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Biology and use of the whitefly parasitoid Encarsia Formosa

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Abstract

Encarsia formosa is a parasitoid used worldwide for the biological control of whiteflies on vegetables and ornamental plants grown in greenhouses. Because of outstanding success in controlling Trialeurodes vaporariorum on tomatoes, the biology and behavior of this wasp have been intensively studied to identify attributes that contribute to successful biological control and how best to manipulate augmentative releases into greenhouses to suppress whitefly population growth. In this article, we review the biology of adult and immature E. formosa, population dynamics of whitefly-parasitoid interactions, and commercial use in greenhouses. Deficits in knowledge of aspects of E. formosa's biology and use are noted.
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Annu. Rev. Entomol. 1998. 43:645–69
Copyright
c
1998 by Annual Reviews Inc. All rights reserved
BIOLOGY AND USE OF THE
WHITEFLY PARASITOID
ENCARSIA FORMOSA
M. S. Hoddle
Department of Entomology, University of California, Riverside, California 92521;
e-mail: mark.hoddle@ucr.edu
R. G. Van Driesche
Department of Entomology, University of Massachusetts, Amherst, Massachusetts
01003; e-mail: vandries@fnr.umass.edu
J. P. Sanderson
Department of Entomology, Cornell University, Ithaca, New York 14853;
e-mail: jps3@cornell.edu
KEY WORDS: Aphelinidae, biological control, integrated pest management, whiteflies,
greenhouses
ABSTRACT
Encarsia formosa is a parasitoid used worldwide for the biological control of
whiteflies on vegetables and ornamental plants grown in greenhouses. Because
of outstanding success in controlling Trialeurodes vaporariorum on tomatoes,
the biology and behavior of this wasp have been intensively studied to identify
attributes that contribute to successful biological control and how best to ma-
nipulate augmentative releases into greenhouses to suppress whitefly population
growth. In this article, we review the biology of adult and immature E. formosa,
population dynamics of whitefly-parasitoid interactions, and commercial use in
greenhouses. Deficits in knowledge of aspects of E. formosas biology and use
are noted.
INTRODUCTION
Encarsia formosa (Hymenoptera: Aphelinidae) is used worldwide for com-
mercial control of whiteflies in greenhouse crops (142, 144). Commercial use
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646 HODDLE ET AL
began in Europe in the 1920s, but by 1945, interest waned owing to devel-
opment of pesticides. After 1970, use of the parasitoid was reinitiated and
has expanded from 100 hectares of greenhouse crops to 4800 hectares in 1993
(130,144). 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 (130). These are areas where increased
use of E. formosa would be possible.
Principal greenhouse crops in which E. formosa is used include tomato
(Lycopersicon esculentum) and cucumber (Cucumis sativus) (144). The par-
asitoid is also used, or being tested, to a lesser extent on eggplant (Solanum
melongena var. esculenta) and gerbera (Gerbera jamesonii) (130), poinsettia
(Euphorbia pulcherrima) (1,56,76,90), marigolds (Tagetes erecta) (49), and
strawberry (Fragaria X ananassa) (30).
E. formosa was described from specimens reared from an unidentified aley-
rodid on geranium (Pelargonium sp.) in 1924 in a greenhouse in Idaho (United
States) (35). There are no synonyms in the literature. Morphological descrip-
tions of all life stages are provided by Speyer (111). Because of releases into
greenhouses worldwide, E. formosa has a cosmopolitan distribution and its na-
tive range isuncertain. However, affinitytotheEncarsialuteolagroupsuggests
a Western Hemisphere origin (92).
The genus Encarsia is in need of revision, and keys at the world level are
currently lacking. A pictorial key to the 27 North American species has been
prepared (104). A world key for species of Encarsia associated with one
important pest host, Bemisia tabaci, is available (92).
E.formosa parasitizesat least 15 hosts in eight aleyrodidgenera(92,104). E.
formosa is hyperparasitized by Signiphora coquilletti, Encarsia pergandiella,
and Encarsia tricolor (5,13,164). Although E. formosa occasionally has been
reported attacking whiteflies on outdoor crops (38,80) or wild plants (39),
information is not available about its ecology or population dynamics in nature.
BIOLOGY OF E. FORMOSA
Foraging Behavior
HOST LOCATION To reproduce successfully in greenhouses, E. formosa must
locate potential hosts, assess host quality, and use nymphs appropriately for
host-feeding or parasitism. Following release into the host’s habitat (i.e. green-
houses), E. formosa apparently employs random searches to find hosts at all
spatial scales. Infested host plants, infested leaves, and whitefly patches are
found via random flight, landing, and walking sequences (136,142,146,150)
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BIOLOGY AND USE OF E. FORMOSA 647
without visual or olfactory cues (83, 136). When searching new leaves, the
parasitoid does not distinguish between upper and lower surfaces and shows no
preference for centers or edges of leaves (146,151). The rate at which hosts
are encountered is dependent on the parasitoid’s walking speed, whitefly size,
and number of hosts on a leaf (136). Walking speed is reduced by leaf venation
(136), high trichome densities (132, 136, 163), excessive honeydew (150,156),
encounters with nymphs suitable for host-feeding and parasitism (136), de-
creasing temperature (150), low barometric pressure (151), and smaller egg
loads (120,150).
Once E. formosa encounters hosts or their products in a patch, residencytime
on infested leaves increases 2- to 10-fold (142, 146, 150, 151). Factors that
trigger increased residency times include contact with honeydew (150,156),
whitefly exuviae, parasitized hosts, and oviposition in unparasitized hosts.
Following oviposition in a patch, E. formosas tendency to change position
from lower leaf surfaces (where whitefly nymphs are most common) to upper
leaf surfaces is significantly reduced. Contact with honeydew does not affect
the tendency of wasps to change leaf sides (146). Walking pattern and speed
on infested leaves are not affected by host encounters and are the same as on
uninfested leaves (142,146,150). Average residency time on tomato leaflets
when hosts are not encountered or since last host contact is approximately 20
min. On larger leaves such as gerbera, leaf residency times average 1 h. How-
ever, there is no general correlation between increasing leaf size and residency
time (151).
Patch abandonment is induced by passage of time since last host encounter
(146,150) and contact with parasitized hosts (137). When high numbers of
parasitized hosts are encountered, time spent cleaning and duration of un-
interrupted walking bouts increase, causing total leaf residency time to in-
crease. Time spent inspecting hosts decreases before wasps leave (137). Po-
tential trade-offs between leaving a patch of declining value in search of better
patches and mortality risks associated with inter-patch travel have not been
studied.
HOST USE E. formosa is a thelytokous, autogenous, synovigenic, solitary en-
doparasitoid that matures 8–10 eggs per day (67, 159). Daily egg maturation
and oviposition rates decline as wasps age (2). Adults obtain energy and nutri-
ents by consuming honeydewand hemolymph of hosts that are pierced with the
ovipositor, but in which no egg is deposited. Killing hosts for adult nutritional
purposes is termed host-feeding.
Egg load, the number of mature eggs available to a parasitoid for oviposi-
tion, and size of available hosts has been shown for some species to influence
the frequency with which hosts are used for either nutrition or reproduction
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648 HODDLE ET AL
(68,78). The influence of egg load on host-feeding by E. formosa has not been
determined.
E. formosa will host-feed on all pre-imaginal stages of T. vaporariorum
except the egg (123), but it prefers second-instar nymphs and pupae (82, 123).
