Entomologia Experimentalis et Applicata 89: 1523, 1998. 1998 Kluwer Academic Publishers. Printed in the Netherlands.

15

The effects of physiological factors and host plant experience on the ovipositional activity of the sweet potato whitey, Bemisia tabaci
Klaas H. Veenstra & David N. Byrne
Department of Entomology, University of Arizona, Tucson, AZ 85721, USA
Accepted: August 5, 1998

Key words: Bemisia tabaci, oviposition, vitellogenin, egg load, host plant experience

Abstract Both egg load and levels of vitellogenin and vitellin increased when Bemisia tabaci Gennadius (Homoptera: Aleyrodidae), were deprived of host plants. These increases resulted in signicant increases in rates of oviposition. There was no difference in total fecundity between whiteies temporarily deprived of hosts and a control treatment that had continuous access to hosts. The results of previous exposure to a preferred host, melon (Cucumis melo), and a non-preferred host, cotton (Gossypium hirsutum), were also examined. B. tabaci deposited signicantly more eggs during a 6-h period on melon than on cotton, regardless of host species they were previously conned to. In addition, whiteies previously exposed to cotton, deposited more eggs than females previously exposed to melon. This higher rate of oviposition resulted in a low egg load as well as lower levels of vitellogenin and vitellin. Conversely, a low rate of oviposition led to high egg load and high levels of vitellogenin and vitellin. Individuals from the same treatment exhibited variation in egg load, which was negatively and signicantly correlated with previous oviposition activity. We conclude that the effects of previous host plant exposure on oviposition were, in part, due to behavioral differences that are not related to the reproductive physiology.

Introduction Studies on oviposition by phytophagous insects tend to emphasize the effects of the chemical and physical characteristics of host plants (see Bernays & Chapman, 1994, for a review). However, the insects physiological state can have important effects upon oviposition behavior as well (Miller & Strickler, 1984; Minkenberg et al., 1992). We previously demonstrated that, when females of Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) are deprived of hosts for feeding and oviposition, the egg load increases considerably (Veenstra & Byrne, 1998). These increases require large quantities of vitellogenins. Vitellogenins are the precursors of vitellins, the major storage proteins of insect eggs (Hagedorn & Kunkel, 1979). Because the increases in egg load coincided with increases in the combined vitellogenin and vitellin content, the synthesis of vitellogenins does not seem to be affected either by oviposition or by food deprivation. These ndings led

us to examine changes in the physiological state that accompany oviposition activity. Phytophagous insects are often more likely to accept non-preferred hosts as oviposition sites if they have not previously been exposed to preferred hosts (Courtney & Kibota, 1990). In addition, the propensity to oviposit on a preferred host may also be increased if individuals have never before encountered preferred hosts. Host use by B. tabaci has a strong seasonal component in the Southwestern United States (Sivasupramaniam et al., 1997). B. tabaci can be found on melon, Cucumis melo L., in the spring, on cotton, Gossypium hirsutum L., in the summer, and again on melon in the fall. Since B. tabaci prefers melon over cotton, in choice experiments (Chu et al., 1995), it is moving in the above sequence from preferred hosts to non-preferred hosts and later back to preferred hosts. Here we report the results from experiments that examined the effects of changes in the physiological state upon oviposition activity by B. tabaci. Ovipo-

