Annals of Applied Biology ISSN 0003-4746
REVIEW ARTICLE
Parasitoids of Asian rice planthopper (Hemiptera: Delphacidae)
pests and prospects for enhancing biological control
by ecological engineering
G.M. Gurr1 , J. Liu2 , D.M.Y. Read3 , J.L.A. Catindig4 , J.A. Cheng5 , L.P. Lan6 & K.L. Heong4
1 EH Graham Centre for Agricultural Innovation (Industry and Innovation NSW and Charles Sturt University), Orange, NSW, Australia
2 Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Fuyang, Zhejiang Province, China
3 School of Agriculture and Wine Science, Charles Sturt University, Orange, NSW, Australia
4 Crop and Environmental Sciences Division, International Rice Research Institute, Los Baños, Metro Manila, Philippines
5 Institute for Insect Sciences, Zhejiang University, Zhejiang Province, China
6 Institute for Agricultural Science of South Vietnam, 121 Nguyen Binh Khiem, District #1, Ho Chi Minh City, Vietnam
Keywords
Bt rice; Delphacidae; ecological engineering;
habitat manipulation; herbivore-induced
plant volatiles; IPM; Laodelphax striatellus;
Nilaparvata lugens; planthopper; Sogatella
furcifera.
Correspondence
G.M. Gurr, EH Graham Centre for Agricultural
Innovation (Industry and Innovation NSW and
Charles Sturt University), PO Box 883, Orange,
NSW 2800, Australia.
Email: ggurr@csu.edu.au
Received: 6 August 2010; revised version
accepted: 31 October 2010.
doi:10.1111/j.1744-7348.2010.00455.x
Abstract
The brown planthopper (BPH) Nilaparvata lugens, whitebacked planthopper
(WBPH) Sogatella furcifera and smaller BPH Laodelphax striatellus increasingly
exhibit resistance to insecticides and adaptation to resistant varieties, so
they threaten food security. This review draws together, for the first time,
information on the parasitoids of planthopper pests of rice from the nonEnglish literature published in Asia. This is integrated with the English
language literature to provide a comprehensive analysis. Planthopper pests
of rice are attacked by a large range of parasitoids from Strepsiptera, Diptera
and, especially, Hymenoptera. Levels of field parasitism vary widely between
parasitoid species and locations. For many taxa, especially within Mymaridae,
there is evidence that non-crop habitats are important as overwintering
habitat in which alternative hosts are available. These source habitats may
promote early season parasitism of pest Hemiptera in rice crops, and their
movement into crops could be manipulated with applications of herbivoreinduced plant volatiles. Non-crop plants can also provide nectar to improve
parasitoid longevity and fecundity. Despite evidence for the importance of
environmental factors affecting parasitoids of rice pests, the use of habitat
manipulation to enhance biological control in the world’s most important crop
is surprisingly underrepresented in the literature. Current research in China,
Vietnam and Thailand on ecological engineering, carefully selected vegetation
diversity introduced without disrupting profitable farming, is briefly reported.
Although the most important pest, BPH (N. lugens), is a migratory species,
maintaining local communities of parasitoids and other natural enemies offers
scope to prevent even r-selected pests from reaching damaging population
densities.
Introduction
The human population is rapidly approaching seven
billion and more than one half depend on rice as their
food staple (International Rice Research Institute, 2010a).
Continued population growth in developing countries
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and the inability of major rice importing countries,
particularly in Africa and the Middle East and the
Philippines, to significantly increase production is forecast
to lead to increasing demand and greater international
rice trade over the next decade (US Department of
Agriculture, 2010). Although annual rice production has
149
Parasitoids of Asian rice planthoppers
more than doubled from less than 200 million tonnes
at the advent of the ‘green revolution’ in the 1960s,
achieving future food security depends on development
of better solutions for key rice pests.
Amongst the most important pests in Asian rice is the
highly migratory brown planthopper (BPH) Nilaparvata
lugens (Stål). This and related delphacids cause direct
feeding damage, ‘hopperburn’, and transmit the viruses
responsible for rice grassy stunt virus (RGSV), rice ragged
stunt virus (RRSV), rice striped virus (RSV), rice black
streaked dwarf virus (RBSDV) and south rice black
streaked dwarf virus (SRBSDV). These Hemiptera are
secondary, largely insecticide-induced, pests (Heinrichs
& Mochida, 1984) and often cause more yield loss than
by Lepidoptera pests such as stem borers or leaffolders
(Dale, 1994).
Management of rice planthoppers employs host plant
resistance (HPR), but field resistance levels are limited
by the rapidity with which the delphacids, especially
N. lugens, are able to overcome resistance genes (Horgan,
2009). As a result there continues to be heavy
dependence on synthetic pesticides and this, in turn,
has led to resistance to widely used neonicotinoid
and phenylpyrazole compounds being reported from
many Asian countries (Matsumura et al., 2009). The
whitebacked planthopper (WBPH) Sogatella furcifera
(Horvath) has also exhibited resistance to compounds
such as fipronil in Japan, China and Vietnam (Matsumura
et al., 2009).
A significant research effort has led to genetically
modified rice expressing several traits. Amongst these,
snowdrop lectin and Allium sativum leaf agglutinin have
been shown experimentally to confer resistance to
delphacids in modified rice (Nagadhara et al., 2004 and
Yarasi et al., 2008, respectively). More widely used traits
are Bacillus thuringiensis (Bt) and cowpea trypsin inhibitor,
but these have no effect on sucking pests (Xia et al., 2010).
In China, the world’s largest rice producer and sixth
largest exporter (US Department of Agriculture, 2010),
Bt rice obtained its biosafety certificates in late 2009
and is now awaiting approval for commercialisation (Jia,
2010). Accordingly, whilst the possible use of this new
technology offers scope to contribute to the management
of key lepidopteran pests such as yellow stemborer,
Scirpophaga incertulas (Walker), and the rice leaffolder,
Cnaphalocrocis medinalis (Guenée) (Fam: Pyralidae) in the
foreseeable future, it will have no direct effect on N. lugens
and other sucking pests. There is, therefore, an urgent
need to improve pest management of non-lepidopteran
pests of rice so that rising levels of resistance to insecticides
and breakdown of HPR do not lead to crop failure.
