Insect Science 12, 401J412
Control of whitefly 401
Mulberry, Morus alba L. has become a popular agricul-
tural crop for silkworm rearing in India. It is affected by a
number of sucking pests such as scale insects, leafhoppers,
mealy bugs, thrip and whitefly. Among them, whitefly is
most common. Dialeuropora decempuncta (Quaintance &
Baker, 1913), Aleurodicus dispersus Russell, Aleuroclava
sp., and Bemisia tabaci Genn are the common whitefly
species reported on mulberry plants (Bandyopadhyay et
al., 1999; Douressamy et al., 1997). Geetha et al. (1998)
recorded spiralling whitefly Aleurodicus dispersus Russell
in Tamil Nadu. Aleurolobus bardensis Maskell, and
Neomaskellia bergii Sign. have also been reported to
damage mulberry plants (Mound & Halsey, 1978).
Dialeuropora decempuncta is a major pest in West
Bengal (Bandyopadhyay et al., 1999), whereas spiralling
whitefly A. dispersus has been reported to attack mulberry
plants in South India (Ramani et al., 2002). A leaf yield loss
up to 24% was recorded in western Bengal areas. It indi-
cates the level of damage caused by the pest to mulberry
plants. Alerodicus dispersus is a native of the Caribbean
region and Central America (Russell, 1965), where it is
known from a wide range of host plants, but not regarded
as a pest. It is more commonly known worldwide as
Correspondence: Ravindra N. Singh, Central Silk Board, B.T.
M. Lay Out, Madiwala, Bangalore 560 068, India. Tel: +91 80
2668 8813; fax: +91 80 26681511; e-mail: firstname.lastname@example.org
Biocoenology and control of whiteflies in sericulture
RAVINDRA N. SINGH, M. MAHESHWARI and B. SARATCHANDRA
Central Silk Board, B.T.M. Layout, Madiwala, Bangalore, India
Abstract The damage caused by the whiteflies Dialeuropora decempuncta (Quaintance
& Baker, 1913), Aleurodicus dispersus Russell, and Aleuroclava sp. to mulberry plants is
extensive and they cause a huge economic loss to mulberry leaves which affects silkworm
rearing. Dialeuropora decempuncta is a major pest in western Bengal, whereas spiralling
whitefly A. dispersus has been reported to attack mulberry plants in South India. The
whiteflies are present throughout the year in south India, with high populations in summer
(MarchJJune) and low ones in winter (OctoberJJanuary). The population is positively
correlated with temperature and negatively correlated with humidity. Chemical control is the
quick solution to minimize the pest population. However, the indiscriminate and large-scale
use of highly poisonous synthetic chemical pesticides has resulted in ecological imbalance,
in addition to their toxic effects on living organisms, including human beings. Hence there
is a need for developing methods and materials within an eco-friendly atmosphere. Previous
investigations indicate that neem-based insecticides may be a suitable alternative for pest
management in sericulture. Use of neem products in sericultural pest control has many
merits. It will also help in the successful introduction of biological controls in India. Several
exotic parasitoids have been found to be highly effective, including two aphelinid parasitoids
Encarsia haitiensis Dozier and E. meritoria Gahan. These are most promising and are
reported to minimize the fly pest population. The parasitization potential and behaviour of
the parasitoids have to be carefully assessed before they are introduced to control fly pest
populations. There is a need for careful assessment of all these advanced biological
technologies in order to develop a profitable, safe and durable approach for whitefly control
Key words biocoenology, ecological and biological control, whitefly
Insect Science (2005) 12, 401J412
Insect Science 12, 401J412
402 R. N. Singh et al.
?spiralling whitefly?because it lays eggs in a typical
spiral pattern (Prathapan, 1996). It was introduced and
assumed pest status in the Canary Islands in 1962, in
Hawaii in 1978, and in American Samoa and Guam in
1981, and then in most of the Pacific islands (Paulson &
Kumashiro, 1985). The whitefly later spread westwards
into several regions including Africa (Neuenschwander,
1994), Asia (Wen et al., 1994) and Australia (Lambkin,
1998). In south Asia, it is presently found in Bangladesh,
Sri Lanka (Wijesekera & Kudagamage, 1990), and the
Maldives (Martin, 1990). It was first reported in India in
1993 from Kerala (Palaniswami et al., 1995) and later from
other parts of peninsular India (David & Regu, 1995) and
the Lakshadweep islands (Ramani, 2000).