However, the pupae and all nymphal instars of B. tabaci are used equally
for host-feeding (27). To host-feed, E. formosa wounds nymphs or pupae
by probing with the ovipositor for up to 6 min and feeds from wounds that
wasps may enlarge with their mandibles (123,135). This probing followed by
feedingkillshosts(82). Nymphsthathavebeenusedforfeedingarenotusedfor
oviposition, and previously parasitized whiteflies are not used for host-feeding
(82).
E. 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 (12,27,81). E. formosa prefers to oviposit
in third- and fourth-instar and prepupal nymphs of both T. vaporariorum and
B. tabaci (12,27,81,82). The rate of successful emergence of the parasitoid
is highest from these preferred stages (81,82). E. formosa does not oviposit
in up to 50% of suitable hosts in 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 (137).
Experimental evidence is lacking as to what cues are used by E. formosa
to determine host size. Wasps may use their antennae to obtain olfactory and
resonance information about hosts, and this information, coupled with stimuli
received while making 180
turns on the dorsum of the nymph, may be used to
determinehostsize(82,135). Behaviorsassociatedwithhostsearching,hostse-
lection, oviposition, and host-feeding have been described (83,123,135,150).
A host of suitable size for parasitism requires further evaluation by par-
asitoids to determine if it has been previously parasitized. E. formosa avoids
self-superparasitism with 100% efficiency (150), but the mechanism is unde-
termined. Wasps avoidsuperparasitism of non-self conspecifics with 90–100%
efficiency, providedthatimmatureparasitoidsin hostsarelarvaeorpupae(137).
Ifimmatureparasitoids are eggs,efficiency of discriminationis86% (150). The
mechanismfordetectionofnon-selfconspecificparasitismhasnotbeenstudied,
but it may involve both antennal inspection of the host and ovipositor inser-
tion. If conspecific eggs are detected in the host, they may be pushed to one
side or pierced with the ovipositor before oviposition by the second wasp (3).
Experienced parasitoids superparasitize as frequently as naive females (150).
In artificial arenas, superparasitism increases as the wasp-host ratio increases
(15). The ability of E. formosa to avoid oviposition in hosts parasitized by
other species has not been determined, and how wasp larvae might compete
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BIOLOGY AND USE OF E. FORMOSA 649
with each other within a single host is unknown following either super- or
mulitple-parasitism.
Biology of the Adult Parasitoid
FECUNDITY AND LONGEVITY E. formosa has 5–16 ovarioles, each with up to
three mature eggs (67, 143, 157–159). Ovariole number and body size (mea-
sured as head width) are positively correlated (157,158). Numbers of mature
eggsincrease when the wasp has access to carbohydrates, and eggsare resorbed
afterthreedaysat 20
Cintheabsence of suitable hosts (143). Oogenesisoccurs
between 10
and 40
C and is greatest at 25
C (159). All available mature eggs
can be laid within 1 h, and oviposition occurs predominantly in the morning
(67). Daily oviposition rates decline as wasps age (2). The morphology of the
reproductive system has been described (126).
Longevity of E. formosa is not correlated with body size (as measured by
headwidth) (143) and decreases with increasing temperature (124). At 20
C,
longevity is greatest when wasps can oviposit and feed at 52 days (143). Natal
plants of the host affectparasitoid longevity. In the laboratory, whenhoneywas
providedasa carbohydratesource, waspsthat emerged from hosts on cucumber
lived significantly longer thanthosefrom hosts on tomatoortobacco (Nicotiana
tabacum) (143).
Bothfecundityandlongevitycan be affectedbythehostfromwhichthe wasp
is reared. E. formosa reared from a large whitefly such as Aleyrodes proletella
have significantly more ovarioles than wasps reared from smaller hosts such
as T. vaporariorum (158). Wasps reared from B. tabaci have lower fecundity
and longevity compared to wasps reared from the larger host T. vaporariorum
(122). Parasitoids foraging on poinsettia live for 9 or 12 days at 21
C when
reared from B. tabaci and T. vaporariorum, respectively (122). These differ-
ences can be reduced after E. formosa has been reared on B. tabaci for 5–18
generations (9). Life-time fecundity, daily oviposition rates, and longevity at
various temperatures have been determined (2,19, 122, 124, 141, 159).
THELYTOKY Thelytoky in E. formosa is mediated by Wolbachia bacterial in-
fections (119,172). Exposure of females to antibiotics or high temperatures
(31
C) for two or more generations (172) suppresses microbial activity, allow-
ing females to successfully produce male offspring. Fecundity is reduced once
symbionts are eliminated (119). Males develop as primary endoparasitoids of
whiteflies (172). The mating behavior of E. formosa has been described (66);
however, males are unable to inseminate females successfully (172).
ADULT DISPERSAL Flight of adult wasps in greenhouses commences 1–3 h
after sunrise and is greatest in the early afternoon under both short and long day
conditions (26). Flight activity is positively correlated with temperature (26)
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650 HODDLE ET AL
and can occur at temperatures as low as 13
C (124). At 18
C on tomato, wasps
migrate up to5min90min(124). Nocturnal flight is rare (26), and wasps
will disperse shorter distances at low light intensities (less than 500 lux) than
at high light intensities (greater than 8000 lux) (140). Short days and low light
intensity may affect the efficacy of E. formosa (88).
Biology of the Immature Parasitoid
The lower thermal threshold for development of pre-imaginal stages is 10.5
13.3
C(27,87,141,149). Eggtoadulteclosionrequires188.9–207day-degrees
above the thermal threshold (27, 87), and development may be faster under
fluctuating temperatures (115). The upper lethal temperature for immature E.
formosa has been estimated as 38.3
C (149).
Whitefly life stage influences E. formosa mortality rates and developmental
times. Eggs laid by E. formosa successfully hatch and develop in all nymphal
stages and the pharate adult of T. vaporariorum [pharate adult stage plus the
transitional substage described by Nechols & Tauber (81) equals the “pupa”
of other workers]. The parasitoid’s development does not pass the first instar
until the host reaches the fourth instar. E. formosa completes its life cycle
and emerges as an adult from fourth-instar whitefly nymphs when oviposi-
tion occurs in prepupal whitefly stages, and from the pharate adult stage when
oviposition occurs at the transitional substage of the pharate adult (81). Wasps
that begin development in third- and fourth-instar nymphs exhibit highest sur-
vivorship, and developmental times are reduced by approximately 38% (81).
Developmental rates for E. formosa in each nymphal stage of T. vaporariorum
at various temperatures have been estimated (2, 149). The physiological mech-
anism synchronizing development of E. formosas larva with that of its host is
unknown, as are mechanisms by which quiescent or developing larvae counter
host defenses.
Whiteflyspeciesidentityaffectsbothmortalityratesanddevelopmentaltimes
of immature wasp stages. When E. formosa is reared in B. tabaci instead of
T. vaporariorum, pre-imaginal mortality increases 1.3-fold to 8-fold (12, 122)
and developmental time increases 22% (122).
The plant host on which the whitefly develops also affects E. formosa devel-
opment. For seven plant species on which Trialeurodes ricini was reared, E.
formosa development times were significantly longer on French bean (Phase-
olus vulgaris) (the poorest host) than on cotton (Gossipium hirsutum) (the best
host). Mortality of immature parasitoids did not differ between host plants
in this experiment (109). At 22.5
–25
C, development of immature E. for-
mosa in fourth-instar T. vaporariorum nymphs required 15 days on tomato
(163), tobacco (2), eggplant, cucumber, and sweet pepper (Capsicum annum)
(163). Development time is longer (24.5 days) on poinsettia (122) at similar
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BIOLOGY AND USE OF E. FORMOSA 651
temperatures. Survival of immature parasitoids varies significantly between
poinsettia cultivars when Bemisia argentifolii (=B. tabaci strain B) is the host
(50).