Settele et al. (2008) go further and call for a ‘switch’ of
research effort from GM to ecological engineering (sensu
150
G.M. Gurr et al.
Gurr et al., 2004) in rice. Ecological engineering employs
carefully selected vegetation diversity introduced without
disrupting profitable farming to suppress pests either
directly or via enhancement of natural enemy activity.
Despite evidence for the importance of environmental
factors affecting parasitoids of rice pests, the use of such
approaches to enhance biological control in the world’s
most important crop is surprisingly underrepresented in
the literature. This is illustrated by a keyword search of
the Web of Science database for ‘habitat manipulation’
or ‘conservation biological control’ finds 348 articles but
only three of these are on the world’s most important
crop species. Just two of these articles address insect pest
management (Van Mele & Cuc, 2000; Drechsler & Settele,
2001); the other is about rats (Mill, 1993). Way & Javier
(2001) also point out the neglect of biodiversity-related
approaches to rice pest management.
That biological control offers scope to contribute to
better rice pest management is indicated by a recently
published food web for planthopper pests of Asian tropical
rice (Dupo & Barrion, 2009). This consists of 244 natural
enemy species, 89% of which are invertebrates, 7%
vertebrates and 4% microbial or nematode pathogens.
Such food webs are useful in indicating the complexity
of trophic relationships in pest/natural enemy systems
and the broad nature of the taxonomic groups in which
antagonists are found. They are, however, limited in
terms of directly supporting pest management. More
detailed information is required to indicate which taxa
are responsible for the highest levels of pest mortality
and which offer scope to be manipulated to enhance
their impact by habitat management (Landis et al., 2000).
Whilst detailed information is available on many natural
enemies of rice planthoppers, much of this exists only in
non-English language (especially Chinese) publications or
in the grey literature including institutional reports. These
factors make much of the useful information inaccessible
to the English-speaking scientific community and inhibit
the flow of important information between differing nonEnglish-speaking countries; for example from China to
Vietnam and vice versa.
This review draws together for the first time, information on the natural enemies of planthopper pests
of rice from the non-English literature published in
Asia. This is integrated with the English language literature to provide a comprehensive analysis. The main
digital tool for literature identification was Web of Science, and full text articles were then obtained either
electronically or via interlibrary loan. In addition, the
personal and institutional collections of books and reports
of the authors were searched. Information from nonEnglish sources was translated by the multilingual author
team. The primary focus of the review is the three
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G.M. Gurr et al.
key delphacid pest species of Asian rice: rice smaller
BPH, Laodelphax striatellus (Fallén); and the previously
mentioned N. lugens and S. furcifera. In terms of natural enemy taxa, this review is concerned with parasitoids
(Hymenoptera, Diptera, Strepsiptera) and considers scope
for ecological engineering methods such as nectar plants
and refuge vegetation (Gurr et al., 2004) to be used to
combat the escalating pest problems. Relevant also is
the availability of alternative hosts for the parasitoids.
Accordingly, information is provided for some of the better researched species including the green rice leafhopper
Nephotettix virescens (Distant) (Hemiptera: Cicadellidae).
Our focus on parasitoids does not detract from the
potential value of predators in biological control of rice
planthoppers but reflects the fact that mortality of delphacid rice pests caused by parasitoids can be very high.
For example, studies in Peninsular Malaysia found total
egg mortality to be as high as 92% for N. lugens and 90%
for S. furcifera with parasitoids responsible for 68% and
69%, respectively (Watanabe et al., 1992). The available
literature suggests that spiders and predatory insects can
also be important mortality factors (Heong et al., 1991;
Settle et al., 1996). The ecological engineering strategies
detailed herein to encourage parasitoids will potentially
benefit predators by providing refuge habitat, moderated
microclimate alternative prey and plant food (pollen).
Parasitoids of delphacid pests in Asian rice
Order: Hymenoptera
Family: Dryinidae
Approximately 20 dryinid species have been reported to
parasitise N. lugens, L. striatellus, S. furcifera and N. virescens
(Table 1). Female dryinids are solitary endoparasitoids
that parasitise adult and all five nymphal stages of
N. lugens (Sahragard et al., 1991). They are obligate host
feeders with chelate fore tarsi adapted for holding prey
which are typically first- to fourth-stage nymphs. Host
feeding by the dryinid usually causes the host to die, and
the cadaver is dropped from the plant whilst parasitised
hosts are released from the forelegs and placed back
on the food plant. Host feeding is important to dryinids
because they are strongly synovigenic but feeding on
host haemolymph is important for survival as well as
egg maturation. An individual will, on average, feed
on 3.2 nymphs and parasitise 4–9 nymphs per day
(Chandra, 1980). Daily fecundity is reported to be 15–25
in Echthrodelphax fairchildii (Perkins) (Ito & Yamada,
2007). Laboratory work indicates that the combined
effect could cause 54.9% host mortality although this
is considered to be an overestimate of typical levels of
field impact (Kitamura, 1982).
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Parasitoids of Asian rice planthoppers
Dryinidae larvae develop within a sac that protrudes
from the host’s abdomen. When ready to pupate, they
emerge from the host and pupate in a spun cocoon
attached to the rice leaf or other substrate (Chiu, 1979).
Host quality appears to affect parasitoid behaviour with
third instar nymphs being preferred by female wasps and
yielding the most strongly female-biased sex for parasitoid
progeny (Kitamura & Iwami, 1998).
Dryinids migrate into rice crops principally within a
parasitised host; indeed the female of many species is
wingless. The food web of Dupo & Barrion (2009) suggests
that dryinids are the most important natural enemies of
nymphal/adult delphacids in terms of numbers of taxa
(10 species). Field records, however, tend to suggest
an inconsistent level of incidence and field parasitism.
