VOL. 34, NO. 4 SOUTHWESTERN ENTOMOLOGIST DEC. 2009

Tritrophic Interactions among Host Plants, , and Parasitoids

Shoil M. Greenberg1, Walker A. Jones2, and Tong-Xian Liu3

Abstract. Effects of cotton, Gossypium hirsutum L.; green bean, Phaseolus vulgaris L.; and sweet potato, Ipomoea batatas (L.) Lam.; on mortality and development of sweetpotato , Bemisia tabaci (Gennadius) biotype B; bandedwinged whitefly, abutilonea (Haldeman); and greenhouse whitefly, T. vaporariorum (Westwood); and on the key biological parameters of an exotic parasitoid species, Eretmocerus mundus Mercet, and an indigenous parasitoid, Encarsia pergandiella Howard, were compared in the laboratory. Cotton was most suitable for sweetpotato whitefly, and bean was most suitable for greenhouse whitefly. No significant differences were found between these two whitefly species on sweet potato. Preimaginal mortality of sweetpotato whitefly on cotton was 35.2% versus 77.3% of greenhouse whitefly. Developmental time of sweetpotato whitefly was significantly shorter (17.5 days) than that of greenhouse whitefly (23.2 days). The mortality and developmental time of bandedwinged whitefly did not differ on the different host plants. Parasitism by Er. mundus was greatest in sweetpotato whitefly and least in greenhouse whitefly when both whiteflies were reared on cotton. Parasitism of bandedwinged whitefly was intermediate. Parasitism by En. pergandiella was significantly greater than that by Er. mundus attacking the same whitefly species reared on bean or cotton, except parasitism of sweetpotato whitefly. Emergence of Er. mundus was greatest from sweetpotato whitefly on cotton, and least for bandedwinged whitefly on bean. Emergence of En. pergandiella was significantly greater than that of Er. mundus among host plants and whitefly species except sweetpotato whitefly.

Introduction

Whiteflies (: Aleyrodidae) are among the most widespread and economically important pests worldwide. The sweetpotato whitefly, Bemisia tabaci (Gennadius), may feed on 506 plants in 74 families (Greathead 1986). Sweetpotato whitefly biotype B ranks among the most noxious attacking agronomic and ornamental crops (Cock 1993). The bandedwinged whitefly, Trialeurodes abutilonea (Haldeman), is a polyphagous feeder on ≈140 species of plants, including many important species in the genus Hibiscus (Russell 1963, Liu and Stansly 2000). Similarly, the greenhouse whitefly, Trialeurodes vaporariorum (Westwood), is an important pest of vegetables and ornamental crops in greenhouses. ______1Beneficial Insects Research Unit, Kika de la Garza Subtropical Agricultural Research Center, Agricultural Research Service, U.S. Department of Agriculture, Weslaco, TX. 2European Biological Control Laboratory, ARS-USDA, Montpellier, France. 3Vegetable IPM Laboratory, Texas AgriLife Research, Texas A&M University System, Weslaco, TX. Correspondence: S. M. Greenberg, Research Entomologist, BIRU-SARC-ARS-USDA, Weslaco, TX; E-mail address: [email protected].

