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J. Asia-Pacific Entomol.

7(1): 5-11 (2004)


www.entomology.or.kr

Review
Recent Development of Biological Control and IPM in Greenhouses in Japan
Eizi Yano*
National Agricultural Research Center, 3-1-1, Kannondai, Tsukuba, Ibaraki, 305-8666 Japan

Abstract Biological control is expected to become enemies are produced on a large scale and released
the basic pest control system in Japan for promoting artificially. This approach has shown rapid progress
safe crop production in greenhouses. Twelve arthropod recently in developed countries (e.g. Albajes et al.,
natural enemy species and three fungus species have 1999). Commercialization of the production and
become available for commercial use in greenhouses. supply of natural enemies is an important reason for
Imported species were commercialized first, with the this progress. In addition, it is not difficult in this
commercial use of indigenous species coming later. approach to standardize the methods for the use of
The extreme temperature conditions in greenhouses, natural enemies. Augmentative release of natural
the delay of release, the effect of chemicals and the enemies is the key technology in IPM of greenhouse
low level of tolerance for pest damage in some crops pests. Because it is difficult to chemically control pests
are major limiting factors in the use of natural enemies in greenhouses, biological control has been developed
in commercial greenhouses. Among the indigenous as an alternative control measure in western countries
Orius species, 0. strigicollis has been commercial- (e.g. Albajes et al., 1999). Biological control is also
ized to control thrips because of its low diapause expected to become the basic system of pest control
incidence and the ease of mass production. A promising in Japan for safe crop production in greenhouses.
parthenogenetic strain of an indigenous eulophid
species, Neochrysocharis formosa, has been found in
Kyushu District and has shown a highly suppressive
effect on Liriomyza trifolii in Okinawa. Cultural Biological Control in Greenhouses in Japan
control measures, such as field hygiene or prevention
of pest immigration, are fundamental for the effective
control of pests. Since it is impossible to control all Pest problems
pest species with natural enemies, the integrated use
of natural enemies and other control measures, which The greenhouse environment in Japan is characterized
include cultural control and the use of selective by: (1) cultivation in small plastic greenhouses; (2)
pesticides, is essential for commercial application. high temperatures from spring to autumn and relatively
low temperatures in winter; (3) high humidity all year
Key words biological control, greenhouse, IPM, round; and (4) immigration of pests from the sur-
Japan, natural enemy roundings because of poor isolation from the outside
environment (Yano, 1993). These conditions cause
several problems in pest and disease control including
the need for frequent application of pesticides and
Introduction fungicides, rapid population growth of pests, and unfa-
vorable conditions for some of the natural enemies.
The use of natural enemies or biological control is Chemical control of pests is difficult to achieve and
essential in integrated pest management (IPM) of is always has a risk of causing a resistance to
vegetable pests. There are three approaches in the pesticides to develop.
use of natural enemies: classical biological control, Most of the greenhouse pests in Japan are cos-
augmentation and conservation (van Driesche and mopolitan. They are small in size and suck fluids from
Bellows, 1996). In augmentative release, natural plants. They belong to several groups of insects or
augmentation and conservation (van Driesche and mites, i.e. aphids, whiteflies, thrips, mites, leaf miners
Bellows, 1996). In augmentative release, natural and nematodes. There are occasional outbreaks of
*Corresponding author.
noctuid moth species such as Spodoptera litura
E-mail: yano@affrc.go.jp (Fabricius)(Lepidoptera: Noctuidae) in the southwestern
Tel: +81-29-838-8846; Fax: +81-29-838-8837 region. Another important fact is that several exotic
(Received September 29, 2003; Accepted December 31, 2003) pests have become serious problems in protected
6 J. Asia-Pacific Entomol. Vol. 7 (2004)

