BREEDING, CULTIVARS, ROOTSTOCKS, & GERMPLASM RESOURCES

HORTSCIENCE 29(7):814-817. 1994. (except the first three weeks of May). Height. diameter, and number of leaves of each plant were also recorded. Counts of whitefly nymphs Response of oleracea L. to were taken from one randomly selected leaf from the lower third of each plant on 19 May Bemisia tabaci (Gennadius) and 10 June. On 2 June, a color reading was made on the upper surface of a randomly K.D. Elsey1 and M.W. Farnham2 selected leaf from the upper third of each plant U.S. Vegetable Laboratory, U.S. Department of Agriculture, Agricultural with a chromameter (model CR-200; Minolta, Research Service, 2875 Savannah Highway, Charleston, SC 29414 Ramsey, N.J.). Data in this and other experi- ments were subjected to analyses of variance Additional index words. cole crops, , , , , , brussels and means were separated using a general sprouts, sweetpotato whitefly linear models procedure together with the least significant difference test at P £ 0.05. Abstract. The relative resistance of 18 cultivars of L. to attack by the Field test. In a separate field test, con- sweetpotato whitefly [Bemisia tabaci (Gennadius)] was studied in screen cage (spring), ducted during late Summer and Autumn 1992, field (autumn), and laboratory tests. The B. oleracea entries consisted of six types, all of the B. oleracea groups and cultivars used including 16 green and two red cultivars. Cabbage (Capitata Group) and broccoli in the spring study (with the exception of ‘Rio (Boytrytis Group) were less infested than other crops in a screen cage test, with kale, Verde’ cabbage substituting for ‘Golden Acre’) collard (Acephala Group), and brussels sprouts (Germmiter Group) experiencing rela- were included. In this test, we relied on natu- tively high and kohlrabi (Gongtlodes Group) intermediate infestations. Relative ranking rally occurring populations of whiteflies to of crops was similar in an autumn field study, with the exception of brussels sprouts, which infest the plants. Plants were seeded in the had an intermediate level of infestation. Differences in numbers of whiteflies among greenhouse on 29 July and transplanted to the cultivars within crops were negligible or inconsistent, except that red cultivars of brussels field on 3 Sept. The plot area was not fumi- sprouts (‘Rubine’) and cabbage (‘Red Acre’) were much less infested than green cultivars. gated, but plots were fertilized as previously In a laboratory test, differences of whitefly oviposition and nymphal survival and described for the screen cage study. Weekly development were small, indicating that nonpreference factors, rather than antibiosis, are measurements of whitefly populations and the best explanations for differences in the numbers of whiteflies among the B. oleracea plant traits were also taken as described for the cultivars that were tested, screen cage study conducted in spring and were recorded for each plant beginning 8 Sept. The sweetpotato whitefly has recently ex- presence or lack of waxy bloom on the leaf and ending 28 Oct. In both outdoor tests, the panded its host range and increasingly has surface can result in different color and ap- cumulative insect days (Johnson et al., 1992; damaged Brassica oleracea. In California, pearance characteristics that have been found Ruppel, 1983) per plant were calculated from damage has been particularly severe in broc- to affect levels of insect infestation (Eigenbrode the weekly adult counts. This statistic com- coli and (Perring et al., 1991), and and Shelton, 1990; Radcliffe and Chapman, bined the number of insects present and the in southern Texas, it has been severe in cab- 1966). time they persist, and it provides a better bage (Committee on Agriculture, U.S. House Our objective was to investigate the effect measure of their overall impact than weekly of Representatives, 1992). These whitefly at- of various crops, cultivars, and color forms of density records. The design and number of tacks have caused economic hardship not only B. oleracea on levels of whitefly infestations experimental units were as previously de- because of direct injury to the crop but also on plants grown in screen cage and field ex- scribed for the spring, screen cage study. because of the monetary loss from decreased periments. In the laboratory, we tested whether Laboratory test. Cultivars used in the screen marketing opportunities. In addition, whitefly the differences observed in the screen-cage cage and field experiments were tested for infestations of vegetable can lead to and field tests were due to nonpreference fac- their effects on oviposition and whitefly nymph an increase of whitefly populations on warm- tors, antibiosis, or both. survival and development in a no-choice labo- weather crops such as cotton (Gossypium ratory test. When greenhouse-grown plants hirsutum L.) and cucurbits by providing a Materials and Methods had five true leaves, they were transplanted to refuge for breeding and development during 800-cm3 clay pots and moved to a controlled- the winter months (Committee on Agricu- Six groups of B. oleracea were tested in environment room held at a constant 25+ 2C, lture, U.S. House of Representatives, 1992). this study: kale and collard, cabbage, broccoli, photoperiod of 12h light: 12 h dark, and alight Brassica oleracea is a polymorphic spe- kohlrabi, and brussels sprouts. Each crop was intensity of 120 µmol•m-2•s-1. The design was cies that provides a variety of vegetables for represented by three cultivars. a split-plot with crops as main plots and culti- human consumption. The various crops of this Screen cage test. For the screen cage test, vars as subplots. Each of the five replications species represent diverse botanical varieties plants were seeded in a greenhouse on 1 Mar. included one plant per cultivar. Five whitefly that produce distinct harvestable plant parts 1992 into a commercial peat mixture. On 1 females were placed in a clip-on sandwich and exhibit unique morphologies. Differences Apr., seedlings were transplanted into a 40 x cage 1.7 cm in diameter (Lewis, 1973) on the in anthocyanin intensity in the foliage and the 20 × 3.4-m, outdoor screen cage. The plot area youngest leaf on which a cage would fit. After consisted of single rows on raised beds 1 m 24 h, the cage and females were removed and Received for publication 22 Oct. 1993. Accepted for apart with 0.7-m spacing between plants in a the eggs counted. The eggs began to hatch publication 27 Jan. 1994. Mention of a trademark, row. This area was fumigated with methyl after 1 week, at which time the total number of proprietary product, or vendor does not constitute a bromide and fertilized at the rate of 1135 kg first-stage nymphs was determined. When guarantee or warranty of the product by the U.S. 10N–10P2O5–10K2O/ha before planting. Plots adults began to eclose, the number of empty Dept. of Agriculture, and does not imply its approval were sidedressed with NH4NO3 as recom- pupal cases was counted daily until eclosion to the exclusion of other products or vendors that mended (Cook and Ezell, 1983). The design ceased. Nymphal mortality on a plant was might also be suitable, We gratefully acknowledge was a randomized complete block with four calculated from the number of newly hatched the technical assistance of Louise Cauthen, Thomas replicates per treatment. Crops were random- nymphs minus the number of empty pupal McFadden, and Eric Gomperts. The cost of publish- ing this paper was defrayed in part by the payment of ized within each block and cultivars were cases. page charges. Under postal regulations, this paper nested within respective crops. Each replicate therefore must be hereby marked advertisement consisted of three plants per cultivar. On 15 Results and Discussion solely to indicate this fact. Apr., »10,000 whitefly adults were released 1Research Entomologist. into the screen cage. From 17 Apr. to 16 June, In the screen cage study, the number of 2Research Geneticist. adult whiteflies per plant were counted weekly released whitefly adults gradually declined