Echthrodelphax fairchildii and Gonatopus yasumatsui (Olmi)
were reported to be uncommon in Peninsular Malaysia
(van Vreden & Ahmadzabidi, 1986). Parasitism of
N. lugens by dryinid wasps was generally under 2% in
Japan, although parasitism of L. striatellus approached
10% in August/September (Kitamura, 1987). Parasitism
of S. furcifera by dryinids tended to be higher, around
10% most of the season and peaking at 20% in June/July
(Kitamura, 1987). In Japan, Haplogonatopus atratus (Esaki
& Hashimoto) was the most dominant dryinid species.
About five dryinid species have been recorded in rice
fields in Vietnam but parasitism of N. lugens and S. furcifera
by Dryinidae was reported to be less than 10% (Lam
et al., 2002).
In the Philippines total parasitism rates for E. fairchildii,
Haplogonatopus spp. and Pseudogonatopus spp. in N. lugens
and S. furcifera were also relatively low: 9.7% and
6.4% in the wet and dry seasons, respectively (Peña
& Shepard, 1986). In contrast, Chandra (1980) reported
parasitism of N. lugens by dryinid wasps in the Philippines
reached 35–40% in September–October in dryland
rice fields. In Sri Lanka 40% parasitism was reached
although this level of attack was not sufficient to
control N. lugens and S. furcifera infestations (Ôtake et al.,
1976). Dryinids appear to be still more important in
China where parasitism of L. striatellus reached close
to 50% as a result of the combined attack by:
Haplogonatopus japonicus (Esaki & Hashimoto), H. atratus
(Esaki & Hashimoto), Pseudogonatopus flavifemur (Esaki
& Hashimoto), Paragonatopus fulgori (Nakagawa) and
Pseudogonatopus sp.
Family: Mymaridae
Mymaridae are egg parasitoids of small to minute size
reported attacking delphacid planthopper pests of rice
widely throughout Asia from India east to China, northwards to Japan and south to Malaysia, Singapore and
151
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 1 Dryinidae parasitoids reported from Hemiptera pests of Asian rice
Parasitoid
Host
Location
References
Anteon yasumatsui (Olmi)
Nephotettix cincticeps (Esaki &
Hashimoto)
China
He & Xu (2002)
India
Indonesia
Thailand
China (Sinan County,
Guizhou)
India
Japan
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
Chen (1989)
Dicondylus indianus (Olmi)
= Pseudogonatopus flavifemur
(Esaki & Hashimoto)
Nilaparvata lugens
India
Japan
Malaysia (Peninsular)
Philippines
Asia
Sahragard et al. (1991) (citing Olmi, 1984)
Chiu (1979) (citing Esaki, 1932; Sakai, 1932; Esaki
& Hashimoto, 1933, 1936); Kitamura (1987)
Barrion et al. (1981); Chua et al. (1984); Dayanan
& Esteban (1996); Sahragard et al. (1991)
(citing Olmi, 1984)
Chu & Hirashima (1981); Sahragard et al. (1991)
(citing Olmi, 1984)
Lam (1992, 1996, 2000, 2001, 2002)
Dupo & Barrion (2009)
Lam (1992, 1996, 2000, 2001, 2002)
Dupo & Barrion (2009)
Dupo & Barrion (2009)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Chiu (1979) (citing Esaki & Hashimoto, 1936)
Chu & Hirashima (1981)
NPPS & ZAU (1991)
Kitamura (1987)
NPPS & ZAU (1991)
Ito & Yamada (2007)
Randhawa et al. (2006); Chiu (1979) (citing Rai,
personal communication)
Manjunath et al. (1978); Yadav & Pawar (1989)
Ito & Yamada (2007); Yamada & Ikawa (2003)
van Vreden & Ahmadzabidi (1986)
Barrion et al. (1981); Peña & Shepard (1986)
Dupo & Barrion (2009)
India
Japan
Philippines
India
Japan
Korea
Philippines
China (Taiwan)
India
Japan
Korea
Philippines
China (Taiwan)
India
Japan
Korea
Philippines
China (Taiwan)
India
Japan
Korea
Philippines
China (Taiwan)
Randhawa et al. (2006); Yadav & Pawar (1989)
Ito & Yamada (2007); Yamada & Ikawa (2003)
Peña & Shepard (1986)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Philippines
China (Taiwan)
Sogatella furcifera
Echthrodelphax bicolor
(Esaki & Hashimoto)
NPPS & ZAU (1991) indicate
E. fairchildii (Perkins) is synonymous
with E. bicolor (Esaki & Hashimoto)
Echthrodelphax fairchildii (Perkins)
Sogatella vibix (Haupt)
Tagosodes pusanus (Distant)
Nilaparvata lugens
Sogatella furcifera
Laodelphax striatellus (Fallén)
Laodelphax striatellus
Nilaparvata lugens
Perkinsiella saccharicida
(Kirkaldy)
Sogatella furcifera
Echthrodelphax spp.