cultivation (Table I). After the rapid development of enemies is important character of the greenhouse
greenhouse cultivation in the 1960s, Trialeurodes environment. Indigenous natural enemies sometimes
vaporariorum (Westwood) (Homoptera: Aleyrodidae) completely suppress the pests in greenhouses after
and Thrips palmi Karny (Thysanoptera: Thripidae) their immigrationinto greenhouses from the surrounding
invaded in 1974 (Nakamura et al., 1975) and around environment (Yano, 2003a).
1978 (Ikeda, 1981; Horikiri, 1981), respectively.
Bemisia argentifolii Bellows and Perring (Homoptera:
Aleyrodidae), Liriomyza trifolii (Burgess) (Diptera: Development of biological control
Agromyzidae) and Frankliniella occidentalis (Pergande)
(Thysanoptera: Thripidae) were reported as new pests In Japan, if natural enemies are to be sold as commercial
around 1990 (Ohto, 1990; Saito, 1992; Hayase and products, it is necessaryto register them as biopesticides.
Fukuda, 1991). More recently, Liriomyza sativae Twelve arthropod natural enemy species and three
Blanchard has invaded the western part of Japan in fungus species have become available for commercial
1999 (Tokumaru and Abe, 2001). These species have use in greenhouses as of 2003 (Table 2). Imported
become established as major pests in protected species such as Phytoseiulus persimilis Athias-Henriot
cultivation in Japan (Japan Plant Protection Association, and Encarsia formosa Gahan were commercialized
1998). The high activity of indigenous natural first, after which indigenous species were put to

Table 1. Major greenhouse pests in Japan. Pests in bold letters are imported species

Crop Pest
Trialeurodes vaporariorum, Bemisia argentifolii, Liriomyza trifolii, Myzus persicae, Aphis gossypii,
Tomato
Aculops lycopersici, Meloidogyne incognita
Thrips palmi, T. vaporariorum, B. argentifolii, M persicae, A. gossypii, Tetranychus urticae,
Eggplant
Tetranychus kanzawaii, Polyphagotarsonemus latus, Spodoptera litura
Sweet pepper Frankliniella occidentalis, Frankliniella intonsa, T. palmi, M persicae, A. gossypii, P. latus, S. litura
T. palmi, T. vaporariorum, B. argentifolii, M persicae, A. gossypii, Rhopalosiphum rufiabdominalis,
Cucumber
M incognita
Watermelon T. palmi, M persicae, A. gossyopii, T. urticae, T. kanzawaii, M incognita
F. occidentalis, A. gossypii, Chaetosiphon minor, Aphis forbesi, T. urticae, T. kanzawaii,
Strawberry
Nothotylenchus acris, Pratylenchus vulnus, S. litura, Anomala cuprea

Table 2. Registered natural enemies for use in pest control in protected culture in Japan (Japan Plant Protection Association)

Natural enemy Type of natural enemy Pest Crop


Phytoseiulus persimilis Predator Spider mites Vegetables
Encarsia formosa Parasitoid Whiteflies Vegetables
Eretmocerus eremicus Parasitoid Whiteflies Tomato
Diglyphus isaea Parasitoid Leaf miners Vegetables
Dacnusa sibirica Parasitoid Leaf miners Vegetables
Amblyseius cucumeris Predator Thrips Vegetables
Orius strigicollis Predator Thrips Vegetables
Aphidius colemani Parasitoid Aphids Vegetables
Aphidoletes aphidimyza Predator Aphids Vegetables
Chrysoperla carnea Predator Aphids Vegetables
Harmonia axyridis Predator Aphids Vegetables
Franklinothripes vespiformis Predator Thrips palmi Eggplant, cucumber
Verticillium lecanii Fungus disease Aphids, whiteflies Vegetables
Paecilomyces fumosoroseus Fungus disease Whiteflies Vegetables
Beauveria bassiana Fungus disease Whiteflies Tomato, cucumber
Biological control and rPM in greenhouses 7