E.formosapupatesfacingthe host’sventer, withitsheaddirected towardsthe
host’s anterior (71). The prepupa excretes two to four meconial pellets along
the lower margins of the host. The pharate adult parasitoid requires 25–98 min
to rotate within the host to face the dorsal surface. From this position, the adult
parasitoidchewsa holethrough the host’s dorsumand emerges(71). Peak wasp
emergence occurs within4hofsunrise (140).
POPULATION DYNAMICS
Sampling
Whitefly population densities must be estimated in order to determine when
to start parasitoid releases and to measure the effectiveness of releases. Such
estimations have been made with three approaches: trap counts, presence-
absence ratios on inspected plants, and direct counts of whitefly stages on
plants. Trap counts (as number of adult whiteflies caught per yellow sticky
trap) are least precise but are widely used as monitoring tools because they are
economical in terms of labor for whitefly monitoring. To detect whiteflies in
the range of 0.01–0.1 adults perplant on tomato requires one trap per 180 plants
(41). This system has been used with tomato crops in Canada to time initial
control measures.
Presence-absence sampling plans are based on correlations of the proportion
ofsamplesbearingeitherhealthyorparasitizedwhiteflystageswithpestdensity.
Such sampling has been used in cucumber (47) and tomato crops (73,74) to
monitor T. vaporariorum and E. formosa population levels.
Accuracyofdirectcountsofwhiteflydensitiesareinfluencedbytheirclumped
distribution. Efficiency of a three-stage (plant, leaf, leaflet) system developed
by Yano (169) was compared to presence-absence and trap count methods on
tomato. Presence-absence sampling and trapping are the least complicated and
are considered to be the most useful for monitoring T. vaporariorum densities
(169). Rumei et al (100) analyzed several sampling plans to monitor the popu-
lation densities of T. vaporariorum for ecological studies and found that none
gave the level of accuracy (10% error, 95% confidence level) needed for such
research. They attributed this deficiency to the highly contagious distribution
of the whitefly.
Host/Parasitoid Dynamics
Attempts to understand the dynamic interaction of E. formosa withits hosthave
been driven by the desire to predict whitefly population growth in commercial
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652 HODDLE ET AL
greenhouses. Secondarily, E. formosas interaction with T. vaporariorum has
also been modeled in an attempt to identify factors that stabilize such interac-
tions (14, 16, 17, 165, 170, 171). Factors affecting population dynamics of E.
formosa and T. vaporariorum in greenhouse vegetable systems include host-
parasitoid ratios, starting density and age structure of whitefly populations at
time of first parasitoid releases (17,31), levels of host-feeding and parasitism
(18), temperature, and host plant (98). Methods used in these studies have
included estimating correlations under non-experimental regimes between ob-
served conditions and outcomes, conducting experiments to identify factors
affecting population dynamics, and developing models to predict the dynam-
ics of population interactions and the effects of parasitoid release regimens on
whitefly population growth.
Burnett studied E. formosas interaction with T. vaporariorum (14,16) and
found that initial whitefly density (17) and the interaction between host-feeding
and whitefly population age structure (18) strongly influenced the dynamic out-
come. Van Lenteren et al (131) concluded that multiple introductions of E.
formosa over a 16-week period were necessary to stabilize E. formosaT. vapo-
rariorum population fluctuations on greenhouse tomatoes. Foster & Kelly (31)
observed that densities of T. vaporariorum on greenhouse tomatoes typically
increased three orders of magnitude after E. formosa releases before declining.
They concluded that an initial population density of 0.1 T. vaporariorum adults
per leaf was the highest on tomato against which E. formosa releases might be
commercially successful (31).
Life tables of T. vaporariorum in the presence and absence of E. formosa
showedthat parasitoids reduced overallwhitefly survival from 68.9% to25.1%,
followinginoculativerelease on tomato in an unheated greenhouse (65). Paired
life tables for B. argentifolii from a commercial greenhouse in which E. for-
mosa was released on poinsettia at an average rate of 6 females/plant/week
showed that whitefly survival from the settled first-instar nymph to the adult
was only 14% in the wasp release area, compared with 67% in caged controls
that excluded E. formosa (56). This level of suppression did not, however, pro-
vide commercially acceptable control on this crop. Spatial effects of whitefly
aggregation on whitefly population dynamics were examined by Eggenkamp-
Rotteveel Mansveld et al (24, 25) by counting whitefly stages and parasitism in
patches of T. vaporariorum on greenhouse tomatoes. In this study, T. vaporari-
orum and E. formosa exhibited stable dynamics because whitefly patches were
not fully exterminated by parasitoids (24,25).
Within-patchdynamicsofthe effectofE.formosaonsurvivorshipofwhitefly
nymphs has also been examined. As the number of whitefly nymphs in a patch
increases, the proportion attacked by individual parasitoids decreases, which
exemplifies a Type II functional response. Type II responses have also been
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BIOLOGY AND USE OF E. FORMOSA 653
observed in the laboratory with T. ricini and in laboratories and greenhouses
with T. vaporariorum, B. tabaci, and B. argentifolii (28,34,55,91,108,168).
The functional response of E. formosa is affected by temperature (28), sub-
lethal insecticide residues on leaves (91), numbers of searching parasitoids
in greenhouses (168), egg load, successful oviposition, and walking activity
(147).
Several types of population models have been used to describe dynamics
between E. formosa and its whitefly hosts. Yamamura & Yano (165) devel-
oped a Lotka-Volterra–type differential equation model and determined that
intermediate values of the host-feeding/parasitism ratio led to the lowest T. va-
porariorum density and the least variation in population size. A simulation
model incorporating a modified disc equation to account for parasitoid func-
tional response has been used to examine variables associated with population
stability (170,171). Stability resulted from declining parasitoid efficiency at
highparasitoid densities thatwere due toseveral factors,including host-feeding
and moderate levels of mutual interference between parasitoids.
A systems model to simulate the host plant–T. vaporariorumE. formosa
system was developed and used to examine the role of host plant, temperature,
and parasitoid release rate on whitefly population dynamics. This model used
relative age instead of physiological time to investigate the effects of varying
conditions on population dynamics (98, 99). Life-history parameters for E.
formosa and T. vaporariorum in relation to host plant, temperature, and, for
the parasitoid, host stage were determined by van Roermund & van Lenteren
(148,149). Using this information together with observations on the foraging
activity of E. formosa, van Roermund developed an individual-based model
that simulates local searching and parasitism behavior of individual parasitoids
in order to simulate parasitoid/host population dynamics in a whitefly-infested
tomato crop (152).
Effect of Cropping System on Parasitoid Efficacy
PHYSICAL FACTORS Among the physical factors of potential importance to
host-parasitoid dynamics are greenhouse temperature, physical spacing of a
crop, and fertilization regime. Among these, most attention has been focused
on effects of greenhouse temperature, mainly low temperature.
Summer temperatures in some greenhouse areas such as the northeastern
United States can be at or above the maximum temperature tolerated by E.
formosa (M Hoddle, unpublished data). E. formosa can survive and reproduce
when daily maximum temperatures exceed 35
C for a few hours for 7–11 days
(75). Survival at these temperatures is greater than that of other Encarsia spp.