431 Although the bioecology of sweetpotato whitefly and greenhouse whitefly is well understood, little information is available on the bioecology of bandedwinged whitefly under different geographical and environmental conditions. During 2008, 30,355 ha of cotton in the Lower Rio Grande Valley of Texas were infested by bandedwinged whitefly while only 4,047 ha were infested by sweetpotato whitefly (Williams 2009). This contrasted with the U.S. trend where sweetpotato whitefly was more damaging than bandedwinged whitefly in cotton during the same year (147,138 versus 109,853 ha infested by sweetpotato whitefly and bandedwinged whitefly, respectively; Williams 2009). Liu and Stansly (2000) speculated that bandedwinged whitefly, originally restricted to Malvaceae had adapted to other host species in areas where malvaceous hosts have become rare. If this is the case, the adaptation process probably will continue and the host range of bandedwinged whitefly may continue to expand. Information on the interactions among plant species, whiteflies, and their natural enemies is important in the development of locally appropriate integrated pest management strategies including biological control. At present, whitefly control programs in the southwestern U.S. are based mostly on the application of insecticide (Palumbo et al. 2001). However, frequent and intensive use of broad-spectrum insecticides increases the risk of resistance to insecticide, environmental contamination, and human exposure. Conservation biological control is one of the most economically feasible alternatives to conventional pest management practices in field crops. Among the most effective natural enemies of Bemisia whiteflies are parasitoids in the family Aphelinidae (Hymenoptera) including Eretmocerus mundus Mercet (exotic) and Encarsia pergandiella Howard (indigenous). Er. mundus is the most common parasitoid of sweetpotato whitefly in southern Europe and has been successfully established in many parts of the US. En. pergandiella is a heteronomous hyperparasitoid (autoparasitoid); females develop as primary parasitoids on immature whiteflies, but males develop as secondary parasitoids on females of their own or on related species (Hunter 1989). En. pergandiella can cause 94% parasitism of sweetpotato whitefly in South Texas (Goolsby et al. 1998). Encarsia formosa Gahan and Er. eremicus Rose and Zolnerowich are perhaps the most effective species for control of greenhouse whitefly (Hoddle et al. 1998, Gelman et al. 2005). However, no information is available on the use of these species to control bandedwinged whitefly (Liu and Stansly 2000) and little information is available on the use of Er. mundus and En. pergandiella to control greenhouse whitefly. This information is important in areas such as the southwestern US where both pests species co-exist in the field and greenhouse. Most investigations tend to focus on direct interactions between whiteflies and their host plants or the insects and their natural enemies. The full set of tritrophic interactions needs to be assessed to provide a basis for effective pest management strategies against whiteflies. Qualities of the host plant may have indirect effects on the fitness of the third trophic level. For example, high host/pest densities leading to abundant parasitoids or low parasitoid:host ratio may result in longer developmental time and smaller size of parasitoid progeny and a greater proportion of male progeny because of possible differences in nutritional quantity. The objectives of this study were to determine the effects of three host plants, bean, cotton, and sweet potato, on key fitness parameters of three whitefly species, sweetpotato whitefly, bandedwinged whitefly, and greenhouse whitefly, and two parasitoid species, Er. mundus and En. pergandiella, developing on these

432 pests and host plants. Parameters measured included survivorship, developmental time, sex ratio, preovipositional period, daily fecundity, and size. Knowledge of the interrelationship among host plants, whiteflies, and their parasitoids is critical to developing rearing techniques, making decisions in augmentative releases, developing predictive models, and understanding the mechanisms involved in competition by parasitoids.