commercial use. greenhouses and the effect of chemicals are two major
Phytoseiulus persimilis has been studied in Japan factors that affect the control capability of P. persimilis
since 1966 (Mori and Shinkaji, 1977). After extensive in commercial greenhouses. Monitoring the early
fundamental studies of its life history and population infestation by spider mites to determine the time of
dynamics, and applied studies of its uses, several introduction of P. persimilis is also crucial for the
production facilities for the predator were constructed, commercial use of the predatory mite, because spider
and the predators produced were distributed in several mite outbreaks occur in spring more readily in Japan
prefectures. However, its use by farmers was not than in Western Europe (Yano, 1993). Delay of release
developed until recently because of limitations of the of in greenhouses and the low temperature condition
supply and a lack of integrated control systems for that are prevalent in winter are two major factors in
greenhouse crops. Phytoseiulus persimilis was first causing the use of P. persimilis to fail (Yano, 1993).
registered as a biotic pesticide and commercialized Monitoring the early infestation of whiteflies is of
in 1995 for controlling spider mites on strawberries. paramount importance, because one of the reasons for
Since then, P. persimilis has been registered to control failure in the use of E. formosa is a delay in its release.
spider mites on greenhouse vegetables, and its area Trapping of adult whiteflies with yellow sticky traps
of release is the largest among the commercialized and the use of binomial sampling to monitor the
natural enemies in Japan. occurrence of adults on each plant were developed
Encarsia formosa was imported from the UK in as monitoring methods (Yano and Koshihara, 1984).
1975, a year after the occurrence of T. vaporariorum Most insecticides are harmful to E. formosa except
was first recognized in Japan. The effects of temperature for some IGRs, while many acaricides and fungicides
and release methods on the control capability of E. are less harmful (Kawai, 1988). The most important
formosa were evaluated in greenhouse trials and by technical factor in commercializing natural enemies
developing a simulation model of the host-parasite is integrating the use of natural enemies with other
population interaction (Yano, 1987, 1989a, b, 1990). control measures that are intended to control other
Use of the imported bumblebee, Bombus terrestris (L.) pests on a crop. If the control measures for other pests
(Hymenoptera: Apidae), for pollination is increasing are incompatible with the use of natural enemies, the
among tomato growers in Japan (Ono and Wada, practical use of natural enemies is almost impossible.
1996). This is helpful for the production of high- Other limiting factors in biological control are: 1)
quality fruits, but the application of insecticides must low tolerance of pest damage, 2) supply of natural
be regulated after the introduction of the bumblebee enemies, 3) poor advisory service for farmers, and
into greenhouses. Encarsia formosa is expected to 4) need for registration (Yano, 1993). Low tolerance
control whiteflies in this case. After its registration of pest damage is the main reason for difficulty in
as a biopesticide in 1995, the area in which the adopting biological control in flower production. The
parasitoid is being released in tomato greenhouses is lack of a system for supplying enough natural enemies
increasing. of good quality was the limiting factor in biological
The use of P. persimilis and E. formosa is not control in Japan, because private companies were not
sufficient to develop a practical IPM system for each interested in biological control in Japan until recently.
greenhouse crop. Aphids are very difficult to control However, many species of arthropod natural enemies
as indigenous pests. Since 1980, imported pests (Table have been registered, and a sufficient number of
1) have also become a serious problem for many crops. imported or indigenous natural enemies are now
Imported natural enemies, which have been supplied by private companies. An advisory service
commercialized in Europe and North America, have for farmers is very important if a good performance
been tested in many agricultural experimental stations of natural enemies for promoting biological control
for registration as biopesticides, and another eight is to be obtained.
species have been registered to control pests on many
kinds of crops (Table 2).
Use of indigenous natural enemies in
biological control
Factors limiting biological control
Most studies of the use of natural enemies in protected
In the augmentative biological control of pests, live culture focused on imported natural enemies, i.e. P.
natural enemies are released artificially. Most natural persimilis in 1970s and E.formosa, in the 1980s. Now,
enemies are effective against only a small group of however, researches on the commercialization of
pest species. Their effects are also dependent on indigenous natural enemy species are being conducted
various physical, chemical and biological environmental in many institutes, universities and private companies.
factors (Yano, 1993). The extreme temperatures in The advantages of using indigenous natural enemies
8 J. Asia-Pacific Entomol. Vol. 7 (2004)

