Biological Control 67 (2013) 8–20

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Biological Control
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Biological control of rice insect pests in China

Yong-Gen Lou a,⇑, Gu-Ren Zhang b, Wen-Qing Zhang b, Yang Hu c, Jin Zhang a
a
State Key Laboratory of Rice Biology, Institute of Insect Science, Zhejiang University, Hangzhou 310058, China
b
State Key Laboratory of Biocontrol, Institute of Entomology, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China
c
Research and Development Center of Rice Production Technology, China National Rice Research Institute, Hangzhou 310006, China

h i g h l i g h t s g r a p h i c a l a b s t r a c t

 Rice is one of the most important food

crops in the world.
 Damage by insect pests is a serious
challenge to rice production in China.
 Biological control is an effective
method for pest control but not
extensively adopted.
 Integration of new strategies in
biological control should be explored.

a r t i c l e i n f o a b s t r a c t

Article history: Rice is one of the most important food crops in the world. China has the second largest area of the rice
Available online 2 July 2013 growing in the world and the highest yield of rice produced. Infestation by insect pests, especially rice
planthoppers, stem borers and leaf folders, is always a serious challenge to rice production in China. Cur-
Keywords: rent methods for controlling insect pests in China mainly include good farming practices, biological con-
Rice trol, breeding and growing resistant varieties, and the use of chemical insecticides. However, for farmers,
Insect pests the favorite method for insect pest control is still the application of chemical insecticide, which not only
Biological control
causes severe environmental pollution and the resurgence of herbivores but also reduces populations of
Ecological engineering
China
the natural enemies of herbivores. To control insect pests safely, effectively and sustainably, strategies
encouraging biological control are currently demanded. Here we review the progress that has been made
in the development and implementation of biological controls for rice in China since the 1970s. Such pro-
gress includes the species identification of the natural enemies of rice insect pests, the characterization of
their biology, and the integration of biological controls in integrated pest management. To develop effec-
tive ecological engineering programs whose aim is to implement conservation biological controls, further
research, including the evaluation of the roles of plants in non-crop habitats in conservation biological
controls, volatiles in enhancing efficiency of natural enemies and natural enemies in manipulating insect
pests, and education to increase farmers’ knowledge of biological controls, is proposed.
Ó 2013 Elsevier Inc. All rights reserved.

1. Introduction food crops. The total rice product yield in China, about 200 bil-
lion kg, is the highest in the world and accounts for about 50% of
Rice is one of the most important food crops in the world. In the nation’s total food yield. About 67% of the population in China
China, the total growing area of rice per year is about 29.4 million depends on rice (Hu and Ding, 2008). Therefore, it is crucial to de-
hectare, which makes up one-third of the total growing area of velop rice production in China.
The rice species grown in China, Oryza sativa, includes two sub-
species, indica and japonica. The six patterns of growing rice in
⇑ Corresponding author. China include double-crop rice in Southern China, double- or
E-mail address: [email protected] (Y.-G. Lou).

1049-9644/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.biocontrol.2013.06.011
 Y.-G. Lou et al. / Biological Control 67 (2013) 8–20 9

single-crop rice in Central China, and single-crop rice in Southwest Table 1

China, North China, Northeast China and Northwest China (Hu and Number and percentage of species of predatory natural enemies of
rice pests in Chinaa.
Ding, 2008). Rice in China suffers from many insect pests; among
these are rice planthoppers, Nilaparvata lugens (Stål), Sogatella fur- Taxon No. species %
cifera (Horváth) and Laodelphax striatellus (Fallen), rice borers, Chilo Coleoptera 191 41.34
suppressalis (Walker) and Tryporyza incertulas (Walker), and rice Hemiptera 87 18.83
leaf folder, Cnaphalocrocis medinalis Guenee. In some regions, the Odonata 61 13.20
Diptera 43 9.31
water weevil Lissorhoptrus oryzophilus Kuschel, the gall midge Ors- Hymenoptera 30 6.49
eoia oryzae (Wood-Mason), and the thrip Chloethrips oryzae (Wil.) Neuroptera 23 4.98
also heavily infest rice. Demaptera 10 2.16
To prevent rice plants from herbivore infestation, many control Mantodea 8 1.73
Orthoptera 7 1.52
methods have been developed. The major control methods since
Thysanoptera 2 0.43
the 1970s include resistant varieties, agricultural controls, biolog- Total 462 100
ical controls and chemical controls. (1) Resistant varieties. Planting
a
Data from He et al. (1991) and Huang et al. (2004).
resistant varieties is an important and safe method of pest control.
So far, some varieties resistant to rice insect pests, especially to rice
planthoppers, such as K89-B5, Zhenongda 724, have been grown in
the field (Lu et al., 2002b). This has decreased the population den- Table 2
sities of rice herbivores and the amount of insecticides that has to Number and percentage of species of dominant families of rice
be applied. However, the number of rice varieties resistant to her- field spiders in Chinaa.
bivores is small; this limits the potential of rice-resistant varieties Taxon No. species %
in herbivore management. (2) Agricultural controls (cultural con-
Araneidae 58 15.47
trols). These mainly include agricultural operations which decrease Lycosidae 49 13.07
the population densities of herbivores, such as plowing the paddy Salticidae 47 12.53
fields in early spring, immersing them in water to kill the over- Linyphiidae 36 9.60
wintering rice borers, and removing the rice plants infested by rice Clubionidae 31 8.27
Tetragnathidae 31 8.27
borers in the fields to reduce the population densities of the herbi-
Theridiidae 27 7.20
vores. (3) Biological controls. These mainly include releasing the Thomisidae 21 5.60
natural enemies of herbivores, such as ducks and Trichogramma 14 other families 75 20.00
japonicum, and enhancing the efficiency and/or population densi- Total 375 100
ties of the natural enemies of herbivores by agricultural operations, a
Data from Wang et al. (1999).
such as planting specific flowering plants. (4) Chemical controls.
The main methods of chemical control for rice insect pests include
applying biological insecticides, such as Bacillus thuringiensis (Bt),
Spinosad and Azadirachtin, and chemical insecticides, The latter Table 3
has been the major control measure for rice insect pests in China. Number and percentage of species of dominant families of parasitic natural enemies
Large amounts of chemical insecticides are applied in rice fields per of rice pests in Chinaa.
year, which not only causes severe environmental pollution and Taxon No. species %
the resurgence of herbivores but also reduces populations of the
Ichneumonidae 110 25.94
natural enemies of herbivores. Therefore, developing safe and Braconidae 70 16.51
effective methods to control rice insect pests is essential. Eulophidae 25 5.90
Biological control is one of the safest and most effective meth- Scelionidae 25 5.90
ods for rice insect pests. However, this method has not been Chalcididae 16 3.77
Dryinidae 16 3.77
adopted by rice growers because it is relatively time-consuming
Tachinidae 51 12.03
and inefficient. Here, we will review the main progress in the Pipunculidae 11 2.59
development and implementation of biological controls in rice in 20 other families 100 23.58
China since the 1970s. Such progress includes the species identifi- Total 424 100
cation of the natural enemies of rice insect pests, the characteriza- a
Data from He et al. (1991) and Tang et al. (2001a,b).
tion of their biology, and the integration of biological controls in
the development and implementation of integrated pest manage-
ment (IPM). Future research directions are also suggested. We
hope that this review paper will promote research into biological 1991). At present, more than 1375 species of natural enemies of
control and its application in rice IPM in China. rice insect pests have been recorded in China (He et al., 1991;
Wang et al., 1999; Tang et al., 2001a,b; Huang et al., 2004).

