Entomologia Experimentalis et Applicata 81: 345±352, 1996. 345

c 1996 Kluwer Academic Publishers. Printed in Belgium.

Performance of the predator pusillus on Bemisia resistant and susceptible tomato lines

Kevin M. Heinz1 & Frank G. Zalom2 1Department of Entomology, Biological Control Laboratory, Texas A&M University, College Station, TX 77843±2475, USA 2Department of Entomology, University of California, Davis, CA 95616, USA

Accepted: June 6, 1996

Key words: Bemisia argentifolii, biological control, host plant resistance, silverleaf white¯y, tritrophic interactions

Abstract

Host plant resistance and biological control are often assumed to act additively to suppress populations of agricultural pests. Using tomato trichome based resistance to the white¯y Bemisia argentifolii, we tested this additivity assumption with Delphastus pusillus, a coccinelid predator of Bemisia. Various life history traits of D. pusillus were measured on the tomato cultivar `Alta,' which possessed foliage with 3-fold greater trichome densities than the second cultivar `VF145B7879.' housed on VF145B7879 exhibited signi®cantly greater lifetime fecundities and walking speeds than beetles housed on Alta. No cultivar-speci®c differences were observed in D. pusillus longevities or handling times. Combining these observations with previously published reports of reduced B. argentifolii population growth rates on Alta compared to VF145B7879, we tested the hypothesis that increased levels of white¯y biological control could be obtained on VF145B7879 by comparison to Alta through releases of D. pusillus. Analyses of results obtained from replicated population trials detected signi®cant reductions in white¯y populations due to D. pusillus releases, but they did not detect a signi®cant in¯uence of tomato cultivar on the ability of D. pusillus to suppress white¯y populations. Signi®cantly longer residence times on Alta than on VF145B7879 may have compensated for the signi®cantly slower walking speeds and reduced lifetime fecundities observed on Alta and produced a neutral effect of foliar trichome densities on B. argentifolii biological control.

Introduction ance together with biological control requires a know- ledge of (1) the causal factor(s) of a plant's resistance, A goal of integrated pest management is to combine (2) the level of pest suppression obtained by the host optimally all available tactics to maintain pest popula- plant resistance, and (3) how the resistance factor(s) tions below levels that will cause economic loss. Two affect the ability of the natural enemies to suppress the strategies, host-plant resistance and biological control, target pest population. are often assumed to be highly compatible and capable Previous work by Heinz & Zalom (1995) identi- of acting additively when used simultaneously in time ®ed a positive correlation between densities of non- and space (Bergman & Tingey, 1979; Duffey & Bloem, glandular leaf trichomes and ovipositions by white¯y 1986). However, plant traits such as allelochemistry, (Bemisia argentifolii Bellows & Perring [Homoptera: nutrition, morphology, and phenologythat often confer Aleyrodidae]) across 20 commercial cultivars of resistance to plant pests may adversely affect bene®cial tomato. Similarly, highly pubescent cotton cultivars . Many excellent reviews discuss various aspects support larger populations of Bemisia tabaci (Genna- of plant effects on natural enemies (Price, 1986; Fritz dius) than do glabrous cultivars (Mound, 1965; But- & Simms, 1992; Gauld & Gaston, 1994). The ability ler & Henneberry, 1984; Ozgur & Sekeroglu, 1986). to quantify the compatibility between host-plant resist- This phenomenon may be a result of the strong pref- 346 erence exhibited by B. tabaci for laying its eggs at odes of mass migrations of white¯y that overwhelm the base of leaf trichomes (Berlinger, 1986), which the natural enemy complex (Heinz et al., 1994; Sim- may be an evolutionary response to selection exerted mons & Minkenberg, 1994). Plant cultivars that may by predators and parasitoids. White¯y natural enemy slow Bemisia population growth have been identi®ed search ef®ciency is greatest on glabrous leaves and (Mound, 1965; Butler & Henneberry, 1984; Berlinger, decreases with increasing trichome densities (Li et al., 1986; Ozgur & Sekeroglu, 1986; Heinz & Zalom, 1987; Hulspas-Jordan & van Lenteren, 1989). White- 1995), but cultivars truly resistant to white¯y ovipos- ¯y offspring placed at the base of leaf trichomes may ition are not yet commercially available. Failure of experience reduced levels of natural enemy-induced each of these pest management strategies to control mortality and confer an increased ®tness on females this severe agricultural pest when used alone will likely exhibiting this appropriate behavior (Heinz & Zalom, promote the use of several strategies in combination. 1995). Considering these observations, the trichome- based resistance mechanism in tomato should be com- Materials and methods patible with biological white¯y control. Testing this prediction provides the framework for the studies we Two commercial cultivars, representing opposite describe in the following text. The goals of our studies extremes in B. argentifolii oviposition rates and trich- are, ®rst, to examine the in¯uence of tomato trichome ome densities (Heinz & Zalom, 1995), were selec- resistance on several female ®tness characters of the ted as test plants to determine how tomato trichome white¯y predator Delphastus pusillus LeConte (Cole- densities in¯uence several life history characters of optera: ) that are likely to in¯uence its female D. pusillus. Average white¯y oviposition rates