Materials and Methods

Host Plants. Bean, cotton, and sweet potato were used as host plants in these studies. Leaves were excised and each leaf petiole was placed in a floral aquapic filled with a hydroponic solution (Aqua-Ponics International, Los Angeles, CA). Excised leaves readily rooted and did not deteriorate under fluorescent lights (20 watt, Vita-Life©, Duro-Test Lighting, Elk Grove, IL) in an incubator. Whitefly Cultures. A culture of sweetpotato whitefly originated from adults collected from cabbage, Brassica oleracea L., in Hidalgo County, TX, and maintained on sweet potato in a greenhouse of the Subtropical Agricultural Research Center, ARS-USDA, Weslaco, TX. A culture of greenhouse whitefly originated from individuals received from the Department of Entomology, University of Georgia, Griffin, GA, where they were reared on green bean. A culture of bandedwinged whitefly was started from individuals collected from cotton in Hidalgo County, TX, and maintained on cotton in a greenhouse. Before the experiment, the sweetpotato whitefly, bandedwinged whitefly, and greenhouse whitefly were cultured for three generations on the three host plants (cotton, bean, and sweet potato). We and others (Van Boxtel et al. 1978, Dorsman and van de Vire 1987, Liu and Stansly 2000) observed that when adult whiteflies were transferred from one plant species to another, the insects required a period of adjustment for at least three generations on the host plant. Parasitoid Cultures. Er. mundus was originally collected from sweetpotato whitefly on cotton near Murcia, Spain, and provided by USDA, APHIS Mission Plant Protection Center, Mission, TX (MPPC culture # M92014). En. pergandiella was collected from sweetpotato whitefly on cotton at Weslaco, TX. We maintained all the parasitoid cultures on sweetpotato whitefly reared on sweet potato. Host Plant Effects on Whiteflies. We determined mortality and developmental time separately by the whitefly instar. Whiteflies were confined within a 4.5-cm-diameter clip cage to the underside of each excised test leaf. Each rooted leaf with eggs was placed in a 120 x 25-mm dish covered with polyester organdy for ventilation. Hydroponics solution was added to floral aquapic as needed. Dishes were kept in an environmental chamber at 25 ± 1ºC, 60 ± 5% relative humidity, and a photoperiod of 16:8 light:dark hours. The development of each instar was monitored daily with the aid of a dissecting microscope until adult eclosion, using the morphological descriptions by Gill (1990) and Lopez-Avila (1988). Number of female progeny was determined by determining the gender of 100-150 adults from each treatment. The preoviposition period was recorded by individually confining 10-15 newly-emerged females per treatment within a clip cage to the underside of tested plant leaves. The leaves were inspected daily until the whitefly species started to oviposit. Number of eggs deposited per female per day was determined from 10 females (2 days old) per treatment during the first 3 days of the experiment. Size of 100-150 fourth-instars per treatment also was recorded. Survival on different whitefly stages (egg, 1st, 2nd, 3rd, and 4th instars, and adult) was recorded.

433 Interactions among Host Plant, Whitefly Species, and Parasitoids. We determined parasitization, development, and emergence rates, as well as progeny sex ratio, longevity, and female size. The leaves were infested with whitefly species as described previously. Second instars were used for parasitization by Er. mundus and third instars by En. pergandiella (Jones and Greenberg 1998, 1999). When the designated instar was reached, all but 35 nymphs were carefully removed by hand with an entomological needle. Subsequently, two mated female parasitoids (<2 days old) were released and confined with the nymphs in a clip cage. After 3 hours, parasitoids were removed, and the leaf with parasitized nymphs was returned to the environmental chamber. Each treatment was replicated three times (§105 total nymphs per treatment). We found this yielded the most satisfactory amount of parasitism while minimizing any advance in development of the exposed nymphs during exposure to the parasitoid. We confined two wasps for the experiment, because using only one would necessitate a much longer exposure period to achieve the desired amount of parasitism necessary for comparisons. Longer exposure times allow individual hosts to transform into the next instar, particularly among the younger stages. Following an initial 10-day incubation period, test leaves were examined daily for development and emergence of parasitoids. Time of emergence was recorded for each individual. All emerged adult parasitoids were placed individually into glass vials (1-cm diameter by 3 cm long) and fed with droplets of undiluted honey to determine the longevity of progeny. Mortality was checked daily at 1100 hours. The number of female parasitoid progeny was recorded by examining the antennae, which are sexually dimorphic (average 50 individuals per treatment). The number of parasitized nymphs produced per female parasitoid was recorded by exposing one parasitoid female daily (during the first 4 days) to a range of numbers of whitefly nymphs. The size of 50 parasitoid females was determined by measuring body length from the frons to the tip of the abdomen. Effects of whitefly species reared on bean and cotton on key biological parameters of Er. mundus and En. pergandiella were studied. Data Analysis. Data were analyzed by using analysis of variance (ANOVA) and the independent t-test function of SYSTAT (Wilkinson et al. 1992). Means were separated using the Tukey-Kramer test (TUKEY option of the LSMEANS statement, SAS Institute 1999). The percentage of parasitism was arcsine transformed for analyses (Sokal and Rohlf 1981), but untransformed means are shown.