16 sition was related, in all experiments, to changes in the physiological state. These changes were documented by comparing egg load and the vitellin and vitellogenin content of whiteies before and after they were conned to oviposition sites. The effects of increases in egg load and vitellogenin and vitellin content on subsequent oviposition were examined in the rst experiment. In a second experiment the effects of previous exposure to either cotton or melon on oviposition on these hosts were examined. Causes of variation in the physiological state, among individuals, within treatments, were also examined. A high egg load or vitellogenin and vitellin content can be indicative of a high reproductive activity. If so, there should be a positive phenotypic correlation between egg load and ovipositional activity, and between the vitellogenin and vitellin content and ovipositional activity. Conversely, eggs, as well as vitellogenins and vitellins, could accumulate in individuals that exhibit a lower than average propensity to oviposit. This would create a negative phenotypic correlation between egg load and oviposition, and between the combined vitellogenin and vitellin content and oviposition. top and bottom. Petri dishes, with whiteies, were placed on top of a 2% agar gel. The agar served to maintain high humidity, and thus minimize desiccation during the experiment. To control for the effects of handeling whiteies were placed on melons in a separate cage. Ten females were also collected and frozen immediately (= treatment group: 0 h of host deprivation). One of the Petri dishes containing whiteies was cooled over ice 6 h later. Ten females were then selected and transferred to individual clip cages on melon leaves (= treatment: previously off plants), while another ten females were frozen for reference (= treatment group: 6 h of host deprivation). At the same time, ten females were collected from the control group and transferred to clip cages (= control always on plants). The clip cages from the treatment group were paired with clip cages from the control group on individual melon leaves. An additional ten females were collected from the control group and frozen (= treatment group: control after 6 h). Twelve hours after the beginning of the experiment, the oviposition experiments were terminated by storing the leaves, with clip cages and whiteies , at 80 C. At this time another ten females were collected from the control treatment group and frozen (= treatment group: control after 12 h). Finally, another ten females were collected out of the other Petri dish that was kept on agar and frozen (= treatment group: 12 h of host deprivation). Five females from each treatment group were assayed for vitellogenin and vitellin content, while the other ve were used for egg load determinations (see below). This experiment was repeated on three consecutive days. However, on the rst day no females were collected from the control group after 12 h. Effects of previous exposure. Cotton and melon plants were infested with B. tabaci eggs by exposing individual plants for several hours to high densities of adults from the colony (> 20 per leaf). The emerging adults were collected daily, and transferred to the same host species as they were reared upon. In this manner, we had whiteies reared on cotton, and whiteies reared on melon. Ten females from each group were transferred to clip cages on cotton leaves, and ten from each group were transferred to clip cages on melon leaves. To each cotton and melon leaf was attached one clip cage with a female previously exposed to cotton and one clip cage with a female previously exposed to melon. Another ten fe-

Material and methods General. All experiments were conducted in a growth chamber at 30 C, and at a photoperiod of L14:D10. Melons, cv Top Mark, or cotton, cv Delta Pine 90 were used as hosts. All hosts were reared in greenhouses before being transferred to growth chambers. Whiteies (Bemisia tabaci, B-biotype = B. argentifolli [Perring and Bellows]) came from a colony maintained in a greenhouse on melons. Females used for the experiments were 2 to 3 days old at the beginning of each experiment. The insects were reared and kept as adults in the same growth chamber used for experiments. All melon and cotton plants had at least two fully expanded true leaves, but no plants had owers or ower buds. Clip cages were always attached to the rst or second expanded leaf. Whiteies were handled as described in Veenstra & Byrne (1998). All experiments were terminated by freezing whiteies (in their clip cages) at 80 C. Afterwards, each female was weighted on a Cahn C-31r microbalance. Effects of the physiological state. At the beginning of the experiment, whiteies were transferred to two small plastic Petri dishes with mesh screen on the