Nephotettix cincticeps
Nephotettix nigropictus (Stål)
(Alternative spelling
N. nigropicta)
Nephotettix virescens (Distant)
Nilaparvata lugens
152
Vietnam
Asia
Vietnam
Asia
Asia
China
Japan
China (Taiwan)
China
Japan (Shimane)
China
Japan
India
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G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 1 Continued
Parasitoid
Epigonatopus sasakii
(Esaki & Hashimoto)
Gonatopus camelinus (Kieffer)
Gonatopus cuscelidivorus (Xu & He)
Gonatopus dromedarius (Costa)
Gonatopus flavifemus
Host
Location
References
Sogatella furcifera
Nephotettix cincticeps
India
Japan
Korea
Philippines
China (Taiwan)
China
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
NPPS & ZAU (1991)
Laodelphax striatellus
Nephotettix cincticeps
Laodelphax striatellus
Nilaparvata lugens
China (Guizhou)
China (Guangxi)
China
China
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
Chen (1989); Chu & Hirashima (1981); NPPS
& ZAU (1991)
Chiu (1979) (citing Esaki, 1932; Esaki & Hashimoto,
1933, 1936; Sakai, 1932)
Kitamura (1987)
Barrion et al. (1981); Chua et al. (1984); Dayanan
& Esteban (1996)
Lam (1992, 1996, 2000, 2001, 2002)
He & Xu (2002)
Dupo & Barrion (2009)
He & Xu (2002)
Lam (1992, 1996, 2000, 2001, 2002)
Dupo & Barrion (2009)
Dupo & Barrion (2009)
He & Xu (2002)
Japan
Japan (Shimane)
Philippines
Laodelphax striatellus
Sogatella furcifera
Gonatopus lucens (Olmi)
Sogatella vibix
Tagosodes pusanus (Distant)
Nephotettix cincticeps
Nilaparvata lugens
Sogatella furcifera
Gonatopus nigricans (Perkins)
Laodelphax striatellus
Nilaparvata lugens
Sogatella furcifera
Gonatopus nudus (Perkins)
Nilaparvata lugens
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Vietnam
China
Asia
China
Vietnam
Asia
Asia
China (Guangxi,
inner Mongolia)
Indonesia
Malaysia
Philippines
China (Guangxi,
inner Mongolia)
Indonesia
Malaysia
Philippines
China (Guangxi,
inner Mongolia),
Indonesia
Malaysia
Philippines
China
Indonesia
Malaysia
Philippines
China
Indonesia
Malaysia
Philippines
China
Indonesia
Malaysia
Philippines
China
India
Indonesia
Malaysia
Philippines
Sri Lanka
Thailand
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
153
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 1 Continued
Parasitoid
Host
Location
References
Sogatella furcifera
China
India
Indonesia
Malaysia
Philippines
Sri Lanka
Thailand
China
India
Indonesia
Malaysia
Philippines
Sri Lanka
Thailand
China
Japan
China (Guangxi)
India
Japan
China (Taiwan)
Malaysia (Peninsular)
Malaysia (Peninsular)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
He & Xu (2002)
van Vreden & Ahmadzabidi (1986)
van Vreden & Ahmadzabidi (1986)
China
India
India (Madhya Pradesh)
Vietnam
China
India
India (Madhya Pradesh)
Japan
Vietnam
China
China
Japan
NPPS & ZAU (1991)
Randhawa et al. (2006)
Yadav & Pawar (1989)
Lam (1992, 1996, 2000, 2001, 2002)
NPPS & ZAU (1991)
Randhawa et al. (2006)
Yadav & Pawar (1989)
Kitamura & Iwami (1998)
Lam (1992, 1996, 2000, 2001, 2002)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
Kitamura (1982); Yamada & Kawamura (1999);
Yamada & Miyamoto (1998)
Kitamura (1987)
NPPS & ZAU (1991)
Kitamura (1982)
NPPS & ZAU (1991)
Li (1982); NPPS & ZAU (1991)
Recilia dorsalis
Gonatopus sakaii (Esaki & Hashmoto)
Nephotettix cincticeps
Gonatopus schenklingi (Strand)
Nilaparvata lugens
Gonatopus yasumatsui (Olmi)
Haplogonatopus sp. nr. americanus
Perkins
Haplogonatopus apicalis (Perkins)
Chen (1989) indicates H. japonicas
is synonymous with H. apicalis
Nilaparvata lugens
Nilaparvata lugens
Nilaparvata lugens
Sogatella furcifera
Haplogonatopus atratus (Esaki
& Hashimoto)
Laodelphax striatellus
Laodelphax striatellus
Nilaparvata lugens
Nilaparvata lugens
Japan (Shimane)
China
Japan
China
China
Nilaparvata lugens
Sogatella furcifera
Laodelphax striatellus
Nilaparvata lugens
Asia
Asia
Asia
India
Sogatella furcifera
Haplogonatopus japonicus (Esaki
& Hashimoto)
Alternative spellings: H. japonica,
H. japonicas
Chen (1989) and Zhang & Jin (1992)
indicate H. japonicas is synonymous
with H. apicalis
Haplogonatopus oratorius
(Westwood)
Haplogonatopus orientalis (Rohwer)
Sogatella furcifera
Haplogonatopus sp./spp.
154
Nephotettix nigropictus
Sri Lanka
India
Sri Lanka
India
Japan
He & Xu (2002)
He & Xu (2002)
Dupo & Barrion (2009)
Randhawa et al. (2006); Shankar & Baskaran
(1988,1992)
Ôtake et al. (1976)
Randhawa et al. (2006)
Ôtake et al. (1976)
Greathead (1982)
Greathead (1982)
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Annals of Applied Biology 2010 Association of Applied Biologists
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 1 Continued
Parasitoid
Host
Nephotettix virescens
Nilaparvata lugens
Location
References
Korea
Philippines
India
Japan
Korea
Philippines
India
Sri Lanka
China (Taiwan)
Thailand
Asia
Malaysia (Peninsular)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982); Chandra (1980)
Chiu (1979) (citing Rai, personal
communication); Greathead (1982)
Manjunath et al. (1978)
Greathead (1982)
Ooi (1982)
Barrion et al. (1981); Chandra (1980);
Greathead (1982); Peña & Shepard (1986)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Ooi (1982)
Chandra (1980); Greathead (1982); Peña &
Shepard (1986)
Chiu (1979)
van Vreden & Ahmadzabidi (1986)
Chu & Hirashima (1981)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
Kitamura (1989)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
Kitamura (1989)
Yadav & Pawar (1989)
Ooi (1982); van Vreden & Ahmadzabidi (1986)
Chiu (1979)
Lam (1992, 1996, 2000, 2001, 2002)
Yadav & Pawar (1989)
Ooi (1982)
Lam (1992, 1996, 2000, 2001, 2002)
Olmi (1991–92)
Olmi (1991–92)
Olmi (1991–92)
Olmi (1991–92)
Chua et al. (1984); Dayanan & Esteban (1996);
Olmi (1991–92)
Olmi (1991–92)
Olmi (1991–92)
Olmi (1991)–92)
Dupo & Barrion (2009)
van Vreden & Ahmadzabidi (1986)
India (Madhya Pradesh)
India (Madhya Pradesh)
Vietnam
Vietnam
Japan
Philippines
China (Taiwan)
Yadav & Pawar (1989)
Yadav & Pawar (1989)
Lam (1992, 1996, 2000, 2001, 2002)
Lam (1992, 1996, 2000, 2001, 2002)
Greathead (1982)
Greathead (1982)
Greathead (1982)
India (Mandya, Karnataka)
Japan, Korea
Malaysia
Philippines
Sogatella furcifera
Monogonatopus orientalis (Rohwer)
Monogonatopus sp.