Results

Host Plant Effect on Whiteflies. Total mortality of sweetpotato whitefly on cotton (35.2 ± 2.5%) was significantly less than on bean (59.8 ± 4.9%), and significantly greater than on sweet potato (26.1 ± 1.4%) (P = 0.007) (Fig. 1). Total mortality of greenhouse whitefly on bean (20.6 ± 1.5 %) was least, and significantly less than that on sweet potato (30.5 ± 3.3%) or cotton (57.4 ± 4.4%) (P = 0.003). Mortality of bandedwinged whitefly on cotton (76.1 ± 4.2%), bean (68.5 ± 1.8%), and sweet potato (72.5 ± 5.6%) were not significantly different (P = 0.286). Total mortality of eggs and young nymphs (1st and 2nd) of each whitefly species on each host plant was 2.5-3.5-fold greater than for older instars (Fig. 2). Developmental time from egg to adult of sweetpotato whitefly was significantly faster on cotton (17.5 ± 0.9 days) than on bean leaves (22.1 ± 1.3 days), while that of greenhouse whitefly was opposite, 20.5 ± 1.3 days on bean and 24.6 ± 2.0 days on cotton (P = 0.001) (Fig. 3). Developmental time of bandedwinged

434 whitefly was not dependent on host plant (23.2 ± 3.9 days on cotton and 21.9 ± 3.6 days on bean, P = 0.188). The greatest portion of the total developmental time was during the egg stage (26.7 to 42.9%) and the fourth instar (19.4 to 33.9%) for all whitefly species or host plants. Sweetpotato whitefly began to oviposit during the first 24-30 hours after emergence, while there was a 48-52 hour preovipositional period for bandedwinged whitefly, and 36-40 hours for greenhouse whitefly (Table 1). The preovipositional period was not significantly different among whitefly species on the different host plants (P = 0.3 for sweetpotato whitefly, P = 0.6 for bandedwinged whitefly, and P = 0.2 for greenhouse whitefly). The number of eggs deposited per day by sweetpotato whitefly females on cotton was significantly greater than on the other hosts (P = 0.001), while oviposition by greenhouse whitefly was significantly greater on bean and sweet potato (P = 0.002). The number of eggs deposited per day by bandedwinged whitefly females was not significantly different between host plants (P = 0.41), but was significantly less than that for the other two species of whiteflies (P = 0.001).

100 B. tabaci

T. abutilonea d d T. vaporariorum 75 d e a

50 b f c 25 g Mortality from egg to adult, %

0 Cotton Bean Sweet potato Host Plant

Fig. 1. Total mortality of whitefly species after development on different host plants. Bars of the same whitefly species with different letters show significantly different total mortality on the different host plants at the 5% level as determined by Tukey’s studentized range test.

435 T. abutilonea 40 Cotton Bean 30 Sweet potato

20

10 Stage-specific mortality, % 0 Egg L1 L2 L3 L4

B. tabaci 40

30

20

10 Stage-specific mortality, % 0 Egg L1 L2 L3 L4

T. vaporariorum 40

30

20

10 Stage-specific mortality, % 0 Egg L1 L2 L3 L4 Stage

Fig. 2. Whitefly species (Trialeurodes abutilonea; Bemisia tabaci; and T. vaporariorum) stage-specific mortality on different host plants.

436 30 T. abutiloneus 25 a cotton a 20 a bean 15 sweetpotato 10

Development time, d 5

0 Eggs 1st 2nd 3rd 4th Total

30 B. tabaci 25

20 a b 15 c

10

Development time, d 5

0 Egg 1st 2nd 3rd 4th Total 30 T. vaporariorum 25 a 20 b b 15

10 Development time, d 5

0 Egg 1st 2nd 3rd 4th Total Stage Fig. 3. Whitefly species (Trialeurodes abutilonea, Bemisia tabaci, T. vaporariorum) stage-specific developmental time on different host plants.