Damage, host range and population dynamics
The amount of damage caused by D. decempuncta and A.
dispersus to mulberry plants is extensive because it causes
huge economic loss to mulberry leaves which affects
silkworm rearing. The damage is done both by nymphs and
adults. Nymphs and adults suck the sap from mulberry
leaves and cause yellowish speckling to appear on the
leaves. Direct feeding damage is caused by piercing and
sucking sap from the foliage of the plants. This feeding
causes weakening and early wilting of the plant and re-
duces the plant growth rate and yield (Bandyopadhyay,
2001). It may also cause leaf chlorosis, leaf withering,
premature dropping of leaves and plant death. Indirect
damage is due to the accumulation of honeydew and white,
waxy flocculent material produced by the whiteflies. Like
other soft-bodied insects such as aphids, leafhoppers, mea-
lybugs and scale, whiteflies produce honeydew. This sweet
and watery excrement is fed on by bees, wasps, ants and
other insects which, in turn, may tend upon and offer
protection to the whiteflies. The honeydew also serves as
a substrate on which sooty mould grows. The mould
reduces the photosynthetic activity of the plant and serves
as a medium for growth of bluish mycelia of sooty mould
fungi, Chaetothyrium and Curvularia affinis Boedijin,
causing mulberry leaf disease. Sooty mould blackens the
leaf, decreases photosynthesis activity, decreases vigor
and often causes disfigurement of the host and lessens the
market value of the plant or makes it unmarketable
(Berlinger, 1986). The flocculent material produced by the
nymphs is scattered by the wind and becomes an unsightly
nuisance (Waterhouse & Norris, 1989). Bandyopadhyay et
al. (2002) determined the economic threshold level of
whitefly, D. decempuncta in mulberry. The third type of
damage is a result of the ability of this insect to act as a plant
disease vector. A small population of whiteflies is suffi-
cient to cause considerable damage (Cohen & Berlinger,
1986). Plant viruses transmitted by whiteflies cause over
40 diseases of vegetable and fiber crops worldwide. Among
the 1 100 recognized species of whiteflies in the world,
only three are recognized as vectors of plant viruses (Cohen
& Berlinger, 1986).
The mulberry whitefly has an extremely wide host range.
It prefers to feed on S1 and S1635 varieties of mulberry
plants. Douressamy et al. (1997) reported that Kanava-2,
MR2, S36 and S54 are the most preferred varieties in
southern Indian conditions. The warm humid conditions
and abundant food are ideal for whitefly build-up. The
whitefly population started appearing in higher numbers
from August onwards and reached its peak during Septem-
berJOctober. Correlation studies have shown that high
humidity (75%J85%), moderate temperature (24J28?)
and moderate rainfall (180J380 mm) are influencing the
maximum incidence of the pest in eastern and north-
eastern regions of India (Bandyopadhyay et al., 2000). The
minimum whitefly number was recorded during MarchJ
June and DecemberJFebruary. The whitefly was present
throughout the year in southern India, with high popula-
tions in summer (MarchJJune) and low ones in winter
(OctoberJJanuary). The population positively correlated
with temperature and negatively correlated with humidity.
Populations of indigenous predators remained low and did
not have any impact on the whitefly populations (Mani &
Krishnamoorthy, 2000). Narayanaswamy et al. (1999)
found a high incidence of the pest on mulberry plants
during AprilJJune in and around Bangalore. Palaniswami
et al. (1995) reported outbreaks in the post-rainy dry season
between November and April and peaks in February in
Kerala. Severe infestation was observed during March in
the Lakshadweeps, which lessened during June with the
onset of rains. Whitefly populations were higher during
MayJOctober in northern India whereas in southern India
the incidence was higher in cooler months (NovemberJ
February) on several trees (Ramani, 2000). This survey
indicates that the adults are found on the topmost two
leaves, whereas eggs and nymphs are found on 2J4th and
7J14th position of leaves respectively. The population of
egg masses per leaf on an average ranged from 25J56.
Eggs are mostly laid on the bottom and middle portion of
the leaves and on matured leaves. The number of adults per
leaf ranged from 40J60. They are mostly found congre-
gated on the lower surface of the leaves. Leaf recovery is
restricted to approximately 15%J25% of affected foliage.
The adults of Aleurodicus dispersus are similar in appear-
Insect Science 12, 401J412
Control of whitefly 403
ance to those of many other species of whiteflies but the
behavior is different. They hatch in 3J5 days in AprilJ
September, 5J7 days in OctoberJNovember and 35 days
in DecemberJJanuary. The nymphs feed on the cell sap
and grow in three stages to form the pupae within 9J14
days in AprilJSeptember and in 17J82 days in October-
March. In 2J8 days pupae change into whiteflies. The life
cycle is completed in 15J125 days and 11 generations are
completed in a year (Waterhouse & Norris, 1989;
Douressamy et al., 1997). The adults of Aleurodicus
dispersus are much larger than the most common Bemisia
tabaci and are white with powdery waxy scales all over the
body and wings. The wings of newly emerged adults are
clear, but develop a covering of white powder over the next
few hours. The eyes are dark reddish-brown and the forew-
ings have two characteristic dark spots. Bandyopadhyay et
al. (2001) reported the biology of Dialeuropora
decempuncta and Aleuroclava sp. on mulberry plants in
western Bengal climatic conditions. Adults congregate on
the lower surface of the leaves where they lay yellow
elliptical eggs. Adults are active during morning hours.