ability to effectively suppress B. argentifolii infesting and tomato leaf trichome densities were 6.4 (SEM =

tomato. Second, we compare levels of white¯y sup- = 0.73, N 50 females) ovipositions per day and

N = pression obtained through the use of this trichome- 388.5 (SEM = 33.94, 115 leaves) trichomes per

dependent host plant resistance to the levels of sup- 25 mm2 of leaf tissue for the cultivar Alta, and 3.3

N =

pression obtained by inundative releases of D. pusillus. (SEM = 0.51, 50 females) ovipositions per day

N = Third, we identify potential incompatibilities between and 125.2 (SEM = 10.26, 124 leaves) trichomes these forms of host plant resistance and biological con- for the cultivar VF145B7879) (Heinz & Zalom, 1995). trol. Delphastus pusillus was selected as the test White¯ies in the genus Bemisia are serious pests because it has previously been shown to signi®cantly of row crops grown in the tropical and subtropical reduce Bemisia populations in laboratory (Hoelmer regions of the world, and they have infested green- et al., 1993), greenhouse (Heinz & Parrella, 1994a), house grown crops worldwide with varying degrees of and ®eld (Heinz et al., 1994) studies. Results from intensity. Management of Bemisia outbreaks in agri- these life history studies were followed by popula- cultural systems relies heavily on repeated applications tion studies in greenhouses to test whether variation in of insecticides. Although these insecticides provide trichome densities and D. pusillus life history charac- some suppression of white¯y populations, their tox- teristics yielded cultivar-speci®c differences in white- icity to the environment and to nontarget species ¯y population growth and white¯y population suppres- may cause increased outbreaks of white¯ies and other sion by D. pusillus. Results from the population studies pests (DeBach & Rose, 1977). Moreover, resistance prompted a ®nal laboratory study with the purpose of to insecticides in Bemisia populations has been well measuring the potential in¯uences of host plant charac- documented (Dittrich et al., 1985, 1990; Prabhaker teristics and availability of white¯y prey on residence et al., 1985, 1988; Cock, 1986). Although biological time, or the time beetles spend foraging on tomato control is often espoused as an alternative to chem- plants. All beetles used in these studies were obtained ical control, it presently has only been effective in from a laboratory culture of D. pusillus maintained managing B. argentifolii infesting selected greenhouse on poinsettia (Euphorbia pulcherrima Wild. ex Koltz) crops (Breene et al., 1992; Heinz & Parrella, 1994a; infested with all developmental stages of B. argentifo- McMahon et al., 1994). Biological control of Bemisia lii.TheD. pusillus laboratory culture was initiated in infesting ®eld crops has been largely unsuccessful 1991 from another laboratory culture maintained on a (Anonymous, 1981; Dittrich et al., 1985; Meyerdirk mix of Bemisia tabaci (Gennadius) and Trialeurodes et al., 1986; Dowell, 1990), presumably due to epis- 347 variabilis (Quaintance) (Heinz & Parrella, 1994b). resulting in consumption of the white¯y larva were omitted from analysis. Between-cultivar differences Cultivar mediated measures of D. pusillus ®tness. Four in beetle handling time were detected using a 1-way measures of female D. pusillus ®tness, presumed to be ANOVA. Prior to conducting the ANOVA, homogen- correlated with its ability to suppress Bemisia popu- eity of variances among treatment groups was veri®ed lations, were quanti®ed using three laboratory experi- with a Scheffe-Box test (Sokal & Rohlf, 1981), and ments. Our studies concentrated on female beetles due normality was con®rmed using a G-test for goodness to severe dif®culties associated with measuring male of ®t (Sokal & Rohlf, 1981). reproductive success (see Visser, 1994 and Kazmer & The speeds at which female beetles traverse the Luck, 1995 for recent discussions). In the ®rst study, blades of uninfested tomato leaves were measured by 2 day-old, mated, female beetles were placed singly placing individual beetles into a 9-cm diameter clear into 21.1 liter sleeve cages. Each cage contained a 1- plastic petri dish together with a tomato lea¯et. Once month-oldtomato plant infested with an excess of 1000 a beetle climbed onto the lea¯et, its position on the B. argentifolii eggs. Ten cages contained beetles on blade of the lea¯et was marked on the lid of the petri Alta tomato plants and ten cages contained beetles on dish at 2 s intervals. Beetle positions were recorded for