437 Table 1. Effect of Host Plant on Biological Parameters of Three Whitefly Species Size of red-eyed Preovipositional Eggs/female/ nymphs Female Host plant period, days day (length x width), mm progeny, %

Bemisia tabaci Cotton 1.2 ± 0.4a 7.6 ± 1.8a 0.701 x 0.423b 67.1 ± 6.2a Bean 1.1 ± 0.3a 4.5 ± 1.6c 0.680 x 0.385c 59.0 ± 7.7b Sweet potato 1.3 ± 0.2a 5.2 ± 0.5b 0.747 x 0.424a 66.2 ± 6.8a

Trialeurodes abutiloneus Cotton 2.1 ± 0.7a 1.9 ± 0.7a 0.655 x 0.347a 61.0 ± 5.5a Bean 2.3 ± 0.7a 1.7 ± 0.4a 0.638 x 0.337a 60.0 ± 3.5a Sweet potato 2.2 ± 0.6a 1.8 ± 0.6a 0.648 x 0.344a 62.0 ± 4.3a

Trialeurodes vaporariorum Cotton 2.1 ± 0.5a 3.9 ± 0.6b 0.804 x 0.295b 58.1 ± 7.6a Bean 1.5 ± 0.5a 4.8 ± 0.5a 0.855 x 0.520a 64.3 ± 6.5a Sweet potato 1.6 ± 0.1a 4.5 ± 0.5a 0.838 x 0.514a 63.0 ± 5.7a Means (± SE) followed by different letters within whitefly species in a column are significantly different at the 5% level as determined by Tukey’s studentized range test.

The largest size of sweetpotato whitefly red-eyed nymphs was on sweet potato, then cotton, with the smallest on bean (P = 0.019), but the reverse was recorded for greenhouse whitefly (P = 0.044). The size of bandedwinged whitefly nymphs was not significantly different among host plants (P = 0.33). The percentage of female progeny was not significantly different among host plants (P = 0.218), except significantly more female sweetpotato whitefly progeny were on cotton and sweet potato than on bean (P = 0.016). Host Plant and Whitefly Effect on Parasitoids. The greatest rate of parasitism by Er. mundus was on sweetpotato whitefly maintained on cotton (88.7%) and bean (79.0%). The least parasitism by this parasitoid was on greenhouse whitefly (35.4% on cotton and 38.4% on bean). Results for bandedwinged whitefly were intermediate (52.7% on cotton and 54.7% on bean) (P = 0.001). Parasitism by En. pergandiella was significantly greater than that by Er. mundus attacking the same whitefly species on bean or cotton, except parasitism in sweetpotato whitefly (P = 0.002). The percentage of parasitism was not significantly different within Er. mundus and En. pergandiella on each of the three whitefly species reared on bean or cotton, except parasitism of En. pergandiella in greenhouse whitefly reared on cotton was significantly less than on bean (Fig. 4A). Percentage of emergence of Er. mundus depended on the host species and host plant. The greatest emergence was from sweetpotato whitefly on cotton (93.5%); least was from bandedwinged whitefly on bean (6.1%). Emergence of Er. mundus from sweetpotato whitefly reared on cotton (93.5%) was significantly greater than when reared on bean (62.1) (P = 0.001). Emergence of En. pergandiella adults was significantly greater than that of Er. mundus, except from sweetpotato whitefly (P = 0.003) (Fig. 4B).

438

Fig. 4. Effects of whitefly species and host plants on parasitism by Eretmocerus mundus and Encarsia pergandiella (A) and on emergence of parasitoids (B). Parasitoid species: Eretmocerus mundus - 1, 3, 5; Encarsia pergandiella - 2, 4, 6.