2. Survey and classification of natural enemies of rice

herbivores from the 1970s to today
2.1. Predatory natural enemies
Since the policy of ‘‘prevention first and integrated control,’’
which shaped the guidelines for plant protection in China in The 889 species of predatory natural enemies of rice insect
1975, more and more attention has been paid to the protection pests recorded in China (including species of Insecta, Arachnida,
and utilization of natural enemies in insect pest control. Extensive Amphibia, Reptilia, Aves and Mammalia) account for 64.74% of
surveys on the natural enemies of crop pests were carried out all the natural enemies. These are made up of 462 species of Insec-
throughout the country from 1979 to 1982, and the major natural ta (Table 1) (Huang et al., 2004), 375 species of Arachnida (Table 2)
enemies of the most important crop pests, including many domi- (Wang et al., 1999), 32 species of Amphibia, one species of Reptilia,
nant species worthy of conservation, were identified (He et al., 7 species of Aves and 12 species of Mammalia (He et al., 1991).
Table 4

10
Major arthropod natural enemies of major rice insect pests.

Natural Taxon of natural Rice stem borer C. suppressalis Yellow rice borer T. incertulas Rice leaf folder C. medinalis Rice planthoppers, including
enemies enemies N. lugens, S. furcifera, and L. striatellus
Parasitoids Ichneumonidae (1) Iseropus kuwanae (Viereck) (1) Itoplectis naranyae (Ashmead) (1) Acropimpla hapaliae (Rao)
(2) Itoplectis naranyae (Ashmead) (2) Leptobatopsis indica (Cameron) (2) Coccygomimus aethiops (Curtis)
(3) Xanthopimpla flavolineata Cameron (3) Diadegma akoensis (Shiraki) (3) C. nipponicus (Uchida)
(4) X. modesta modesta (Smith) (4) Eriborus sinicus (Holmgren) (4) Iseropus kuwanae (Viereck)
(5) X. predator (Fabricius) (5) E. terebrans (Gravenhorst) (5) Itoplectis naranyae (Ashmead)
(6) X. punctata (Fabricius) (6) Temelucha biguttula (Matsumura) (6) Xanthopimpla flavolineata Cameron
(7) X. stemmator (Thunberg) (7) T. philippinensis (Ashmead) (7) X. punctata (Fabricius)
(8) Lissonota mandschurica (Uchida) (8) T. stangli (Ashmead) (8) Leptobatopsis indica (Cameron)
(9) Eriborus sinicus (Holmgren) (9) Trathala flavo-orbitalis (Cameron) (9) Casinaria simillima Maheshwary et
Gupta
(10) E. terebrans (Gravenhorst) (10) Amanuromorpha accepta metathoracica (10) Charops bicolor (Szepligeta)
Ashmead
(11) Pristomerus chinensis Ashmead (11) A. accepta schoenobii (Viereck) (11) Eriborus vulgaris (Morley)
(12) Temelucha biguttula (Matsumura) (12) Gambroides javensis (Rohwer) (12) T. philippinensis (Ashmead)
(13) T. philippinensis (Ashmead) (13) Goryphus basilaris Holmgren (13) Trathala flavo-orbitalis (Cameron)
(14) Trathala flavo-orbitalis (Cameron) (14) Ishnojoppa luteator (Fabricius) (14) Chirinaeus facialis Chao
(15) Amauromorpha accepta schoenobii (15) Triclistus aitkini (Cameron)

Y.-G. Lou et al. / Biological Control 67 (2013) 8–20

(Viereck)
(16) Gambrus ruficoxatus (Sonn) (16) Agrypon suzukii (Matsumura)
(17) G. wadui (Uchida) (17) Trichomma cnaphalocrosis Uchida
(18) Goryphus basilaris Holmgren (18) Goryphus basilaris Holmgren
(19) Auberteterus alternecoloratus (19) Vulgicheumon diminutus
(Cushman) (Matsumura)
(20) Vulgichneumon taiwanensis (Ushida)

Parasitoids Braconidae (21) Amyosoma chinensis Szepligeti (15) Amyosoma chinensis Szepligeti (20) Aulacocentrum philippinensis
(Ashmead)
(22) Bracon onukii Watanabe (16) Bracon onukii Watanabe (21) Macrocentrus cnaphalocrosis He et
Lou
(23) Stenobracon nicevillei (Bingham) (17) Stenobracon nicevillei (Bingham) (22) Apanteles cypris Nixon
(24) Tropobracon schoenobii (Viereck) (18) Tropobracon schoenobii (Viereck) (23) A. ruficrus (Haliday)
(25) Chelonus munakatae Mutsumura (19) Rhoconotus schoenobivorus (Rohwer)
(26) Apanteles chilonis Watanable (20) Apanteles armaris Nixon
(27) A. flavipes (Cameron) (21) A. flavipes (Cameron)
(28) A. ruficrus (Haliday) (22) A. ruficrus (Haliday)
(29) A. schoenobii Wilkinson (23) A. schoenobii Wilkinson
(30) Microgaster russata Haliday (24) Microgaster russata Haliday
Parasitoids Chalcididae (25) Brachymeria excarinata Gahan (24) Brachymeria excarinata Gahan
(25) B. lasus (Walker)
(26) Antrocephalus apicalis (Walker)
Parasitoids Eulophidae (31) Tetrastichus ayyara Rohwer (26) Tetrastichus schoenobii Feriere (27) Stenomesius maculates Liao
(28) Pediobius mitsukurii (Ashmead)
(29) Dimmockia parnarae (Chu et Liao)
(30) Tetrastichus shaxianensis Liao
Parasitoids Elasmidae (27) Elasmus albipictus Crawford (31) Elasmus corbetti Ferriere
Parasitoids Trichogrammatidae (32) Trichogramma confusum Viggiani (28) Trichogramma confusum Viggiani (32) Trichogramma closterae Pang et (1) Oligosita nephotettica Mani
Chen
(33) T. dendrolimi Matsumura (29) T. dendrolimi Matsumura (33) Trichogramma confusum Viggiani (2) O. shibuyae Ishii
(34) T. japonicum Ashmead (30) T. evenscens Westwood (34) T. dendrolimi Matsumura (3) Paracentrobia andoi (Ishii)
(35) T. astriniae Pang et Chen (31) T. japonicum Ashmead (35) T. japonicum Ashmead
(32) T. leucaniae Pang et Chen (36) T. leucaniae Pang et Chen
(33) T. astriniae Pang et Chen (37) T. astriniae Pang et Chen
Parasitoids Scelionidae (36) Telenomus chilocolus Wu et Chen (34) Telenomus dignoides Nixon
(35) T. dignus Gahan
(36) T. rowani Gahan
Parasitoids Mymaridai (4) Anagrus longitubulosus Pang et Wang
(5) A. nilaparvatae Pang et Wang
(6) A. paranilaparvatae Pang et Wang
(7) Gonatocerus longicrus (Kieffer)
(8) Mymar taprobanicum Ward
Parasitoids Dryinidae (9) Echthrodelphax fairchildii Perkin
(10) Haplogonatopus apicalis Perkin
(11) H. atratus Esaki et Hashimoto
(12) Paragonatopus fulgori (Nakagawa)
(13) Pseudogonatopus flavifemur Esaki et
Hashimoto
Parasitoids Sarcophagidae (37) Pierretia caudagalli (Bottcher) (38) Pierretia caudagalli (Bottcher)
Parasitoids Pipunculidae (14) Tomosvaryella oryzaetora (Koizumi)
(15) T. subvirescens (Leow)
Tachinidae (38) Ceromyia flaviseta Villeneuve (37) Gonia bimaculata Wiedemann (39) Exorista japonica Townsend
(39) Lydella grisescens Robineau-Desvoidy (38) Lydella grisescens Robineau-Desvoidy (40) Halidaya luteicornis Walker
(40) Metoposisyrops scirpophagae Chao et (39) Metoposisyrops scirpophagae Chao et Shi (41) Lydella grisescens Robineau-