The mean length of the adult measures 0.7 mm and wings
expand 2.1 mm. Like other whitefly species it emerges
during the cool hours. This pest is most active during
SeptemberJOctober. The female lays approximately 120J
150 eggs in circular or semi-circular masses on the under-
surface of the leaves during an oviposition period of 2J3
days. The freshly laid white eggs are elliptical in shape and
they turn black later on. The eggs hatch in 2J3 days. On
hatching, the tiny first instar nymphs settle on suitable
places. The second and subsequent instar nymphs usually
remain feeding in the same place. Nymphs with reddish
eyespots are covered with white waxy material. The pupal
stage lasts 7J10 days and the life cycle is completed in 15J
18 days in September and 18J25 days from October
Ecological control involves the removal, destruction,
modification, or isolation of material that might favor the
survival of an insect pest by affording food or making a site
suitable for breeding. Ecological control refers to applica-
tion of cultural control measures, judicious use of chemicals,
biological control agents and resistant varieties (Singh et
al., 2000). This concept describes procedures for evalua-
tion and consolidation of the available techniques into a
unified program for managing pest populations. This leads
to avoidance of economic damage and adverse side-effects
on the environment (Southwood, 1978). In the past, several
cultural practices were implemented to control the whitefly
population in sericulture. Beneficial organisms and resis-
tant mulberry varieties were screened through trial and
error and natural substances were discovered. This laid the
foundation for pest management of whitefly based on the
biology of the ecosystem. Successful strategies were pre-
dominantly those that served to maintain the ecological
balance of the region and the natural balance of whiteflies
and their enemies (Goolsby et al., 1996). It has been
observed that such practices, combined with the advanced
biological technologies now available, are the most logical
approach to developing a profitable, safe, and durable
(long-lasting and self-maintaining) approach to pest
management. This system is identified as ecologically
based pest management (EBPM). The concept of EBPM
builds on the cultural and biological approaches to pest
management and includes many practices, such as crop
rotation, intercropping, tilling, trap crop, sanitation, host
resistance/plant resistance. Apart from this, physical barri-
ers have been used effectively for decades to reduce the
impact of pests. Regular farm operations and cultivation of
soil are conducted to destroy the insects or to prevent
whitefly from causing injury.
Generally, mechanical and physical control methods are
popular with farm workers, and are adopted during the leaf-
harvesting period. Mulberry leaves with eggs of whitefly
are collected and destroyed. Mechanical control methods
can be rapid and effective, but are mostly suited for small
acute pest problems. Mechanical controls have relatively
little impact on natural enemies and other non-target
organisms, and are therefore well suited for use with
biological controls (Srinivasan & Mohanasundaram, 1997).
Under physical control methods, insect pests are physi-
cally kept away from reaching their hosts.
Crop rotation interrupts the normal life cycle of insect
pests by placing the insects in a non-host habitat. Rotation
is generally most successful against arthropod pest species
with long generation cycles and with limited dispersal
capabilities (Wang, 1992). Whitefly adults lay many eggs
when fed on mulberry leaves and cause heavy damage to
this crop. However, some leguminous crops, including
cow pea, horse gram and pigeon pea are in some way
nutritionally deficient to support feeding, and do not suffer
damage from whitefly. So, a mulberry/leguminous rota-
tion is effective and economical. Crop rotation interrupts
the life cycle of the whitefly, and both species can be
effectively controlled by rotation throughout the temperate
region of India. Further, crop monocultures are often
damaged more severely by pests. There are cases where
such diversity can aggravate pest problems. It is in these
situations where trap crops can be important. Besides this,
intercropping is another important method to reduce pest
problems. Several field trials have been conducted using
Insect Science 12, 401J412
404 R. N. Singh et al.
different intercrops such as tomato, garlic, onion, corian-
der and carrot. The intercrops were grown in alternate rows
with mulberry, and their influence on the pest population
was estimated. It was observed that the intercropped plots
had significantly lower numbers of whitefly nymphs and
pupae, and a higher yield of good quality leaf, as compared
to the control. Similarly, garlic in inter-rows of mulberry
also has been reported to decrease whitefly numbers
(Anonymous, 1976). Two parallel tests, one on different
crops, including tomato, bean and cucumber and one on
different tomato cultivars, were conducted. Bemisia tabaci
showed a distinct behavioural preference for cucumber
when exposed to the different crops simultaneously. Cu-
cumber thus seems to be a high-ranking host for B. tabaci
(Botha et al., 2004). This suggests that B. tabaci has no
problem in choosing a host plant, that is, showing a
preference when one of the plants in the test is a high-
ranking host plant. However, when only low-ranking host
plants giving similar, but not identical, stimuli were present,
female whiteflies tended to have difficulty in making a
selection, resulting in increased movement and reduced
fecundity. If the above results can be confirmed under
different conditions, the value of intercropping with differ-
ent cultivars could contribute toward reducing pest popu-
lation build-up in an integrated pest management program.
Tillage operation is the most common practice in mul-
berry cultivation. It is conducted for soil-turning and resi-
due-burying practices, seedbed preparation, and cultiva-
tion (Reddy & Kotikal, 1998). Some forms of tillage can
reduce pest populations indirectly by destroying wild veg-
etation (weeds) and volunteer crop plants in and around
crop-production habitats. Overwintering populations of
whitefly may be greatly reduced by either fall or spring
plowing operations. These characteristics also influence
the quality of food, which determines the abundance of
whitefly. Thus with the proper stirring and management of
the soil, the whitefly population can be controlled.