Neogonatopus sp.
Paragonatopus fulgori (Nakagawa)
Nilaparvata lugens
Nilaparvata lugens
Nephotettix cincticeps
Nephotettix virescens
Laodelphax striatellus
Nilaparvata lugens
Sogatella furcifera
Pseudogonatopus hospes (Perkins)
Nilaparvata lugens
Sogatella furcifera
Pseudogonatopus nudus (Perkins)
Pseudogonatopus otaki (Olmi)
Pseudogonatopus ponomarenkoi
Moczar
Pseudogonatopus nr. pusanus (Olmi)
Pseudogonatopus sarawaki (Moczar)
Pseudogonatopus sp./ spp.
Nilaparvata lugens
Sogatella furcifera
Nilaparvata lugens
Sogatella furcifera
Nilaparvata lugens
Sogatella furcifera
Nilaparvata lugens
Sogatella furcifera
Nephotettix cincticeps
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
India
Japan
Korea
Malaysia
Philippines
Sri Lanka
Malaysia (Peninsular)
China (Taiwan)
China (Guangxi)
China (Guangxi)
China
Japan
China
China
Japan
India
Malaysia
Thailand
Vietnam
India (Madhya Pradesh)
Malaysia
Vietnam
China
India
Indonesia
Malaysia
Philippines
155
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 1 Continued
Parasitoid
Host
Location
References
Nephotettix nigropictus
Japan
Philippines
China (Taiwan)
Japan
Philippines
China (Taiwan)
Japan
Philippines
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Chandra (1980); Greathead (1982); Peña
& Shepard (1986)
Chu & Hirashima (1981); Greathead (1982)
Chandra (1980); Greathead (1982)
Chandra (1980); Greathead (1982); Peña
& Shepard (1986)
Greathead (1982
Chandra (1980); Greathead (1982)
Chandra (1980); Greathead (1982); Peña
& Shepard (1986
Greathead (1982
Nephotettix virescens
Nilaparvata lugens
Sogatella furcifera
China (Taiwan)
Japan
Philippines
Sogatella furcifera
China (Taiwan)
Japan
Philippines
China (Taiwan)
Vietnam (Table 2). Major hosts are S. furcifera, N. lugens,
Nephotettix cincticeps (Uhler), Nephotettix nigropictus and
N. virescens (Distant) (Greathead, 1982). Chandra (1980)
describes the behaviour of the gravid Anagrus spp.
females. On landing upon a plant the wasp walks rapidly
over the substrate, drumming on the surface with the
antennae. Drumming intensifies when a host egg mass
is located. Oviposition occurs by the wasp first drilling
through the leaf epidermis. The drumming appears to
be involved in locating the eggs and locating a suitable
position to drill. Failure rate is high; 95% attempts fail to
penetrate and, of those that do, 89% do not successfully
oviposit in an egg. When parasitoid density is high, one
to three eggs are laid but only one will develop. Parasitism is readily detected through the transparent chorion
of the host egg when the parasitoid larva is at least half
grown.
Most species of egg parasitoids attacking delphacid
planthopper pests of rice are mymarids (Dupo &
Barrion, 2009). Mymarid egg parasitoids quickly migrate
into crops from alternative hosts in other habitats,
rapidly establish and cause pest mortality; consequently
they are considered important biological control agents
(Chandra, 1980).
The most important genus in this family is Anagrus.
Anagrus sp. nr flaveolus Waterhouse has been reported
to be the dominant parasitoid of L. striatellus in Japan
(Ôtake, 1970a). This species did not show a preference
between N. lugens, S. furcifera and L. striatellus (Ôtake,
1977). Parasitism rates of up to 95% have been reported
for A. sp. nr flaveolus in L. striatellus (Hachiya, 1995).
Published parasitism rates for mymarids and other egg
156
parasitoids are more reliable and comparable across
studies than those for parasitoids such as dryinids that
attack other life stages. This is because a standard
method based on bait plants has been developed,
promoted by IRRI and widely used. Bait plants are
prepared by introducing three to five gravid female
planthoppers of the species of interest (most commonly
N. lugens) to a 30-day-old rice plant for 24 h. Plants
bearing host eggs are then placed in the field for 72 h
before recovery to the laboratory. There, a piece of
the leaf sheath containing an egg mass is placed in
a closed Petri dish lined with paper towel moistened
with antifungal solution. Numbers of host nymphs and
adult parasitoids that emerge are counted and parasitism
calculated by dividing numbers of the latter by the
total number of insects (Reissig et al., 1986). Prior to
the widespread use of this standard method, Chandra
(1980) obtained adult egg parasitoids by dissecting fieldcollected rice leafsheaths containing host eggs and reared
the parasitised eggs on a moist filter paper in Petri
dish. The standard method is less labour intensive than
direct observation and dissection of hosts but caution
needs to be exercised when dealing with samples that
contain polyembryonic parasitoids (e.g. Trichogramma)
and facultative hyperparasitoids.
The parasitoid complex of Vietnamese rice includes
the mymarid genera Anagrus and Gonatocerus and can
give parasitism rates in range of 21.2–47.8% (Lam
et al., 2002). Higher rates of parasitism, up to 72.5%,
have been reported for Anagrus spp. in S. furcifera in
Vietnam (Tao Ngoan, 1970). Anagrus is also considered
the dominant parasitoid genus on N. lugens and S. furcifera
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 2 Mymaridae parasitoids reported from Hemiptera pests of Asian rice
Parasitoid
Host
Location
References
Acmopolynema spp.