Y.-G. Lou et al. / Biological Control 67 (2013) 8–20

Shi Desvoidy
(41) Pseudoperichaeta nigrolinea Walker (40) Nemorilla maculose Meigen (42) Nemorilla maculose Meigen
(42) Sturmiopsis inferens Townsend (41) Thecocarcelia oculata Baranov (43) Pseudoperichaeta nigrolinea Walker
(44) Thecocarcelia oculata Baranov
Parasitoids Elenchidae (16) Elenchinus japonicas Esaki et Hashimato
Predators Carabidae (43) Ophionea indica (Thunberg) (42) Ophionea indica (Thunberg) (45) Ophionea indica (Thunberg) (17) Ophionea indica (Thunberg)
(44) Archicolliuris bimaculata Redtenbacher (43) Colliuris chaudoiri Bohem (46) Colliuris chaudoiri Bohem (18) Colliuris chaudoiri Bohem
(44) Archicolliuris bimaculata Redtenbacher (47) Archicolliuris bimaculata (19) Archicolliuris bimaculata Redtenbacher
Redtenbacher
Predators Staphylinidae (45) Paederus fuscipes Curtis (45) Paederus fuscipes Curtis (48)Paederus fuscipes Curtis (20)Paederus fuscipes Curtis
(46)P. tamulus Erichson (49)P. tamulus Erichson (21)P. tamulus Erichson
Predators Coccinellidae (46) Micraspis discolor (Fabricius) (47) Coccinella transversalis Fabricius (50) Micraspis discolor (Fabricius) (22) Coccinella transversalis Fabricius
(48) Harmonia octomaculata (Fabricius) (23) Harmonia octomaculata (Fabricius)
(49) Micraspis discolor (Fabricius) (24) Micraspis discolor (Fabricius)
(50) Propylea japonica (Thunberg) (25) Propylea japonica (Thunberg)
Predators Hydrometridae (26)Hydrometra albolineata (Scott)
Predators Veliidae (47) Microvelia horvathi Lundblad (51) Microvelia horvathi Lundblad (27) Microvelia horvathi Lundblad
Predators Miridae (28) Cyrtorrhinus livdipennis Reuter
Predators Reduviidae (29) Polididus armatissimus Stal
Predators Lycosidae (48) Pardosa pseudoannulata (Boes. et Str.) (51) Pardosa pseudoannulata (Boes. et Str.) (52) Pardosa pseudoannulata (Boes. et (30) Pardosa pseudoannulata (Boes. et Str.)
Str.)
(52) P. laura Karsc (53) P. laura Karsc (31) P. astrigera L. Koch
(53) Pirata clercki (Boes. et Str.) (32)P. laura Karsch
(33) P. tschekiangensis Schenkel
(34) Pirata subpiraticus Boes. et Str.
(35) P. piratoides (Boes. et Str.)
(36) P. clercki (Boes. et Str.)
(37) P. piraticus (Clerck)
Predators Linyphiidae (38) Ummeliata insecticeps (Boes. et Str.)
Predators Oxyopidae (49) Oxyopes lineatipse L. Koch (54) Oxyopes lineatipse L. Koch (54) Oxyopes lineatipse L. Koch (39) Oxyopes lineatipse L. Koch
(50) O. sertatus L. Koch (55) O. sertatus L. Koch (55) O. sertatus L. Koch (40) O. sertatus L. Koch

(continued on next page)

11
12 Y.-G. Lou et al. / Biological Control 67 (2013) 8–20

2.2. Parasitic natural enemies

Plexippus paykulli Savigny at Audouin

Four hundred and twenty-four species of the parasitic natural
(44) Chiracanthium japonicum Boes. et Str.
(45) Misumenops tricuspidatus (Fabricius)

(46) Philodromus cespitum (Walckenaer)

enemies of rice pests, all belonging to Insecta, were identified in
N. lugens, S. furcifera, and L. striatellus

Menemerus confusus Boes. et Str.

(41) Clubiona japonicola Boes. et Str.

the rice paddy fields of China, including 350 species of 22 families

of Hymenoptera (parasitic wasp), 69 species of four families of

Maspissa magister (Karsch)

(48) Xysticus ephippiatus Simon
Bianor aenescens (Simon)

Ecarcha albaria (L. Koch)

(43) C. corrugata Boes. et Str.
(42) C. kurilensis Boes. et Str.
Rice planthoppers, including

B. hotingchiehi Schenkel
Diptera (parasitic fly) and 5 species of two families of Strepsipter-
(47) P. spinitarsis Simon a. Among the parasitic flies, 51 species of Tachinidae parasitize le-
pidopteran pests, and 11 species of Pipunculidae parasitize rice

P. setipes Karsch
planthoppers and leafhoppers (Table 3) (He et al., 1991; Tang
et al., 2001a,b).

2.3. Pathogenic microorganisms

(49)
(51)
(52)
(53)
(54)
(55)
(56)
There were 64 species of pathogenic microorganisms of rice
pests reported in China, including 36 species of fungi, 5 species
(58) Chiracanthium japonicum Boes. et
(56) Clubiona japonicola Boes. et Str.

of bacteria, 6 species of viruses, two species of microsporidia,

and 15 species of nematodes (He et al., 1991).
(60) Xysticus ephippiatus Simon
(59) Misumenops tricuspidatus

(61) Bianor aenescens (Simon)

(57) C. kurilensis Boes. et Str.
Rice leaf folder C. medinalis

2.4. Arthropod natural enemies of major insect pests

The major arthropod natural enemies of major rice insect

pests, including the rice stem borer C. suppressalis (Walker), the
(Fabricius)

yellow rice borer T. incertulas (Walker), the rice leaf folder C. med-
inalis Guenee, and three species of planthoppers including N. lu-
Str.

gens (Stål), S. furcifera (Horváth), and L. striatellus (Fallén), are

shown in Table 4 (data from He et al., 1991). Among these are
53 species of natural enemies of C. suppressalis (42 species of par-
asitoids and 9 species of predators), 58 species of natural enemies
(56) Misumenops tricuspidatus (Fabricius)

of T. incertulas (41 parasitoids and 17 predators), 61 species of C.

medinalis (44 parasitoids and 17 predators), and 56 species of the
three rice planthoppers (16 parasitoids and 40 predators)
(57) Xysticus ephippiatus Simon

(58) Bianor aenescens (Simon)

Yellow rice borer T. incertulas

(Table 4).

3. Brief introduction to some major natural enemies

In China, research on the natural enemies of rice insect pests is

mainly focused on arthropods. Therefore, here we introduce 10
species of arthropod natural enemies with economic importance,
including 4 species of parasitoids and 6 species of predators. Since
the morphology of these species has been described in detail in
various books, morphological identification for each species is
omitted. Because few studies exist for pathogenic microorgan-
(51) Clubiona kurilensis Boes. et Str.

isms, we provide only a general introduction.

(52) Xysticus ephippiatus Simon
Rice stem borer C. suppressalis

(53) Bianor aenescens (Simon)

3.1. T. japonicum Ashmead (Hymenoptera: Trichogrammatidae)

3.1.1. Biology
There are four developmental stages of T. japonicum; however,
the first three stages finish developing inside the host egg. The
generation period varies according to temperature. For example,
the generation period is 30.2 days at 16 °C and only 8 days at
27 °C. High temperatures, such as 35 °C, stop the development
of immature insects and kill adults (Pu, 1978). The most suitable
Taxon of natural

temperature for wasps is 30 °C. The sex ratio of the parasitoid is

biased toward females and ranges from 1:1 to 3:1 in the field.
Clubionidae

Thomisidae

Generally, male wasps emerge prior to females and mate imme-

Salticidae
enemies

diately after their eclosion. Both females and males can mate
multiple times. Females produce male offspring if they are not
Table 4 (continued)

mated. T. japonicum overwinter at their larval or pre-pupal stage.