VF145B7879 plants. Plants were replaced daily with a period of 10 s after which the distance between each = B. argentifolii egg-infested plants for as long as each mark was measured and summed. All beetles (N 20 female beetle was alive. Immediately after removing per tomato cultivar) were only used in a single obser- plants from the sleeve cages, the number of eggs ovi- vation period, and the hind tibias of all beetles were posited onto the tomato foliage by each female was measured at the conclusion of an observation period.

censused with the aid of a dissecting microscope (30 Homogeneity of variances and normality were veri- power). After the death of all beetles, the right hind ®ed, and between-cultivar differences in beetle walk- tibia of each was measured with the aid of a dissect- ing speeds were detected using a 1-way ANOVA with

ing microscope (100 power) equipped with an ocular hind tibia length as a covariate. micrometer as an index of body size. The numbers

of eggs oviposited by each female were pooled across Population study. Four white¯y enclosure cages meas-  her lifespan and whether lifetime fecundities differed uring1m  1.2 m 2 m were positioned in a green- signi®cantly between cultivars were detected using a house maintained at an average temperature of 27  C. 1-way ANOVA. Similarly, whether adult longevities Three 1000-W metal halide lamps within the green- differed signi®cantly between cultivars were detected house maintained a L16:D8 photoperiod. Twelve 1- using a 1-way ANOVA. In both analyses, hind tibia month-old tomato transplants were planted into 4-liter lengths were included as covariates to correct for inad- pots within each cage; 2 cages were planted with the vertent differences in beetle size associated with each cultivar Alta and 2 cages were planted with the cul- treatment. tivar VF145B7879. White¯y populations were estab- Two other measures, handling time of prey and lished in the four cages by inoculating each cage with walking speed, were obtained by direct observation. 100 adult B. argentifolii per week for 3 wk. After this We de®ne handling time as the total time a beetle inoculation, one cage of each cultivar received weekly spends in assessing and consuming prey when an releases of D. pusillus at the rate of 1 adult beetle per

encounter with a white¯y larva results in an attack. plant. For a period of ten weeks starting with the ®rst = Individual beetles (N 20 per tomato cultivar), D. pusillus release, one leaf was sampled indiscrimin- obtained from the laboratory colony described previ- ately from the top 1/3, the middle 1/3, and the bottom ously, were placed into a 9-cm. diameter clear plastic 1/3 of 6 randomly selected plants per cage to yield a petri dish together with a tomato leaf (either Alta or total sample size of 18 leaves per cage per week. VF145B7879) infested with 4th instar B. argentifolii. Leaves were censused with the aid of a dissecting Beetles were observed continuously under a dissect- microscope (30 power) for white¯y and D. pusillus

ing microscope (30 power) for 30 min or until a activity. The census included live or dead (due to nat- beetle completed an attack, whichever occurred ®rst. ural causes or due to D. pusillus ) white¯y Whenever a white¯y larva was encountered, the times eggs, 1st±2nd instar white¯y nymphs, 3rd±early 4th spent assessing the potential prey item and feeding on instar nymphs, and late 4th instar white¯y nymphs. acceptable prey were recorded. All beetles were only Upon completing this microscopic examination, the used in a single observation period. Encounters not adaxial surface area of each leaf was determined with 348 an area meter (Li-Cor LI±3100, Lincoln, NE, USA) so white¯y densities could be standardized to the num- ber per cm2 of leaf tissue per plant. The study was replicated 3 times, and tomato cultivars were assigned randomly to cages to control for position effects with- in the greenhouse. Homogeneity of variances and nor- mality were veri®ed, and signi®cant among treatment differences in white¯y densities (numbers per square centimeter of leaf surface areas) among the 2 cultivar and 2 D. pusillus release treatments were detected with repeated measures ANOVA (StatSoft, 1994).