Phytosanitary is very important parameter in integrated
pest mamangement (IPM). Destroying dead and decaying
materials from nearby rearing houses is important in reduc-
ing viruses and protozoas (Etebari et al., 2004). Since crop
residues can harbor whiteflies and virus inoculum, they
should be rapidly and completely destroyed after the final
harvest. The subsequent planting of susceptible crops
should be avoided until migration has ended. This practice
can reduce whitefly infestation as well as carryover of
viral inoculum. Although these practices may not com-
pletely eliminate whitefly problems, they can help reduce
pest populations and damage to manageable levels. These
practices should be modified only to preserve known
populations of natural enemies of whiteflies. Physical
barriers, use of synthetic sex pheromones, repellants and
confusants help in containing whitefly population (Heinz
& Parrella, 1991). In general, host plant resistance to insect
pests is likely to play an ever increasing role in pest
management. Planting the mulberry varieties that are less
susceptible to whitefly may also affect the level of
Studies on the biological control of whitefly has been
widely used in glasshouses, especially since the develop-
ment of insecticide-resistant whiteflies, and is chiefly
based on parasitoids (Encarsia sp. and Eretmocerus sp.),
predators (Anegleis sp., Coelophora sp., Cryptolaemus
sp.) and entomopathogenic fungi (Paecilomyces sp.). At-
tempts have been made to search for appropriate biological
control agents in native natural habitats. Polaszek et al.
(1992) reported 19 previously described parasitoids be-
longing to the Encarsia and Eretmocerus genera, as well as
many more yet undescribed that attack the mulberry
whitefly. A key to the known Encarsia species is provided
by Polaszek et al. (1992). Among important parasitoids,
two aphelinid parasitoids Encarsia haitiensis Dozier and
E. meritoria have the most potential (Srinivasan, 2000).
Encarsia sp. nr. haitiensis and E. sp. nr. meritoria were first
recorded from Kerala in 1998 (Beevi et al., 1999). Ramani
(2000) reported Encarsia guadeloupae as another impor-
tant pupal parasitoid of whitefly. Besides this, Eretmoceras
delhiensis Mani, Encarsia neomaskelliae Prasad and E.
isaaci Mani have also been reported to attack up to 45% of
whitefly pupa (Mani et al., 2000). The parasitized puparia
turn dark in color and can easily be distinguished from non-
parasitized ones. For the control of Dialeurodes spp.,
Encarsia lahorensis (How) has been reported as the key
parasitoid other than Aphelinus fuscipennis How (Rosen &
DeBach, 1981; Wen et al., 1995). Chien et al. (2000)
reported introduction, propagation and liberation of two
parasitoids for the control of spiraling whitefly (Homoptera:
Aleyrodidae) in Taiwan, China. The life table characteris-
tics of the parasitoids have been studied and it was found
that it has a high potential for the biological control of
whitefly in seri-ecosystems (Ramani, 2000; Srinivasan et
Among predators of whiteflies, true bugs (Hemiptera:
especially Anthocoridae and predatory Miridae), beetles
(Coleoptera: Coccinellidae), lacewings (Neuroptera:
Chrysopidae, Hemerobiidae, Coniopterygidae), flies
(Diptera: Dolichopodidae, Syrphidae, Anthomyoodae), ants
(Hymenoptera: Formicidae), spiders (Araneida) and mites
(Acarina: Phytoseiidae, Stigmaeidae) have been reported
(Ramani et al., 2002). Some of these are opportunistic
Insect Science 12, 401J412
Control of whitefly 405
predators, others are general feeders and some are specific
predators of whiteflies. More than 40 indigenous predators,
mostly generalists and few specialist species have been
recorded in India. Coelophora unicolor has also been
recorded as a potential predator of whitefly. Hoelmer et al.
(1994) reported the interaction of the whitefly predator
Delphastus pusillus (Coleoptera: Coccinellidae) with para-
sitized sweet potato whitefly. Anegleis cardoni (Weise),
Anegleis perrotteti (Mulsant), Axinoscymnus puttarudriahi
(Kapur & Munshi), Cheilomenes sexmaculata (F), Jauravia
sp., Nephus regularis (Sicard), Pseudoscymnus sp.,
Pseudaspidimerus flaviceps (Walker), Pseudaspidimerus
trinotatus (Thunberg), and Scymnus saciformis
(Motschulsky) are the most common predator (Hagen,
1962). Jallali and Singh (1989) studied the biotic potential
of three coccinellid predators on various diaspine hosts.