(e.g. E. tricolor) thathave beenevaluatedfor use ingreenhouseswhere summer
temperatures are high (4).
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654 HODDLE ET AL
Low temperature regimes in greenhouses have been used to reduce produc-
tion costs associated with fuel consumption. Optimal greenhouse temperature
for T. vaporariorum control with E. formosa is around 23
C (51). However,
van Lenteren and colleagues (133) in reviewing the literature stated that the
parasitoid might perform better at lower temperatures than previously thought.
Control by E. formosa was effective when 8 parasitoid pupae per plant were
introduced every 2–3 weeks when nocturnal temperatures were 5
,8
,or11
C
on tomato in Japan (166). Releases of E. formosa suppressed whitefly popu-
lations by week 13 when greenhouse temperature was maintained at 18
Cin
the day and reduced to 7
C at night in trials on tomato in the Netherlands (62).
Values ofintrinsic rates ofincrease for E. formosa at several temperatures (12
,
15
, and 24
C) have been compared to those for T. vaporariorum to estimate
the ability of E. formosa to suppress the whitefly under reduced temperature
regimes on tomatoes (134). Enkegaard (27) determined developmental time
and juvenile mortality of E. formosa parasitizing B. tabaci on poinsettia at 16
,
22
, and 28
C. Intrinsic rates of increase for E. formosa were greater than those
for T. vaporariorum and B. tabaci at the temperatures tested (27,134).
Physical factors such as greenhouse size and interplant spacing of the crop
may also affect parasitoid foraging efficiency. Biological control is less stable
in smaller greenhouses (<1000 m
2
) (24,25,101,142). A suggested reason for
this lower stability is that in small greenhouses, releases of parasitoids often
achieve higher initial wasp-whitefly nymph ratios and at these higher ratios
host-feeding and superparasitism reach high levels, which result in extinction
of pest and parasitoid (24, 25, 101). Reinvasion of greenhouses by whiteflies
and subsequent uncontrolled pest population growth may then result (142).
Crop fertilization can sometimes disrupt the controlling action of natural
enemy populations if pest populations experience greater increases in their
population growth rates owing to increased nitrogen in their diet than their nat-
ural enemies do. For B. tabaci, fertilization of poinsettia plants did not affect
whitefly developmental time but did reduce mortality of immature stages (7).
Fertilized poinsettia plants (which received either calcium nitrate or ammo-
nium nitrate) infested with B. argentifolii attracted more E. formosa (Beltsville
strain) adults than unfertilized controls, and wasps on fertilized plants in a no-
choice experimental design killed more whiteflies through host-feeding than
on unfertilized control plants (8). However, long-term effects of fertilization
on the population balance between whiteflies and parasitoids have not been
investigated.
PLANT FACTORS Among the plant factors that might affect the efficacy of E.
formosa are plant species, variety, morphological features such as trichome
number and kind, and increases in canopy size over the cropping period.
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BIOLOGY AND USE OF E. FORMOSA 655
Greenhouse whitefly control with E. formosa is good on tomato and sweet
pepper, poor on cucumber, and intermediate on eggplant (145,163). At least
two factors contribute to these outcomes: the quality of the plant for growth of
immature whiteflies and the suitability of the plant surface for parasitoid forag-
ing. Tomato, for example, is a relatively poor host for whitefly development,
and its leaves are suitable for parasitoid foraging. These factors together confer
a population advantage to the parasitoid (163). In contrast, cucumber is a more
favorable host for T. vaporariorum, and its leavesare lesssuitable for parasitoid
foraging because of retentiform venation and large trichomes (163).
Within crops, cultivars may vary in their effects on the interactions between
parasitoid and whitefly populations. Among 12 tomato cultivars, few differ-
encesin parasitism rates were found; however, some evidencesuggested greater
suitability of one cultivar for the whitefly (45). Among 5 poinsettia cultivars,
those with lower trichome densities, such as Annette Hegg Brilliant Diamond,
supported higher levels of host-feeding and parasitism by E. formosa than did
other cultivars (50). Cotton varietieswith lowtrichome density and an alternate
leaf shape (termed okra) supported higher parasitism levels by E. formosa and
lower densities of B. tabaci (110).
The plant feature investigated most often in relation to parasitoid efficacy
has been the density of leaf trichomes (63,100, 121, 132). Crop cultivars with
low trichome densities have been found to be more favorable than those with
high densities in cotton (110) and cucumber (132). On G. jamesonii cultivars
with trichome densities from 80–1000 per cm
2
, no differences could be de-
tected in parasitoid foraging abilities (121). Comparisons across crop species
showedthatparasitoidwalkingspeed (which correlates positivelywithforaging
success) was greatest on species with lower trichome density (63). Glandular
trichomes that exude sticky or toxic materials are particularly unfavorable to
parasitoid foraging (22).
When E. formosa is used where little in-crop reproduction is expected and
parasitoid density depends on weekly releases, simple growth of the crop plant
willstronglyinfluencetheeffectivenessoftheparasitoid. Increaseinthecanopy
volume to be searched by parasitoids will lower the parasitoid-to-leaf area ratio
progressively if weekly releases remain constant (55).
COMMERCIAL USE
Mass Rearing, Product Control, and Storage
E. formosa was first mass reared for T. vaporariorum control in England in
1927, and by 1930, 1.5 million parasitized whitefly nymphs were produced
annually and distributed on tomato leaves (112,113). Details of mass rearing
systems for E. formosa are available (105,106). Tobacco is currently the host
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656 HODDLE ET AL
plant commonly used for commercial production (95). Parasitized T. vaporari-
orum nymphs were originally distributed on plant material (113), but problems
associated with this practice [e.g. distribution of pests or diseases on leaves
(95)] led to the development of other distribution methods. Currently, para-
sitized whitefly nymphs are removedfrom leaves by brushing (106)or washing
(93) and glued to cardboard strips for distribution (95).
Failure of biological control with E. formosa has sometimes been associated
with use of parasitoids of poor quality (129) or inconsistencies between num-
bers of parasitoids ordered and numbers received, which affect release rates
(103). Quality control tests for E. formosa have been designed to determine if
mass-reared wasps can fulfill their intended role after release into greenhouses
(128,138). Product control standards for companies that mass produce natural
enemies have been developed (129, 139), and in several European countries,
registration of natural enemies for pest control is contingent on availability of
quality and efficacy data (129).
Quality assessment for E. formosa includes validation of quantities of par-
asitized nymphs shipped and emergence rates, adult size, fecundity, and flight
ability (95,138,139). Testing just before shipping is recommended (139).
Cold storage of parasitized pupae following harvest is possible and may be
necessary in some instances (107). Parasitized pupae can be stored at 9
–12
C
for 15–20 days without affecting adult emergence rates (36). Storage at low
temperatures (9
C) for more than 5 days, however, reduces adult longevity and
fecundity (37).
Methods of Use
RELEASE METHODS Four distinct methods of releasing E. formosa into green-
houses for whitefly control have been suggested. Three of these (“pest in first,
“dribble, and “banker plants”) are inoculative in nature and establish a re-
producing 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. In these cases, whitefly mortality results
from host-feeding or superparasitism (55,58).
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 (42)]. E. formosa is later introduced one to three times at a standard rate
[e.g. eight parasitized nymphs per tomato plant (42)] at regular intervals that
coincide with availability of host stages suitable for parasitism (42, 88). This
method has not been widely adopted because of concern over releasing pests
onto the crop.
