By Mark Hoddle, Department of Entomology, University of California, Riverside
Encarsia formosa Gahan is used worldwide for commercial control of whiteflies in greenhouse crops. Commercial use began in Europe in the 1920s, but by 1945 interest waned due to the development of pesticides. After 1970, use was reinitiated and has expanded from 100 hectares of greenhouse crops to 4800 hectares in 1993 (van Lenteren and Woets, 1988; Hoddle et al., 1998).
Comparison of the greenhouse area in various parts of the world with the area employing biological control agents shows that most usage of E. formosa occurs in Europe and Russia and that the largest concentrations of greenhouse production in which E. formosa is not extensively used are in North America and Asia, particularly Japan (Hoddle et al. 1998). These are areas where increased use of E. formosa would be possible.
Encarsia formosa was originally described from specimens reared from an unidentified aleyrodid on geranium (Pelargonium sp.) in 1924 in a greenhouse in Idaho (USA) (Gahan 1924). There are no synonyms in the literature. Morphological descriptions of all life stages are provided by Speyer (1927). Because of releases into greenhouses worldwide, E. formosa has a cosmopolitan distribution and its native range is uncertain.
Encarsia formosa females are small (~ 0.6mm in length), have a black head and thorax and yellow abdomen. Males are rare and dark in color.
Principal greenhouse crops in which E. formosa is used include tomato (Lycopersicon lycopersicus) and cucumber (Cucumis sativus). The parasitoid is also used, or is being tested, on much smaller areas of eggplant (Solanum melongena var. esculenta) and gerbera (Gerbera jamesonii), poinsettia (Euphorbia pulcherrima), marigolds (Tagetes erecta), and strawberry (Fragaria X ananassa). Virtually nothing is known about the ecology of E. formosa in outdoor agricultural systems (Hoddle et al. 1988).
Pests Attacked (Host Range)
Encarsia formosa parasitizes at least fifteen species of whiteflies in eight genera. Most work has looked at the ability of E. formosa to control greenhouse whitefly Trialeurodes vaporariorum, sweetpotato whitefly, Bemisia tabaci, and silverleaf whitefly, Bemisia argentifolii (= Bemisia tabaci strain B). Encarsia formosa is hyperparasitized by Signiphora coquilletti, Encarsia pergandiella, and Encarsia tricolor (Hoddle et al. 1998).
To successfully reproduce in greenhouses, E. formosa must locate potential hosts, assess host quality, and use nymphs appropriately for host feeding or parasitism. Following release into the hosts' habitat (i.e., greenhouses), E. formosa employs visual and olfactory cues to find infested host plants (Guerrieri 1997). When searching new leaves, the parasitoid does not distinguish between upper and lower surfaces and shows no preference for middles or edges of leaves. The rate at which hosts are encountered is dependent on the parasitoids' walking speed, whitefly size, and number of hosts on a leaf. Walking speed is reduced by leaf venation, high trichome densities, excessive honeydew, encounters with nymphs suitable for host feeding and parasitism, decreasing temperature, low barometric pressure, and smaller egg loads (Hoddle et al. 1998).
Encarsia formosa is a solitary endoparasitoid that matures 8-10 eggs per day. Daily egg maturation and oviposition rates decline as wasps age. Adults obtain energy and nutrients by consuming honeydew and hemolymph of hosts that are pierced with the ovipositor, but in which no egg is deposited.
Killing hosts for nutritional purposes is termed host feeding. Encarsia formosa will host feed on all pre-imaginal stages of T. vaporariorum except the egg, but prefers second instar nymphs and pupae. However, the pupae and all nymphal stages of B. tabaci are used equally for host feeding. To host feed, E. formosa wounds nymphs or pupae by probing with the ovipositor for up to six minutes and feeds from wounds which wasps may enlarge with their mandibles. This probing followed by feeding kills hosts. Nymphs that have been used for feeding are not used for oviposition, and previously parasitized whiteflies are not used for host feeding (Hoddle et al. 1998).
Encarsia formosa will oviposit in all immature stages of T. vaporariorum, except the egg and the mobile first instar, and in all immature stages of B. tabaci older than the settled first instar nymph. Encarsia formosa prefers to oviposit in third, fourth, and prepupal nymphs of both T. vaporariorum and B. tabaci. The rate of successful emergence of the parasitoid is highest from these preferred stages. Encarsia formosa does not oviposit in up to 50% of suitable hosts in the preferred stages even when these are not parasitized or mutilated from host feeding. Such hosts may be parasitized at a later encounter. Failure to oviposit in such hosts may result from defensive host movements (Hoddle et al. 1998).
Encarsia formosa reared on T. vaporariorum can lay five eggs per day (will oviposit a total of 59 eggs before death), host feed on three nymphs per day, and kill on average a total of 95 nymphs over a 12 day life expectancy. Adult females chew a round exit hole on the dorsal surface of fourth instar nymphs before emerging. At 21°C, and with third instar T. vaporariorum as hosts, the time from oviposition to adult emergence is 25 days.