are: (1) natural enemies are adapted to the domestic L. trifolii were surveyed in Japan. Twenty-eight
environment and (2) non-target environmental effects species were recorded as parasitoids of L. trifolii. An
are avoided (Yano, 1999). illustrated identification system was developed to
Five indigenous Orius species, 0. sauteri (Poppius), identify these parasitoid species of L. trifolii (Konishi,
0. minutus (Linnaeus), 0. strigicollis (Poppius), 0. 1998). Twenty-one ofthe species are eulophid species,
nagaii Yasunaga and 0. tantillus (Motschlsky), are and the others belong to Braconidae, Eucoilidae, and
considered to be major natural enemies of thrips in Pteromalidae. Four eulophid species, Hemiptarsenus
the field (Yasunaga, 1997). Many biological studies varicornis (Girault), Chrysocharis pentheus (Walker),
regarding 0. sauteri have been performed because its Neochrysocharis formosa (Westwood) and N Okazakii
effectiveness in suppressing T. palmi has been dem- (Kamijo), are the predominant species in Japan. In
onstrated both in the field and in greenhouses (Nagai, Shizuoka Prefecture, central Japan, all four species
1993a,b; Kawai, 1995). The low reproduction and are found both in fields and greenhouses as parasitoids
predation rates of 0. sauteri under low temperature of L. trifolii. Hemiptarsenus varicornis was the most
conditions mean that this species is ineffective in important species in greenhouses where synthetic
winter (Nagai and Yano, 1999, 2000). Table 3 shows pesticides were applied frequently (Saito et aI., 1996).
the effect of temperature on the reproduction of 0. The development period from egg to adult emergence
sauteri. Another important factor limiting the of H. varicornis was studied at different temperatures
effectiveness of Orius spp. as biological control agents (Saito et al., 1997). Hemiptarsenus varicornis is an
is the induction of reproductive diapause. The use of ectoparasitic parasitoid. Adults kill many larvae of L.
non-diapause strains or species is desirable for the trifolii not only by parasitization but also by host
year-round use of natural enemies. Orius sauteri exhibits feeding. A parthenogenetic strain of N formosa was
reproductive diapause under a short photoperiod. found recently in Kagoshima and Okinawa Prefectures
Orius minutus shows almost the same reproductive and is expected to be a promising biological control
diapause as 0. sauteri (Kohno, 1997, 1998; Ito and agent to control L. trifolii (Arakaki and Kinjo, 1998).
Nakata, 1998). Orius strigicollis, which is mainly Mass production and release trials of N fomosa are
distributed in western Japan, shows a lower diapause now being intensively conducted in Okinawa Prefecture
incidence than 0. sauteri (Shimizu and Kawasaki, in order to attain commercialization in the near future.
2001). Orius tantillus, which is found only on grass
weeds in Okinawa Prefecture, and 0. nagaii living
mainly in rice fields, are not considered as proper
species to be used for biological control of pests of IPM in Greenhouses in Japan
greenhouse vegetables (Yasunaga, 1997). Orius sauteri
and 0. strigicollis were registered as biopesticides in
1998 and 2001, respectively, in Japan. Orius Other control measures for IPM
strigicollis is preferred to 0. sauteri for commercial
use because of its lower reproductive diapause Although cultural and physical control measures do
incidence and the ease for mass production. Orius not have a curative effect after heavy infestations of
strigicollis is widely used for controlling T. palmi on greenhouse pests, their preventive effect on the rapid
eggplants and T. palmi and F. occidentalis on sweet increase of pests is of great importance in integrated
peppers in Kochi Prefecture in the southwestern part control. Their effectiveness is related to the regulation
of Japan (Yano, 2003a). A few years ago, a species of life histories or of dispersal of pests.
of predatory thrips, Franklinothripes vespiformis, was Thrips palmi is a species of subtropical or tropical
shown to control T. palmi in greenhouses very origin and is considered to be unable to survive in
effectively in Okinawa Prefecture (Yano, 2003a). the field in Japan in winter (Ikeda, 1983). Suppression
The domestic parasitoid species fauna that attack of T. palmi in greenhouses before winter should decrease

Table 3. Development, longevity and reproduction of 0. sauteri at different temperatures (Nagai and Yano, 1999)

