BIOLOGY OF Bemisia tabaci (GENN.) B-BIOTYPE AND PARASITISM BY Encarsia formosa (GAHAN) ON COLLARD, SOYBEAN AND TOMATO PLANTS

The silverleaf whitefly Bemisia tabaci (Genn.) B-biotype (= B. argentifolii) (Hemiptera: Aleyrodidae) is a polyphagous insect attacking many plant species of economic importance. A comparison study was conducted on the duration of the egg-to-adult period, and the percentage of hatching eggs of Bemisia tabaci (Genn.) B-biotype on collard (Brassica oleracea L. var. acephala D.C.), soybean (Glycine max (L.) Merr.) and tomato (Lycopersicon esculentum Mill.) plants, as well as the egg-to-adult period of Encarsia formosa (Gahan) on the 1, 2, 3 and 4 whitefly nymphal instars on these three plant species. The experiments were conducted in a laboratory (25oC, 70 ± 10% RH, 14-hour photophase). The duration of the egg-to-adult period of B. tabaci was 19.8 days on collard, 21.2 days on soybean and 22.0 days on tomato. The number of hatched eggs was higher on collard when compared to soybean and tomato plants. Concerning E. formosa regardless of plant species, the duration for the egg-to-adult period was shorter for the 3 and 4 instar nymphs as compared with the other instars.


INTRODUCTION
The silverleaf whitefly Bemisia tabaci (Genn.) B-biotype (= B. argentifolii) (Hemiptera: Aleyrodidae) is a polyphagous insect attacking many plant species of economic importance, such as vegetables, oil and ornamental plants (Oliveira et al., 2001). The intensive use of chemicals in crop management, together with the high reproductive potential of this insect are considered the reasons why B. tabaci B-biotype reached the status of important pest species (Brown et al., 1995). According to Lima et al. (2000), B.tabaci is known as a pest problem in all of the Brazilian states.
Chemical control (mainly with neonicotinoids and insect growth regulators) is currently the method available. However, the prevalent use of these insecti-cides may cause problems related to insect resistance, environmental pollution and residues in crop products. These concerns have led to alternative methods of control, including the biological control of B. tabaci with the parasitoid Encarsia formosa (Gahan) (Hymenoptera: Aphelinidae). This parasitoid is probably the most worldwide used for the control of Trialeuroides vaporariorum (Westwood) and Bemisia spp. in greenhouses (Hoddle et al., 1998). However, there is limited information on the laboratory rearing of this beneficial insect (Hu et al., 2002). Biological parameters are important to ascertain the role of natural enemies in the management of recently introduced pest species mainly when focusing on their natural enemies. Therefore, the objectives of this research were to determine the duration of the egg-to-adult developmental period and the percentage of hatching eggs of B. tabaci Bbiotype on collard, soybean and tomato plants, as well as the egg-to-adult period of E. formosa (Gahan) on the 1 st , 2 nd , 3 rd and 4 th whitefly nymphal instars on these three plant species.

Biological parameters of B. tabaci B-biotype
A whitefly population of B. tabaci B-biotype, previously identified by Dr. Judith K. Brown, University of Arizona, USA, was provided by the "Instituto Agronômico de Campinas (IAC)", São Paulo, Brazil. This population was then maintained on poinsettia in a greenhouse protected by a 0.2 × 0.2 mm mesh screen. Plants of soybean (cultivar IAC-15), tomato (cultivar Santa Clara) and collard (30 cm high) were infested with 30 adults of B. tabaci B-biotype per plant. The insects were collected by aspirating them with a straw with one of the ends closed with cotton.
A total of 30 plants of each species were infested and maintained in plastic cages (plastic pet covered with voile). After 24 hours the leaves containing 30 eggs of B. tabaci B-biotype were cut in discs (40 mm diameter) which were placed on top of an agar + nipagin layer in plastic dishes (60 × 20 mm) with a lid on top. The duration of the egg-to-adult period and the number of hatched eggs on each plant species were evaluated in laboratory conditions (25ºC; 70 ± 10% RH; 14-hour photophase). A randomized experimental design was set up with the parcel represented by one plant of each host species with 30 replications. The results were subjected to the analyses of variance and the means were compared by the Tukey's test (p ≤ 0.05).

Biological parameters of E. formosa on B. tabaci B-biotype
One couple (a male and a female) of E. formosa was placed in each plastic dish (60 × 20 mm) for a 24 hour period, with 30 replications for each nymphal instar of B.tabaci B-biotype on all the plants tested. The dishes were maintained in laboratory conditions (25ºC; 70 ± 10% RH; 14-hour photophase). The life cycle of E. formosa parasitizing the four nymphal instars of B. tabaci B-biotype was evaluated daily. The percentages of parasitism were evaluated for whiteflies on each plant species. The experimental design was a randomized factorial scheme (4 × 3) with 30 replications. The treatments were the nymphal instars of B. tabaci B-biotype on collard, soybean and tomato plants. To determine the effect of each factor, the analysis of variance (F test; p ≤ 0.05), was performed and the means between the nymphal instars of the pest and the plant species were evaluated by using the Tukey's test (p = 0.05).