17 males, from each group, were transferred to clip cages attached to Petri dishes with a 2% agar gel. An additional ten females from each group were collected and frozen immediately. This sample was used to determine the physiological state of females at the beginning of the experiment as described below. The clip cages attached to Petri dishes with agar were frozen 6 h after females had been transferred. Five females from each of the treatment groups were assayed for vitellogenin and vitellin content, while the other ve were used for egg load determinations (see below). This experiment was repeated on four consecutive days. Physiological assays. The amount of vitellogenin and vitellin per individual were measured with a quantitative ELISA assay as described elsewhere (Blackmer et al., 1995; Veenstra & Byrne, 1998). The monoclonal antibody employed does not distinguish between vitellogenin and vitellin (Tu et al., 1997). Twenty individuals were assayed on each ELISA plate. Treatments were randomized on each ELISA plate. Egg load was determined by counting the number of visible eggs per female under a transmission light microscope. Individual females were kept for 10 min in a xylene solution prior to mounting on a microscope slide. Statistical analysis. All statistical models were tested using PROC GLM of SAS (SAS Institute, 1988). Effects due to differences between days or ELISA plates were treated as block variables. Treatment means were calculated using a LSMEANS statement. Phenotypic correlations were calculated by estimating the slope of the covariable symbolized by number of eggs deposited in previous 6 h in the appropriate statistical models. Because the directions of differences in the rst experiment can be predicted from previous experiments (e.g., increases in egg load when off host, which should decrease after transfer back to hosts) we used one-tailed t-test. To minimize the Type II error (Sokal & Rohlf, 1981), i.e., maximizing the detection of existing treatment differences, we did not apply corrections for multiple comparisons in the rst experiment. This approach is most appropriate because our hypothesis predicts that specic treatment means should be similar. It also allowed us to test pre-planned comparisons directly from the gures. Corrections for multiple comparisons were also not employed in those parts of the second experiment that examined physiological changes. Predictions on changes in the physiological state could be made from the results on oviposition. For example, we would expect that a high oviposition activity results in low egg load, and low oviposition activity should result in high egg load. Two-tailed t-test were used in the second experiment. In order to test the hypothesis that the increase in oviposition activity in 6 h due to the treatment (= host deprivation for 6 h) equals the oviposition activity by the control in 6 h, the following procedure was used. The analysis of covariance was rst analyzed as a regression model with binary independent variables (Neter et al., 1989). The mean of each independent variable was then subtracted from its value, except for the treatment variable. As a result, the intercept of the model becomes the treatment mean for the control, while the regression coefcient for the treatment variable becomes the difference due to treatment. The ESTIMATE procedure from PROC GLM was then used to test the difference between the regression coefcients.

Results Effects of the physiological state. Females that had previously been deprived of hosts for 6 h deposited signicantly more eggs during the next 6 h, compared to a control subjected to the same amount of handling (7.08 0.44 and 3.98 0.44 respectively; F = 24.72; df = 1, 55; P = 0.0001). If there were negative effects of host deprivation on total fecundity over a 12 h period, the increase in deposited eggs, due to previous host deprivation should be signicantly lower than the number of eggs deposited by the control treatment. However, this increase (3.10 0.62) was not significantly lower than the number of eggs deposited by the control group (t = 0.90; df = 55; P = 0.19). As expected, host deprivation did result in signicant increases of both egg load and the levels of vitellogenin and vitellin (Figure 1A). But the transfer of females, previously deprived of hosts, back to hosts resulted in signicant decreases in both egg load and vitellogenin and vitellin levels (Figures 1A and 1B). The physiological state in females 6 h after access to hosts, preceded by 6 h of host deprivation, was not signicantly different from any of the control treatments (Figures 1B and 1C). This indicates

18

Figure 1. The mean combined vitellogenin and vitellin content (top, SEM) and egg load (bottom, SEM) when females were taken off plants for 0, 6 or 12 h (A), or were transferred back to plants after being off plants for 6 h (B), and for the controls for handeling (C). Means with no letter in common are signicantly different (P = 0.05; one-tailed t-test). No correction for multiple comparisons was applied, in order to minimize type II errors (comparisons are across A, B, & C panels).

that previous increases, due to host deprivation, were completely reversed. Although the overall differences between treatment categories in both the vitellogenin and vitellin content and in egg load were highly significant (F = 4.29; df = 6, 84; P = 0.008 and F = 32.48; df = 6, 91; P = 0.0001, respectively), no changes over time in either egg load or the combined vitellin and vitellogenin content were observed in the control group (Figure 1C). Effects of previous exposure. Oviposition activity was signicantly effected by both previous host exposure and by the host species to which the whiteies had been conned (Table 1). Although oviposition activity was signicantly correlated with the weight of females, the inclusion of weight as a covariate did not affect the signicance level in any of the treat-

ments. There was no signicant interaction between previous exposure and host species to which whiteies were conned to. This indicates that oviposition activity was always higher on melon leaves than on cotton leaves, and that females previously exposed to cotton always deposited more eggs than females previously exposed to melon (Figure 2). At the beginning of the experiment, females previously exposed to cotton had a signicantly higher egg load, relative to weight, than females previously conned to melon (Figure 3). The interaction between previous exposure and host species transferred to was signicant (Table 2a). This indicates that the differences in egg load between females previously exposed to cotton and females previously exposed to melon, changed signicantly after 6 h of connement to either cotton or melon. The patterns in the combined