814 HORTSCtENCE, VOL. 29(7), JULY 1994 (Table 1), and by early May, only immatures fly counts were highest on kale, brussels and collard again had more whitefly adults and were present on the plants. Adults from this sprouts, and collard; counts were usually lower higher cumulative insect days than other crops, generation began to emerge in late May, and on broccoli, kohlrabi, and cabbage (Table 1). although broccoli and cabbage harbored the the whitefly population increased for the dura- This difference was particularly evident in lowest populations (Table 2). Contrary to ob- tion of the experiment as the temperature in- comparisons of cumulative insect days for the servations in the screen cage experiment where creased. In contrast, the numbers of naturally six crops (Table 1). Additionally, fewer white- brussels sprouts had high whitefly populations occurring adult whiteflies were relatively con- fly nymphs were found on cabbage and broc- (Table 1), the number of whiteflies were inter- stant in the field experiment (Table 2). coli by 16 June than on the other four crops mediate on autumn-grown brussels sprouts In the screen cage experiment, adult white- (Table 3). In the autumn field experiment, kale (Table 2).

Table 1. Mean number of adult whiteflies per plant on Brassica oleracea crops and cultivars grown in screen cage experiment (spring).

z Mean separation in columns for crops by LSD test at P £ 0.05, y Mean separation of individual cultivar within each crop by LSD test at P £ 0.05.

Table 2. Mean number of adult whiteflies per plant on Brassica oleracea crops and cultivars grown in field experiment (autumn).

