Preference of Bemisia argentifolii (Homoptera: Aleyrodidae) for Selected Vegetable Hosts Relative to Tomato 1

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1 Preference of Bemisia argentifolii (Homoptera: Aleyrodidae) for Selected Vegetable Hosts Relative to Tomato 1 David J. Schuster University of Florida, Gulf Coast Research & Education Center, Bradenton, Florida J. Agric. Urban Entomol. 20(2): (April 2003) ABSTRACT The silverleaf whitefly, B. argentifolii Bellows & Perring (Homoptera: Aleyrodidae) [also known as strain B of B. tabaci(gennadius)], is a pest of many important vegetable crops, including tomato (Lycopersicon esculentum Mill.). Adults transmit extremely damaging plant viruses, especially Tomato yellow leaf curl virus, and feeding by nymphs induces a systemic, irregular ripening disorder of tomato fruit. The use of a trap crop might be useful in managing this pest on tomato. To identify potential candidate trap crops, two screenhouse and three field experiments were conducted to determine the preferences of B. argentifolii adults for selected vegetable crops, including cucumber (Cucumis sativus L.), eggplant (Solanum melongena L.), okra [Abelmoschus esculentus (L.) Moench], snap bean (Phaseolus vulgaris L.), and squash (Cucurbita pepo L.), relative to tomato. On the basis of the number of whitefly adults or eggs and nymphs per leaf or per leaf area, no crop plant appeared more preferred than tomato; however, on a per-plant basis, more whitefly adults or immature lifestages were consistently observed on squash plants than on tomato plants. The results could be the result of the more rapid growth of squash relative to tomato. Squash is a better sink for whitefly adults than tomato and could be useful as a trap crop by attracting and holding whitefly adults, thus keeping them from moving to tomato. KEY WORDS Homoptera, Aleyrodidae, Bemisia argentifolii, Bemisia tabaci, sweet potato whitefly, silverleaf whitefly, host preference, squash, Cucurbita pepo, tomato, Lycopersicon esculentum The silverleaf whitefly, B. argentifolii Bellows & Perring (Homoptera: Aleyrodidae) [also known as strain B of B. tabaci (Gennadius)], is the key pest of tomatoes, Lycopersicon esculentum Mill., in south Florida (Schuster et al. 1996). Nymphal feeding induces a systemic, irregular ripening disorder of fruit (Schuster et al. 1990), and adults can transmit plant viruses, particularly geminiviruses (Polston & Anderson 1997), that can be extremely damaging, especially tomato yellow leaf curl virus (Polston et al. 1999). Insecticides have been used most often to manage the whitefly and avoid losses; however, resistance to every major class of insecticide has been reported in Bemisia (as recently summarized by Palumbo et al. 2001). The use of a trap crop may be a useful component of an 1 Accepted for publication 17 December

2 60 J. Agric. Urban Entomol. Vol. 20, No. 2 (2003) integrated approach to managing B. argentifolii and associated geminiviruses. Unfortunately, studies to date have been inconsistent. Interplanting tomato with cucumber (Cucumis sativus L.) reduced the incidence of tomato yellow leaf curl virus (Al-Musa 1982), whereas interplanting tomato with eggplant (Solanum melongena L.) (Stansly et al. 1998) or bean (Phaseolus vulgaris L.) (Arias & Hilje 1993, Peralta & Hilje 1993) had no effect on the numbers of whiteflies or incidence of virus and actually increased whitefly numbers in the case of eggplant. These inconsistent results could have been the result of the choice of a trap crop that was less than ideal. In greenhouse and field experiments, cucurbit crops such as cantaloupe (Cucumis melo L.), cucumber, and squash (Cucurbita pepo L.) generally were more attractive to Bemisia adults than other crops, including alfalfa (Medicago sativa L.), broccoli (Brassica oleracea L.), carrots (Daucus carota L.), cotton (Gossypium hirsutum L.), lettuce (Lactuca sativa L.), and sugar beet (Beta vulgaris L.) (Butler et al. 1989, Blua et al. 1995, Chu et al. 1995, Yee & Toscano 1996, Foda 2000). In a greenhouse experiment, more eggs were deposited on foliage of squash and watermelon [Citrullus lanatus (Thunberg)] than on foliage of tomato; however, in a second greenhouse experiment in which both the numbers of eggs and nymphs were recorded, snap bean as well as squash also seemed more preferred than tomato whereas watermelon did not (Simmons 1994). In two field experiments, more eggs were deposited on foliage of squash than on that of tomato in one trial but not in the other, whereas the number of eggs on foliage of beans did not differ from the number on tomato (Simmons 1994). In both experiments fewer eggs were deposited on watermelon foliage than on tomato foliage. In a greenhouse cage study, more eggs were deposited on foliage of snap bean than on foliage of tomato (Liu & Oetting 1994). In a survey of vegetable crop fields, similar numbers of adults and immatures per 2.5 cm 2 were observed on foliage of cantaloupe, cucumber, and tomato (Foda 2000). The objective of the present investigations was to identify potential candidate trap crops by determining in screenhouse and field experiments the preferences of B. argentifolii adults for selected vegetable crops relative to tomato. Materials and Methods Screenhouse experiments. Two experiments were conducted in a screenhouse at the Gulf Coast Research & Education Center (GCREC), Bradenton, Florida. In the first, acorn squash Table Ace, snap bean Strike, okra [Abelmoschus esculentus (L.) Moench] Annie Oakley, eggplant Black Bell, tomato Sunny, and cucumber Hybrid Stryker were seeded in 10.2-cm diameter plastic pots. When the plants were approximately 10.2 cm tall, one pot of each crop plant was placed in each of four cm screen-covered cages and were randomly arranged equidistant from each other on the inside perimeter of the cages. Randomness was achieved by giving a number to each crop species and then using a table of random numbers to assign each crop species a location within each cage. Approximately 300 B. argentifolii adults of unknown sex and age were collected from a colony maintained for approximately 2 yr on poinsettia and were released in the center of each cage. After 7 d, the numbers of eggs and crawlers were counted on each plant and the area of all of the leaves of each plant was measured with a LI-COR Model LI-3000A portable leaf area meter fitted into a LI-3050A