Host plant and prey in¯uences on predator residence time. The amount of time female beetles resided on Figure 1. The in¯uences of tomato cultivar and D. pusillus releases tomato plants was measured using a 2  2 factorial design that included the pubescent cultivar Alta and on B. argentifolii population dynamics. Means  SEM for Alta and VF145B7879 were calculated for each sample week across 3 glabrous cultivar VF145B7879 either infested with an replicates. Best-®t lines were plotted for each tomato cultivar and excess of 1000 B. argentifolii eggs or free of any white- D. pusillus release treatment with the aid of a computerized curve-

¯y. Single, 1-month-old tomato plants were placed ®tting algorithm (Jandel, 1994). The equations of theses lines were: :

0 :5 1 5 2

= : + : x r = : F = Alta ± Control: y 0 783 0 025 , 0 793,

in 21.1 liter sleeve cages for which the inner walls 0 :5

 : y = : + 95:515, P 0 001; Alta ± D. pusillus Release: 0 268

1 :5 2

x r = : F = :  :

had been coated with a thin ®lm of sticky material 0:098 , 0 766, 91 545, P 0 001; VF145B7878 :

0 :5 1 5 2

= : + : x r = : F = : (Tanglefoot Pest Barrier, Grand Rapids, MI, USA). ± Control: y 0 541 0 025 , 0 696, 64 234,

0 :5

: y = : + Groups of 10, 2-day-old female beetles were released P  0 001; VF145B7879 ± D. pusillus Release: 0 666

1 :5 2

x r = : F = : < : onto tomato plants within 40 cages, 10 cages of every 0:039 , 0 290, 11 451, P 0 005. cultivar-white¯y infestation combination. The cages were housed in an environmentally controlled room with a mean daily temperature of 27.6  C (range 25.8± speeds measured on Alta. D. pusillus longevities and

30.1  C) and a L14:D10 photoperiod. The numbers of handling times did not differ signi®cantly between the beetles trapped on the sticky walls of the cages were tomato cultivars (Table 1). censused every 2 h over a period of 8 h after the beetle Heinz & Zalom (1995) reported decreasing inoculation. The initial number of beetles released B. argentifolii population growth rates with decreas- minus the cumulative number of beetles trapped on ing leaf trichome densities. These trichome density the cage wall yields the number residing on each plant dependent differences in the pest population together during a census period. Signi®cant effects of white¯y with the increasing D. pusillus lifetime fecundities and density and tomato cultivar on beetle residence time walking speeds with decreasing leaf trichome densities were detected with a repeated measures ANOVA(Stat- generated the hypothesis that biological control should Soft, 1994). be more effective on glabrous cultivars compared to pubescent cultivars. We tested this hypothesis in the following population level study. Results Population study. We expected releases of D. pusillus Cultivar mediated measures of D. pusillus ®tness onto white¯y infested VF145B7879 to suppress white- ¯y populations to a greater extent than beetle releases Tomato cultivar and presumably trichome density onto white¯y infested Alta. Results from our test of had a signi®cant and negative in¯uence on D. pusil- this expectation are presented in Figure 1 and Table 2. lus lifetime fecundity and walking speed (Table 1). Densities of immature B. argentifolii were signi- Beetles residing on the glabrous tomato cultivar ®cantly greater on Alta compared with VF145B7879, (VF145B7879) exhibited almost 5-fold greater lifetime signi®cantly greater in the no release compared with fecundities than beetles residing on the pubescent cul- the D. pusillus release treatment, and increased sig- tivar (Alta). Beetle walking speeds were approximately ni®cantly with sample date. The in¯uence of tomato 15% faster on VF145B7879 compared to the walking cultivar on white¯y density was independent of the 349

Table 1. Cultivar mediated measures of D. pusillus ®tness

1 1

D. pusillus ®tness character cv. Alta cv. VF145B7879 F df P

 <

Lifetime fecundity (eggs) 7.9  1.22 34.5 3.69 120.339 1,17 0.0001 

Adult longevity (d) 21.2  1.10 20.0 0.75 0.858 1,17 0.3673 

Handling time (min) 4.15  0.433 3.02 0.401 3.630 1,28 0.0671  Walking speed (mm/s) 2.09  0.247 2.41 0.298 9.098 1,37 0.0046

1  Values represent the x 1 SEM per individual or observation.

Table 2. Results of repeated measures ANOVA conducted on numbers of immature B. argentifolii censused in population level studies

Effect df F P

Cultivar 1,8 52.51 <0.001 Predatory release 1,8 21.09 0.002

Sample week 9,72 28.32 <0.001

Cultivar  predator release 1,8 4.30 0.072 < Predator release  sample week 9,72 8.21 0.001