Temperature Developmental time (day)" Female longevity Lifetime


(OC) rm/day
Egg Nymph (day)" fecundity"
15 13.7±0.2a 40.9±0.6a 35.8±12.9a 12.2±5.3a 0.0135
20 7.5±0.2b 18.9±0.3b 19.6±7.1b 51.3±7.2b 0.0763
25 4.5±0.lc 11.5±0.2c 20.3±1.7b 74.5±10.7b 0.128
30 3.2±0.ld 9.5±0.2d 9.0±0.5c 52.8±5.4b 0.166
a Mean ± S.E. Means followed by the same letter in the same column are not significantly different at p ~ 0.05 (Tukey-Kramer HSD test or Scheffe test).
Biological control and lPM in greenhouses 9

its density in the next season. Bemisia argentifolii also IPM in protected crops
has difficulty surviving in winter. Most of the
greenhouse pests are polyphagous and can infest many Since we cannot control all pests infesting a greenhouse
kinds of crops and weeds as host plants. If suitable crop with only natural enemies, and since the suitable
host crops are cultivated, or if host weeds grow, near period for biological control is limited, the integrated
greenhouses, the pests can migrate from the use of natural enemies and other control measures is
greenhouse to the surrounding fields and vice versa. essential for commercial application. Suitable crops
Host weeds growing in greenhouses are also important for integrated control using natural enemies can be
for the survival of pests after harvesting. The removal assumed to be crops that are attacked by a small
of host weeds inside and near greenhouses and number of serious pests, crops for which a low level
avoidanceofthe cultivationof host crops are fundamental of pest damage is tolerable, and crops requiring insect
conditions for preventive cultural control. pollinators. Tomato, strawberry and sweet pepper are
Helgesen and Tauber (1974) pointed out three three good candidates for which integrated control can
possible routes ofintroduction of T. vaporariorum into be developed in Japan. Table 4 shows an integrated
greenhouses: (1) artificial introduction of infested control scheme for tomatoes combining the use of
seedlings; (2) infestation from weeds or other crops natural enemies and selective pesticides. Noctuid
in the greenhouse; (3) infestation from host plants moths sometimes cause severe damage in south-
outside but near the greenhouse. This list of routes western Japan, but they can be controlled by Bacillus
suggests several possibilities for control by preventing thuringiensis Berliner or some IGRs. Soil application
the artificial introduction or dispersal of pests. The of systemic pesticides and spot treatment with
cultivation of uninfested seedlings in nurseries, the non-selective pesticides are also possible options in
removal of host weeds in greenhouses and the use integrated control.
of nets to cover the openings of greenhouses could In Western Europe, integration of the use of natural
prevent the immigration of pests from outside. These enemies and selective pesticides is emphasized (Rav-
techniques are also applicable to other pests. Plastic ensberg, 1992). However, the greenhouse environment
films that absorb ultraviolet rays are commonly used in Japan is less favorable for biological control
as covering materials for plastic greenhouses in Japan. because of the extreme temperature conditions and
One of the important and interesting effects of the the incomplete isolation of the greenhouse environment
use of these plastic films is the prevention of the from the surroundings. Integration with other control
immigration of pests from outside. This technique is techniques is needed for more satisfactory biological
effective against aphids, whiteflies and thrips. Another control. For example, cultural control, including pre-
important physical control measure is the use of vention of the immigration of pests, the removal of
colored traps. Winged aphids and whitefly adults are host weeds within and outside greenhouses and
attracted to yellow, while thrips adults prefer white avoidance of the cultivation of host plants near
or blue (Yano, 2003b). Many types of colored sticky greenhouses are fundamental for effective control.
traps have been developed and used for the mass After infestation, pests increase almost exponentially
trapping or monitoring of these pests. Their usefulness under the high temperatures that are prevalent from
most likely consists in their use in supervised chemical spring to autumn (Yano, 1993, 2003a). In such cases,
control. Yellow sticky traps can be used to determine delay of the release of natural enemies often results
the time of release of E. formosa and to evaluate the in the failure of biological control (Yano, 1993,
effectiveness of control. 2003a). Systems that monitor early infestation by pests
in greenhouses are crucial for successful biological
control. Another possibility for biological control is

Table 4. A scheme of lPM for tomatoes in greenhouses in Japan (T. Ishii, personal communication)

Period Control measures Pests


Middle of July Application of granules in soil Thrips, aphids
Late August Sulfur application Rust mites
September - October E. formosa, D. isaea Whiteflies, leaf miners
Early October lGR application Noctuid moths
Middle of January lGR application Whiteflies
Late March lGR application Thrips
April - May E. formosa, D. isaea Whiteflies, leaf miners
10 J. Asia-Pacific Entomo!. Vo!. 7 (2004)

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