19
Table 1. Results of ANOVA on number of eggs deposited in 6 h on cotton or melon as a function of previous exposure to cotton or melon Effect F df P Table 2. Results of ANCOVA on combined vitellogenin and vitellin content and egg load before and after being on cotton or melon for 6 h, as a function of previous exposure to cotton or melon Effect F df P

(a) Weight included as covariate (r 2 -model = 0.41) Days (=block) Previous exposure Host type transferred to Previous exposure transfer Weight1 4.32 39.09 48.03 0.00 9.46 3, 152 1, 152 1, 152 1, 152 1, 152 0.0059 0.0001 0.0001 0.98 0.0025

(a) Combined vitellogenin and vitellin content (r 2 -model = 0.58) Days (=block I) 0.07 ELISA plate (=block II) 7.73 Previous exposure 1.63 Host type transferred to 1 9.32 Previous exposure transfer 2.92 Weight 2 40.45 (b) Egg load (r 2 -model = 0.52) Days (=block) 2.01 3, 110 Previous exposure 2.37 1, 110 Host type transferred to 1 12.72 2, 110 Previous exposure transfer 20.84 2, 110 Weight3 38.29 1, 110 0.12 0.13 0.0001 0.0001 0.0001 3, 102 7, 102 1, 102 2, 102 2, 102 1, 102 0.98 0.0001 0.20 0.0002 0.058 0.001

(b) Weight excluded (r 2 - model = 0.37) Days (=block) Previous exposure Host type transferred to Previous exposure transfer 3.78 28.78 51.64 0.01 3, 153 1, 153 1, 153 1, 153 0.012 0.0001 0.0001 0.92

1 Slope of regression = 0.11 0.04 eggs / gram.

1 Treatment categories: before transfer, 6 h after transfer to cotton,

and 6 h after transfer to melon.

2 Slope: 1.4 0.2 egg equivalents / gram. 3 Slope: 0.26 0.04 eggs / gram

Figure 2. Mean number of eggs deposited in 6 h on either cotton or melon leaves ( SEM) when females had been previously conned to either cotton or melon. Means with no letter in common are signicantly different (P = 0.05). Correction for multiple comparisons (Bonferroni approach [SAS institute, 1988]) had no effect on the distribution of letters on means. Adjustments for weight differences resulted in slightly larger differences with respect to previous exposure on both host species.

ned to melon (Figure 3, Table 3). These increases were less than increases due to host deprivation in similar females (Table 2). When females were conned to melon, after they had previously been exposed to cotton, the vitellogenin and vitellin content and the egg load (both relative to weight), decreased signicantly (Figure 3). The net decreases showed a similar pattern, but were not statistically signicant (Table 2). When females previously conned to melon were conned again to melon, the egg load increased signicantly, both in absolute amount (Table 2), and after corrections for weight differences (Figure 3). The increases in egg load were considerably less than increases due to host deprivation in similar females (Table 3). No signicant changes could be detected for the vitellogenin and vitellin levels in these females (Figure 3, Table 3). Phenotypic correlations. In both experiments there was a signicant negative correlation between egg load and previous oviposition activity (Table 4.). Analysis of vitellogenin and vitellin content indicate that there is either no relationship (i.e., slope 0), or a negative correlation between previous oviposition activity and the vitellogenin and vitellin content (Table 4).

vitellogenin and vitellin content were similar to those for egg load (Figure 3), although no signicant effects were observed for the interaction (Table 2b). No signicant changes in the physiological state were detected after 6 h of connement to cotton in females, that were previously conned to cotton (Figure 3, Table 3). However the vitellogenin and vitellin levels, as well as the egg load, increased signicantly after connement to cotton in females previously con-

20

Figure 3. The effects of previous exposure on the mean combined vitellogenin and vitellin content (top, SEM) and egg load (bottom, SEM) after 6 h of exposure to either cotton or melon. Means are adjusted for weight differences between treatments. Means with no letter in common are signicantly different (P = 0.05). No correction for multiple comparisons was applied, in order to minimize type II errors.