Developmental time of B.tabaci B-biotype
The developmental time from egg-to-adult of Bemisia tabaci B-biotype was 19.8 days on collard, 21.2 days on soybean and 22.0 days on tomato (Table  1). Simmons (2002) evaluated five host plant species of B. tabaci B-biotype and observed that collard was the most attractive among those species for nymphs to establish and feed. That information supports our results that collard provided a shorter egg-to-adult cycle and is a good host plant for the development of this whitefly. Salas & Mendoza (1995) reported that the egg-to-adult period of B. tabaci on tomato leaves at 25ºC and 65% RH is 22.3 days, which is a similar value to that observed in our research (22.0 days). Conversely, Villas-Bôas et al. (2002) reported the devel-  (2002) who observed 70.9 days at 15ºC, 21.8 days at 30ºC, and 64% and 90% viability, respectively. The mean number of whitefly nymphs on collard was higher than those observed for soybean and tomato, although the values did not differ between them (Table 1). Collard was the host plant on which B. tabaci presented the lowest life cycle (19.8 days) and the highest mean number of hatched eggs (90.2). Also, this species provided the longest durability. Therefore, this plant is the most suitable among the ones tested for the development of B. tabaci B-biotype when dealing with laboratory rearing of this whitefly.

Biological features of E. formosa on B. tabaci Bbiotype
The period of egg-to-adult of E. formosa on the first and second whitefly instars did not differ, either on collard or on tomato plants (Table 2). However, on the soybean plant the developmental period on the first instar nymph was higher than the observed on the second instar (Table 2). This period was higher on third instar nymphs when compared to fourth instar ones on collard plants, but no difference was observed on soybean and tomato concerning these two instars. Among the three plant species, the egg-to-adult periods of E. formosa were shorter on third and fourth instar nymphs, thus indicating a better performance for development of this parasitoid on these nymphal instars of B. tabaci B-biotype.
Regarding the first and second instar nymphs, the egg-to-adult periods on collard and on tomato plants were lower than that observed on soybean plants. In all of the evaluated plant species no difference was detected in the egg-to-adult periods of E. formosa on third instar nymphs of B. tabaci B-bio-type. However, on fourth instar nymphs, the developmental period on collard was lower than those observed on soybean and tomato plants, but no difference was detected between these two last ones.
Because different tritrophic interactions were involved, it is not fair to make a direct comparison between our results with those obtained from studies dealing with different species of whiteflies and host plants. The developmental period of E. formosa parasitizing the four nymphal instars of T. vaporariorum at 25ºC was 15 days on tobacco (Arakawa, 1982) and 15 days on tomato plants (Burnett, 1949). The eggto-adult period of Encarsia transversa on B. tabaci at 15ºC and 30ºC and 70 to 75% RH, ranged from 11.3 to 15.1 days for the females and from 12.1 to 14.6 days for the males (Anthony et al., 2003). Woets & Lenteren (1976) reported that the control of T. vaporariorum by the parasitoid E. formosa was highly efficient on tomato and red pepper plants, fairly efficient on egg-plant, but less efficient on cucumber plants. They suggested that such results might be due to plant unsuitability for the development of the whitefly immature stages and/or the characteristics of plant leaf surface influencing the parasitoid searching ability. So, notwithstanding the cucumber being a good host plant for T. vaporariorum, it seems that its leaves are less suitable for the parasitoid searching ability. Based on the results of our research on nymphs of B. tabaci B-biotype, the suggestion of Woets & Lenteren (1976) may be applied to the soybean plants. Although it is a good host plant for the whitefly development, soybean seemed to be less suitable for E. formosa. This aspect should be of greatest importance for the parasitoid development, though the external morphology of the evaluated plants was not the scope of our research.
According to Soto et al. (2001), the egg-toadult period of E. formosa was long at low temperature (29.5 days at 14.6ºC), but shortened as the temperature increased, reaching 10 days at 33.5ºC. Developmental time by this parasitoid on the third nymphal instar of T. vaporariorum was lower than that on the fourth instar, at the six temperatures evaluated. The parasitoid selects the most suitable host instar for its reproduction, by lowering the mortality rate of the immature stages and increasing the chance for oviposition and host utilization. Younger host stages are more abundant and easy to find. However, younger stages have lower amounts of nutrients, thus slowering parasitoid immature development and increasing the time of exposition to negative environmental influences (Gerling, 1990). E. formosa prefers to parasitize third nymphal instar whitefly, but when these instars are absent the parasitoid oviposits on younger nymphs, causing their death and hindering the establishment of the host-parasite interaction (Gould et al., 1975).