The overwintering period normally increases as latitude in-
Predators

Predators
Predators
enemies
Natural

creases. In field conditions, there are 30 generations in Guang-

dong, 18–19 generations in Chengdu, 19–20 generations in
Zhejiang.
 Y.-G. Lou et al. / Biological Control 67 (2013) 8–20 13

3.1.2. Parasitism rates of rice planthopper eggs by A. nilaparvatae in early and late
Trichogramma japonicum is a dominant egg parasitoid against stages of rice development in the field are 35.1% and 20.1%, respec-
rice lepidoptera. For instance, the parasitism rate of the first gener- tively (Luo and Zhuo, 1980); in Jiangsu, the parasitism rates in July,
ation of the T. incertulas egg mass could be as high as 100% in August and September in a single rice field are 4–16.7%, 17.3–38.7%
Changshu and Jintan, in Jiangsu Province (Guo et al., 2002). How- and 32.5–55.6%, respectively (Lin and Hu, 1985). The major hosts of
ever, since the egg mass of T. incertulas consists of several layers, the parasitoid in the field also change with the season: L. striatellus
the covered layers can escape parasitization. With a life-table in May–June, S. furcifera in July–August and N. lugens in Septem-
method, Chen et al. (2010) proposed that T. japonicum can control ber–November. Rice variety can obviously influence the effective-
both C. suppressalis and Chilo auricili effectively. T. japonicum is very ness of the parasitoid in the field (Lin and Hu, 1985). This may
sensitive to insecticides (Guo et al., 2002). Thus, the abuse of insec- be partly owing to the difference in volatiles among varieties,
ticides may be the reason for the observed reduction in population which results in different attractiveness to the parasitoid (Lou
density of the parasitoid. et al., 2006). In addition, the morphological character of rice variety
Trichogramma japonicum has been artificially reared and re- may also affect the efficiency of the parasitoid by indirectly influ-
leased into the field for over half a century in China. The eggs of encing the vertical distribution of rice planthopper eggs on plants
Corcyra cephalonica (rice moth) are used as the alternative host. (Lou and Cheng, 1996b). Pesticides also have an obvious effect on
The parasitized C. cephalonica eggs can be stored at 3–4 °C for the parasitoid (Xu and Cheng, 1988; Liu et al., 2010). After pesticide
about 10 days; at this time, the eclosion rate of the parasitoid application, for instance, the parasitism rates of rice planthopper
may still be as high as 70% (Pu, 1978). When C. cephalonica eggs eggs by the parasitoid reduce from 53.52% to 11.11% (Xu and
are used for culturing T. japonicum on a large scale, a single wasp Cheng, 1988).
provided with 20 moth eggs produces the most efficient results
(Guo, 1992). 3.2.3. Hosts
Nilaparvata lugens (Stål), N. muiri China, N. bakeri (Muir), S. fur-
3.1.3. Hosts cifera (Horváth), Sogatella longifurcifera (Ksak. Et Ishihara), L. stria-
Pyralidae, Noctuidae, Hesperiidae, Arctiidae Lycaenidae. Agri- tellus (Fallen), Toya propinqua (Fieber), T. tuberculosa (Distant)
culturally important pests: T. incertulas, C. suppressalis, Sesamia and Saccharosydne procerus (Matsumura).
inferens, Pyrausta nubilalis, Naranga aenesc, Casinaria cloacae, Chi-
laraea auricili, Agrotis ypsilon, Prodenia litura, Mythimna separate, 3.2.4. Districts that the parasitoid has been found
Sitotroga cerealella. Guizhou, Jiangsu, Zhejiang, Jiangxi, Hunan, Sichuan, Taiwan,
Fujian, Guangdong, Guangxi, and Yunnan.
3.1.4. Districts that the parasitoid has been found
Liaoning, Hebei, Henan, Shaanxi, Jiangsu, Zhejiang, Anhui, Jiang- 3.3. Cotesia chilonis Matsumura (Hymenoptera: Braconidae)
xi, Hubei, Hunan, Sichuan, Fujian, Taiwan, Guangdong, Guangxi,
Guizhou, and Yunnan. 3.3.1. Biology
The developmental threshold temperature of C. chilonis is
3.2. Anagrus nilaparvatae Pang et Wang (Hymenoptera: Mymaridae) 11.6 °C. C. chilonis overwinters at its larval stage by staying inside
its host. Adult sex ratio is biased toward females, ranging from
3.2.1. Biology 3.4:1 to 2.2:1 under field conditions (Hang and Lin, 1989). Gener-
The developmental threshold temperature and thermal con- ally, a female wasp can oviposit several C. suppressalis larvae (more
stant of A. nilaparvatae in its immature stage are 10.6 °C and than 10 eggs can be laid inside each larva). In total, a female can
162.3 day degree, respectively (Zhu et al., 1991). The lifespan of reproduce more than 100 eggs. Male wasps emerge earlier and
adults is short, ranging from 1 to 3 days. Temperature influences make a round opening on a cocoon. Females emerge from the same
the survival rate, lifespan and fecundity of the parasitoid, but not opening and are ready to mate briefly after eclosion. Both females
the developmental rate (Xu and Cheng, 1989; Zhu et al., 1991). and males can mate multiple times. Females produce male off-
The optimum temperature for the population growth of the para- spring if they are not mated; the fertilized eggs develop as females.
sitoid is 27.3 °C. Generally, male wasps emerge prior to females The number of wasps emerging is positively related to the age of
and mate immediately after eclosion. A male adult can mate multi- host larvae; that is, old host larvae provide better nutrition than
ple times, whereas a female generally mates once. The adult sex ra- do younger larvae. However, body length is negatively related to
tio is biased toward females, ranging from 2:1 to 4:1. However, the number of emerged wasps. At a temperature of 26 °C, 70% rel-
females produce male offspring if they are not mated. Supplemen- ative humidity (RH) and provided with 10% honey water, the aver-
tal food, such as honeydew, can extend the lifespan and enhance age lifespan of female adults is 2.74 days; males, 3.84 days.
fecundity of the parasitoid (Zhu et al., 1991; Zheng et al., 2003).
Rice variety can also influence the development, surviva1 and 3.3.2. Parasitism
fecundity of the parasitoid, either directly through the physical Cotesia chilonis plays an important role in regulating density of
structure of the plant or indirectly through the hosts of the parasit- C. suppressalis. C. chilonis has been reported to be an obligate ento-
oid, such as N. lugens eggs (Lou and Cheng, 1996a). The parasitoid parasitoid of C. suppressalis. However, C. chilonis can also parasitize
prefers to parasitize eggs of N. lugens over those of S. furcifera when other Chilo species such as Chilo partellus or Chilo luteellus if these
both of them are present (Zhu et al., 1993). Volatiles emitted from insects are artificially provided. Normal parasitism rates range
rice plants infested by N. lugens or S. furcifera and kairomones pro- from 10% to 30% and may be as high as 90%, for example, in Jiangsu
duced from hosts play an important role in host location of the par- Province (Hang and Lin, 1989). In Zhejiang, the averaged parasitism
asitoid (Lou and Cheng, 1994, 2001a; Lou et al., 2005b). rates in the late stage of rice field were 10–18% and more than 20%
in wild rice, Zizania fields (Jiang et al., 1999). Parasitism rates
3.2.2. Parasitism among overwintering larvae are even greater; for example, the re-
Anagrus nilaparvatae is an important egg parasitoid of rice ported parasitism rates of overwintering generations in Hanjiang,
planthoppers, including N. lugens, S. furcifera, L. striatellus. The par- Jiangsu Province, were 26% and 31%, in 1985 and 1986, respec-
asitism rates of eggs of rice planthoppers by the parasitoid change tively. Han et al. (2009) reported that C. chilonis was the dominant
with the season. For example, in Fujian, the average parasitism parasitoid, leading to more than 50% mortality of C. suppressalis in
14 Y.-G. Lou et al. / Biological Control 67 (2013) 8–20

the Beijing area both before and after the overwintering stage of C. 3.5. Cyrtorrhinus livdipennis Reuter (Hemioptera, Miridae)
suppressalis larvae. Interestingly, in Zizania fields, C. chilonis plays a
minor role in killing C. suppressalis. But parasitism rates of C. chilo- 3.5.1. Biology
nis against C. suppressalis are higher in Zizania fields in southern Temperature significantly influences the generation duration of
areas of China. Since C. chilonis is very sensitive to insecticides, C. livdipennis: 21.8, 27.8 or 36.7 days at the daily mean tempera-
their overuse may have led to the lower density seen nowadays tures of 30.4, 27.8 or 23.9 °C, respectively, are required for C. livdi-
compared to the 1980s. pennis to complete a generation (Wu and Chen, 1987); there are 6–
8 generations per year (Chen and Zhou, 1981; Chen et al., 1981).
Eggs, laid individually on the rice leaf sheath and midrib, appear
3.3.3. Hosts milky white when newly deposited and become blue-green; a pair
In field conditions in China and Japan, only C. suppressalis larvae of red eyespots emerges before hatching (Chen and Zhou, 1981).
were reported to have been parasitized by C. chilonis. However, C. The nymph has four to six instars, usually five (Chen and Zhou,
chilonis can survive if provided with other Chilo species, such as 1981), which last 10–11 days (Chen et al., 1981). Adult mating oc-
C. partellus, C. luteellus, Chilo zacconius, Chilo orichalcociliella. curs within 2–3 days after eclosion and lasts for about one hour.
The longevity and oviposition of adult are related to factors such
3.3.4. Districts that the parasitoid has been found as temperature, humidity, and the type, quantity and growth per-
Jiangsu, Zhejiang, Hunan; Japan, Indonesia, North Korea. iod of prey species (Chen et al., 1992).