Mani and Krishnamoorthy (1997) observed that the natu-
ralized Australian ladybird beetle, Cryptolaemus
montrouzieri (Mulsant) preyed on the whitefly almost
throughout the year, but had little effect in reducing the pest
population. Mani and Krishnamoorthy (1999) studied the
predatory potential and developmental period of C.
montrouzieri on the whitefly in the laboratory. Chilocorus
nigrita (F.) is another important predator feeding on the
whitefly and it attacks almost all the developmental stages
of whitefly. Hagen et al. (1976) reported biology and
ecology of some predaceous coccinellids beetles. Several
birds, ants and spiders have also been recorded feeding on
A. dispersus in India.
Among pathogens, Paecilomyces farinosus (Holm.) has
been recorded on A. dispersus from India (Mani et al.,
2000). Although many fungi have been found in associa-
tion with Bemisia, only Verticillium lecanii, Paecilomyces
fumosoroseus, Peacilomyces farinosus, Aschersonia
aleyrodis, and Beauveria bassiana have been demon-
strated to be pathogenic. Studies on fungal pathogens
indicate some success in controlling whitefly. However,
these products are not yet commercially available, and
reliable programs based solely on biological agents have
not been developed (Botha et al., 2004).
To ensure this, selection of most suitable natural parasi-
toids is desirable. Sometimes the potential parasitoid in the
laboratory may prove to be inadequate under field
conditions. Such was the case with the commercially
available natural enemy, Encarsia formosa, which has a
proven track record of successful whitefly control in green-
houses but was less than satisfactory when used for control
under field conditions (Parrella et al., 1991). A search for
new, effective natural enemies must be assessed with its
host-searching capacity, specificity, power of increase and
adaptability (Waage, 1986; van Lenteren, 1983). A high
reproductive rate is important so that populations of the
natural enemy can rapidly increase when hosts are available.
The natural enemy must be effective at searching for its
host and it should be searching for only one or a few host
species. All these attributes are of course closely related to
each other and influence the population density of parasi-
toids in the natural habitat.
Searching capacity, manifested by the ability to find the
host even when it is scarce, is commonly regarded as the
most important attributes of effective natural enemies. A
parasitoid beneficial as a bioagent must successfully utilize
the low-density population of the pest. Encarsia haitiensis
and E. meritoria have been found capable of attacking
more than 50% of the whitefly pupa within an hour. This
indicates its high searching capacity, that is, the ability to
find hosts, when the host density is low. They are attuned
to the physiology, behavior, habitat preferences, and pat-
terns of dispersion and phenology of whitefly (Kirk et al.,
2001). These parasitoids have a degree of biological adap-
tation to the pupa of whitefly and also have a greater degree
of direct and rapid responsiveness to density changes in the
whitefly population (Goolsby et al., 1998). Most of the
whitefly parasitoids have received host regulation in a
stable environment that has reached the hypothetical steady
state and would only require a power of increase sufficient
for replacement of the parent population in each generation.
The actual power of increase of a natural enemy in the field
may be affected by its fecundity and rate of development,
as well as by other factors such as its searching capacity and
adaptability to the conditions of the particular habitat
(Clausen, 1978; Goolsby & Ciomperlik, 1999). Fitness and
adaptability are other important attributes. To be effective
in a new habitat, an introduced natural enemy should
preferably be pre-adapted to it. However, the possibility of
possible gradual post-colonization adaptation cannot be
discounted. A well-adapted natural enemy should not
require any essential requisites that are not present in the
new habitat. It should be able to tolerate the prevailing
climatic conditions, and should be effectively synchro-
nized with the biology and phenology of its host in the
habitat. Ideally, a natural enemy should be adapted to all
the habitats and niches occupied by the target pest. It
should frequent all the host plants and tolerate all the same
climatic regimes as its host does, and should be equally
effective in all of them. Just as the natural enemy should be
well adapted to the various natural aspect of the ecosystem,
it should also be adapted to cope with man-made hazards,
such as pesticidal treatments (Rosen & Huffaker, 1983).
Although the outlook for biological control through natural
enemies is promising, several situations limit the effective-
ness of predators and parasites of the whitefly. These
instances were discussed by van Lenteren (1983) and
outlined by Gerling (1986).
Insect Science 12, 401J412
406 R. N. Singh et al.
In a well design integrated pest management program,
the pest population is maintained at a lower level by the
action of three basic approaches to applied biological
control: conservation, importation and augmentation. Spe-
cific techniques within these approaches are constantly
being developed and adapted to meet the changing needs of
pest management. Improvements in rearing and release
techniques and genetic improvement of natural enemies
have resulted in more effective augmentation programs.