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BIOLOGY AND USE OF E. FORMOSA 657
With the dribble method, parasitoid introductions begin at planting in antic-
ipation of natural development of a whitefly population (42, 88, 118). Regular
parasitoid releases at a low rate (e.g. one parasitized nymph per plant) continue
until parasitized nymphs are found in the crop (42).
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 (114). Banker plants are introduced at a fixed rate [e.g. 1 banker
plant per 352 crop plants (114)]. 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 (10).
Inundative programs require regular releases of high numbers of E. formosa;
establishment and reproduction of the parasitoid in the crop are not expected.
This method is applied most frequently to ornamental crops (55,56,90).
EFFICACY OF RELEASE RATES AND METHODS The pest-in-first, dribble, and
bankerplant techniqueshave providedsuccessfulcontrol of T. vaporariorumon
cucumber and tomato crops (42,88,114,118). 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.
>0.02–0.03 nymphs per cm
2
in poinsettias (M Hoddle, unpublished data)] is
considered damaging, and market standards require greater levels of whitefly
suppressionthanareusedforvegetablecrops[e.g.7.0nymphspercm
2
intomato
(64)]. Consequently, use of E. formosa has been more extensive on vegetables
than on floral crops (89,144).
Inundative releases of E. formosa have been successful in some instances for
control of T. vaporariorum on poinsettia (76). Control of B. argentifolii with
weekly releases of more than three adult parasitoids per plant per week, has
not been accomplished (56,90). However, control of this whitefly species has
been reported with lower weekly release rates (under two parasitoids per plant)
(97,117), or when T. vaporariorum co-occurred in the crop (1). In one study,
as the number of parasitoids released per plant increased, parasitoid efficacy
decreased, and B. argentifolii survivorship increased (60).
Effective testing of parasitoid release strategies and rates requires the use of
replicated treatments in independent greenhouses (e.g. 55,58,59,88,118) and
the use of experimental controls either in cages (e.g. 56,90) or separate green-
houses (e.g. 55, 58, 59). Whitefly populations in control areas that develop in
the absence of E. formosa provide comparisons with whitefly densities in bio-
logical control or chemically treated greenhouses (e.g. 55, 56, 58, 59). These
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October 27, 1997 17:49 Annual Reviews AR048-28
658 HODDLE ET AL
comparisons provide explicit measures of whitefly suppression [e.g. compar-
ative life tables (e.g. 55, 56, 58, 59), whitefly densities, and crop quality (e.g.
42,56,88,90,114,118)].
Observations from experiments in which treatments were unreplicated (e.g.
42,56,90,114), lacked controls (e.g. 42,88,114,118), or lacked comparisons
with whitefly populations treated with insecticides under commercial growing
conditions (e.g. 42, 114, 118) are not useful in determining the magnitude and
variabilityofsuppressionofwhiteflypopulationgrowthbyE.formosa. Efficacy
and cost effectiveness of parasitoid releases can be determined by comparing
whiteflydensitiesonplantssubjectedtoprevailinginsecticidepractices(56, 58–
60). Furthermore, percentage parasitism estimates as indicators of the attained
levelsof control should beusedcautiouslybecause theycanbe unreliable (125).
Integration of E. formosa into IPM Programs
IPM MONITORING AND GROWER TRAINING Use of E. formosa in the produc-
tion of greenhouse crops has been most successful where grower support ser-
vices are available. Training growers in monitoring, correct use of biological
control agents, and techniques for integrating wasp releases with other control
measureshavebeenessentialactivities. Suchtrainingbeginswithmakingavail-
able descriptions of the pests and their management with the biological control
agents (57). More specific information on topics such as integration with pesti-
cides (e.g. 69, 116) and monitoring techniques (41, 47, 74) is required. Simple
models for making decisions about need for and timing of parasitoid releases
(57,86) can be useful. Guidance on ordering and release of parasitoids is of
value to growers not previously experienced in the use of biological control
(57). Adoption by growers can be encouraged by demonstrations that provide
growers opportunities to observe field trials (72).
INTEGRATION WITH OTHER CONTROL METHODS Use of E. formosa may re-
quire integration with other controls for whiteflies or other pests. Techniques
with which E. formosa releases might need to be combined include cultural
control, use of other biological control agents, and pesticides.
Cultural practices The principal forms of cultural control that can be com-
bined with releases of E. formosa are inspection of new plants, sanitation,
monitoring, and use of yellow sticky traps. New plant inspection is intended to
identify infested plant materials before theyare introduced into the greenhouse.
Incoming materials should be examined, and, if possible, infested plants iso-
lated and treated with compatible controls before placement with other plants.
Sanitation (e.g. weed control and roguing infested plants) eliminates sources
of whiteflies. Monitoring is necessary to enable growers to identify developing
pest infestations early and to treat localized pest populations before they are
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October 27, 1997 17:49 Annual Reviews AR048-28
BIOLOGY AND USE OF E. FORMOSA 659
spread by plant movement or plant disposal in composting areas, from which
pests might invade previously uninfested greenhouses. Yellow sticky traps,
in addition to use in monitoring whitefly populations, may be used as control
measures to trap out small whitefly populations (153,155,162). In tomato
(11,153,155) and eggplant (11) crops, traps enhanced whitefly control while
allowing percentage parasitism to increase, although some authors felt the in-
crease in pest control from the addition of traps was slight compared to control
by parasitoid releases alone (167). Screening materials can prevent pests en-
tering greenhouses through intake vents (10).
Other natural enemies Other natural enemies of greenhouse whiteflies have
been examined as agents that might either be combined with releases of E.
formosa or might be substitutes for E. formosa to enhance efficacy of biolog-
ical control for whiteflies. Agents considered for use in combination with E.
formosa include several species of entomopathogenic fungi and a predacious
bug and beetle. Among the fungi, most attention has been focused on Ascher-
sonia aleyrodis (32,33). Selectivity of this species has been observed in that
fungal spores do not infect parasitized whiteflies bearing immature parasitoids
older than three days (33) and foraging parasitoids rarely oviposit in white-
flies infected by the fungus (32). This species appears to be compatible with
use of E. formosa. Other fungal species of interest for combination with para-
sitoid releases include Verticillium lecanii (96) and Paecilomyces fumosoroseus
(154). In Europe, E. formosa has been usedwith the mirid, Macrolophus calig-
inosus until this predator exerted an effect on whitefly population growth(102).
Another predator, the coccinellid Delphastus pusillus, has been tested for com-
patibility with use of E. formosa and found to be valuable in suppressing high
density whitefly patches (48).
Various other species of aphelinids have been considered as alternatives to
E. formosa. Among these have been Eretmocerus spp. (23,58,160) and two
hyperparasitic species, E. tricolor (4, 6) and E. pergandiella (13,160). Models
suggest that the efficacy of biological control is reduced if heteronomous and
primary parasitoids such as E. formosa are used together (77). No definitive
study has provided data on this issue.
Integration of controls for several different pests has also been of concern.
Where use of E. formosa for whitefly control is practiced, biological controls
for other pests such as leaf miners (79, 144), fungus gnats (46), aphids, spider
mites, and thrips (144) may also be needed.
Pesticides More than 70 articles have been published that examine interac-
tions 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
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October 27, 1997 17:49 Annual Reviews AR048-28
660 HODDLE ET AL
(43,61,84). The effects of more than 100 different compounds on E. formosa
have been determined (see especially 52,70,85). Selective materials of inter-
est for possible combination with E. formosa include insecticidal soap (94),
buprofezin (40), azadirachtin (29), abamectin (173), and resmethrin (86).