Cultivar  sample week 9,72 2.65 0.010 

Cultivar  predator release sample week 9,72 0.88 0.545

: x = : = N = presence or absence of D. pusillus (P > 0 05 for the B. argentifolii eggs ( 3 8h,SEM 0.31, 200

cultivar  predator release interaction), indicating the beetles), and these differences were also statistically

= : = < : lack of a signi®cant difference in white¯y suppression signi®cant (F 46 36, df 1, 36, P 0 0001). No from D. pusillus predation between the two tomato signi®cant 2-way or 3-way interactions were detected cultivars. White¯y population growth rates varied sig- from the ANOVA.

ni®cantly between cultivars (cultivar  sample week interaction) and between D. pusillus treatments (pred-

ator release  sample week interaction). The 3-way Discussion interaction among cultivar, D. pusillus treatment, and sample week was not signi®cant. Due to the lack of a Plant trichomes form the basis of resistance against a

signi®cant cultivar  predator release interaction, the number of pests (see Levin, 1973; Norris hypothesis that biological control of B. argentifolii by & Kogan, 1980; and Stipanovic, 1983 for reviews). D. pusillus should be more effective on a glabrous cul- However, whether white¯y oviposition rates increase tivar (VF145B7879) compared to a pubescent cultivar or decrease with increasing densities of leaf trichomes (Alta) was not supported by our population level exper- varies greatly across host plants. Highly pubescent cul- iment. tivars support larger populations of white¯y in the genus Bemisia than do glabrous cultivars of cotton Host plant and prey in¯uences on predator residence (Mound, 1965; Butler & Henneberry, 1984; Ozgur & time. Tomato cultivar and presence of prey affected the Sekeroglu, 1986) and tomato (Berlinger, 1986; Heinz

amount of time beetles resided on plants (Figure 2). & Zalom, 1995). However, in various species of cucur-

= : =

Residence times on Alta ( x 4 7h,SEM 0.32, bits leaf pubescence is negatively correlated with dens- =

N 200 beetles) were signi®cantly greater than the ities of Bemisia sp. (McCreight & Kishaba, 1991;

= :

residence times observed on VF145B7898 (x 3 9h, Kishaba et al., 1992). Densities of B. tabaci meas-

N =

SEM = 0.30, 200 beetles) at comparable sample ured on 10 vegetable crops were not found to increase =

times, and these differences were signi®cant ( F with increasing trichome densities (Simmons, 1994).

= < :

29:93, df 1, 36, P 0 0001). Residence times Responses to trichomes by natural enemies exhibit

= :

on plants with B. argentifolii eggs (x 4 8h,SEM similar degrees of variability as that found in white-

N = = 0.32, 200 beetles) were signi®cantly longer ¯ies. Obrycki et al. (1983) demonstrated that the com- than the residence times of beetles on plants without bination of the sticky potato trichomes in hybrids of 350

the ef®cacy of searching by the parasitoid Gahan for its host, the greenhouse white- ¯y Trialeurodes vaporariorum (Westwood), is greatly reduced by the presence of stiff foliar hairs that slow the parasitoid's walking, and also force the parasitoid to expend more time grooming if the hair's are coated with sticky honeydew (see Price et al., 1980; Li et al., 1987; Hulspas-Jordan & van Lenteren, 1989). In the tomato±white¯y±coccinellid predator sys- tem we have described here, greater levels of B. argen- tifolii population suppression were obtained through the use of a glabrous tomato cultivar than were obtained through the release of D. pusillus (Figure 1). Although walking speeds and lifetime fecundity were reduced signi®cantly in beetles housed on the pubes- cent compared to the glabrous cultivar, beetle resid- ence times were signi®cantly longer on the pubescent cultivar compared to the glabrous cultivar. Trichome- Figure 2. The in¯uences of tomato cultivar and prey densities induced variation in these characteristics (and possibly (B. argentifolii eggs) on the amount of time adult beetles reside other characters) produced a counterbalancing effect

( = residence time) on tomato plants before attempting to disperse. whereby the levels of white¯y suppression resulting

Mean numbers of beetles  SEM obtained from 10 replications of each cultivar and prey density are graphed across the 8 h sampling from D. pusillus predation were not signi®cantly dif- periods. ferent between cultivars differing in trichome density. The reduced residence times on the glabrous cul- tivar may be a result of various `decisions' made by

