The Parasitism of Greenhouse Whitefly, Trialeurodes vaporariorum, by the Parasitic Wasp, Encarsia formosa: A Biological Control Method in Greenhouses

Abstract

The greenhouse functions to serve as an ideal, controlled, sheltered growing environment for plants.  
Unfortunately, the same conditions favorable for plant growth are favorable for plant pest infestations and 
reproduction.  Additionally, IPM practices stress the importance of sanitation.  The desirable sanitation 
created by good IPM management coupled with the use of chemical pesticides results in a detrimental  
"blank slate" environment which is vulnerable to new pests or resistant pests.  An environmentally 
friendly, humane goal of greenhouses should be to grow plants in a balanced, natural system with the aid 
of biological insects.

The greenhouse whitefly, Trialeurodes vaporariorum Westwood, is one of the most harmful, costly 
greenhouse insects.  Whiteflies are the worst insect problem on many greenhouse ornamental crops such 
as poinsettias and on many food crops, such as tomatoes, eggplant, cucumbers, and basil.  In 
greenhouses, Trialeurodes vaporariorum Westwood is believed to be the most critical insect pest on 
vegetable crops and ornamentals (Kassis 1993).  There are a limited number of pesticides approved for use 
on greenhouse food crops.  The whitefly pesticides currently labeled for use on edible greenhouse food 
crops are Azatin and M-pede (Safer Soap).  Yellow sticky cards are another means of non-chemical control 
of whitefly because they take advantage of the whitefly's yellow tropism.  

The desire to protect human health and environmental health as well as the frustration with the 
unintentional culturing of resistant pests has caused greenhouse managers to turn to biological controls as 
an alternative to chemical pesticides.  Conventional chemical pesticides have become unreliable due to the 
discontinuance of many chemicals by pesticide regulations and the high cost of developing new pesticides 
(McMahon 1992).  In 1979, the United Nations Environment Program listed pesticide resistance as one of 
the four most severe environmental problems in the world (Pedigo 1996).  Since that year, pesticide 
resistance has continued to be a constant battle for growers.  In 1990, the whitefly, Bemisia tabaci, was 
number two out of twelve on a list of insects identified as critical cases of resistance to available, 
affordable insecticides (Pedigo 1996).  

Introduction

Despite the recent trend towards biological controls, the use of beneficial insects is not new.  The whitefly 
parasitoid, Encarsia formosa, was first applied as a biological control of the greenhouse whitefly in the 
1920s (Roermund 1995).  It has been estimated that by 1988, 3800 ha of the greenhouse area in the world 
use E. formosa to biologically control greenhouse whitefly (Shishehbor 1996).  Research has been 
conducted to test various IPM strategies and combinations of different control methods against whiteflies.  
In particular, this paper explores the behavior of Encarsia formosa and its successful integration into a 
biological control program against whitefly.  

Greenhouse Whitefly, Trialeurodes vaporariorum Westwood  

Whiteflies' stationary habit, piercing-sucking feeding, and small size are attributes which make detection 
of the pest difficult and damage to the plants severe.  Whiteflies are descriptively named for their white 
color caused by the waxy powder covering their wings.  The insects are 2-3 mm long, and both sexes fly.  
The immatures are sedentary and emit a scale-like, waxy secretion while they develop.  Whiteflies are in 
the family Aleyrodidae and are members of the order homoptera.  The order homoptera was appropriately 
named (homo = uniform, ptera = wings) for the insects' uniformly textured forewings (Peters 1993).  

The homoptera order feeds only on the sap of terrestrial plants. The piercing sucking mouthparts 
characteristic of the order homoptera enable whiteflies to pierce leaves and extract nutrients from the plant 
without physically demolishing the host.  However, the piercing-sucking mouthparts of the insect cause 
discoloration of leaves and act as "living hypodermics" transmitting viruses and other diseases (Peters 
1993).  Whiteflies excrete a liquid feces high in carbohydrates commonly called honeydew.  The sticky 
substance taints edible plants and provides a home for the noxious black fungus sooty mold 
(Cladosporium spp.).  The honeydew also slows and deters mobility of natural, biological insects.  The 
stages of whitefly development are egg, first stage larvae, second stage larvae, third stage larvae, fourth 
stage larvae, prepupal stage, quiescent nonfeeding pupa-like stage, and adult (see figure 1).

Parasitic Wasp, Encarsia formosa

Encarsia formosa is a parasitic wasp used as a biological control of whiteflies in greenhouses throughout 
Europe, Australia, New Zealand, Japan, and North America (Weeden 1997).  E. formosa  is in the 
Aphelinidae family and is a member of the order hymenoptera.  The tiny wasp is native to the tropics and 
approximately 0.6 mm long.  The adult females have a black head, black thorax, and yellow abdomen, 
while the males are dark brown (Weeden 1997).  E. Formosa searches for its prey only during daylight 
(van Lenteren 1995).  The wasp flies or hops from leaf to leaf.  On the leaf, the parasitoid walks and 
drums the leaf with its antennae to search and feel for whitefly larva on the leaf.  