GENETIC IMPROVEMENT Genetic improvement to E. formosa has been at-
tempted with regard to insecticide resistance (20,161), increased fecundity
(157,158), and improved performance on B. tabaci (53,54). Efforts to se-
lect for resistance to bioresmethrin, deltamethrin, and parathion failed (20,21).
Selection for resistance to lindane was partially successful (161). Selection
for increased ovarial number was not successful (157,158). Populations of E.
formosa exhibit differential reproductive performances on whitefly hosts, with
somewasppopulationsoutperformingothers on a particularhost(9,50,53,54).
Variation between E. formosa populations in levels of parasitism and host con-
tact times on B. tabaci, for example, may be due to genetic factors (54) rather
than conditioned responses to hosts from which wasps eclosed (53). Devel-
opment of molecular techniques to identify strains of E. formosa would be
useful.
ECONOMICS Few data are available that measure the cost of using biological
control compared with other forms of whitefly control. Assessment of use on
tomato concluded that beginning E. formosa releases earlywas the most secure
method of control, but it was often unjustifiable economically (88). Danish
growers preferred biological control of whiteflies in cucumber and tomato and
perceived biological control to be less expensive than insecticides (44). Com-
parison of control costs on vegetables in Europe found E. formosa use to be less
expensive then chemical control (127). On poinsettia in Germany, releases of
E. formosa were found to be about two thirds the cost of chemical control (1).
In Massachusetts, however, releases of E. formosa combined with insecticide
applications were 9.5 times more expensive than the use of insecticides alone
to produce a marketable crop (56).
CONCLUSIONS
E. formosa is widely employed for control of whiteflies on greenhouse crops,
especially vegetables, and factors contributing to successful biological control
have been identified. First, whitefly population growth is reduced when E.
formosas intrinsic rate of increase is greater than the host’s intrinsic rate of
increase in the presence of parasitoids. This situation arises when host plants
facilitateparasitoid searching and exhibit partial resistance to whitefly develop-
ment. Second, giving-up time on infested leaves increases when hosts or host
products are located, increasing the likelihood that parasitoids will encounter
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October 27, 1997 17:49 Annual Reviews AR048-28
BIOLOGY AND USE OF E. FORMOSA 661
suitable hosts in a patch. Third, spatial refuges for whiteflies from parasitoids
exist in large greenhouses (>1000 m
2
), thus promoting stable host/parasitoid
dynamics.
Although many aspects of E. formosas biology have been well studied,
significant gaps in our understanding of this parasitoid still exist. For example,
little is known about E. formosas ecology in nature, the influence of egg load
on host-feeding, what cues are used to determine host stage, and how larvae
affect the cellular immune responses of a wide range of whitefly hosts.
At present, biological control of whiteflies on ornamentals with E. formosa
is generally not commercially feasible. Further research is needed to improve
our ability to use E. formosa inundatively to produce ornamental crops with
very low whitefly densities at harvest. One avenue of investigation would be
to adjust release rates and timings to compensate for differences in foliage and
pest density and for changes in levels of parasitism over the growing season.
Several strains of E. formosa obtained from various localities around the world
are currently in culture. Development of molecular techniques for strain iden-
tification and efficacy trials against B. argentifolii on greenhouse ornamentals
with these parasitoids are needed.
A
CKNOWLEDGMENTS
We thank OPJM Minkenberg and TS Bellows Jr for reviewing this manuscript
and providing useful comments.
Visit the Annual Reviews home page at
http://www.AnnualReviews.org.
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... Encarsia formosa Gahan (Hymenoptera: Aphelinidae) ( Figure 1) is a small, parasitoid wasp that attacks several species of whiteflies. It is one of the most commercialized natural enemies and used worldwide in controlled production systems (greenhouses and nurseries) for biological control of whiteflies on ornamentals and vegetables (Hoddle et al. 1998). The earliest record of E. formosa parasitic activity was observed in 1926, when an English tomato grower observed black pupae among greenhouse whitefly pupae, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae) on the leaves (Figure 2) and over time observed E. formosa emerging from these pupae. ...
... Encarsia formosa is a cosmopolitan parasitoid with an ambiguous native range (Hoddle et al. 1998). Its similarity to Encarsia luteola Howard suggests that this species first emerged in the Western Hemisphere (Hoddle et al. 1998;Polaszek et al. 1992). ...
... Encarsia formosa is a cosmopolitan parasitoid with an ambiguous native range (Hoddle et al. 1998). Its similarity to Encarsia luteola Howard suggests that this species first emerged in the Western Hemisphere (Hoddle et al. 1998;Polaszek et al. 1992). Current records of its greenhouse usage show that it is widely utilized in various parts of Europe and Russia, and there are excellent prospects for its use in greenhouse production systems in North America and Asia as well, where this species is currently underutilized. ...
Article
Full-text available
Encarsia formosa Gahan (Hymenoptera: Aphelinidae) is a small, parasitoid wasp that attacks several species of whiteflies. It is one of the most commercialized natural enemies and used worldwide in controlled production systems (greenhouses and nurseries) for biological control of whiteflies on ornamentals and vegetables (Hoddle et al. 1998). The earliest record of E. formosa parasitic activity was observed in 1926, when an English tomato grower observed black pupae among greenhouse whitefly pupae, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae) on the leaves and over time observed E. formosa emerging from these pupae. In England, E. formosa was first used commercially a year later to control T. vaporariorum in hothouses (Speyer 1927), and by the 1930’s, E. formosa hademerged as a successful commercialized natural enemy for whiteflies and was sold to nurseries both within and outside of Europe (Van Lenteren and Woets 1988). With the growing popularity of synthetic chemical insecticides after World War II, biological control methods became less common, and the demand for the parasitic wasps declined substantially. However, reports of insecticide resistance development among pest insects in the following decades brought biological control methods back into vogue.
... The endoparasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae) is known to be efficient in controlling the greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) (Hoddle et al. 1998;De Vis and van Lenteren, 2008;Liu et al. 2015). In the absence of control measures, T. vaporariorum can cause between 30 to 100% yield losses to tomato (Solanum lycopersicum L. (Solanaceae)) in both open fields and greenhouses in many parts of the world (Hanssen and Lapidot 2012; Gamarra et al. 2016;Perring et al. 2018). ...
... In addition, the use of these insecticides is associated with human and environmental health risks (reviewed by Thompson et al. 2020). The use of biocontrol agents such as the parasitoid E. formosa has been reported to play a key role in controlling T. vaporariorum on tomato plants grown in greenhouses (Hoddle et al. 1998;Hu et al. 2002;De Vis and van Lenteren, 2008). In the field, this parasitoid has shown parasitism rates of 30-50% on T. vaporariorum and a related whitefly species, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) (Udayagiri and Bigelow 2000;Zhang et al. 2011). ...