3 SCHUSTER: Bemisia Preference for Vegetable Hosts 61 transparent belt conveyor accessory (LI-COR, Inc., Lincoln, Nebraska). The number of eggs and crawlers per cm 2 was calculated by dividing the counts by the leaf area. Eggs and crawlers were used as an indirect measure of adult preference. The experiment was repeated three times for a total of 12 replicates in a randomized complete block design. In the second experiment, single, four to five leaf seedlings of tomato Lanai, eggplant Black Beauty, and yellow squash Dixie Hybrid grown in 10.2-cm diameter pots were placed randomly in each of three rows (replicates) on a bench (randomized complete block design). Plants of the weeds Ludwigia spp. (primrose willow), Indigofera hirsuta Harv. (hairy indigo), and Chamaesyce spp. (spurge) infested with B. argentifolii were placed around the three rows of crop plants. Three, 11, and 19 d after placing the pots in the screenhouse, the number of leaves and the number of whitefly adults were determined for each test plant, and the number of adults per leaf was calculated. Field experiments. Three experiments were conducted during the spring and fall of 1991 and spring of 1992 at the GCREC comparing tomato Sunny, eggplant Black Beauty, yellow squash Dixie Hybrid, and okra Annie Oakley. All experiments were conducted on 20-cm-high and 81-cm-wide beds of EauGallie fine sand covered with white (fall experiment) or black (spring experiments) polyethylene mulch. Each plot consisted of a single 10-plant row. Transplants of each crop were set March 22 and October 29 in 1991 and April 17 in 1992 and replicated four times in randomized complete blocks designs. Each block contained a 10-plant plot for each host crop. Beginning 2 wk after transplanting in 1991 and 3 wk in 1992 and continuing until 8 wk after transplanting, the top of each plant was tapped three times with a 30.5-cm garden stake over a vegetable oil-coated cake pan and the numbers of B. argentifolii adults dislodged and trapped in the oil were counted. Counts were averaged per plant. In 1992, one lower leaf of each plant was collected 4, 6, and 8 wk after transplanting and the numbers of immature lifestages of B. argentifolii were counted on an 8.0-cm diameter disk (50 cm 2 ) from each leaf. Counts were averaged per 50 cm 2. Variances were determined to be homogeneous using Bartlett s test; therefore, no transformation was used on the data. Data for all experiments were subjected to analyses of variance using the general linear models procedure of SAS (SAS Institute Inc. 1989) and, where significant F values were obtained, means were separated with the least significant difference. Results and Discussion Screenhouse experiments. In the first experiment, squash appeared to be the only crop more preferred than tomato, as indicated by the greater numbers of eggs and crawlers present per plant (Table 1); however, when considering the numbers of eggs and crawlers/cm 2 of foliage, no crop was more preferred than tomato. Eggplant had greater numbers of eggs and nymphs/cm 2 of foliage and was, thus, more preferred, than squash, cucumber, bean, or okra. Nevertheless, squash was a greater sink for ovipositing whitefly females than was tomato, that is, more eggs and crawlers accumulated on squash plants. This may have resulted at least in part because squash plants grew at a faster rate than did tomato plants, that is, plants that were approximately the same size at the beginning of