Discussion Egg load and vitellin and vitellogenin content, as well as previous exposure to particular hosts, seem to affect oviposition in B. tabaci. Our results also indicate that egg load and the vitellogenin and vitellin content can change rapidly over a 6 h period. These short term changes in the physiological state seem to be related primarily to oviposition. In a previous paper (Veenstra & Byrne, 1998), we concluded that the production of mature eggs or the synthesis of vitellogenins in B. tabaci did not seem to depend upon either feeding or oviposition. The results from our rst experiments conrm these conclusions. The increases in egg load and in vitellogenin and vitellin content, due to host deprivation, did seem to correspond to an increased ability to oviposit. We found no evidence that 6 h of host deprivation had any negative effects on total fecundity. Increases and decreases in egg load or in the combined vitellogenin and vitellin content, therefore, likely reect differences in numbers of eggs that can be oviposited by females.

The results also indicate that females have a higher propensity to oviposit if they were previously exposed to a non-preferred host (i.e., cotton). This is contrary to expectations assuming that fecundity is the only factor determining oviposition. Oviposition was positively correlated with weight, but females previously exposed to melon were 14% heavier than females previously exposed to cotton (Table 3). In addition, host deprivation leads to a higher increase in egg load and in vitellogenin and vitellin content in females previously exposed to melon (Table 1). Both ndings indicates that females, previously exposed to melon, have the highest fecundity and this may help explain the preference for melon over cotton. Females previously exposed to cotton had, at the beginning of the experiment, a signicantly higher egg load, relative to weight, than females previously exposed to melons. As demonstrated in the rst experiment, a higher egg load may correspond with an ability to oviposit more eggs. Thus, this could help explain the fact that females previously exposed to cotton deposited consistently more eggs. However, if this was

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Table 3. Net increases in the vitellogenin and vitellin content, egg load, and weight 6 h after transfer to cotton or melon, as a function of previous exposure to cotton or melon Previousl exposure Transfer host Increase ( SEM) P (H0 : increase = 0)

(a) Combined vitellogenin content (egg equivalents per female)1 Cotton Melon Cotton Melon Cotton Melon cotton cotton melon melon off plants off plants 0.5 3.9 9.8 3.9 6.0 3.9 0.3 3.9 1.9 3.9 12.4 3.9 0.89 0.019 0.12 0.94 0.63 0.0017

(b) Egg load (eggs per female)2 Cotton Melon Cotton Melon Cotton Melon cotton cotton melon melon off plants off plants 0.35 0.79 4.70 0.79 1.35 0.79 2.30 0.79 4.35 0.83 5.66 0.80 0.66 0.0001 0.091 0.0043 0.0001 0.0001

(c) Weight ( gram per female) 3 Cotton cotton Melon cotton Cotton Melon Cotton Melon (P = 0.34). melon melon off plants off plants

0.6 1.1 2.1 1.1 1.5 1.1 0.4 1.1 5.0 1.1 4.6 1.1

0.57 0.062 0.17 0.75 0.0001 0.0001

1 Means before transfer: 27.8 0.8 and 31.3 2.7 from cotton and melon respectively 2 Means before transfer: 5.2 0.6 and 4.0 0.6 from cotton and melon respectively (P 3 Means before transfer: 44.1 0.8 and 50.3 0.8 from cotton and melon respectively

= 0.14).