3.5.2. Predation
3.4. Apanteles cypris Nixon (Hymenoptera: Braconidae) As a major predator of rice planthoppers N. lugens and S. furcif-
era, C. livdipennis is an important factor in regulating the planthop-
3.4.1. Biology per (Chen et al., 1992). In the rice fields of Xiaoshan County of
Apanteles cypris is an important endoparasitoid against Cnap- Zhejiang Province, 39.1% eggs of N. lugens were predated by C. liv-
halocrocis medinalis (Cheng, 1984; Chen et al., 2002). Since A. cypris dipennis, including 29.8% in early rice fields and 54.9% in late rice
cannot overwinter in regions near the Yangzi River, it is considered fields in 1982 (Wu and Chen, 1987). Approximately 40–50% of S.
a migratory species along with C. medinalis. The duration of gener- furcifera eggs are predated at the early stage of late rice in August
ation varies from area to area. For example, the parasitoid can com- and September in Shaxian County of Fujian Province (Luo and
plete up to 7 generations in Zhejiang Province, 9 generations in Zhuo, 1986). The predation of C. livdipennis is influenced by a num-
Hunan Province. The parasitoid prefers to parasitize the 2nd instar ber of factors, such as rice variety (Lou et al., 2001c; Liu et al.,
of C. medinalis, as the smaller biomass of the 1st-instar larvae pro- 2002), the amount of nitrogen fertilizer used in rice fields (Lu
vides limited nutrient for the parasitoid; the older larvae are also et al., 2005), rice volatiles (Lou and Cheng, 2001b), chemical insec-
not preferred, given their ability to resist predation. When parasit- ticides (Zhao et al., 2008), prey density (Chen et al., 1993; Huang
izing hosts, the wasp places her ovipositor into the membrane be- and Huang, 2010), and so on.
tween the third and fourth segments of the larval abdomen.
Normally, at the 4th instar, the mature parasitoid larva emerges 3.5.3. Prey
from between the third and fourth segments and makes a cocoon Eggs of N. lugens, Sagatella furcifea, L. striatellus, Nephotettix
nearby. Adult sex ratio is biased toward females, nearly 2.3:1. Both cincticeps, Nephotettix apicalis, and Deltpcephalus dorsalis.
sexes are ready to copulate shortly after eclosion. Adulthood is
fairly long, lasting an average of 13 days for females and 12 days 3.5.4. Districts that the predator has been found
for males at 26 °C. The mated female parasitoid locates C. medinalis Hebei, Tianjin, Henan, Shanxi, Jiangsu, Shanghai, Zhejiang,
larvae by detecting chemical cues released from their frass (Zhou Anhui, Jiangxi, Hubei, Hunan, Taiwan, Fujian, Sichuan, Guangdong,
et al., 2012). Guangxi, Guizhou, and Yunnan.

3.6. Microvelia horvathi Lundblad (Hemioptera, Veliidae)

3.4.2. Parasitism
Apanteles cypris is a common parasitoid in rice fields and it is a 3.6.1. Biology
main natural enemy of C. medinalis. According to results reported One generation lasts 74–76, 56–64 and 41 days at temperatures
by Cheng (1984), in Huzhou and Zhejiang provinces, the overall of 22 °C, 25 °C and 28 °C, respectively. When preying on S. furcifera
parasitism rate was 37%. The actual rates changed with the gener- or N. lugens only, the duration of one generation is 25.86 or
ation, ranging from 18% to 51% from the second to fourth genera- 22.67 days, respectively (Chen et al., 1998). Eggs are laid individu-
tion of C. medinalis. A similar parasitism rate (>34%) was reported ally or together on the surface of rice culms close to water. Nymphs
in Changsha, Hunan Province (Chen et al., 1983). Chen et al. pass through 5 instars. Adults are able to mate repeatedly; alate
(1983) also found that the wasps normally locate hosts and lay and apterous adults can copulate with each other, and their off-
their eggs in the morning and afternoon. A. cypris is very sensitive spring might be either alate or apterous (Xiao et al., 1987). The
to the application of insecticides. Zhu et al. (2004) reported that growth, development, survival and fecundity of M. horvathi are
Methamidophos significantly reduced the population density of influenced by rice variety (Tang, 2004; Tang et al., 2005). However,
A. cypris. In addition, the reduction lasted over two weeks under the effects of transgenic Bt-Cry1Ab rice (Bai et al., 2005) and three
field conditions. kinds of bactericide on M. horvathi are not remarkable (Chen et al.,
1997).
3.4.3. Hosts
Cnaphalocrocis medinalis. 3.6.2. Predation
As an euryphagous predator, M. horvathi preys on homopterans
mostly (e.g. N. lugens, S. furcifera, N. bipunctatus, etc.), as well as on
3.4.4. Districts that the parasitoid has been found the young larvae of lepidopterans (e.g. C. medinalis, C. suppressalis,
Jiangsu, Zhejiang, Anhui, Jiangxi, Hubei, Hunan, Sichuan, Fujian, Casinaria colacae, Mycalesis gotama, etc.), aphids (Homoptera),
Taiwang, and Guangdong. springtails (Collembola), thrips (Thysanoptera), mosquitos
 Y.-G. Lou et al. / Biological Control 67 (2013) 8–20 15