Application of new ecological theory is transforming the
methods for conservation of natural enemies. Continued
refinement and adaptation of biological control approaches
and applications are necessary if the full potential of this
biologically based pest management strategy is to be
The conservation of natural enemies is probably the most
important and readily available biological control practice
available to farmers. Natural enemies occur in all produc-
tion systems, from the backyard garden to the commercial
field. They are adapted to the local environment and to the
target pest, and their conservation is generally simple and cost-
effective. Conservation involves identifying the factor(s)
which may limit the effectiveness of a particular natural
enemy and modifying them to increase the effectiveness of
the beneficial species. In general, conservation of natural
enemies involves either reducing factors which interfere
with natural enemies or providing resources that natural
enemies need in their environment. Many factors can
interfere with the effectiveness of a natural enemy. Pesti-
cide applications may directly kill natural enemies or have
indirect effects through reduction in the numbers or avail-
ability of hosts. Various cultural practices such as tillage or
burning of crop debris can kill natural enemies or make the
crop habitat unsuitable. In orchards, repeated tillage may
create dust deposits on leaves, killing small predators and
parasites and causing increases in certain insect and mite
pests. Ensuring that the ecological requirements of the
natural enemy are met in the cropping environment is the
other major means of conserving natural enemies. To be
effective, natural enemies may need access to: alternate
hosts; adult food resources; overwintering habitats; con-
stant food supply; and appropriate microclimates (Rabb et
al., 1976). Conservation involves permeated action to
protect and preserve existing parasites, predators and
pathogens: basically not taking actions that would be
detrimental to natural enemies (Nordlund, 1984; Rabb et
al., 1976). IPM programs that result in a reduction in
pesticide use generally contribute to conservation. Conser-
vation and augmentation in biocontrol involves two phases:
first, the maintenance of existing parasitoids by avoiding
harmful practices; and secondly, the augmentation of
parasitoids, either directly releasing them in the field or by
indirectly making the field environment more favorable for
them. Although a number of species of eulophid parasi-
toids have been reported, it is rather easy to identify more
effective parasitoids based on their parasitization
capabilities. Encarsia haitiensis Dozie and E. meritoria,
both multivoltine parasitoids, have been identified as such
potential parasitoids. These parasitoids which appear after
the arrival of whitefly pupa need to be conserved from the
use of pesticides which is very intensive on mulberry
Importation (classical biological control) has been by far
the most important and most promising approach to date,
and has accounted for the great majority of outstanding
successes in applied biological control. It is also the least
expensive method of natural enemy utilization. However,
in certain instances an already established natural enemy,
whether indigenous or introduced, may show considerable
promise but fall short of fulfilling its potential due to
inadequacies of its own attributes or the environment.
There are several potential natural parasitoids of whitefly
but their exploitation has not been achieved due to lack of
sufficient information on the behavioral response of the
parasitoids. Even well known natural enemies of proven
high efficiency still await transfer into many areas where
whitefly is a serious problem. There are several hy-
menopteran natural parasitoids which can be utilized to
control the whitefly population. These unknown species
are considered as potential weapons and may be applied as
biological control tools (Kerrich, 1960). The first step in
the process of classical biological control is to determine
the origin of the introduced pest and then collect appropri-
ate natural enemies (from that location or similar locations)
associated with the pest or closely related species. The
natural enemy is then passed through a rigorous quarantine
process, to ensure that no unwanted organisms (such as
hyperparasitoids) are introduced, then reared, ideally in
large numbers, and released. Follow-up studies are con-
ducted to determine if the natural enemy has successfully
established at the site of release, and to assess the long-term
benefits of its presence. There are many examples of
successful classical biological control programs. Introduc-
tion of Trichogramma ostriniae, from China to control the
European corn borer is one of the most successful ex-
amples of classical biological control. Classical biological
control is long-lasting and inexpensive. Other than the
initial costs of collection, importation, and rearing, little
expense is incurred. When a natural enemy is successfully
established it rarely requires additional input and it contin-
ues to kill the pest with no direct help from humans and at
Augmentation is the direct manipulation of natural en-
emies to increase their effectiveness. This can be accom-
Insect Science 12, 401J412
Control of whitefly 407
plished by mass production and periodic colonization; or
genetic enhancement of natural enemies. The most com-
monly used of these approaches is mass production, in
which natural enemies are produced in insectaries, then
released either inoculatively or inundatively. Augmenta-
tion involves actions to increase the populations of benefi-
cial parasitoids, predators or pathogens (Alphen & Vet,
1986; Ridgway & Vinson, 1977). There are two basic
approaches to augmentation: environmental manipulation
and periodic releases (Stinner & Bradley, 1989). Periodic
releases can be inoculative or inundative. Inoculative re-
leases are releases of a relatively small number of biologi-
cal control agents, often on a seasonal basis. The control in
inoculative release programs is expected to come primarily
from the progeny of these agents being released. Inundative
releases are releases of relatively large numbers of biologi-
cal control agents, and the control is expected to come from
the released agents, not necessarily from their progeny
(DeBach & Hagen, 1964). Inundative releases programs
usually involve a number of releases during the season,
while inoculative release programs may involve only one
release. It is possible by sustained release of laboratory-
reared parasitoids. Our ability to use periodic releases of
the parasitoid to control whitefly, is to rear, transport and
effectively release large numbers of high quality biological
control agents. Periodic release requires continuous re-
lease program, and thus has commercial potential and fits
IPM programs well. The growing number of commercial
suppliers of biocontrol agents is evidence of this potential
(Thomson, 1992). Adoption of biological controls has
had positive economic impact. An example of the inocu-
lative release method is the use of the parasitoid wasp,
Encarsia formosa Gahan, to suppress populations of the
greenhouse whitefly, Trialeurodes vaporariorum
(Westwood), (Parrella, 1991). The greenhouse whitefly
is a ubiquitous pest of moriculture and floriculture crops
that is notoriously difficult to manage, even with pesticides.