Tagosodes pusanus
Toya propinqua (Distant)
Laodelphax striatellus
Asia
Asia
China (Fujian)
Japan
China (Taiwan)
China
China (Fujian)
India
Japan
Anagrus sp. nr flaveolus
Waterhouse
Sogatella longifurcifera
(Esaki & Ishihara)
Sogatella panicicola (Ishihara)
Terthron albovittatum (Matsumura)
Zuleica nipponica (Matsumura
& Ishihara)
Laodelphax striatellus
Nilaparvata lugens
Japan
Dupo & Barrion (2009)
Dupo & Barrion (2009)
Lo & Zhuo (1980)
Hachiya (1995); Ôtake (1970a); 1977
Chu & Hirashima (1981)
Yu (1996); Yu et al. (1998)
Lo & Zhuo (1980)
Singh et al. (1993)
Chiu (1979) (citing Ôtake 1970a, b, 1976a, b;
Yasumatsu & Watanabe, 1965); Ôtake (1977)
Barrion et al. (1981)
Fowler et al. (1991)
Chu & Hirashima (1981)
Lam (1992, 1996, 2000, 2001, 2002)
Yu (1996); Yu et al. (1998)
Lo & Zhuo (1980)
Nalini (2005); Randhawa et al. (2006)
Ôtake (1977)
Watanabe et al. (1992)
Lam (1992, 1996, 2000, 2001, 2002)
Yu (1996); Yu et al. (1998)
Yu (1996)
Randhawa et al. (2006)
Watanabe et al. (1992)
Triapitsyn & Beardsley (2000)
Chantarasa-ard et al. (1984a)
Chantarasa-ard et al. (1984a)
Chantarasa-ard et al. (1984a)
Chantarasa-ard et al. (1984a)
Chantarasa-ard et al. (1984a)
Chen & Yu (1989)
Chiappini & Lin (1998)
Chantarasa-ard (1984); Chantarasa-ard et al.
(1984a); Chen & Yu (1989)
Chen & Yu (1989)
Chen & Yu (1989)
Chantarasa-ard et al. (1984a)
Chantarasa-ard (1984); Chantarasa-ard et al.
(1984a;1984b)
Chantarasa-ard et al. (1984a)
Japan
Japan
Japan
Chantarasa-ard et al. (1984a)
Chantarasa-ard et al. (1984a)
Chantarasa-ard et al. (1984a)
China
China
Sogatella furcifera
China
Laodelphax striatellus
China
Nilaparvata bakeri
China
Luo & Zhuo (1980); NPPS & ZAU (1991)
Luo & Zhuo (1980); NPPS & ZAU (1991)
Mao et al. (1999); Mao et al. (2002b);
NPPS & ZAU (1991)
Lo & Zhuo (1980); Luo & Zhuo (1980);
NPPS & ZAU (1991)
Chiappini & Lin (1998); Luo & Zhuo (1980);
Mao et al. (2002a); NPPS & ZAU (1991)
Chiappini & Lin (1998); Li & He (1991);
NPPS & ZAU (1991)
Nephotettix cincticeps
Nilaparvata lugens
Sogatella furcifera
Anagrus frequens (Perkins)
Synonyms: Anagrus armatus,
A. cicadulinae, A. toyae
Anagrus incarnatus (Haliday)
Tagosodes pusanus
Toya spp.
Sogatella furcifera
Perkinsella sp.
Harmalia albicolli (Motschulsky)
Laodelphax striatellus
Macrosteles orientalis (Vilbaste)
Nephotettix cincticeps
Nilaparvata bakeri (Muir)
Nilaparvata lugens
Nilaparvata muiri (Caldwell)
Sogatella furcifera
Anagrus longitubulosus
(Pang & Wang)
Anagrus nilaparvatae
(Pang & Wang)
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
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Philippines
Sri Lanka
China (Taiwan)
Vietnam
China
China (Fujian)
India
Japan
Malaysia
Vietnam
China
China
India
Malaysia
China (Taiwan)
Japan
Japan
Japan
Japan
Japan
Bangladesh
China
Japan
Korea
China (Taiwan)
Japan
Japan
157
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 2 Continued
Parasitoid
Anagrus optabilis (Perkins)
Mao et al. (2002a) indicate
A. paranilaparvatae is a pseudonym
of A. optabilis Triapitsyn, 2001
proposes the synonymy of
A. paranilaparvatae under
A. optabilis
Synonyms: Paranagrus optabilis
Perkins, Paranagrus osborni Fullway,
Anagrus panicicola Sahad (Triapitsyn
& Beardsley, 2000)
Host
Location
References
Nilaparvata lugens
China
Nilaparvata muiri
Sogatella furcifera
India
China
China
Chiappini & Lin (1998); Li & He (1991); Luo &
Zhuo (1980); Lou et al. (2005a); Mao et al.
(1999); Mao et al. (2002a); NPPS & ZAU
(1991); Xiang et al. (2008); Zheng et al.
(2003b)
Randhawa et al. (2006)
Chiappini & Lin (1998)
Chiappini & Lin (1998); Li & He (1991);
Luo & Zhuo (1980); (Mao et al. 2002a);
NPPS & ZAU (1991); Zheng et al. (2003b)
Randhawa et al. (2006)
Li & He (1991)
Sogatella panicicola
(Synonymous with S. vibix)
Toya propinqua
Toya tuberculosa (Distant)
Laodelphax striatellus
Nephotettix spp.
Nilaparvata lugens
India
China (Guangdong)
China (Guangdong)
China (Guangdong)
Japan
China (Taiwan)
Thailand
China
India
Japan
Malaysia
Sri Lanka
China (Taiwan)
Thailand
Sogatella furcifera
Anagrus paranilaparvatae
(Pang & Wang)
Tagosodes pusanus
Toya propinqua
Toya spp.