Article
Full-text available
Kairomones are semiochemicals that are emitted by an organism and which mediate interspecific interaction that is of benefit to an organism of another species that receives these chemical substances. Parasitoids find and recognize their hosts through eavesdropping on the kairomones emitted from the by-products or the body of the host. Hemipteran insect pests feed on plant sap and excrete the digested plant materials as honeydew. Honeydew serves as a nutritional food source for parasitoids and a medium for micro-organisms whose activity induces the release of volatiles exploited by parasitoids for host location. The parasitoid Encarsia formosa preferentially parasitizes its host, the greenhouse whitefly, Trialeurodes vaporariorum, on tomato Solanum lycopersicum, but little is known about the chemicals that mediate these interactions. We investigated the olfactory responses of the parasitoid E. formosa to odours from honeydew and nymphs of T. vaporariorum in a Y-tube olfactometer. Arrestment behaviour of the parasitoid to honeydew and nymph extracts, as well as to synthetic hydrocarbons, was also observed in Petri-dish bioassays. We found that T. vaporariorum honeydew volatiles attracted the parasitoid E. formosa but odours from the whitefly nymphs did not. We also found that the parasitoid spent more time searching on areas treated with extracts of honeydew and nymphs than on untreated areas. Gas-chromatography-mass spectrometric analysis revealed that the honeydew volatiles contained compounds such as (Z)-3-hexenol, δ-3-carene, 3-octanone, α-phellandrene, methyl salicylate, β-ocimene, β-myrcene, and (E)-β-caryophyllene which are known to be attractive to E. formosa. The cuticular extracts of the nymphs predominantly contained alkanes, alkenes, and esters. Among the alkanes, synthetic nonacosane arrested the parasitoid. Our findings are discussed in relation to how the parasitoid E. formosa uses these chemicals to locate its host, T. vaporariorum.
... u Europi se korištenje proširilo na 5000 ha. E. formosa prikladna je za korištenje na svim kulturama koje napada cvjetni štitasti moljac(Hoddle et al., 1998). Nizozemska tvrtka Koppert Biological Systems navodi kako u jednom tjednu proizvedu 20 milijuna jedinki, te da u zemljama s razvijenom poljoprivrednom proizvodnjom, primjerice u Novom Zelandu, E. formosa predstavlja primarnu biološku zaštitu koja se koristi u suzbijanju cvjetnog štitastog moljca (Koppert Biological Systems, 2021a). ...
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Invazivna alohtona vrsta europski mračnjak (Abutilon theophrasti Medik.) danas je jedna od najagresivnijih i najštetnijih korovnih vrsta u Hrvatskoj. Jakim habitusom s naglašeno velikim listovima vrlo brzo može zasjeniti uzgajanu kulturu uzrokujući značajne gubitke prinosa. Relativno krupno sjeme omogućuje mu nicanje i iz dubljih slojeva tla što zbog kontinuiranog nicanja s različitih dubina iz tla predstavlja problem u suzbijanju. Uz spomenuto, dormantnost sjemena ograničava prognozu nicanja i uspješno suzbijanje ove vrste. Kompeticija mračnjaka, osim morfološkim značajkama, izražena je i alelopatskim sposobnostima. Europski mračnjak eksudatima svih biljnih dijelova može izazvati inhibiciju rasta i razvoja biljaka u svojoj blizini. Za pouzdano i učinkovito suzbijanje europskog mračnjaka, osobito u kulturama slabijih kompetitivnih sposobnosti, nužno je integrirati sve raspoložive mjere suzbijanja
... 7 -11 In recent decades, biological control of greenhouse whitefly, Trialeurodes vaporariorum (Westwood), has been most commonly practised in greenhouses worldwide using Encarsia formosa Gahan. 9,12 However, compared to E. formosa, some Eretmocerus species may be more effective against T. vaporariorum because of their greater tolerance of a wide range of temperatures, 13 higher effectiveness in locating host patches, higher parasitism rates 12 and shorter pre-oviposition period. 13 Among the six Eretmocerus species that have been reared from T. vaporariorum, 14 E. warrae Naumann and Schmidt (Hymenoptera: Aphelinidae) is a thelytokous (no males) and specialist parasitoid. ...
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Full-text available
BACKGROUND: Mechanisms behind the success and failure of whitefly biological control using parasitoids are largely unknown. Here we use the Eretmocerus warrae−greenhouse whitefly system to investigate how the fluctuating density of the parasitoid and its host affects three key parasitoid fitness parameters, host searching, host feeding and parasitization, providing critical knowledge for evaluation and development of whitefly biological control programmes. This is the first such study in a parasitoid−whitefly system. RESULTS: Models used and developed here show that (1) both host feeding and parasitism fit a type II functional response; (2) overall parasitoid-caused whitefly mortality significantly increases with growing density of both organisms and the parasitoid density has a significantlymore positive effect; (3) with a pro-synovigenic nature, E.warrae allocate significantlymore resources to parasitization than to host feeding activity inlowwhiteflydensity andhighparasitoiddensity; and(4) lowmutual interference among searching parasitoids encourages parasitoid aggregation on host patches of high density. CONCLUSION: Regardless of greenhouse whitefly density, the pest can be effectively controlled by release of E. warrae. Our study provides insight into the success of whitefly biological control programmes using the parasitoid augmentation approach. Models used and developed here can also be employed to evaluate biological control programmesfor other parasitoid−whitefly systems.
... In addition to the introduction of natural enemies from the region of invasive insect habitats, biological controls include the occasional extraction of certain people from insect repression. Increased production of large parasitoids has led to the development of commercial pesticides in many parts of the world over the last 30 years, and it is predicted that more than 125 species of natural enemies are commonly accessible and utilized on around 16 million hectares worldwide per year [63]. At the beginning of the season, breeds of natural enemies in plants or in targeted surroundings, along with several inventors, are produced with the help of inoculative extracts. ...
Article
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Nowadays, the biological diseases in crop production are continuously increasing day by day. Organic agriculture has considerably augmented in significance in the current eras. Crop diseases are also a severe delinquent over the decades, and it’s a chief hazard for the yield food manufacture. Biological control agents for herbal syndromes are presently existence inspected as substitutes to artificial insecticides owing to their apparent improved level of care and negligible ecological influences. It affects the plants also by the biological diseases of the organic food production. Plant diseases can disturb florae by intrusive with numerous procedures such as the absorbance and translocation of water and nutrients, photosynthesis, flower and fruit growth, plant growth and expansion, and cell separation and increase. In this paper, we explain how biological diseases affect organic crop production.
... In IPM and organic farming, other possible options include the use of essential oil extracts and of biological control agents. However, while the effects of the essential oils on the human health and on natural enemies are still controversial, the efficacy of the biological control agents is not always easy to achieve, depending upon numerous factors such as host plant quality, temperature, usage of fertilizer, dimension of the greenhouse, stage of infestation 14 . In this context, together with the increasing request of new environmentally sound approaches, the development of innovative techniques that do not rely on the use of chemicals, that can be easy to apply and with constant efficacy to control the GW, are largely demanded. ...
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The greenhouse whitefly (GW), Trialeurodes vaporariorum is considered one of the most harmful insect pests in greenhouses worldwide. The GW mating behavior has been partially investigated and its vibrational communication is only in part known. A deeper knowledge of its intraspecific communication is required to evaluate the applicability of control methods based on techniques of behavioral manipulation. In this study, for the first time, we provided a detailed ethogram of the GW mating behavior and we characterized the vibrational signals emitted during the process of pair formation. We characterized two types of male vibrational emissions (“chirp” and “pulses”), differently arranged according to the behavioral stage to form stage-specific signals, and a previously undescribed Male Rivalry Signal. We recorded and characterized two new female signals: The Female Responding Signal and the Female Rejective Signal. The mating behavior of GW can be divided into six different stages that we named “call”, “alternated duet”, “courtship”, “overlapped duet”, “mating”, “failed mating attempt”. The analysis performed with the Markovian behavioral transition matrix showed that the “courtship” is the key stage in which male exhibits its quality and can lead to the “overlapped duet” stage. The latter is strictly associated to the female acceptance and therefore it plays a crucial role to achieve mating success. Based on our findings, we consider the use of vibrational playbacks interfering with GW mating communication a promising option for pest control in greenhouses. We discuss the possibility to start a research program of behavioral manipulation to control the populations of GW.