(Diptera), etc. (Xiao et al., 1987). Both adults and nymphs of M. hor- female lays 3–6 egg-sacs, and each egg-sac contains 25–130 eggs.
vathi assault prey when they fall on the water’s surface; M. horvathi P. subpiraticus does not make a web but does have the web-making
adults either hunt individually or surround and annihilate prey to- habit during the breeding season. Female spiders sometimes put
gether (Xiao et al., 1987). One adult can reportedly predate 4.2 1st- egg-sacs temporarily on a web and later take them back on the
instar larvae or 2.2 3rd-instar nymphs of the rice planthopper in spinneret in the ventral posterior. The newly hatched spiderlings
one day (Plant Protection Group of Agricultural Sciece Academy first cluster on the mother’s back and 3–5 days later, disperse to
et al., 1978). hunt for prey. Spiderlings generally molt 7–8 times. The female-
to-male sex ratio is more than 1:1 in all generations except the first
3.6.3. Prey (Li et al., 2002). The spiders overwinter at all stages – adult, sub-
Nilaparvata lugens, S. furcifea, N. cincticeps, C. medinalis, C. sup- adult and nymph – though mostly as nymphs (Wu and Wang,
pressalis, C. colacae, M. gotama, aphid, etc. 1986). Cannibalistic behavior exists among individuals of P. subpi-
raticus (Wu and Wang, 1986; Huang et al., 1993).
3.6.4. Districts that the predator has been found
Jiangsu, Zhejiang, Hubei, Hunan, Taiwan, Fujian, Guangdong, 3.8.2. Predation
Guangxi. Pirata subpiraticus is one of the dominant species of arthropod
communities in rice paddy ecosystem (Ye et al., 1991; Lu et al.,
3.7. Paederus fuscipes Curtis (Coloptera, Staphylinidae) 2002a; Yin et al., 2010). Both adults and nymphs are euryphagous
predators; most prey on rice planthoppers and leafhoppers (Wu
3.7.1. Biology and Wang, 1986). One individual of P. subpiraticus has been known
The number of generations of P. fuscipes per year changes with to predate 64.4 nymphs, 37.4 macropterous males, 42.8 macrop-
region, e.g., 2–3 generations in Anhui (Liu et al., 2004) and 5 gen- terous females, 28.1 brachypterous males, or 35.1 brachypterous
erations in Fuzhou (Luo et al., 1990). Eggs are randomly laid on females of N. lugens (Ma et al., 2010). The spatial distribution of
the bottom of rice clusters; the larvae have two instars; the newly P. subpiraticus is consistent with that of its target pests, such as rice
hatched larvae actively hunt for prey; 2nd-instar larvae are rela- planthoppers and leafhoppers. The spiders play an important role
tively slow, live mostly on the bottom of rice plants or the surface in regulating the occurrence of rice planthoppers and leafhoppers
of the soil, and prey more than the adults do. Mature larvae mostly (Yin et al., 2010). The predation of the spiders is influenced by a
pupate at the bottom of rice clusters (Luo et al., 1990). Female number of factors, including their developmental stage, physiolog-
adults mate often and have a long spawning time (Luo et al., ical state and density (Ye et al., 1991; Lin and Tao, 1992; Shen et al.,
1990); adults hunt for prey frequently on rice plants and live as 2006a,b), prey species and density (Lin and Tao, 1992; Tang et al.,
long as 6 (Luo et al., 1990) to 11 months (Gu et al., 1989). Adults 2001a,b; Shen et al., 2006a,b), rice growth stage (Zhou et al., 1998),
mostly occur in paddy fields and disperse easily to surrounding etc.
habitats, e.g. sugarcane fields (Lin and Gu, 1988).
3.8.3. Prey
3.7.2. Predation
Nilaparvata lugens, S. furcifera, L. striatellus, rice leafhoppers.
Both adults and larvae of P. fuscipes are predators of the major
rice insect pests, such as N. lugens, S. furcifera, N. cincticeps, the
3.8.4. Districts that the predator has been found
newly hatched larvae of C. suppressalis and T. incertulas, the larvae
Heilongjiang, Hebei, Beijing, Shandong, Henan, Shaanxi, Jiangsu,
of C. medinalis, Naranga aenescens, C. oryzae and criocerid larvae,
Shanghai, Zhejiang, Anhui, Jiangxi, Hubei, Hunan, Taiwan, Fujian,
etc., especially of small insects like rice planthoppers and leafhop-
Sichuan, Guangdong, Guangxi, Guizhou.
pers (Luo et al., 1989). The 2nd-instar larvae mainly predate at the
bottom of rice clusters and have been recorded predating 4.2–11.7
of 3rd–5th instar nymphs of S. furcifera and 3.6–5.5 of 1st–3rd in- 3.9. Clubiona japonicola Boesenberg et Strand (Araneae, Clubionidae)
star nymphs of N. cincticeps per day; the adults are active in all
parts of rice plants and can predate 3.7–10.1 of 3rd-5th instar 3.9.1. Biology
nymphs of S. furcifera and 2.0–3.6 of 3rd–5th instar nymphs of N. Clubiona japonicola is widely distributed on the leaves of rice.
cincticeps per day (Luo et al., 1989). When ovipositing, females roll the leaf into a dumpling-like tri-
ple-fold so-called delivery room, in which three side-walls are
3.7.3. Prey made by a thin layer of silk close to the leaf. Female spiders usually
Adults and nymphs of N. lugens, S. furcifera, L. striatellus, C. ory- oviposit from July to August, and the newly hatched spiderlings
zae and N. cincticeps, the newly hatched larvae of C. suppressalis and first cluster in the ‘‘delivery room’’ for several days and then dis-
T. incertulas, the larvae of C. medinalis, N. aenescens and criocerid perse. Subadult spiders usually weave a flat nest of silk open at
larvae, etc. both ends on the rice leaf surface, hide inside, and escape rapidly
when scared (Feng, 1990). Spiderlings have a total of seven instars
3.7.4. Districts that the predator has been found at the immature stage. The female-to-male sex ratio may be as
Beijing, Hebei, Shandong, Henan, Shanxi, Gansu, Jiangsu, Shang- high as 4:1 in the field. One female lays 4–6 egg-sacs, and each
hai, Zhejiang, Anhui, Jiangxi, Hubei, Hunan, Sichuan, Taiwan, Fuj- egg-sac contains 63–167 eggs.
ian, Guangdong, Hainan, Guangxi, Guizhou, Yunnan.
3.9.2. Predation
3.8. Pirata subpiraticus Boesenberg et Strand (Araneae, Lycosidae) Clubiona japonicola play an important role in controlling rice
planthoppers and C. medinalis (Qi et al., 1989; Wu et al., 1993),
3.8.1. Biology especially C. medinalis larvae (Tao et al., 1993; Shen et al.,
The number of generations of P. subpiraticus per year changes 2006a,b). Investigation showed the highest predation of C. japoni-
with region, e.g. 2 generations in Changsha (Wu and Wang, cola on N. lugens in a system comprising three dominant species
1986) and 3–4 generations in Chongqing (Li et al., 2002). Both fe- of spiders – Ummeliata insecticeps, P. subpiraticus and C. japonicola
males and males mate many times. Females have a habit of pro- – that coexist with the major rice pest N. lugens. The predation of
tecting their eggs by carrying their egg-sacs with them. One C. japonicola is also related to the species composition and
16 Y.-G. Lou et al. / Biological Control 67 (2013) 8–20

population density of natural enemies and the density of pests (Li Panonychus citri and aphids (Li et al., 2008). In rice, B. bassiana
et al., 2001). has been reported to parasitize N. lugens, S. furcifera, N. cincticeps,
C. suppressalis and C. medinalis. In Hunan province, the application
3.9.3. Prey of B. bassiana in rice fields reduced the population density of the
Nilaparvata lugens, S. furcifera, L. striatellus, rice leafhopper, C. green paddy leafhopper, N. cincticeps, by 77–81% for the overwin-
medinalis, N. aenescens, C. colacae, etc. tering generation and 73–83% for the second generation (Bao and
Gu, 1998).
3.9.4. Districts that the predator has been found Paecilomyces carnrus belongs to Paecilomyces, Moniliaceae,
Heilongjiang, Jilin, Liaoning, Hebei, Beijing, Tianjin, Shandong, Moniliales. It can parasitize rice planthoppers. The application of
Henan, Shanxi, Jiangsu, Shanghai, Zhejiang, Anhui, Jiangxi, Hubei, P. carnrus caused 66.17–90.78% of rice planthoppers to die in the
Hunan, Sichuan, Taiwan, Fujian, Guangdong, Guangxi, Guizhou, field at 3–7 days (Bao and Gu, 1998).
Yunnan.