Hirozuunka japonica
(Matsumura & Ishihara)
Laodelphax striatellus
Megamelus proserpina
(Kirkaldy)
Nephotettix virescens
Nilaparvata lugens
Sogatella furcifera
158
Vietnam
China
Japan
Malaysia
China (Taiwan)
Thailand
Vietnam
China
China (Guangdong)
China
Japan
China
Li & He (1991
Li & He (1991)
Baquero & Jordana (1999) (citing Sahad &
Hirashima (1984); Sahad (1984)
Miura et al. (1981)
Wongsiri et al. (1980)
Chiappini & Lin (1998); Yu et al. (1996);
Zheng et al. (1999, 2003b)
CAB International (2005); Shankar &
Baskaran, (1988, 1992)
Baquero & Jordana (1999) (citing Sahad
& Hirashima 1984); Sahad (1984)
Ooi (1982); van Vreden & Ahmadzabidi
(1986); Watanabe et al. (1992)
CAB International (2005); Fowler et al. (1991)
Miura et al. (1981)
Chiu (1979) (citing Yasumatsu et al., 1975;
Nishida et al., 1976); Hirashima et al.
(1979); Wongsiri et al. (1980)
Lam (1992, 1996, 2000, 2001, 2002)
Miura et al. (1981); Yu et al. (1996)
Sahad (1984)
Ooi (1982)
Miura et al. (1979)
Hirashima et al. (1979); Miura et al. (1979)
Lam (1992, 1996, 2000, 2001, 2002)
Yu (1996); Yu et al. (1998)
Li & He (1991)
Yu (1996); Yu et al. (1998)
Triapitsyn & Beardsley (2000)
Lo & Zhuo (1980); Luo & Zhuo (1980);
NPPS & ZAU (1991)
Triapitsyn & Beardsley (2000)
Philippines
Philippines
China
India
India (Andhra Pradesh)
Malaysia (Peninsular)
China
Triapitsyn & Beardsley (2000)
Li & He (1991); Lo & Zhuo (1980); Luo & Zhuo
(1980); Mao et al. (1999, 2002a); NPPS &
ZAU (1991)
Randhawa et al. (2006)
CAB International (2005)
Watanabe et al. (1992);
Chiappini & Lin (1998); Lo & Zhuo (1980);
Luo & Zhuo (1980); NPPS & ZAU (1991)
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 2 Continued
Parasitoid
Anagrus shortitubulosus
Pang & Wang
Anagrus spp.
Host
Laodelphax striatellus
Nilaparvata lugens
Sogatella furcifera
Laodelphax striatellus
Nephotettix cincticeps
Nephotettix nigropictus
Nephotettix virescens
Nilaparvata lugens
Sogatella furcifera
Anaphes spp
Nephotettix cincticeps
Nilaparvata lugens
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
Location
References
India
Philippines
China
China
China
China
Japan
Korea
Malaysia
Philippines
Sri Lanka
China (Taiwan)
Thailand
Vietnam
Japan
Korea
Malaysia
Philippines
Sri Lanka
China (Taiwan)
Thailand
Vietnam
Japan
Korea
Malaysia
Philippines
Sri Lanka
China (Taiwan)
Thailand
Vietnam
China
India
Indonesia
Japan
Korea
Malaysia
Philippines
Randhawa et al. (2006)
Triapitsyn & Beardsley (2000)
Luo & Zhuo (1980); NPPS & ZAU (1991)
Luo & Zhuo (1980); NPPS & ZAU (1991)
Luo & Zhuo (1980); NPPS & ZAU (1991)
Luo et al. (1981); Luo & Zhuo (1983)
Greathead (1982)
Greathead (1982)
Greathead (1982
Greathead (1982)
Greathead (1982)
Chu & Hirashima (1981); Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Chandra (1980); Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Luo et al. (1981); Luo & Zhuo (1983); Mao et al. (1999)
Gupta & Pawar (1989)
Claridge et al. (1999)
Greathead (1982)
Greathead (1982)
Greathead (1982); Ooi (1982)
Barrion et al. (1981); Chandra (1980);
Greathead (1982)
Greathead (1982)
Chu & Hirashima (1981); Chui (1979); Greathead (1982)
Greathead (1982); Vungsilabutr (1981)
Greathead (1982)
Luo et al. (1981); Luo & Zhuo (1983); Luo & Zhuo (1986);
Zhang (1991)
Greathead (1982)
Greathead (1982)
Greathead (1982); Ooi (1982)
Chandra (1980); Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982); Vungsilabutr (1981)
Greathead (1982); Tao & Ngoan (1970)
Chu & Hirashima (1981)
Chu & Hirashima (1981)
Fowler et al. (1991)
Chu & Hirashima (1981)
Lam (1992, 1996, 2000, 2001, 2002)
Sri Lanka
China (Taiwan)
Thailand
Vietnam
China (Fujian)
Japan
Korea
Malaysia
Philippines
Sri Lanka
China (Taiwan)
Thailand
Vietnam
China (Taiwan)
China (Taiwan)
Sri Lanka
China (Taiwan)
Vietnam
159
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 2 Continued
Parasitoid
Emoemas sp.
Gonatocerus longicrus (Kieffer)
Gonatocerus sp.
Host
Location
References
Sogatella furcifera
China
China (Fujian)
India
Japan
Malaysia
Vietnam
China
China
China (Guangxi)
China
China
Korea, Philippines
China (Taiwan)
Thailand
Korea, Philippines, Taiwan
Thailand
Korea
Philippines
China (Taiwan)
Thailand
China (Guangxi)
Korea
Yu (1996); Yu et al. (1998)
Lo & Zhuo (1980)
Nalini (2005); Randhawa et al. (2006)
Ôtake (1977)
Watanabe et al. (1992)
Lam (1992, 1996, 2000, 2001, 2002)
Yu (1996); Yu et al. (1998)
Yu (1996)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
Greathead (1982)
Chu & Hirashima (1981); Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982); Vungsilabutr (1981)
Greathead (1982)
Chandra (1980); Greathead (1982)
Greathead (1982)
Greathead (1982); Vungsilabutr (1981)
NPPS & ZAU (1991)
Ôtake (1977) (citing Yasumatsu, personal
communication)
van Vreden & Ahmadzabidi (1986)
Chu & Hirashima (1981)
Wongsiri et al. (1980); Chiu (1979) (citing,
Yasumatsu et al.,1975)
Lam (1992, 1996, 2000, 2001, 2002)
Lam (1992, 1996, 2000, 2001, 2002)
Lo & Zhou (1980)
Chu & Hirashima (1981)
Chiu (1979) (citing Lin 1974)
Chiu (1979) (citing, Yasumatsu et al.,1975)
van Vreden & Ahmadzabidi (1986)
Barrion et al. (1981); Chandra (1980)
NPPS & ZAU (1991)
Chiu (1979) (citing Yasumatsu et al., 1975);
Wongsiri et al. (1980); NPPS & ZAU (1991)
Lam (1992, 1996, 2000, 2001, 2002)
Wongsiri et al.(1980)
Lam (1992, 1996, 2000, 2001, 2002)
NPPS & ZAU, (1991)
Barrion et al. (1981)
NPPS & ZAU (1991)
Tagosodes pusanus
Toya spp.