HORTSCIENCE, VOL. 29(7), JULY 1994 815 B REEDING, CULTIVARS, ROOTSTOCKS, & GERMPLASM R ESOURCES

Variation exhibited by cultivars within numerous on brussels sprouts in the autumn fly infestations occurring on collard and kale crops depended on the crop group (Tables 1 field test; even so, ‘Rubine’ had significantly and low ones on broccoli and cabbage. Also, and 2). No differences in cumulative insect fewer whiteflies than ‘Catskill’ or ‘Jade’ (Table whitefly populations were low on red cultivars days (P £ 0.05) were found among broccoli, 2). in both outdoor tests. kohlrabi, or kale cultivars in either test, al- Consistent and significantly different white- There was little difference in oviposition though adult counts on some dates were sig- fly populations also occurred among cabbage by whiteflies isolated by clip cages on leaves nificant. The three collard cultivars consisted cultivars. Similar to our brussels sprouts ob- of B. oleracea crops and cultivars grown in a of ‘Vates’ and ‘Morris Heading’, cultivars servations, the red ‘Red Acre’ cabbage was the controlled environment (Table 4). This result with normal waxy bloom on foliage, and ‘Green cabbage least preferred by whiteflies as well indicates that once female whiteflies were Glaze’, a cultivar with leaves exhibiting a as the least preferred of all cultivars in both brought into contact with foliage, there were “glossy” appearance because of less waxy outdoor tests (Tables 1 and 2). Fewer nymphs no chemical or physical factors present to bloom. per leaf also were present on ‘Red Acre’ than deter egg laying under our experimental con- Low amount of waxy bloom has been linked on any other cultivar (Table 2). ditions. Survival of nymphs was high among with resistance to diamondback moth, im- Whitefly populations were higher on brus- all cultivars, although some significant differ- ported cabbage worm, and cabbage whitefly sels sprouts relative to the other crops in the ences occurred among crops (Table 4). The (Stoner, 1992; Thompson, 1963). Although screen-cage test (Table 1) than in the autumn length of nymphal development differed only not usually statistically significant, ‘Green field test (Table 3). A comparison between the slightly among crops. The two red cultivars Glaze’ had fewer whiteflies than the other two smaller plants and the other Red Acre cabbage and Rubine brussels sprouts, cultivars on all dates in the screen cage and on cole crops in the autumn study may account found to have such low densities of whiteflies some dates in the field test (Tables 1 and 2). for the reduction in whitefly infestation. How- in the previous two tests, differed little from Significantly fewer whitefly nymphs were ever, the respective environments of the spring other cultivars in oviposition, survival, or de- found on ‘Green Glaze’ (21.8 per leaf) com- and autumn trials possibly conditioned plants velopment. Optimally, whitefly antibiosis tests pared to ‘Vates’ (83.3) and ‘Morris Heading’ so that the relative resistance of crops was such as these would also be conducted under (85.5) in the 10 June count. altered. There is considerable evidence that field conditions. However, considering the The greatest differences in whitefly counts environmental conditions (e.g., temperature) difficulty of eliminating contamination by natu- occurred among the brussels sprout cultivars. can affect plant resistance to insect attack rally occurring whiteflies and their natural ‘Catskill’ and ‘Jade’ suffered the heaviest cu- (Tingey and Singh, 1980). Although our two enemies in the greenhouse or field, we chose mulative insect days over all cultivars in the outdoor tests were conducted in different sea- to use controlled conditions. At the same time, screen cage experiment. In contrast, ‘Rubine’, sons, the temperature and moisture conditions we are aware that the production of chemicals a red cultivar, had the third lowest cumulative to which plants were subjected were similar. repellent or toxic to whiteflies may occur to a population (Table 1). Whiteflies were not as Average spring and autumn temperatures for greater degree in one environment than in the durations of the tests were 22 and 20C, another. The lack of evidence for antibiosis in Table 3. Number of whitefly nymphs on Brassica respectively. In addition, soil moisture condi- the laboratory is not entirely surprising, be- crops during screen cage experiment. tions were maintained at an optimum in both cause examples of resistance involving white- seasons by supplementing rainfall with irrig- flies and most cases of cole crop resistance to ation. The photoperiod was the environmental insect pests involve antixenosis rather than condition that varied the most between tests, antibiosis (Gerling, 1990; Maxwell and and this difference cannot be ruled out as a Jennings, 1980). possible factor altering relative resistances. Unlike the laboratory test, in which white- With the exception of observations of the fly adults were confined to specific plants, relative resistance of brussels sprouts in the whiteflies in the screen cage and field tests autumn field study, results of the spring and were free to select plants on which to alight z Mean separation within columns by LSD at P £ 0.05. autumn studies were similar, with high white- and become established. In these situations, nonpreference mechanisms such as visual cues and plant odors affect whitefly choices. Of Table 4. Oviposition, survival, and development of immature whiteflies on Brassica crops and cultivars. these, vision is of primary importance in white- flies and is used for discrimination of shapes, sizes, and colors (Vaishampayan et al., 1975a, 1975b; van Lenteren and Noldus, 1990). In outdoor tests, the largest differences in white- fly counts among cultivars appeared to be a response to color. Color reading of the selected cultivars with the chromameter provided an objective mea- sure of color values on the Hunter L, a, and b scale (Hunter and Harold, 1987). The tristimulus values considered, a and b, match the color stimulus considered. The red leaf cultivars Rubine brussels sprouts and Red Acre cabbage had significantly lower b values (closer to blue) and higher a values (closer to red) than two of their normal-colored counter- parts, and they had consistently lower whitefly counts (Table 5). Whiteflies are attracted to yellow or yellow-green in laboratory and field tests (Berlinger, 1980; Husain and Trehan, 1940; Mound, 1962). Mound (1962) found that whiteflies were attracted by blue and ultraviolet light. However, Mound theorized zMean separation in columns for crops followed by LSD test at P £ 0.05. that this was shortwave, light-induced, migra- yMean separation of individual cultivars within each crop by LSD test at P £ 0.05. tory behavior and would direct whitefly flight