Developmental time for Er. mundus was significantly longer on sweetpotato whitefly and on greenhouse whitefly than on bandedwinged whitefly reared on either bean (P = 0.0001) or cotton (P = 0.003) (Table 2). Developmental time for En. pergandiella was significantly longer on sweetpotato whitefly than on bandedwinged

439

Table 2. Effects of Host Plant and Whitefly Species on Development, Longevity, and Size of Eretmocerus mundus and Encarsia pergandiella Eretmocerus mundus Encarsia pergandiella Whitefly host Bean Cotton Bean Cotton Developmental time, days ± SE B. tabaci 18.1 ± 0.2Aa 17.0 ± 0.1Ab 17.3 ± 0.2Aa 15.7 ± 0.1Ab T. abutilonea 15.2 ± 0.5Ba 15.6 ± 0.4Ba 13.8 ± 0.1Ba 13.6 ± 0.2Ba T. vaporariorum 17.2 ± 0.3Aa 17.6 ± 0.4Aa 13.0 ± 0.1Bb 15.6 ± 0.3Aa

Longevity, days ± SE B. tabaci 5.7 ± 0.4Bb 7.1 ± 0.3Aa 8.8 ± 0.6Bb 10.3 ± 0.2Aa T. abutilonea 7.0 ± 0.6Ba 6.8 ± 0.7Aa 12.1 ± 0.5Aa 11.3 ±1.0Aa T. vaporariorum 10.8 ± 0.7Aa 7.0 ± 0.9Ab 12.8 ± 1.5Aa 7.9 ± 1.6Bb

Female size, mm ± SE B. tabaci 0.517±0.007Bb 0.556±0.006Aa 0.498±0.005Ab 0.526±0.005Aa T. abutilonea 0.503±0.004Cb 0.520±0.004Ba 0.462±0.007Ba 0.493±0.008Ba T. vaporariorum 0.541±0.01Aa 0.504±0.01Cb 0.446±0.008Ba 0.420±0.004Cb

Female progeny, % ± SE B. tabaci 42.7 ± 9.0Bb 55.0 ± 2.5ABa 100 100 T. abutilonea 60.0 ± 1.6Aa 61.0 ± 2.4Aa 100 100 T. vaporariorum 65.6 ± 2.9Aa 46.7 ± 3.3Bb 100 100 Means (± SE) for each parasitoid species in each whitefly host between the two host plants (sub-row) with the same lower-case letter and those among the three whitefly hosts on the same host (sub-column) followed by the same upper-case letters are not significantly different at the 5% level as determined by Tukey’s studentized range test.

whitefly or greenhouse whitefly when reared on bean (P = 0.0001), but significantly longer on sweetpotato whitefly and greenhouse whitefly than on bandedwinged whitefly reared on cotton (P = 0.0001). Both Er. mundus and En. pergandiella required significantly longer to develop on sweetpotato whitefly reared on bean (P = 0.002), while En. pergandiella developed significantly longer on greenhouse whitefly reared on cotton (P = 0.003). There were no significant differences when parasitoids developed on bandedwinged whitefly on bean or cotton. The longevity of Er. mundus developed on greenhouse whitefly on bean was significantly longer than on sweetpotato whitefly or bandedwinged whitefly (P = 0.001). The longevity of Er. mundus developed in three whitefly species on cotton was not significantly different (P = 0.949) (Table 2). The longevity of En. pergandiella maintained in greenhouse whitefly or bandedwinged whitefly on bean was significantly longer than in sweetpotato whitefly (P = 0.049), while those on sweetpotato whitefly or bandedwinged whitefly on cotton was significantly longer than in greenhouse whitefly (P = 0.049). The longevity of both Er. mundus and En. pergandiella progeny was significantly shorter following development in sweetpotato whitefly maintained on bean (5.7 and 8.8 days, respectively) than on cotton (7.1 and 10.3 days,

