phase than the C-strain whiteies, but no signicance was observed on cu-

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Table 3. Proportional increment (%) in cucumber (Cucumis sativus) phloem distance from lower epidermis, in comparison with the increased whitey pathway time before the 1st phloem phase and 1st sustained phloem phase in the probe concerned (Parameters 6 and 8 in Table 2) Tomato Phloem distance (m) Time to 1st E in probe (min) T-strain C-strain Time to 1st sustained e in probe T-strain C-strain 97 23 16 18 15 Cucumber 108 35 42 35 44 % increment in cucumber 11 52 163 94 193

cumber plants. Other parameters, such as those related to the two key events (Parameters 510, Table 2) showed no clear strain differences. In the course of their rearing history, a certain selection pressure has been effective on the insects. On the other hand, a long-time association with a host-plant species may result in behavioural modications, known as hostplant induction (Bernays & Weiss, 1996). The adults tested in our experiments were reared on their strain host plants and had no previous experience on any other plants. So, the resulting effect could be partly genetic and partly phenotypic. Our experiments do not allow the separation of these two components. Host-plant induced changes on the whiteys performance have been previously reported. Enkegaard (1993) examined the performance of two cotton whitey (Bemisia tabaci (Gennadius)) strains (poinsettia strain and tobacco strain) on poinsettia plants and discovered that the poinsettia-strain whiteies had longer longevity and higher fecundity than the tobacco-strain whiteies. In our experiments, the only parameter that showed signicant interactive effects in the ANOVA was the time to the rst phloem phase in a probe (Parameter 6, Table 1). This time was longer on cucumber than on tomato, as shown in plant effects, but this effect was not independent. Instead, the whitey strains interacted so that the ranking of the strains on tomato, according to the values of this parameter, was the reverse of that on cucumber (Figure 1). Actually, some other parameters (Parameters 7, 8 and 10, Table 2) showed the same non-signicant tendency. This interactive effect indicates that a previous experience can cause the insects to spend a longer time on pathway probing. This might be a favourable strategy for whiteies to nd the phloem vessel by exploring

the tissue more extensively. Besides the prolonged pathway probing, previous experience also resulted in more persistent phloem feeding after the 1st phloem phase (Parameter 10, Table 2). In conclusion, the probing and feeding prole of whiteies is mainly determined by plant factors at all tissue levels. Long-time rearing of whiteies on a single host-plant species can form a certain strain with its own probing characteristics. The host-plant origin of whiteies should be taken into account when performing EPG tests on different host plants.

Acknowledgements This study was part of the co-operative research program between Wageningen Agricultural University (WAU), the Netherlands and Beijing Normal University, P.R. China. The senior author was nancially supported by the Dutch Royal Academy of Sciences (KNAW), the Dutch Ministry of Agriculture & Fisheries and WAU.

References
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