816 HORTSCIENCE, VOL. 29(7), JULY 1994 Table 5. Differences in number of whitefly adults, (Butler et al., 1986) unfit or unavailable for Husain, M.A. and K.N. Trehan. 1940. Final report and a and b color values (2 June 1992). feeding and oviposition. on the scheme of investigations on the whitefly Due to the significant damage that white- on cotton in the Punjab. Ind. J. Agr. Sci. 10:101– flies can inflict on cole crops, further study of 109. plant characters, such as red or glossy foliage, Johnson, M.W., L.C. Cario, J.A. Coughlin, B.E. Tabashnik, J.A. Roseheim, and S.C. Welter. is warranted to evaluate the potential of using 1992. Effect of Trialeurodes vaporariorum such characters to minimize whitefly infesta- (Homoptera: Aleyrodidae) on yield of fresh tions. Altieri and Schmidt ( 1987) showed that market tomatoes. J. Econ. Entomol. 85:2370- mixed plantings of different broccoli cultivars 2376. experienced lower cabbage aphid infestation Lewis, T. 1973. Thrips, their biology, ecology and than uniform cultivar plantings. Although the economic importance. Academic, New York. zPaired comparisons between Catskill and Rubine, resistance associated with red foliage described Maxwell, F.G. and P.R. Jennings (eds.). 1980. Breed- and Golden Acre and Red Acre for mean adults and in this study may not be transferable to green- ing plants resistant to insects. Wiley & Sons, a and b tristimulus values significantly different at P colored cultivars, it is possible that mixed New York. Mound, L.A. 1962. Studies on the olfaction and £ 0.05. plantings of red and green ctdtivars might yMean number of whitefly adults. colour sensitivity of Bemisia tabaci (Germ.) provide a management strategy for reducing (Homoptera, Aleyrodidae). Entomol. Expt. & whitefly infestations. Appl. 5:99-104. toward the sky rather than foliage; there- Literature Cited Perring, T. M., A. Cooper, D.J. Kazmer, and C. fore, it would not be involved in host find- Shields. 1991. New strain of sweet potato white- ing. Burrows et al. (1983) studied visual at- Altieri, M.A. and L.L, Schmidt. 1987. Mixing broc- fly invades California vegetables. Calif. Agr. traction in the potato aphid and found that coli cultivars reduces cabbage aphid numbers. 45:10-12, attractiveness could be expressed as a yellow Calif. Agr. Nov.-Dec. 41:24-26. Radcliffe, E.B. and R.K. Chapman. 1966. Varietal Berlinger, M.J. 1980. A yellow sticky trap for white- resistance to insect attack in various cruciferous : blue wavelength distimulus ratio, with higher flies: Trialeurodes vaporariorum and Bemisia crops. J. Econ. Entomol. 59: 120-125, ratios being more attractive. Whether a similar tabaci (Aleyrodidae), Entomol. Expt. & Appl. Ruppel, R.F. 1983. Cumulative insect-days as an color preference with whiteflies exists at dif- 27:98-102, index of crop protection. J. Econ. Entomol. ferent wavelengths is not known. However, Burrows, P. M., O.W. Barnett, and M.T. Zimmerman. 76:375–377, foliage that reflects peak wavelengths in the 1983. Color attraction and perception in Stoner, K.A. 1992. Density of imported cabbage- red or blue-green clearly is not attractive to the Macrosiphum euphorbae. Can. J. Zoology worms (Lepidoptera: Pieridae), cabbage aphids flies. 61:202-210. (Homoptera: Aphidae), and flea beetles (Co- The visual response to shape and size of Butler, G. D., Jr., T.L. Henneberry, and W.D. leoptera: Chrysomelidae) on glossy and tri- plants also may influence insect attraction. Hutchinson. 