440 respectively) (P = 0.001). When these parasitoids developed on greenhouse whitefly maintained on bean, the longevity of progeny of both parasitoid species was significantly longer than that on cotton (P = 0.002). There were no host plant effects on the longevity of parasitoids reared on bandedwinged whitefly (Table 2). Progeny of Er. mundus females developed on bandedwinged whitefly or greenhouse whitefly reared with bean were a significantly greater proportion of females than on sweetpotato whitefly (P = 0.045), while those on cotton were significantly less in greenhouse whitefly (P = 0.017). Er. mundus on sweetpotato whitefly reared with cotton produced a greater proportion of females than when reared on bean (55.0 versus 42.7%). When reared in greenhouse whitefly on bean, Er. mundus produced more female progeny than when reared on cotton (65.6 versus 46.7%) (P = 0.014) (Table 2). The size of Er. mundus females developed in greenhouse whitefly on bean was significantly larger than those in bandedwinged whitefly or sweetpotato whitefly (P = 0.003), while the size of Er. mundus females in sweetpotato whitefly on cotton was significantly larger than in bandedwinged whitefly or greenhouse whitefly (P = 0.001). En. pergandiella females developed in sweetpotato whitefly on cotton or bean were significantly larger than those in bandedwinged whitefly or greenhouse whitefly (P = 0.001). Er..mundus and En. pergandiella in sweetpotato whitefly were significantly larger on cotton than on bean, while those in greenhouse whitefly were larger on bean than on cotton (P = 0.001) (Table 2).

Discussion

Mortality of sweetpotato whitefly was least when reared on cotton, while mortality of greenhouse whitefly was least on bean. Costa et al. (1991) found greater mortality of sweetpotato whitefly on cantaloupe, Cucumis melo L.; cotton; pumpkin, Cucurbita maxima Dene.; lettuce, Lactuca sativa L.; and tomato, Lycopersicum esculentum L., but less mortality on zucchini, Cucurbita pepo L. On cotton, mortality of sweetpotato whitefly from egg to adult of 25% at 25ºC was reported by Horowitz et al. (1984) and on poinsettia, Euphorbia pulcherrima L., 39% was reported by Enkegaard (1993). Powell and Bellows (1992b) observed that natural mortality of sweetpotato whitefly on cotton at 25.5ºC was 55.2%, while on cucumber only 14%. Merendonk and Lenteren (1978) showed that total mortality of greenhouse whitefly increased from eggplant (8.8%), to cucumber (10.6%), tomato (21.2%), and paprika (92.5%). We assumed, based on observation of changing biological parameters of whitefly species on different host-plants, that the nutritional value of the food-plant might be the most important factor controlling the whitefly species. Our data demonstrated that sweetpotato whitefly developed significantly faster on cotton than on bean, while development of greenhouse whitefly was significantly faster on bean than on cotton. Coudriet et al. (1985) reported the developmental time of sweetpotato whitefly on 17 plant species. The minimum developmental time was 16 days on sweet potato, with a maximum of 29.8 days on carrot, Daucus carota L. The mean developmental period for sweetpotato whitefly on cotton was 17.7 days and 20.2 days on cucumber at 25.5ºC. Our results agree with other authors in showing the species of host plant exerts significant effects on whitefly preovipositional period (Butler and Henneberry 1985, Enkegaard 1993), number of eggs deposited per day (Van Lenteren et al. 1977), percentage of female progeny (Gameel 1978, Sharaf and Batta 1985), and adult size (Bethke et al. 1991).