Solanum tuberosum  S. berthaultii and the action of foraging beetles. If beetles use the rate of encounter aphid predators and parasitoids (coccinellids, chrysop- with suitable prey as means of measuring patch qual- ids, and aphidids) was more effective in reducing aph- ity (as described by Stephens & Krebs, 1986), and if id populations than either enemies or trichomes alone. this encounter rate declines more quickly for beetles Heinz & Parrella (1994b) report that adult longevity foraging on glabrous than on pubescent cultivars, then of D. pusillus and four species of Encarsia (Hymen- beetles may spend less total time foraging on glabrous optera: Aphelinidae) did not vary between poinset- cultivars. Encounter rates may decrease more quickly tia cultivars exhibiting different leaf trichome densit- on glabrous cultivars due to the increased search ef®- ies. Predator prey consumption, parasitoid host feed- ciency (as indicated by faster walking speeds) of for- ing, parasitism and the total number of B. argentifolii aging beetles in comparison to beetles foraging on killed were signi®cantly greater on the cultivar with pubescent cultivars where their walking speeds are less dense trichomes, but the numbers of emer- relatively slow. Furthermore, because beetles used in ging from parasitised hosts were signi®cantly fewer these studies were obtained from laboratory colon- on this same comparatively glabrous cultivar (Heinz & ies where they were continually provided with a Parrella, 1994b). superabundance of prey, exit thresholds based upon In several crops the simultaneous use of trichomes encounter rates may be abnormally low. Because we with parasitoids has proved to be an incompatible com- did not explicitly test this hypothesis, it is also pos- bination. In tobacco, the secretory hairs on foliage were sible that the lack of a difference in white¯y suppres- found to interfere signi®cantly with the ability of Telen- sion from D. pusillus predation may be due to plant omus sphingis (Ashmead) and Trichogramma minutum characteristics other than trichome densities. Riley to parasitize the eggs of the tobacco hornworm, The patterns described here warrant further study Manduca sexta (L.) (Rabb & Bradley, 1968) because due to the in¯uence these counterbalancing proper- the sticky trichomal exudate restricted the movement ties may have on predator foraging behavior and due of the parasitoids. Similar effects of tobacco trichomes to their importance in developing effective control on other parasitoid-host interactions have been repor- programs for B. argentifolii. Considering our cur- ted (Elsey & Chaplin, 1978). In cucumber and tomato rent knowledge, agriculturists should obtain bene®ts 351 in terms of white¯y control by planting glabrous rather Dowell, R. V., 1990. Integrating biological control of white¯ies into than pubescent tomato cultivars due to their negative crop management systems. In: D. Gerling (ed.), White¯ies: their effect on B. argentifolii population growth and neutral Bionomics, Pest Status and Management. Intercept, Andover, UK, pp. 315±335. effect on D. pusillus ef®cacy. Further, the lack of evid- Duffey, S. S. & K. A. Bloem, 1986. Plant defense-herbivore- parasite ence to suggest that biological control may the inhib- interactions and biological control. In: Kogan, M. (ed.), Ecolo- ited by a lack of foliar trichomes suggests that selection gical Theory and Integrated Pest Management Practice. Wiley, New York, pp. 135±183. for glabrous foliage may lead to sustained or increased Elsey, K. D. & J. F. Chaplin, 1978. Resistance of tobacco introduction biological control for a wide range of arthropod pests 1112 to the tobacco budworm and green peach aphid. Journal of tomato. of Economic Entomology 71: 723±725. Fritz, R. S. & E. L. Simms, 1992. Plant Resistance to Herbivores and Pathogens. Ecology, Evolution, and Genetics. University of Chicago Press. 