The majority of residence time on a leaf is spent walking, preening or sitting still, while only 20% of the 
time is spent handling the host (Roermund 1995).  E. formosa spends an average of 20 minutes on a clean 
tomato leaflet.  The walking activity of E. formosa is low at 15 to 18 degrees C.  The parasitoids were 
active only at temperatures above 18 degrees C.  However, walking activity was not effected by 
temperature at 20 degrees C or higher, by leaf side introduction, or by the existence of honeydew at 25 
degrees C (Roermund 1995).  Walking speed quickened as the temperatures rose from 15 to 25 degrees C, 
with no difference between 25 and 30 degrees C (Roermund 1995).  The parasites' walking activity slows 
with the decreasing egg load.  E. forsmosa's walking activity stops when the insect meets and ovipositions 
an unparasitized hosts, encounters an parasitized host, or comes in contact with honeydew. 

E. formosa females parasitize whitefly larval by laying their eggs singly in the whitefly nymphs.  E. 
formosa develops in the third and fourth stage larvae of the whitefly (Michelakis 1995).  E. formosa larvae 
eat the parasitized nymphs in order to develop into and emerge as adults (McMahon 1992).  A parasitized 
whitefly pupa will cause the pupae of the greenhouse whitefly to turn black and will cause the pupae of the 
sweetpotato whitefly to turn a rusty brown from their normal white color.  The time needed for the 
parasitoid to reject a host after contacting the whitefly with its antennae is 5-35 seconds, the handling time 
for oviposition or ovipositorial host rejection is 298-654 seconds, and the time for host feeding is 1063-
1626 seconds (Roermund 1995).  A complete diagram illustrating the foraging behavior of E. formosa on 
tomatoes in shown in figure 2.      

E. formosa is most effective when released weekly at the start of the crop when greenhouse whitefly 
infestation is low (McMahon 1992).  Encarsia should be released once whiteflies are detected on yellow 
sticky monitoring cards. The parasitic wasp should be released at 1-2 week intervals.  Research on release 
rates in a poinsettia greenhouse reveal that a rate of fourteen E. formosa per plant was most effective in 
controlling greenhouse whitefly in the shortest time.  E. formosa lays around 10-15 eggs daily (Weeden 
1997). The wasps are shipped inside blackened whitefly larvae attached to release cards.  It takes the wasp 
3-4 weeks to develop from egg to adult.  Development time at 30 degrees C is 10 days while development 
time at 18 degrees C is 40 days (Weeden 1997).  The ideal temperature for quick development and egg 
production is 27 degrees C, and the ideal humidity is between 50% and 80% (Weeden 1997).  At 25 
degrees C, previous studies reported the development time of immatures at 15.49 days, 15 days, 15.2 
days, and 15.8 days (Shishehbor 1996).  E. formosa needs a mean number of 200 degree-days in order to 
complete total immature development (Shishehbor 1996).  The adult wasps that emerge feed on honeydew 
and whitefly larvae.      

Tritrophic Interactions	

When implementing a control program with biological insects, it is important to recognize that a tritrophic 
interaction exists between the host plant morphology, the host's herbivore, and the herbivore's natural 
enemies (van Lenteren 1995).  Breeding for insect-resistant plants may affect herbivore and natural enemy 
interactions which in turn may make the plant more vulnerable to the pest.  Breeders of insect-resistant 
plants and growers must understand tritrophic interactions in order to identify detrimental interactions and 
to ameliorate beneficial interactions.

Greenhouse whitefly can be controlled effectively with the parasitoid Encarsia formosa on many, but not 
all, greenhouse crops.  Cucumbers are one crop which has not benefited from the implementation of E. 
formosa as a biological control for whitefly. Research has been conducted on host-plant resistance to deter 
whitefly infestations and on host-plant characteristics to ease the parasitoid's searching ability for 
whiteflies (van Lenteren 1995).  The walking speed of E. formosa slows linearly with increasing hair 
density (van Lenteren 1995).  Walking speed of the parasitoids was three times faster on hairless 
cucumber mutants than on hairy cucumbers.  Consequently, the net area searched per unit of time 
increased by 3.5 times.  However, the parasitoids walked so fast that they passed over the whitefly larvae 
on the smooth leaves (van Lenteren 1995).  Walking patterns of E. formosa are altered due to the 
parasitoids loss of direction on the hairy leaf caused by chaotic, nonsystematic turning.  Droplets of 
honeydew excreted by the whitefly are trapped in the leaf hairs which catch and drown a traveling E. 
formosa.  Research demonstrated that E. formosa's parasitism was greater on half-haired breeded 
cucumbers than on hairy cucumbers (van Lenteren 1995).  Raised leaf veins, hairs, waxes, and plant leaf 
shape influence insect maneuverability.