4. Conservation biological controls in the development and

3.10. U. insecticeps (Boesenberg et Strand) (Araneae, Linyphiidae)
implementation of IPM
3.10.1. Biology
4.1. Species pool and conservation of arthropod natural enemies
Ummeliata insecticeps, one of the most common species in pad-
dy fields, prefers wet habitats and lives in rice fields by making
The species pool that form communities inside and outside of
small irregular nets at the bottom of rice clusters (Yu and Wang,
the crop agro-ecosystem represent a potentially important source
1990). Female spiders oviposit more than 10 times throughout
of natural biological control agents for crop pests (Liss et al.,
their lifespan in the rice fields around Jiangsu and Zhejiang (Feng,
1986). In the rice ecosystem, the species pool includes arthropod
1990). Temperature and humidity play key roles in the population
communities on ridges within rice fields, along roadsides, in non-
size of U. insecticeps (Yu and Wang, 1991). The number of genera-
rice crop habitats, and in fields with no crops (Zhang et al.,
tions of U. insecticeps per year change in different rice areas, e.g. 4
2001). Recognizing the roles of weeds in ridges and roadsides in
generations in Wuhan, Hubei Province (Zhao and Liu, 1987), 6 gen-
conserving natural enemies, measures to retain weeds in ridges
erations in Nanning, Guangxi Province (Zhang et al., 1987). The
and roadsides have been used for a long period in China. Our re-
overwintering adult spiders start to act in early March; the devel-
sults showed that the dominant species of natural enemies in
opmental duration of the first through sixth generation lasts 62, 47,
ridges were often the same as those found during the reestablish-
44, 53, 53, and 100 days, respectively (Chang and Ho, 1981). The
ment of arthropod community in rice fields (Table 5). It has been
spiders overwinter at the stages of adult and egg in the ridge crack
reported that some plants, such as soybean (Glycine max L. Merr.)
and weeds along the trench (Zhao and Liu, 1987).
and sesame (Sesamum indicum (L.), growing in non-rice habitats
were important reservoirs of natural enemies of rice pests, and
3.10.2. Predation
they enhanced the efficiency of the natural enemies by providing
The habits of U. insecticeps, living at the bottom of rice clusters,
food and alternative prey/hosts (International Rice Research Insti-
are similar to those of rice planthoppers in both spatial and spatio–
tute, 2010; Gurr et al., 2011; Zhu et al., 2013). In order to increase
temporal niches (Zhang et al., 1995; Luo et al., 2006), suggesting a
soil fertility and conserve natural enemies, Chinese farmers often
potential role of U. insecticeps in the control of rice planthoppers
plant green manure crops such as Astragalus smicus and Lolium per-
(Liu et al., 2002). Analyses of ELISA (enzyme-linked immunosor-
enne in winter. These kinds of measures significantly increase
bent assay) (Zhang et al., 1999) and fluorescent labeling (Xiao
amounts of predators and parasitoids, with up to 3 million spiders
et al., 2007) detection demonstrated the predation of U. insecticeps
per hectare in the spring (Wang, 1981).
on rice planthoppers. The predation is influenced by some factors,
such as the body size and population density of the predator, the
ratio of predator to prey, and pesticides (Pan et al., 1995; Xiao, 4.2. Evaluation of arthropod natural enemies
2004; Liu et al., 2006). Moreover, U. insecticeps is an important nat-
ural enemy of rice aphids, the young larvae of C. medinalis, C. sup- According to results of natural life-tables of major rice insect
pressalis and T. incertulas (He et al., 1991). pests, T. incertulas, C. medinalis and N. lugens, predatory natural
enemies were the species used to suppress populations of above
3.10.3. Prey insect pests (Gu et al., 1983; Zhang et al., 1994; Pang and Liang,
Nilaparvata lugens, S. furcifera, rice leafhoppers, rice aphids, 1995).
young larvae of C. medinalis, newly hatched larvae of C. suppressalis In Dasha Town of Sihui City (County), Guangdong Province, the
and T. incertula. spider U. insecticeps first moves from species pools in rice fields
early in the rice-growing season and becomes the dominant spe-
3.10.4. Districts that the predator has been found cies of the arthropod community (Table 5). It has the biggest
Hebei, Beijing, Shandong, Henan, Shanxi, Jiangsu, Shanghai, time–space niche overlapping value with rice planthoppers, fol-
Zhejiang, Anhui, Jiangxi, Hubei, Hunan, Sichuan, Taiwan, Fujian, lowed by P. subpiraticus (Zhang et al., 1995). Using ELISA, the fre-
Guangdong, Guangxi, Guizhou, Yunnan, Jilin. quencies of the above 2 spiders scoring positive for the remains
of two planthoppers N. lugens and S. furcifera were the highest
3.11. Pathogenic microorganisms (Zhang et al., 1999). These results showed that two spider species,
U. insecticeps and P. subpiraticus, are keynote predators against rice
There are only a few reports on the effects of pathogenic micro- planthoppers.
organisms on rice insect pests. These microorganisms mainly in- In the early 1970s, billions of Trichogramma spp were produced
clude Beauveria bassiana and Paecilomyces carnrus. B. bassiana to control lepidopteran pests of food crops, cotton, cane and so on.
belongs to Beauveria, Moniliaceae, Moniliales. The technique for In Guangdong Province, for example, Trichogramma was released in
reproducing B. bassiana by solid state fermentation has been devel- about 13,000 hectare of paddy fields to control C. medinalis, with
oped. B. bassiana has been applied to control many agricultural and about 80% eggs parasitized (Collaborative Research Group of Bio-
forest insect pests, such as P. nubilalis, Dendrolimus punctatus, logical Control of Rice Pests and Guangdong Province, 1974). The
 Y.-G. Lou et al. / Biological Control 67 (2013) 8–20 17

Table 5
Comparison of dominant species of predators and parasitoids in ridges of rice fields and reestablishment period of arthropod community in rice fieldsa.

Natural enemies Experimental sites Ridges in winterc RP in early rice seasonb Ridges in summerd RP in late rice season
Predators Dasha Township U. insecticeps U. insecticeps – –
P. subpiraticus P. subpiraticus
Paederus spp Tetragnatha spp
Dinghu District U. insecticeps U. insecticeps – –
Clubiona spp
Paederus spp
Parasitoids Dasha Township A. nilarparvatae Anagrus sp1 A. paranilarparvatae A. nilarparvatae
A. nilarparvatae A. nilarparvatae A. paranilarparvatae
Dinghu District A. longitubulosus A. nilarparvatae P. andoi A. nilarparvatae
A. nilarparvatae Anagrus sp1 A. nilarparvatae O. nephotettica
Gonatocerus sp

U. insecticeps: Ummeliata insecticeps:

P. subpiraticus: Pirata subpiraticus.
A. nilarparvatae: Anagrus nilarparvatae.
A. paranilarparvatae: Anagrus paranilarparvatae.
P. andoi: Paracentrobia andoi.
O. nephotettica: Oligosita nephotettica.
a
Dominant species: dominance index > 10%, in descending order. Data are cited from Zhang et al. (2001).
b
RP: reestablishment period of arthropod community, 1–21 days after transplanting rice seedlings.
c
In the winter without rice.
d
In the summer between two rice seasons.

most common used species were T. japonicum, T. australicum and T. application of synthetic herbivore-induced volatiles enhances the
dendrolimi. Currently, T. japonicum is recommended as the first effectiveness of natural enemies on herbivores (James, 2003,
Trichogramma species against lepidopteran rice pests (Chen et al., 2005; Yu et al., 2008; Lee, 2010; Orre et al., 2010). In rice, it has also
2010). been reported that herbivore-induced rice volatiles are very attrac-
tive to the natural enemies of herbivores (Lou et al., 2005a,b; Qi
4.3. Evaluation of ducks and fishes et al., 2011). The production of herbivore-induced rice volatiles is
modulated by the jasmonic acid (JA), salicylic acid and ethylene
Raising ducks and fish in paddy fields was recorded in Chinese signaling pathways (Lu et al., 2006; Qi et al., 2011; Li et al.,
history 1700 years ago. Rice–duck and/or rice–fish farming is pro- 2012). Moreover, using chemical genetics, Xin et al. (2012) identi-
ven to have important economic and ecological benefits, including fied 2,4-dicholorophenoxyacetic acid (2,4-D) as a potent elicitor of
suppressing rice diseases, decreasing rice insect pests and weeds rice defenses and found that the exogenous application of 2,4-D
and producing a safe rice product. can enhance basal and herbivore-induced JA and ethylene levels.
Raising fish Carassius auratus var. pengzenensis in paddy fields High JA and ethylene levels subsequently elicit the release of rice
decreased the density of rice planthoppers by 34.56–46.26% (Xiao volatiles and attract BPH and its egg parasitoid, A. nilaparvatae.
et al., 2001). Raising ducks in paddy fields reduced rice pest density The result is high parasitism of BPH eggs in the field. Recently,
by 53.2–76.8%, including striped rice borer C. suppressalis (Liu et al., S-linalool, a compound that is strongly induced by BPH infestation,
2005) and rice planthoppers (Yang et al., 2004). The population was found to be attractive to the parasitoid A. nilaparvatae as well
densities of spiders in the field where ducks were released were as to predatory spiders. At the same time S-linalool has been found
2.66–3.61-fold higher than those in conventional rice fields (Yu to repel BPH, making it an effective compound for reducing pest
et al., 2004). pressure in the field. On the other hand, (E)-b-caryophyllene, a con-
stitutively emitted volatile that is not inducible by BPH, attracted
4.4. Evaluation of biological insecticides and pathogenic both BPH and its natural enemies, causing an increase in the BPH
microorganisms population (Xiao et al., 2012).
These results illustrate that specific herbivore-induced rice vol-
Microbial insecticides such as B. thuringiensis (Bt) and the path- atiles can indeed protect plants by recruiting natural enemies from
ogenic microorganism B. bassiana have been used to control rice in- the environment and repelling pest insects in the field. In contrast,
sect pests. Bt has been used against lepidopteran rice insect pests, other compounds exact a price from the plants by giving away the
including T. incertulas, C. suppressalis and C. medinalis, resulting in a plants’ presence to herbivores. Exploiting volatile-based herbivore
75% or higher reduction in population densities of these pests. B. management methods, such as applying specific volatiles or chem-
bassiana could control N. lugens, C. suppressalis and C. medinalis, ical elicitors that can elicit the release of volatiles, and breeding
which caused more than 80% of pests dead in the field (Hu et al., rice varieties with specific volatile profiles, combined with other
2010; Kong et al., 2010). management strategies, such as push–pull (Cook et al., 2007) and
an ecological engineering program (Gurr et al., 2011), may greatly
4.5. Role of herbivore-induced rice volatiles in augmenting the enhance the effectiveness of biological agents. For example, if rice
efficiency of natural enemies plants that produce (E)-b-caryophyllene but not S-linalool are
sown at the edges of the field, both BPH and its natural enemies
It has been well documented that herbivore-induced plant vol- could be strongly attracted. If the rest of the plants are engineered
atiles play an important role in the host/prey searching behavior of to produce high amounts of S-linalool but not (E)-b-caryophyllene,
predators and of the parasitoids of herbivores (Turlings et al., 1990; they will likely remain pest free (Xiao et al., 2012). If rice plants at
De Moraes et al., 1998; Rasmann et al., 2005; Dicke et al., 2009; All- the edge of a field are sprayed with 2,4-D, a trapping zone is cre-
mann and Baldwin, 2010). Researchers have confirmed that the ated that reduces pest damage in the inner parts of the field. This
18 Y.-G. Lou et al. / Biological Control 67 (2013) 8–20