Thelytoky (parthenogenetic reproduction in which only females are produced) in E. formosa is mediated by Wolbachia bacterial infections. Exposure of females to antibiotics or high temperatures (31°C) for two or more generations suppresses microbial activity, allowing females to successfully produce male offspring. Fecundity is reduced once symbionts are eliminated. Males develop as primary endoparasitoids of whiteflies. The mating behavior of E. formosa has been described but males are unable to successfully inseminate females (Kajita, 1989; Zchori-Fein et al. 1992).
Four distinct methods of releasing E. formosa into greenhouses for whitefly control have been suggested. Three of these ("pest in first," "dribble," and "banker plants") are inoculative in nature and establish a reproducing parasitoid population, after which releases are discontinued. The fourth approach, in which repeated parasitoid releases are made throughout the cropping season, is used when a reproducing population of parasitoids is not expected to develop, either because the cropping season is too short or the whitefly or host plant are unfavorable. Whitefly mortality results from host feeding or superparasitism.
The "pest in first" method begins with the deliberate introduction of adult whiteflies into greenhouses at a fixed rate (e.g., two whitefly adults per tomato plant). Encarsia formosa is later introduced one to three times at a standard rate (e.g., eight parasitized nymphs per tomato plant) at regular intervals which coincide with availability of host stages suitable for parasitism. This method has not been widely adopted due to concern over releasing pests onto the crop.
With the "dribble method", parasitoid introductions begin at planting in anticipation of natural development of a whitefly population. Regular parasitoid releases at a low rate (e.g., one parasitized nymph per plant) continue until parasitized nymphs are found in the crop.
The "banker plant" system utilizes established breeding colonies of whiteflies and parasitoids on earlier grown plants from which wasp and whitefly disperse into the crop. Banker plants are introduced at a fixed rate (e.g., one banker plant per 352 crop plants). Mesh screens can be used to cage banker plants to contain whiteflies while allowing the smaller adults of E. formosa to migrate into crop production areas.
Inundative programs require regular releases of high numbers E. formosa; establishment and reproduction of the parasitoid in the crop are not expected. This method is applied most frequently to ornamental crops (Hoddle et al. 1998).
The pest in first, dribble, and banker plant techniques have provided successful control of T. vaporariorum on cucumber and tomato crops. Success in these cases has been defined in relation to levels of sooty mold (Cladosporium sp.) contamination of foliage and fruit. If at harvest sooty mold levels are within commercially acceptable limits, adequate control of T. vaporariorum is considered to have been achieved.
In floral crops, the presence of whiteflies at even very low densities (e.g., 0.02 to 0.03 nymphs per cm2 in poinsettias [unpublished M.H.]) is considered damaging and market standards require greater levels of whitefly suppression than are used for vegetable crops (e.g., 7.0 nymphs per cm2 in tomato). Consequently, use of E. formosa has been more extensive in vegetables than in floral crops.
Inundative releases of E. formosa have been successful in some instances for control of T. vaporariorum on poinsettia. Control of B. argentifolii with weekly releases of more than three adult parasitoids per plant per week, has not been accomplished. However, control of this whitefly species has been reported with lower weekly release rates (under two parasitoids per plant), or when T. vaporariorum co-occurred in the crop. In one study, as the number of parasitoids released per plant increased, parasitoid efficacy decreased, and B. argentifolii survivorship increased (Hoddle et al. 1998).
More than seventy articles have been published that examine interactions between E. formosa and one or more pesticides, either in laboratory tests or under conditions of practical use in greenhouses. Standardized methods for determining the effects of pesticides on E. formosa have been developed and the effects of more than one hundred different compounds on E. formosa have been determined. Selective materials of interest for possible combination with E. formosa include insecticidal soap, buprofezin, azadirachtin, abamectin, and resmethrin (Hoddle et al., 1998).
Encarsia formosa is readily available from North American insectaries.
Gahan, A.B. (1924) Some new parasitic Hymenoptera with notes on several described forms. Proc. U.S. Nat. Mus. 65 #2517 Art. 4: 1-23.
Guerrieri, E. (1997) Flight behavior of Encarsia formosa in response to plant and host stimuli. Entomologia Experimentalis et Applicata 82: 129-133.
Hoddle, M.S., R.G. VanDriesche, and J.P. Sanderson (1998) Biology and use of the Whitefly parasitoid Encarsia formosa. Annual Review of Ent. 43: 645-669.
Kajita H. (1989) Mating and oviposition of three Encarsia species (Hymenoptera: Aphelinidae) on the greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae). Appl. Entomol. Zool. 24:11-19.
Speyer, E.R. (1927) An important parasite of the greenhouse whitefly (Trialeurodes vaporariorum Westwood). Bulletin of Entomological Research 17: 301-08.
Van Lenteren J.C., and J. Woets (1988) Biological and integrated control in greenhouses. Ann. Rev. of Ent. 33: 239-269.
Zchori-Fein, E., R.T. Roush, M.S. Hunter (1992) Male production induced by antibiotic treatment in Encarsia formosa (Hymenoptera: Aphelinidae), an asexual species. Experientia 48: 102-105.