Releases of relatively low densities (typically 0.25J2.00
per plant, depending on the crop) of E. formosa immedi-
ately after the first whiteflies are detected on crops can
effectively prevent populations from developing to dam-
aging levels. However, releases should be made within
the context of an integrated crop management program
that takes into account the low tolerance of the parasitoids
Habitat or environmental manipulation is another form
of augmentation. This tactic involves altering the cropping
system to augment or enhance the effectiveness of a natural
enemy. Many adult parasitoids and predators benefit from
sources of nectar and the protection provided by refuges
such as hedgerows, cover crops, and weedy borders. Mixed
plantings and the provision of flowering borders can in-
crease the diversity of habitats and provide shelter and
alternative food sources. They are easily incorporated into
home gardens and even small-scale commercial plantings,
but are more difficult to accommodate in large-scale crop
production. There may also be some conflict with pest
control for the large producer because of the difficulty of
targeting the pest species and the use of refuges by the pest
insects as well as natural enemies.
Importation, augmentation and conservation of natural
enemies constitute the three basic approaches to biologi-
cal control of insects. Specific techniques within these
approaches are constantly being developed and adapted to
meet the changing needs of pest management. Improve-
ments in rearing and release techniques and genetic im-
provement of natural enemies have resulted in more effec-
tive augmentation programs. Application of new ecologi-
cal theory is transforming the way we look at conservation
of natural enemies. To enhance biological control of insect
pests in greenhouses, facilities and procedures for mass
production of parasitoids, Eretmocerus sp., Encarsia-
formosa (Aphelinidae), and Trichogramma brassicae
(Trichogrammatidaea), and of predator, Aphidoletes
aphidimyza (Cecidomyidae) were successfully developed
in Hengshui, Hebei Province, China (Zheng et al., 2005).
Mass production of aphelinid was achieved by using dif-
ferent plant varieties and host insect species, as well as
specific rearing procedures and techniques. Commercial
production of T. brassicae was greatly progressed through
designing special devices and improving rearing techniques.
Annual productivity of various species of natural enemies
in our institution totalled two billion individuals. Accord-
ing to the type of greenhouse (sunlight greenhouse and
plastic house), bio-control strategies have been devised.
Inoculative release techniques for these enemies were
established, including preparation before release, release
time, release rate and special measures. Parasitism rates of
whitefly, Trialeurodes vaporariorum, and tobacco whitefly,
Bemisia tabasi, by their natural enemies were as high as
85%J96% in the greenhouse.
Trichogramma are the most widely augmented species
of natural enemy, having been mass-produced and field-
released for almost 70 years in biological control efforts.
Worldwidety, over 32 million ha of agricultural crops and
forests are treated annually with Trichogramma spp. in 19
countries, mostly in China and the republics of the former
Soviet Union (Li, 1994). In India about 18 Trichogramma
species are recorded, of which T. chilonis, T. japonicum
and T. achaeae are widely distributed and are key mortality
Insect Science 12, 401J412
408 R. N. Singh et al.
factors for many crop pests. These parasitoids attack many
lepidopterous pests. In China, agricultural production and
pest management systems capitalize on low labor costs,
and generally follow highly innovative yet technologically
simple processes. For example, Trichogramma spp. that
are inundatively released to suppress sugarcane borer,
Chilo spp. populations in sugarcane, are protected from
rain and predators inside emergence packets. Insectary-
reared parasitized eggs are wrapped in sections of leaves
which are then slipped by hand over blades of sugarcane.
Most Trichogramma production in China takes place in
facilities producing material for a localized area. These
facilities range from open air insectaries to mechanized
facilities that are leading the world in the development of
artificial host eggs. Genetic improvement of several preda-
tors and parasitoids has been accomplished with traditional
selection methods (Hoy, 1992), and appears possible with
recombinant DNA technology. Continued refinement and
adaptation of biological control approaches and applica-
tions are necessary if the full potential of this biologically
based pest management strategy is to be fulfilled.
Botanicals derived from neem (Azadirachta indica) and
other plant species are traditionally used in sericultural pest
control operations. They are not only popular but also very
effective in certain conditions. Neem has diverse biologi-
cal effects on insects. It has antifeedant, oviposition,
deterrent, repellent, insect growth regulator, sterilant, mat-
ing disruptor and toxic properties (Schmutterer, 1990). The
use of neem and pongamia (Pongamia pinnata L.) cake for
the management of sericultural pests was successfully
demonstrated (Singh & Saratchandra, 2004a). Neem leaves
and seed kernels, when incorporated into potting soil
containing earthworms, increase the earthworm popula-
tion by 25%. Neem products have proven to be remark-
ably benign to spiders and also other insects which act as
parasitoids on various crop pests. Neem products have to
be ingested to be effective. Neem products work by inter-
vening at several stages of the life of whitefly. They may
not kill the pest instantaneously but incapacitate it in a
number of ways. When the neem components, especially
azadirachtin, enter the body of the larva, the activity of
ecdysone is suppressed and the larva fails to moult, remains
in the larval stage and ultimately dies (Singh &
Saratchanddra, 2004b). If the concentration of azadirachtin
is not high enough the larva will die only after it has entered
the pupal stage. If the concentration is lower still, the adult
emerging from the pupa will be 100% malformed, and
Why not insecticides?