4 62 J. Agric. Urban Entomol. Vol. 20, No. 2 (2003) Table 1. Mean (± SE) a leaf area and numbers of eggs and crawlers present on foliage of selected vegetable host plants following exposure to Bemisia argentifolii adults in a free-choice, screenhouse experiment, GCREC, Host plant Mean leaf area (cm 2 )/plant Mean no./plant No. eggs and crawlers Mean no./cm 2 leaf area Squash ± 18.3ab ± 304.7a 4.9 ± 1.3bc Eggplant 63.6 ± 6.4c ± 167.2ab 10.4 ± 2.3a Cucumber ± 10.2b ± 107.7abc 5.2 ± 1.7b Bean ± 9.5a ± 237.0abc 3.1 ± 1.6bc Tomato 55.6 ± 6.1c ± 92.4bc 6.4 ± 2.1ab Okra 76.6 ± 14.6c 76.8 ± 23.3c 0.9 ± 0.1c F df 5, 50 5, 54 5, 50 P < LSD a Means followed by the same letter are not significantly different (P < 0.05; LSD. LSD least significant difference). the experiment were greatly different in leaf area when the experiment was completed. In the second experiment, the number of adults/plant did not differ among the crop plants 3 d after initiating the experiment (F 2.50; df 3,6; P 0.16; Fig. 1A); however, 8 d later, significantly more adults were present on plants of squash than on plants of any of the other crop plants (F 6.73; df 3,6; P 0.02). By 19 d after exposing the plants to whitefly adults, the number of adults/plant once again did not differ among the crop plants (F 2.03; df 3,4; P 0.25). On the basis of the number of adults/leaf, there were no differences among the crops and no crop plant appeared more preferred than tomato 3 (F 3.62; df 3,6; P 0.08), 11 (F 3.61; df 3,6; P 0.08), or 19 d (F 2.51; df 3,4; P 0.20) after initiating the experiment (Fig. 1B). Again, these results can be attributed at least in part to the differences in growth rate (Fig. 1C). The numbers of leaves per plant were similar for all crop plants 3 d after initiating the experiment (F 4.00; df 3,6; P 0.07), but by the eleventh day, squash plants had significantly more leaves than did plants of the other host plants (F 46.82; df 3,6; P ). The differences in the numbers of leaves between squash and tomato were not significant after 19 d (F 7.65; df 3,4; P 0.04). Field experiments. Significant differences among crop hosts were detected on all sampling dates in all field experiments (Table 2). The numbers of B. argentifolii adults dislodged per squash plant were always significantly greater than the number dislodged per tomato plant on all sampling dates in all three field experiments (Figs. 2 & 3). For the other crop plants, a significant difference relative to tomato was observed only on the sixth week after transplanting for eggplant in the spring of 1992 (Fig. 3). The numbers of adults present on the

5 SCHUSTER: Bemisia Preference for Vegetable Hosts 63 Fig. 1. The number of adults of Bemisia argentifolii per plant (A) and per leaf (B) and the number of leaves per plant (C) of selected host plants when the whiteflies were given a choice of the hosts in a screenhouse in the summer of 1991 at GCREC, Bradenton, Florida.

6 64 J. Agric. Urban Entomol. Vol. 20, No. 2 (2003) Table 2. Results of statistical analyses of the numbers of adult Bemisia argentifolii dislodged in beat pan sampling and the numbers of nymphs on foliage of selected host plants grown in the field, GCREC, Bradenton, Florida. Statistic a Weeks after transplanting Spring 1991, no. adults/plant F P < < Fall 1991, no. adults/plant F P < < < Spring 1992, no. adults/plant F P < < < Spring 1992, no. nymphs/50 cm 2 F P a The df for all of the experiments were 3, 9.

7 SCHUSTER: Bemisia Preference for Vegetable Hosts 65 Fig. 2. The number of adults of Bemisia argentifolii dislodged in beat pan sampling of selected host plants grown in the field in the spring (top) and fall (bottom) of 1991 at GCREC, Bradenton, Florida. An * indicates the mean is significantly different from that of tomato. plants for the first 2 4 wk after transplanting were largely from dispersing individuals. Thereafter, the number of immigrant adults would be expected to be supplemented by the numbers of adult progeny of eggs deposited earlier. In 1992 significantly more nymphs/50 cm 2 leaf area were observed for squash than tomato on all sampling dates, particularly 6 and 8 wk after transplanting. This probably would account for the sharp increase in the numbers of adults observed on squash plants after the sixth week after transplanting, which would suggest that a large proportion of the emergent adults preferred to stay on the squash plants. On the basis of the numbers of whiteflies per leaf or per leaf area, no crop plant appeared more preferred than tomato; however, more whitefly adults or immature lifestages were consistently observed on a per plant basis for squash than for tomato. The same could not be said of any other crop in this study. The results