1986. Biology, sampling and popu- chome-bearing lines of Brassica oleracea. J. lation dynamics of Bemisia tabaci, p. 167-196. Econ. Entomol. 85: 1023–1 030. Elsey (unpublished) found that the number of In: G.E. Russell (ed.). Agricultural zoology re- Thompson, K.F. 1963. Resistance to the cabbage whiteflies landing on collard plants during 24 views, vol. 1. Intercept, Ponteland, Newcastle- aphid (Brevicoryna brassicae) in brassica plants. h was correlated with plant size. An aphid pest upon-Tyne, England. Nature 198:209. of carrots (Dancus carota L.) was found to Committee on Agriculture, U.S. House of Repre- Tingey, W.M. and S.R. Singh. 1980. Environmental settle in numbers proportional to the area of sentatives. 1992. Economic damage caused by factors influencing the magnitude and expres- foliage available to them (Dunn, 1969). In our the sweetpotato whitefly. Serial no. 102-171. sion of resistance, p, 87–1 14. In: F.G. Maxwell work, the use of regression analysis to detect Cook, W.P. and D.O. Ezell. 1983. Commercial and P.R. Jennings (eds.). Breeding plants resis- an association between the number of whitefly broccoli production in South Carolina. Clemson tance to insects. Wiley & Sons, New York. adults with plant dimensions was ambiguous. Univ. Coop. Ext. Serv. Hort. Lflt. 52. Vaishampayan, S.M., M. Kogan, G.P. Waldbauer, Dunn, J.A. 1969. The colonization by Cavriella and J.T. Woolley. 1975a. Spectral specific re- The most efficient linear regression model [by aegopodii of carrot plants of different sizes. sponses in the visual behavior of the greenhouse R’ selection method (Freund and Lettell, 1991)] Proc. Assn. Applied Biol. 63:318-324, whitefly, Trialeurodes vaporariorum included the variables plant diameter and leaf Eigenbrode, S.D. and A.M. Shelton. 1990. Behavior (Homoptera: Aleyrodidae). Entomol. Expt. & count. This model usually resulted in a signifi- of neonate diamondback moth larvae (Lepi- Appl. 18:344-356. cant regression, but the percentage of this doptera Plutellidae) on glossy-leafed resistant Vaishampayan, S. M., G.P. Waldbauer, and M. variation explained by the model varied from Brassica oleracea L. Environ. Entomol. Kogan. 1975b, Visual and olfactory responses negligible to 40%. 19:1566-1571. in orientation of plants by greenhouse whitefly, Apart from antixenosis factors, gross struc- Freund, R.J. and R.C. Lettell. 1991. SAS system for Trialeurodes vaporariorum (Homoptera: tural differences among the crops may have regression, 2nd ed. SAS Institute, Cary, N.C. Aleyrodidae). Entomol. Expt. & Appl. 18:412– Gerling, D. (ed,). 1990. Whiteflies: Their bionom- 422. contributed to differences in whitefly counts. ics, pest status and management. Intercept, van Lenteren, J.C. and L.P.J.J. Noldus. 1990. White- For example, fewer whiteflies were found on Andover, Hants, U.K. fly-plant relationships: Behavioral and ecologi- cabbage than the other crops. This may be due Hunter, R.S. and R.W. Harold. 1987. The measure- cal aspects. In: D. Gerling (ed.). Whiteflies: in part to the head formation in cabbage that ment of appearance. 2nd ed. Wiley & Sons, New Their bionomics, pest status and management, renders the favored upper portion of the plant York. Intercept, Andover, Hants, U.K.

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