441 Our study demonstrated that parasitism by Er. mundus is independent of host plant species. The greatest parasitization rate was on sweetpotato whitefly and the least on greenhouse whitefly. Emergence of Er. mundus was dependent on both host plant and whitefly species. The survival of parasitoids to emergence was greatest in sweetpotato whitefly and least in bandedwinged whitefly. Emergence of Er. mundus from sweetpotato whitefly reared on cotton was significantly greater than when sweetpotato whitefly was reared on bean. Parasitism and emergence by En. pergandiella was greater than by Er. mundus when sweetpotato whitefly was the host. Er. mundus from sweetpotato whitefly reared on cotton produced more female progeny than those that emerged from sweetpotato whitefly reared on bean. Er. mundus that developed on greenhouse whitefly on bean produced more female progeny than those from greenhouse whitefly reared on cotton. Both Er. mundus and En. pergandiella on sweetpotato whitefly on cotton had significantly shorter developmental time and greater longevity and size than when the parasitoids were reared on sweetpotato whitefly on bean. Developmental time was significantly shorter and longevity and size were greater when the two parasitoids developed from greenhouse whitefly reared on bean than on cotton. Interactions in whitefly parasitoid systems have been reported by others. Powell and Bellows (1992a) found that the mean longevity of females of a Hawaiian population of Eretmocerus sp. from sweetpotato whitefly on cotton or cucumber was greater than that of a California population. Milliron (1940) found that degree of parasitization was affected by the pubescence of the plant and by excretions of the host plant and whitefly nymphs. Vet et al. (1980) reported that parasitization of greenhouse whitefly by En. formosa on cucumber leaves was much less than on tomato, eggplant, or paprika leaves. Kapadia and Puri (1990) demonstrated that developmental time of En. transvena (Timberlake) (= En. sophia Girault & Dodd) on sweetpotato whitefly reared on eggplant was shorter (12.3 days) than on cotton (18.7 days), while development of Er. mundus was shorter on cotton (15.9 days) than on eggplant (20.1 days). Er. mundus produced significantly greater parasitism of sweetpotato whitefly developing on tomato compared with that in greenhouse whitefly (Greenberg et al. 2002). The same trend was observed with survival of Er. mundus on the same whitefly species. Parasitism and emergence rates by Er. eremicus on sweetpotato whitefly and greenhouse whitefly on tomato were not significantly different. Er. eremicus was recommended to producers as a promising species for management of B. argentifolii Bellows and Perring and greenhouse whitefly, especially in greenhouses. Knowledge of interrelationship among host plants, whiteflies, and their parasitoids is necessary for management of whiteflies, to know which plants are affected by them, to understand their damage, and how to monitor whitefly populations (sites, population dynamics, and action thresholds). These are also critical for developing various control tactics, which include cultural control, plant resistance, chemical and natural controls. Evaluating tritrophic interactions will help reduce abundance and damage by pests to manageable levels. These practices can be modified to preserve natural enemies of whiteflies. Crop rotation helps escape most whiteflies. Temporal or spatial separation between fall and spring crops are helpful in reducing whitefly migration and primary inoculation by virus. These are helpful in understanding the mechanisms involved in competition by parasitoids, making decisions in augmentative release experiments, increasing knowledge of whiteflies and the biology of their parasitoids and host-parasitoid

442 relationships, and developing predictive models. They also can be useful for the development of rearing strategies for parasitoids of whiteflies. Based on our data we conclude that cotton is most suitable for sweetpotato whitefly while bean is best for greenhouse whitefly. Sweet potato had no significant impact on sweetpotato or greenhouse whiteflies. The greatest rate of parasitism by Er. mundus was observed in sweetpotato whitefly whether developing on cotton or bean. The least parasitism by this parasitoid was in greenhouse whitefly developing on cotton or bean. Parasitism by Er. mundus in bandedwinged whitefly nymphs developing on cotton or bean was intermediate. Parasitization rates by En. pergandiella also depended on whitefly species and host plants and was similar to that by Er. mundus.

Acknowledgment

We thank Drs. Donald Thomas (SARC-ARS-USDA) and Carlos E. Bográn (Texas AgriLife Extension Service, Texas A&M University System) for reviewing this manuscript, and W. C. Warfield, Y. M. Zhang, and J. Alejandro for technical assistance.

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