may also lead to higher numbers of egg parasitoids in these zones, thus reducing the amount of chemical insecticides applied by
keeping pest reproduction to a minimum and creating a source of 80% (Zhu, 2012).
parasitoids that can attack the next generation of the pest in the
untreated parts of the fields (Xin et al., 2012). Combined with an
5. Conclusion and perspectives
ecological engineering program, such volatile-based methods
may further enhance the effect of natural enemies by helping them
As stated above, several major biological control methods for
to locate their hosts/prey, an effect that neither of the two mea-
rice insect pests in China, such as applying biological insecticides,
sures can achieve alone (Gurr et al., 2011).
releasing natural enemies and conserving natural enemies by
planting specific flowering plants or grasses in non-rice crop hab-
4.6. Implementation of conservation biological controls
itats, have been developed. Furthermore, based on these measures,
a primary ecological engineering program that aims to enhance the
Since the early 1970s, Chinese IPM experts have established rice
population density and efficiency of natural enemies of insect pests
IPM areas with the support of local government, including those in
has been assembled and applied. The results have shown that such
Dasha Township in Sihui County of Guangdong Province, Hailing
a program can effectively augment the effect of natural enemies,
Island in Guangdong Province, Xiangyin in Hunan Province, Jinhua
decreasing the frequency of insect pest outbreaks and the need
in Zhejiang Province and Jiading in Shanghai City, emphasizing
for pesticides (Gurr et al., 2011). However, these methods have
conservation and the utilization of natural enemies. The successful
only been applied in small areas. Most farmers still mainly use
models and measures were not only adopted and extended domes-
chemical insecticides to control rice insect pests for these reasons:
tically, but also received very positive comments abroad (National
(1) biological control methods are relatively time-consuming, inef-
Academy of Sciences of USA, 1977; FAO, 1979).
ficient, costly and labor-intensive, compared to chemical insecti-
As one of the model examples, the rice IPM program in Dasha
cides; (2) farmers receive little income from rice production,
Township, located at N23°190 , E112°400 , started in 1973 in a
which impedes their willingness to spend more money and labor
1.6 ha rice field, and reached 4000 ha in 1975. Its aims are to sup-
for pest control; (3) farmers have not understood the significance
press the population of major insect pests, to restore natural ene-
of biological control methods for the health of the environment;
mies, and to reduce use of pesticides. In order to ensure the
(4) family-based small-scale rice production (in most cases, the
program is successful, IPM experts have taken many measures;
area of rice field per family is less than one thousand square me-
these mainly include (1) teaching farmers basic IPM knowledge,
ters) makes it difficult to apply some biological control methods,
such as distinguishing insect pests and natural enemies, in a so-
such as planting natural enemies-augmenting plants in non-rice
called field farmer school; (2) plowing the paddy fields in early
crop habitats. Developing new, highly efficient biological methods
spring followed by immersing them in water to kill over-wintering
that enhance the effectiveness of natural enemies; promoting the
herbivores, such as the larvae of T. incertulas and C. suppressalis in
effectiveness of methods of biological control currently applied;
rice stubble; (3) growing resistant rice varieties; (4) conserving
enhancing farmers’ understanding of biological controls; and alter-
natural enemies, including frogs; (5) raising ducks in paddy fields;
ing the mode of rice production – adopting farm-based large-scale
(6) releasing masses of Trichogramma spp; (7) spraying B. thuringi-
rice production, for example – will eliminate the constraints of bio-
ensis and (8) spraying chemical pesticides only as needed in heav-
logical control and improve pest management.
ily infested areas (Pu et al., 1984). The program is very successful
This work requires the collaboration of entomologists, ecolo-
and has achieved significant long-term benefits, including (1)
gists, chemists and plant physiologists. Future research needs to
farmers have basic IPM knowledge; (2) the dominant position of
answer the following questions: Which plants planted in non-crop
natural enemies in rice fields has been restored; for example, the
habitats can enhance the effectiveness of natural enemies of rice
ratio of herbivores to predatory arthropods in the IPM area de-
insect pests and what are the mechanisms? How many area of such
creased by 16.22–90.24% compared to the ratio in the control area
non-crop habitats are needed for a given rice field? Which chemi-
in 1979; (3) chemical pesticide use has decreased significantly, e.g.
cals can attract a pest’s natural enemies directly or indirectly by
by nearly 80% in 1979 compared to 1972 and (4) the agricultural
eliciting plants? How should these chemicals be applied? Which
environment has improved and become suitable for ‘‘green food’’
biological control agents are important for regulating population
production (Pu et al., 1984; Zhang et al., 1996).
densities of rice insect pests and can be exploited and applied in
Recently, to encourage the biological control of rice insect pests,
the field? And so on. To achieve these, a series of experiments
an ecological engineering program has been introduced that fo-
should be carried out in the lab and field by combining bioassays,
cuses on vegetation diversity without disrupting profitable farm-
chemical analysis, and molecular biology. These results could be
ing (Gurr et al., 2011). The program tries to suppress insect pests
used to improve the efficiency of methods of biological control
directly or indirectly by providing refuge habitats to parasitoids
and develop new methods of biological control that adapt to vari-
and predators, moderating microclimates and offering alternative
ous areas, such as volatile-based methods and the release of bio-
prey/host and food (Gurr et al., 2011). Such a program has been
logical control agents. Thus, effective ecological engineering
established in areas in Jinhua (ca 37 ha) and in Sanmen (ca
programs that enhance population densities and the effectiveness
20 ha), Zhejiang Province; there, a range of ecologically based pest
of the natural enemies of insect pests and are appropriate for dif-
management strategies, including growing soybean and sesame on
ferent areas could be set up. We hope farmers will see the benefits
the ridges of rice fields, applying sex pheromones to stem borers
of applying these programs. In effective ecologically engineered
and leaf folders and using ducks for pest control, has been imple-
programs, population densities of natural enemies and their effi-
mented (International Rice Research Institute, 2010). The program
ciency will be kept at high levels. Such levels will decrease the pop-
has helped enhance the biological control of rice insect pests and
ulation levels of rice insect pests and thus reduce the amount of
reduce the population levels of insect pests. In Jinhua, for example,
insecticides and environmental pollution.
the population densities of parasitoids of eggs of rice planthoppers
and predatory spiders in the ecological engineering-based area
were 2- to 4-fold higher than those in the control area, and the Acknowledgments
number of damselflies and frogs, predators of the rice insect pests,
were 5- to 10-fold higher than the latter; the increased population We thank Emily Wheeler for editorial assistance. The study was
levels of natural enemies decreased the number of insect pests, jointly sponsored by the National Basic Research Program of China
 Y.-G. Lou et al. / Biological Control 67 (2013) 8–20 19

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