590 pp. Acknowledgments Gauld, I. D. & K. J. Gaston, 1994. The taste of enemy-free space: parasitoids and nasty hosts. In: Hawkins, B. A. & W. Sheehan We are thankful for the use of the facilities housed (eds), Parasitoid Community Ecology. Oxford University Press, New York, pp. 300±318. within the laboratory of M. P. Parrella (University of Gerling, D. & R. T. Mayer (eds.), 1996. Bemisia 1995: , California, Davis). The technical assistance provided Biology, Damage and Management. Intercept, Andover, UK, by J. Brazzle, T. Fletcher, & K. Smallwood (Uni- 448 pp. versity of California, Davis) was critical in completing Heinz, K. M. & M. P. Parrella, 1994a. Biological control of Bemisia argentifolii (Gennadius) (Homoptera: Aleyrodidae) infesting this project. Tomato seed was provided by W. Sims Euphorbia pulcherrima: evaluations of releases of Encarsia (University of California, Davis). This manuscript luteola (Hymenoptera: Aphelinidae) and Delphastus pusillus bene®ted greatly from comments provided by anonym- (Coleoptera: Coccinellidae). Environmental Entomology 23: ous reviewers on a previous draft. Funding for this pro- 1346±1353. Heinz, K. M. & M. P. Parrella, 1994b. Poinsettia (Euphorbia pulcher- ject was provided by a California Tomato Board grant rima Willd. ex Koltz.) cultivar-mediated differences in perform- to K.M.H. and a USDA-OICD grant to F.G.Z. ance of ®ve natural enemies of Bemisia argentifolii Bellows and Perring, n. sp. (Homoptera: Aleyrodidae). Biological Control 4: 305±318. Heinz, K. M. & F. G. Zalom, 1995. Variation in trichome-based References resistance to Bemisia argentifolii (Homoptera: Aleyrodidae) oviposition on tomato. Journal of Economic Entomology 88: Anonymous, 1981. Possibilities for the use of biotic agents in the 1494±1502. control of white¯y Bemisia tabaci. Biocontrol News and Inform- Heinz, K. M. , J. R. Brazzle, C. H. Pickett, E. T. Natwick, J. M. ation 2: 7±13. Nelson, & M. P. Parrella, 1994. Predatory beetle may suppress Bergman, J. M. & W. M. Tingey, 1979. Aspects of interaction silverleaf white¯y. California Agriculture 48(2): 35±40. between plant genotypes and biological control. Bulletin of the Hoelmer, K. A., L. S. Osborne, & R. K. Yokomi, 1993. Reproduction Entomological Society of America 25: 275±279. and feeding behavior of Delphastus pusillus (Coleoptera, Coc- Berlinger, M. J., 1986. Host plant resistance to Bemisia tabaci. cinellidae), a predator of Bemisia tabaci (Homoptera, Aleyro- Agriculture, Ecosystems, and Environment 17: 69±82. didae). Journal of Economic Entomology 86: 322±329. Breene, R. G., R. L. Meagher, Jr., D. A. Nordlund, & Y. T. Wang, Hulspas-Jordan, P. M. & J. C. van Lenteren, 1989. The parasite-host 1992. Biological control of Bemisia tabaci (Homoptera: Aleyro- relationship between Encarsia formosa (Hymenoptera: Aph- didae) in a greenhouse using Chrysoperla ru®labris (Neurop- elinidae) and Trialeurodes vaporariorum (Homoptera: Aleyro- tera: Chrysopidae). Biological Control 2: 9±14. didae). XXX. Modeling population growth of greenhouse white- Butler, G. D., Jr. & T. J. Henneberry, 1984. Bemisia tabaci: effect of ¯y on tomato. Agricultural University Wageningen Papers cotton leaf pubescence on abundance. Southwestern Entomolo- 89(2): 1±54. gist 9: 91±94. Jandel Scienti®c, 1994. TableCurve 2D Windows version 2.0 soft- Cock, M. J. W. (ed.), 1986. Bemisia tabaci ± a literature survey ware. Jandel Scienti®c, San Rafael, CA. with an annotated bibliography. Food and Agriculture Organiz- Kazmer, D. J. & R. F. Luck, 1995. Field tests of the size-®tness hypo- ation of the United Nations and CAB International Institute of thesis in the egg parasitoid Trichogramma pretiosum. Ecology Biological Control 1±21. 76: 412±425. DeBach, P. & M. Rose, 1977. Environmental upsets caused by chem- Kishaba, A.N., S. Castle, J.D. McCreight, & P.R. Desjardins, 1992. ical eradication. California Agriculture 31(7): 8±10. Resistance of white-¯owered gourd to sweetpotato white¯y. Dittrich, V., S. O. Hassan, & G. H. Ernst, 1985. Sudanese cotton and HortScience 27: 1217±1221. the white¯y: a case study of the emergence of a new primary Levin, D. A., 1973. The role of trichomes in plant defense. Quarterly pest. Crop Protection 4: 161±176. Review of Biology 48: 3±15. Dittrich, V., S. Uk, & G. H. Ernst, 1990. Chemical control and Li, Z. H., F. Lammes, J. C. van Lenteren, P. W. T. Huisman, A. insecticide resistance of white¯ies. In: D. Gerling (ed.), White- van Vianen, & O. M. B. DePonti, 1987. The parasite-host rela- ¯ies: their Bionomics, Pest Status and Management. Intercept, tionship between Encarsia formosa (Hymenoptera: Aphelinid- Andover, UK, pp. 263±285. ae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). XXV. In¯uence of leaf structure on the searching activity of 352