A second approach to managing whitefly on crops such as cucumbers which are susceptible whitefly hosts 
and are disruptive to E. formosa's parasitization efficiency is the addition of another selective control that 
is compatible with E. formosa.  A possible additional control is the entomopathogenic fungus Aschersonia 
aleyrodis Webber because it infects whitefly species, including greenhouse whitefly (Fransen 1993).  The 
fungus infects the first, second and third larval instars, but does not effect the fourth larval instar, the 
prepupal stage, and the pupal stage (Fransen 1993).  The interaction between E. formosa and A. aleyrodis 
was examined in order to determine the ideal timing and frequency of the application of A. aleyrodis in 
conjunction with the application of E. formosa.  The study concluded that E. forsmosa took the 
oviposition posture on untreated and treated hosts at all stages of infection by the fungus (Fransen 1993).  
Only after the ovipositor probes the interior of the host can the wasp detect infection of the fungus by signs 
of hyphal bodies or mycelium in the haemolymph (Fransen 1993).  The wasp rejects the unhealthy 
whitefly host, does not parasitize the host, and does not lay eggs in the host.  The two biological controls 
are most effective when E. formosa is applied seven days after A. aleyrodis since the parasitoid is capable 
of detecting an infected or healthy host from that point in time (Fransen 1993).  The study concluded that 
the complementary activity of E. formosa and A. aleyrodis successfully managed greenhouse whitefly on a 
crop which was initially difficult to implement biological controls.

Control methods

Various research comparing control methods of Trialeurodes vaporariorum Westwood reveals the 
strengths and weaknesses of the different approaches to managing this pest.  An experiment in 1993 
compared chromo-attractive physical control with yellow sticky traps, chemical control with the systemic 
insecticide Vydate, and biological control with E. formosa. Yellow sticky traps showed the quickest, 
immediate control, while the Vydate systemic insecticide had slower control.  The drawbacks of traps are 
that they lose efficacy over time when they become crowded, and they have no affect on whitefly larvae on 
the lower leaves because the suspended traps have no contact with the plant.  Control with E. formosa was 
the slowest to start, but the most successful method when introduced with a low initial whitefly population 
(Kassis 1993). The lower the initial whitefly population, then the higher the percentage parasitization 
(Kassis 1993).  It is speculated that the greater the whitefly population, then the greater the presence of 
honeydew which impede the parasites' mobility.  The timing of control depends on the whitefly infestation 
density.

Research in 1995 again studied the strengths and weaknesses of different control methods of greenhouse 
whitefly.  The research compared chromo-attractive physical control with yellow sticky traps, chemical 
control with specific action Quinomethionate (Morestan) and the pirimiphos methyl (Actellic), and 
biological control with E. formosa.  Success of the treatments was evaluated according to the adult insect 
population and the percentage of fruits covered with sooty mold growing in response to the presence of 
honeydew (Michelakis 1995).  Similar to the results from Kassis' study, the results of Michelakis' 
research found that the quickest controls were the treatments which included traps.  However, the traps 
alone were not sufficient in controlling whiteflies after the early stages.  Quinomethionate was effective 
only when used with E. formosa or with traps (Michelakis 1995).  Fruit damage from sooty mold was 
significantly lower on the plants treated with yellow sticky traps combined with E. formosa than on plants 
treated with Quinomethionate combined with E. formosa.   
  
	A third research project studied the compatibility of abamectin with E. formosa in an integrated pest 
management program of greenhouse whitefly.  The experiment showed that the combined treatment of 
abamectin and E. formosa significantly decreased the whitefly population on poinsettias in comparison to 
use of abamectin alone or E. formosa alone (Zchori-fein 1994).  Additionally, the combined biological and 
chemical treatment required fewer abamectin applications than when abamectin was used alone.  The 
chemical abamectin was found to be compatible with E. formosa because the percentage of parasitism was 
not significantly different for plants treated with and without abamectin (Zchori-fein 1994).  The research 
showed no death of adult parasitic wasps emerging from treated whitefly pupae.  However, exposure to 
abamectin can cause toxic effects on E. formosa when adult E. formosa walk on plant surfaces treated 
within 2 hours of application and through secondary exposure due to the adult female feeding on the 
poisoned whitefly larvae (Zchori-fein 1994).  Despite abamectin's slight toxicity to Encarsia, the chemical 
is more toxic to whiteflies.  Therefore, enough E. formosa survive the application of abamectin to 
effectively parasitize and control whiteflies.

Conclusion

	Research has demonstrated the effectiveness of E. formosa as a biological control of greenhouise 
whitefly.  E. formosa can be successfully and easily incorporated into an IPM program.  IPM stands for 
integrated pest management.  However, IPM more appropriately should stand for integrated plant 
management.  Pest problems are too often the consequence of poor plant management.  Chemical controls 
cannot be depended on to fix poor plant management.  IPM strategies include preventative measures such 
as sanitation, scouting for insects, and proper watering techniques as well as control measures such as 
biological insects, chemical insecticides, and traps.  The parasitism of greenhouse whitefly by E. formosa 
is a model example of managing whitefly pests without relying solely on chemicals.

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