(P<0.001).

the only factor responsible for the observed effects of previous exposure, the effects of previous exposure on a particular host should either disappear or decrease over time. Instead, the differences in egg load are reversed after 6 h of connement on either cotton or melon. This clearly indicates that previous differences in the physiological state are not sufcient to explain the effects of previous exposure on oviposition. We, therefore, conclude that effects of previous exposure on oviposition activity are, in part, due to behavioral factors not related to the reproductive physiology. Because these effects do not seem to be secondary effects of the reproductive physiology, the propensity to oviposit may well relate to the probability of colonizing agricultural elds after a dispersal

phase. If so, females that dispersed from melon elds should have a high propensity to continue the dispersal phase after they have alighted into cotton elds, while females that disperse from cotton elds and alight into melon elds are the most likely to stay. The transfer to a different host species for 6 h is similar to host deprivation in that it also does not seem to affect the production of mature eggs or the synthesis of vitellogenins. For example, females that were previously exposed to melon and were transferred to cotton, exhibited the lowest oviposition activity. Consequently, they had the highest egg load and the highest vitellogenin and vitellin content. Transfer to a higher quality host, i.e., from cotton to melon, resulted in the highest oviposition activity of the experiment,

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Table 4. Effects of oviposition activity in the previous 6 h on the combined vitellogenin and vitellin content or egg load Experiment Regression coefcient ( SE)1 t (H0: slope = 0) df P

(a) Combined vitellogenin and vitellin content On and off plants: treatment 2 On and off plants: control 2 Previous experience: combined 3 (b) Egg load On and off plants: combined4 Previous experience: combined5 0.34 0.15 0.25 0.10 2.20 2.46 24 71 0.038 0.016 1.44 0.55 0.18 0.58 0.99 0.63 2.63 0.31 1.57 19 19 63 0.016 0.76 0.12

1 Coefcients for eggs laid in the statistical models:

Combined vitellogenin and vitellin content = day effects + plate effects + weight + eggs laid (a). Egg load = day effects + weight + eggs laid (b). 2 Test for homogeneity of slopes: F = 5.79; df = 1, 19; P = 0.027. 3 Test for homogeneity of slopes: F = 0.17; df = 3, 60; P = 0.92. 4 Test for homogeneity of slopes: F = 0.06; df = 1, 23; P = 0.81. 5 Test for homogeneity of slopes: F = 0.40; df = 3, 68; P = 0.75.

but this coincided with a decrease in egg load and vitellogenin and vitellin content. Thus, there is no evidence that a high oviposition activity in the 6 h after transfer to a higher quality host is due to an increase in fecundity. If the average oviposition activity of each treatment combination is compared to the average egg load or the average vitellogenin and vitellin content at the end of the experiment, a low oviposition activity appears to result in a high egg load and a high vitellogenin and vitellin content. At the same time, a high oviposition activity seems to result in a low egg load and a low vitellogenin and vitellin content. The same conclusion can be drawn from the results of the phenotypic correlations. Variation between individuals, within treatments, in egg load and in the vitellogenin and vitellin content seem to be caused foremost by differences in oviposition activity. Because the phenotypic correlations were never positive and signicant, variation in egg load or the vitellogenin and vitellin content does not seem to be related to differences in fecundity. However, this conclusion only applies to 2- to 3-day-old females (and to correlations that adjusted for weight). Oviposition activity increases over time, in the rst days after adult emergence (Wang & Tsai, 1996), as does the vitellogenin and vitellin content (Tu et al., 1997) and the egg load (Veenstra & Byrne, unpubl.). This creates a positive correlation between oviposition activity and the physiological state. Nevertheless, the results from the phenotypic correlations are in agreement with

other results in that they conrm the hypothesis that the physiological state is related to prior oviposition activity. From the results, the following model of oviposition behavior in B. tabaci can be constructed. The model assumes that the propensity to oviposit is, on all substrates, positively correlated with egg load. In addition, the model assumes that females use the chemical and physical properties of a site to evaluate its suitability for oviposition. This evaluation can be thought of as comparing the suitability for oviposition to a standard. The standard reects the suitability for oviposition of previous sites that the female has previously encountered, and may change over time, as a result of host experience. The more the perceived suitability is below the standard, the lower the propensity to oviposit. If the perceived suitability is below the standard, the rate at which eggs are deposited will be lower than the rate at which females mature eggs, and consequently the egg load increases over time. But as the egg load increases, so does the propensity to oviposit. This will continue until the rate of oviposition equals again the rate at which eggs are matured. If, on the other hand, the site is perceived to be more suitable for oviposition than the standard, more eggs will be deposited than are matured, and consequently the egg load will decrease. However the decrease in egg load will also decrease the propensity to oviposit, until a new balance is achieved. A similar model may be constructed with the combined vitellogenin and vitellin content.