Encarsia formosa. Journal of Applied Entomology 104: 297± Price, P. W., 1986. Ecological aspects of host plant resistance and 304. biological control: Interactions among three trophic levels. In: McCreight, J.D. & A.N. Kishaba, 1991. Reaction of cucurbit species Boethel, D. J. & R. D. Eikenbary (eds), Interactions of Plant to squash leaf curl virus and sweetpotato white¯y. Journal of the Resistance and Parasitoids and Predators of Insects. Ellis Hor- American Society of Horticultural Science 116: 137±141. wood, Chichester, pp. 11±30. McMahon, R.W., R.K. Lindquist, B.D. Baith, T.L. Makin, & M.L. Price, P. W., C. E. Bouton, P. Gross, B. A. McPheron, J. N. Casey, 1994. Comparison of commercially and locally produced Thompson, & A. E. Weiss, 1980. Interactions among three Encarsia formosa Gahan on the control of sweetpotato white¯y trophic levels: In¯uence of plants on interactions between on poinsettias. HortTechnology 4(3): 295±298. herbivores and natural enemies. Annual Review of Ecology and Meyerdirk, D. E., D. L. Coudriet, & N. Prabhaker, 1986. Population Systematics 11: 41±65. dynamics and control strategy for Bemisia tabaci in the Imperial Rabb, R. L. & J. R. Bradley, 1968. The in¯uence of host plants on Valley, California. Agriculture, Ecosystems, and Environment parasitism of eggs of the tobacco hornworm. Journal of Eco- 17: 83±88. nomic Entomology 61: 1249±1252. Mound, L. A, 1965. Effects of leaf hair on cotton white¯y popula- Simmons, A. M., 1994. Oviposition on vegetables by Bemisia tabaci tions in the Sudan. Gezira Empire Cotton Grower's Review 42: (Homoptera: Aleyrodidae): temporal and leaf surface factors. 33±40. Environmental Entomology 23: 381±389. Norris, D. M. & M. Kogan, 1980. Biochemical and morphological Simmons, G. S. & O. P. J. M. Minkenberg, 1994. Field-cage eval- bases of resistance. In: F. B. Maxwell & P. R. Jennings (eds), uation of augmentative biological control of Bemisia argenti- Breeding Plants Resistant. Wiley, N.Y., pp. 23±61. folii (Homoptera: Aleyrodidae) in southern California cotton Obrycki, J. J., M. J. Tauber, & W. M. Tingey, 1983. Predator and with the parasitoid Eretmocerus nr. californicus (Hymenoptera: parasitoid interaction with aphid-resistant potatoes to reduce Aphelinidae). Environmental Entomology 23: 1552±1557. aphid densities: A two-year ®eld study. Journal of Economic Sokal, R. R. & F. J. Rohlf, 1981. Biometry, 2nd edition. W. H. Entomology 76: 456±462. Freeman & Company, San Francisco, CA, 859 pp. Ozgur, A. F. & E. Sekeroglu, 1986. Population development of StatSoft, 1994. Statistica v4.5 for the Windows operating system, Bemisia tabaci (Homoptera: Aleurodidae) on various cotton reference for statistical procedures. StatSoft, Tulsa, OK. cultivars in Cukurova, Turkey. Agriculture, Ecosystems, and Stephens, D. W. & J. R. Krebs, 1986. Foraging Theory. Princeton Environment 17: 83±88. University Press, Princeton, NJ, 247 pp. Prabhaker, N., D. L. Coudriet, & D. E. Meyerdirk, 1985. Insect- Stipanovic, R. D., 1983. Function and chemistry of plant trichomes icide resistance in the sweetpotato white¯y, Bemisia tabaci and glands in insect resistance. In: P. A. Hedin (ed.), Plant (Homoptera: Aleyrodidae). Journal of Economic Entomology Resistance to Insects, ACS Symposium Series 208, American 78: 748±752. Chemical Society, Washington, D.C., pp. 70±100. Prabhaker, N., D. L. Coudriet, & N. C. Toscano, 1988. Effects of syn- Visser, M. E., 1994. The importance of being large: the relationship ergists on organophosphate and permethrin resistance in sweet- between size and ®tness in females of the parasitoid Aphaereta potato white¯y (Homoptera: Aleyrodidae). Journal of Economic minuta (Hymenoptera: Braconidae). Journal of Animal Ecology Entomology 81: 34±39. 63: 963±978.