Article
Ryanodine receptors (RyRs) are the targets of diamide insecticides, which have been identified and characterized in a dozen insect pests of Lepidoptera, Hemiptera, Diptera and Coleoptera, but limited attention has been paid to the RyR in parasitoid natural enemies. Without this knowledge, it will hinder our effective and efficient application using both parasitoid natural enemies and diamide insecticides simultaneously in the integrated pest management (IPM). In this study, the full-length cDNA of RyR was cloned from Encarsia formosa (EfRyR), a parasitic wasp used worldwide for the biological control of whitefly. Its expression profile was examined in various tissues of E. formosa adults. The toxicities of four diamide insecticides to E. formosa were measured, and then the expression profile of EfRyR after 12 h and 24 h exposure to the LC50 dosages of diamide insecticides was investigated. The results showed that the full-length cDNA of EfRyR was 16, 778 bp including a 15, 345 bp open reading frame, and two alternative splice (AS) sites. Comparing to its expression in the abdomen, EfRyR was highly expressed in the head (11.9-fold) and the thorax (3.7-fold). The toxicities of four dimide insecticides against E. formosa from low to high were chlorantraniliprole (LC50 = 367.84 mg L⁻¹), cyantraniliprole (221.72 mg L⁻¹), cyclaniliprole (51.77 mg L⁻¹), and tetrachlorantraniliprole (8.35 mg L⁻¹). The expressions of EfRyR and its variants with AS were significantly increased after E. formosa adults were exposed to different diamide insecticides. This study improves our understanding of the RyR in parasitoid wasps and provides useful information on IPM by using E. formosa.
Article
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Background The greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae), is a cosmopolitan, polyphagous and a serious pest of vegetables and ornamentals in greenhouse. Encarsia formosa Gahan (Hymenoptera: Aphelinidae) is an important primary endoparasitoid species of the greenhouse whitefly. Results In the present study, per cent parasitisation attained 50% on the 4th instar and 46% on the third 3rd instar of T. vaporariorum by E . formosa. The mean duration period of the parasitoid from egg to host mummification, mummification to adult emergence (pupal period) was 11 and 7.8 days on 3rd instar and 8.5 and 7.6 days on 4th instar, respectively. The total time period from egg to adult emergence reached 18.8 days on 3rd instar and 16.2 days on 4th instar. Longevity of the female parasitoids was 8.3 and 8.8 days on 3rd and 4th instars, respectively. The pre-ovipositional, ovipositional and post-ovipositional periods of the parasitoid were 1.2, 6.4 and 1.0 days on 3rd instar and 1.2, 6.7 and 1.0 days on 4th instar, respectively. The finite rate of natural increase ( λ ), doubling time and weekly multiplication rate of the 3rd instar was 1.16±0.002 times per day, 4.71±0.04 days and 2.80±0.03 folds, respectively and 1.17±0.002 times per day, 4.34±0.04 days and 3.06±0.03 folds for the 4th instar. Conclusions Studies indicated that the 4th nymphal instar of the host was more suitable for parasitisation with E. formosa. The parasitoid species could be mass multiplied and utilised as a component of integrated pest management programme of T. vaporariorum after evaluation under field conditions .
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Parasitoid wasps from the Aphelinidae family (Hymenoptera) are important control agents of Bemisia tabaci (Gennadius, 1889) cryptic species, both through reproduction and feeding processes. Identifying native parasitoid species within agricultural systems affected by Bemisia whitefly species is the first step to developing guidelines for the creation and release of biological control agents aiming at this highly damaging pest species complex. Taxonomic and phylogenetic analyses based on morphological and molecular characters, respectively, confirmed the occurrence of Encarsia formosa (Gahan, 1924) in greenhouse tomatoes from Santa Maria, Encarsia porteri (Mercet, 1928) in open-field soybean from Santa Maria, and Eretmocerus mundus Mercet, 1931 in greenhouse tomatoes from São José do Hortêncio, all within Rio Grande do Sul state (South Brazil). This is the first report of En. formosa, En. porteri and Er. mundus parasitising B. tabaci in South Brazil, and the first En. porteri partial mtCOI gene sequence being reported and characterised. The high temperature inside the tomato greenhouses can be a possible cause for the predominance of Er. mundus in São José do Hortêncio, and sex ratios in the surveyed populations point to female and male prevalence within Encarsia and Eretmocerus genera, respectively. The combined use of taxonomic and molecular characterisation highlights the importance of combining both morphological and molecular approaches in the assessment of previously unidentified whitefly parasitoids.
Article
To learn whether an introduced parasite, Encarsia formosa gahan can be used as a biological control agent for the greenhouse whitefly, Trialeurodes vaporariorum (westwood) in greenhouses where night temperatures fall to a low level, a release experiment was done in an unheated plastic greenhouse during the period December, 1978 to February, 1979. The parasite was responsible for 43.8% of the host mortality, of which death rate due to host feeding accounted for 12.9%. The results obtained demonstrated that the parasite can survive low night temperatures (about 5°C) and parasitize a substantial fraction of the host when day temperatures are sufficiently high (about 30°C). © 1982, JAPANESE SOCIETY OF APPLIED ENTOMOLOGY AND ZOOLOGY. All rights reserved.
Article
Greenhouse experiments were carried out to control the greenhouse whitefly (Trialeurodes vaporariorum Westwood) On tomatoes by the combined use of yellow sticky traps with the parasite Encarsia formosa Gahan. In the treatments where the parasites were introduced after monitoring by yellow sticky traps, the results were successful. Whitefly infestations were maintained at low levels throughout the season. In the treatment where many yellow sticky traps were used to control whiteflies by mass trapping with the parasite, the result was also successful. However, the combined effect of the parasite and the mass trapping was not significantly evident. From the practical point of view, use of yellow sticky traps was thought to be more promising for monitoring than for mass trapping. © 1987, JAPANESE SOCIETY OF APPLIED ENTOMOLOGY AND ZOOLOGY. All rights reserved.
Article
To select a promising agent for biological control of the greenhouse whitefly, Trialeurodes vaporariorum (Westwood), mating and oviposition behaviors of two native species, Encarsia sp. (A) and Encarsia sp. (B), and an introduced one, Encarsia formosa Gahan, were observed. Mating behavior of Encarsia sp. (A) and Encarsia sp. (B) differed from that of E. formosa : the male of the former two species mounted the female before and after copulation, while the male of the latter did not. Encarsia sp. (A) and Encarsia sp. (B), which are arrhenotokous, laid fertilized female-producing eggs in healthy whiteflies, and unfertilized male-producing eggs on fully-grown larvae or pupae of E. formosa in whitefly pupae. The thelytokous parasitoid E. formosa laid all its eggs in unparasitized whiteflies, but the mechanism of its male occurrence is not clear. Fecundities of Encarsia sp. (A) and E. formosa were similar to each other and higher than that of Encarsia sp. (B). © 1989, JAPANESE SOCIETY OF APPLIED ENTOMOLOGY AND ZOOLOGY. All rights reserved.