23 This system may exist in order to deal with variation in suitability for feeding and oviposition on a small scale (i.e., within plants and between adjacent plants). Whiteies seem to have a limited ability to asses suitability for oviposition before penetrating the cuticle (Walker & Perring, 1994). A site can differ in its nutritional rewards and its suitability for oviposition, since the latter depends in part upon nutritional conditions for the immatures from deposited eggs (Veenstra & Byrne, 1998). After penetration of the cuticle, a female may limit the time spent feeding, and oviposit instead, or she could engage in feeding without oviposition. In summary, the physiological state of B. tabaci seems to be very dynamic over a 6 h period, although the underlying physiological processes seem to be quite invariant. The results showed signicant effects of the physiological state upon subsequent oviposition activity and signicant effects of oviposition activity upon the physiological state. Because we examined concurrent changes in the physiological state during oviposition we were also able to demonstrate the effects of behavioral factors that were not the direct result of the reproductive physiology.
Blackmer, J. L., D. N. Byrne & Z. Tu, 1995. Behavioral, morphological and physiological traits associated with migratory Bemisia tabaci (Homoptera: Aleroididae). Journal of Insect Behavior 8: 251267. Chu, C. C., T. J. Henneberry & A. C. Cohen. 1995. Bemisia argentifolii (Homoptera: Aleyrodiae): host preference and factors affecting oviposition and feeding site preference. Environmental Entomology. 24: 354360. Courtney, S. P. & T. T. Kibota, 1990. Mother doesnt know best: selection of hosts by ovipositing insects. In: E. A. Bernays (ed.), Insect-Plant Interactions, CRC, Boca Raton FL, Volume II, pp. 161188. Hagedorn, H. H. & J. G. Kunkel, 1979. Vitellogenin and vitellin in insects. Annual Review of Entomology 24: 475505. Miller, J. R. & K. L. Strickler, 1984. Finding and accepting host plants. In: W. J. Bell & R. T. Card (eds.), Chemical Ecology of Insects. Sinauer, Massachusetts, pp. 127157. Minkenberg, O. P. J. M., M. Tatar & J. A. Rosenheim, 1992. Egg load as a major source of variability in insect foraging and oviposition behavior. Oikos 65: 134142. Neter, J. W. Wasserman & M. H. Kutner, 1989. Applied Linear Regression Models. Irwin, Homewood IL. SAS Institute, 1988. SAS users guide: statistics, 6th ed. SAS Institute, Cary NC. Sivasupramaniam, S., S. Johnson, T. F. Watson, A. A. Osman & R. Jassim, 1997. A glass-vial technique for monitoring tolerance of Bemisia argentifolii (Homoptera: Aleyrodidae) to selected insecticides. Journal of Economic Entomology 90: 6674. Sokal, R. R. & F. J. Rohlf, 1981. Biometry. Freeman, New York Tu, Z., D. N. Byrne & H. H. Hagedorn. 1997. Vitellin of the sweet potato whitey, Bemisia tabaci: biochemical characterization and titre change in the adult. Archives of Insect Biochemistry and Physiology 34: 223237. Veenstra, K. H. & D. N. Byrne, 1998. Effects of starvation and oviposition activity on the reproductive physiology of the sweet potato whitey Bemisia tabaci. Physiological Entomology, 23: 6268. Walker, G. P. & T. M. Perring, 1994. Feeding and oviposition behavior of whiteies (Homoptera: Aleyrodidae) interpreted from AC electronic feeding monitor waveforms. Annals of the Entomological Society of America 87: 363374. Wang, K. & J. H. Tsai, 1996. Temperature effect on development and reproduction of silverleaf whitey (Homoptera: Aleyrodidae). Annals of the Entomological Society of America 89: 375384.

Acknowledgements We would like to thank Sandy Jimenez for technical assistance. Special thanks go to Zhijian Tu for supplying us with the primary antibody for the ELISA. This study was supported by grant No. 94373020541 from the USDA.

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