8 66 J. Agric. Urban Entomol. Vol. 20, No. 2 (2003) Fig. 3. The number of adults of Bemisia argentifolii dislodged in beat pan sampling (top) and the numbers of nymphs on foliage of selected host plants (bottom) grown in the field in the spring of 1992 at GCREC, Bradenton, Florida. An * indicates the mean is significantly different from that of tomato. with squash corroborate the observations of Simmons (1994) and could be the result of the rapid growth and resulting greater leaf area of squash plants relative to tomato plants. Whatever the reason for more whiteflies on squash, from a biological and practical basis, squash is more of a sink for whitefly adults than tomato. This has implications for whitefly management. Squash could be useful as a trap crop by attracting and holding whitefly adults, thus keeping them from moving to tomato.

9 SCHUSTER: Bemisia Preference for Vegetable Hosts 67 Acknowledgments The author thanks Emily Vasquez for assistance in preparing the graphics for publication. This research was supported by the Florida Agricultural Experiment Station, and approved for publication as Journal Series No. R References Cited Al-musa, A Incidence, economic importance, and control of tomato yellow leaf curl in Jordan. Plant Dis. 66: Arias, R. & L. Hilje Uso del frijol como cultivo trampa y de un aceite agrícola para disminuir la incidencia de virosis transmitida por Bemisia tabaci (Gennadius) en el tomate. Manejo Integrado de Plagas 27: Blua, M. J., H. A. Yoshida & N. C. Toscano Oviposition preference of two Bemisia species (Homoptera: Aleyrodidae). Environ. Entomol. 24: Butler, G. D., D. L. Coudriet & T. J. Henneberry Sweetpotato whitefly: host plant preference and repellent effect of plant-derived oils on cotton, squash, lettuce and cantaloupe. Southwestern Entomol. 14: Chu, C.-C., T. J. Henneberry & A. C. Cohen Bemisia argentifolii (Homoptera: Aleyrodidae): host preference and factors affecting oviposition and feeding site preference. Environ. Entomol. 24: Foda, M. E Population dynamics, host preference and seasonal distribution patterns of whitefly, Bemisia tabaci (Genn.), in Middle Egypt, pp In Beltwide Cotton Conferences, Memphis, TN. Liu, T.-X. & R. D. Oetting Oviposition preference of Bemisia tabaci (Gennadius) on eight species of greenhouse-grown plants. J. Agric. Entomol. 11: Palumbo, J. E., A. R. Horowitz & N. Prabhaker Insecticidal control and resistance management for Bemisia tabaci. Crop Protection 20: Peralta, L. & L. Hilje Un intento de control de Bemisia tabaci con insecticidas sistémicos incorporados a la vainica como cultivo trampa, más aplicaciones de aceite en el tomate. Manejo Integrado de Plagas 30: Polston, J. E. & P. K. Anderson The emergence of whitefly-transmitted geminiviruses of tomato in the Western Hemisphere. Plant Dis. 81: Polston, J. E., R. J. McGovern & L. G. Brown Introduction of tomato yellow leaf curl virus in Florida and implications for the spread of this and other geminiviruses of tomato. Plant Dis. 83: SAS Institute Inc SAS/STAT User s guide, Version 6, 4th ed., Vol. 2. SAS Institute Inc., Cary, North Carolina, 846 pp. Schuster, D. J., T. F. Mueller, J. Kring & J. F. Price Relationship of the sweetpotato whitefly to a new tomato fruit disorder in Florida. HortScience 25: Schuster, D. J., J. E. Funderburk & P. A. Stansly IPM in tomatoes, pp In D. Rosen, J. L. Capinera and F. D. Bennet [eds], Integrated Pest Management A Florida Perspective. Intercept. Ltd, Andover, Hants, UK. Simmons, A. M Oviposition on vegetables by Bemisia tabaci (Homoptera: Aleyrodidae): temporal and leaf surface factors. Environ. Entomol. 23: Stansly, P. A., T.-X. Liu & C. S. Vavrina Response of Bemisia argentifolii (Homoptera: Aleyrodidae) to imidacloprid under greenhouse, field and laboratory conditions. J. Econ. Entomol. 91: Yee, W. L. & N. C. Toscano Ovipositional preference and development of Bemisia argentifolii (Homoptera: Aleyrodidae) in relation to alfalfa. J. Econ. Entomol. 89:

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