It must be borne in mind that there is no feasible 100%
alternative to chemical pesticides and they are a must when
the situation is demanding. Previously, several chemicals
and synthesized mimics of natural products, or completely
synthetic materials, were in practice to minimize pest
populations. Synthetic organic insecticides have been de-
veloped for nearly every insect pest (Cremlyn, 1979).
Some of the insecticides such as dieldrin, aldrin (chlori-
nated hydrocarbon), malathion, parathion, dichlorvos
(organophosphate), carbaryl, aldicard (carbamates),
permethrin, cypermethrin, phenothrin (pyrethroids)
methropene, fenoxycarb, pyriproxyfen, diflubenzuron
(insect growth regulator), were frequently used to control
various pests of silkworm and its host plants (Singh et al.,
2000). Bandyopadhyay and Santhakumar (2000) reported
the effect of carbaryl, monocrotophos and quinalphos for
control of whitefly D. decempuncta on mulberry M. alba.
Alam et al. (1998) reported the effectiveness of three
insecticides for the control of spiraling whitefly, A.
dispersus. Chemical control of whitefly is both uneco-
nomic and impractical because of the pest? s broad host
range, widespread distribution and presence in areas with
high human habitation (Kajita et al., 1991).
Synthetic organic insecticides were used widely on seri-
cultural crops in the hope that they would control pests. It
is now clear that their use has some unfortunate
consequences. Pests develop resistance to synthetic or-
ganic insecticides. In fact, pest resistance currently limits
the efficacy of many insecticides, fungicides and herbicides.
Many synthetic organic insecticides are broad-spectrum,
killing not only arthropod and pathogen pests but also
beneficial organisms that serve as natural pest-control
systems. Without benefit of the natural controls that keep
pest populations in check, farmers become increasingly
dependent on chemical insecticides to which pests may
eventually develop resistance. Thus there is an urgent need
for an alternative approach to pest management that can
complement and partially replace current chemically based
pest management practices.
Integrated pest management (IPM) is the blending of all
effective, economical and environmentally sound pest
control methods into a single but flexible approach to
managing pests. When human intervention is necessary,
the least invasive practices, such as plant resistance, bio-
logical control, and cultural control, should be used be-
cause these are the practices that fit best into sustainable
Insect Science 12, 401J412
Control of whitefly 409
sericulture (Singh & Saratchandra, 2002a). Highly disrup-
tive or environmentally damaging practices should be used
only as a last resort. IPM strives to manage pests using
ecological principles of natural pest mortality factors; pest-
predator relationships; genetic resistance; and cultural
practices (Singh & Saratchandra, 2002b). This theoretical
basis of IPM is similar to ecologically based pest
management. The practice of IPM, unfortunately, is not
always consistent with its theory. The focus of early IPM
programs was devoted to control of insects, setting a
precedent for the focus of IPM on arthropod pest
management. In many cases, this management was limited
to pest scouting and precise applications of insecticides.
Consequently, this focus has been at the expense of IPM of
sericultural pests (Singh et al., 2004). The ecological
concepts of the IPM framework are the departure point for
this new information-rich management strategy. The EBPM
will rely on an improved knowledge base of the complex
ecological processes that occur in plant production. Inte-
grated pest management is a dynamic and evolving practice.
Specific management strategies will vary from crop to
crop, location to location, and year to year, based upon
changes in pest populations and their natural controls. As
specific new approaches are developed, these too can be
incorporated into the program as appropriate. Modern pest
managers will be most effective if they are knowledgeable
about their pests and all of the control options available.
The knowledge needed to build the foundation of ecologi-
cally based pest management will come from nearly all
disciplines of both the biological and social sciences and
will require research from laboratory to field levels. Eco-
logical research on identification and conservation of
resources, development of better research and diagnostic
techniques, crop protection strategies, managed ecosys-
tems on implementation of ecologically based pest man-
agement and development of new institutional approaches
to encourage interdisciplinary cooperation, is required for
successful pest management in sericulture. New methods
must be developed to study, monitor, and evaluate pests
and potential biological control organisms in order to
expedite the acquisition of knowledge needed to imple-
ment EBPM. The lack of effective methodologies to char-
acterize ecological systems hampers research aimed at
generating the conceptual framework of sericulture eco-
systems on which EBPM will be based. The development
of molecular techniques useful in genetic manipulation of
plants, insects, and microorganisms provide an unprec-
edented opportunity for optimization of host plant resis-
tance or biological control activity; but these techniques
must be amended substantially to expand their usefulness
from model organisms to the diverse groups of plants and
biological control organisms that will comprise ecologi-
cally based pest management.
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