Nilaparvata lugens
Laodelphax striatellus
Nephotettix cincticeps
Nephotettix cincticeps
Nephotettix nigropictus
Nephotettix virescens
Nilaparvata lugens
Malaysia (Peninsular)
China (Taiwan)
Thailand
Lymaenon sp.
Mymar indica (Mani)
Sogatella furcifera
Planthoppers
Nephotettix cincticeps
Nilaparvata lugens
Mymar taprobanicum (Ward)
Nilaparvata lugens
Sogatella furcifera
Polynema sp.
Ooctonus sp.
Nephotettix cincticeps
Nilaparvata lugens
Nilaparvata lugens
in the central plain of Thailand (Vungsilabutr, 1981).
In Malaysia a parasitism rate of 47% was reported in
S. furcifera (Watanabe et al., 1992).
Mymarid parasitoids tend to be favoured by moderate
temperatures. For example, Anagrus nilaparvatae (Pang
& Wang) has an optimum temperature of 27◦ C and
both fecundity and survival of immature stages is greatly
reduced at high temperatures (Chiappini & Lin, 1998).
Reflecting this general tendency, parasitism rates in Japan
by Anagrus sp. nr flaveolus are greatest in May and June
160
Vietnam
Vietnam
China (Fujian)
China (Taiwan)
China (Taiwan)
Thailand
Malaysia (Peninsular)
Philippines
China (Taiwan)
Thailand
Vietnam
Thailand
Vietnam
China (Taiwan)
Philippines
China (Guangxi)
(11.3–29.6%) and September–November (3.3–38.1%)
(Chiu, 1979). The low threshold temperature for
development of female Anagrus longitubulosus (Pang
& Wang) was found to be 11.7◦ C and 11.3◦ C for
A. nilaparvatae (Li & He, 1991).
Anagrus nr. flaveolus has a strong tendency to disperse
and this is important for its ability to overwintering
in habitat other than paddy fields where it may
use both delphacid and non-delphacid hosts (Ôtake,
1977). Anagrus flaveolus, the dominant parasitoid in
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
G.M. Gurr et al.
China, favours Tagosodes pusanus (Distant) when in
grassy, non-rice habitat (Yu et al., 1998). Similarly,
Anagrus incarnatus (Haliday) is capable of overwintering
in eggs of Nilaparvata muiri (Caldwell) (Chantarasaard, 1984). Furthermore, A. incarnatus exhibits a wide
host range including Nilaparvata bakeri (Muir), Harmalia
albicollis (Motchulsky), Sogatella longifurcifera (Esaki &
Ishihara), Sogatella panicicola (Ishihara), Terthron albovittata
(Matsumura), Zuleica nipponica (Matsumura & Ishihara),
N. cincticeps (Uhler) and Macrosteles orientalis (Vilbaste)
(Chantarasa-ard et al., 1984a). Non-crop vegetation in
which these host insects overwinter is, therefore,
important habitat for Mymaridae that immigrate into rice
crops early in the growing season. During the winter these
potentially important biological control agents can use the
alternative hosts in these habitats, either reproducing (in
warmer tropical areas) or developing within the host (in
areas with a cool winter).
Considerable information is available on the role of
non-crop vegetation on mymarids in rice production
systems of Asia, particularly from Chinese language
journals. A. nilaparvatae is known to use several grassy
plants during the winter in Guangdong Province,
southern China (Li & He, 1991), particularly Leersia
hexandra (Swartz), Scirpus juncoides (Roxb.), Paspalum
orbiculare (G. Forst.). The final, 14th, generation of
Anagrus paranilaparvatae (Pang & Wang) in Fujian
Province of China, used grassy habitats as overwintering
sites when rice crops were seasonally absent (Lo &
Zhou, 1980).
Anagrus nr. flaveolus is known to develop in eggs
of planthoppers living on weeds around the rice field
during winter (Lo & Zhuo, 1980). Two of the 20
generations occurring in Fujian Province China take
place in this non-crop habitat. Hosts used outside of
rice crops are Toya propinqua (Muir) and T. tuberculosa
(Distant) on Panicum repens (L.); Kakuna sapporonis
(Matsumura) on Paspalum distichum (L.); S. panicicola
on Echinochloa crusgalli (L.) P. Beauv.; N. bakeri on
L. hexandra. In the case of A. longitubulosus, another
species that overwinters in grassy areas, parasitoids
were associated with the grasses E. crusgalli, P. orbiculare,
Adiantum capillus-veneris (L.) (Li & He, 1991). Importantly,
that work demonstrated that wasps emerging from eggs
of a mixed community of planthopper species on weeds
are smaller than those from the eggs of S. furcifera in
rice. Taken in isolation, this finding suggests that the
extent to which mymarids are readily able to ‘switch’
from non-crop habitats to parasitising major delphacid
pests in rice crops is questionable. Indeed, later work by
Yu et al. (1996) showed that the reproductive success of
female parasitoids emerging from bait plants carrying
N. lugens eggs is indeed significantly lower for wasps
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
Parasitoids of Asian rice planthoppers
recovered from weedy areas than from rice or corn
fields: 2.0, 9.6 and 12.6 offspring per female, respectively.
Importantly, however, for the second generation of wasps
the performance recovered; such that there were no
significant differences between females, all producing
between 8 and 11 progeny. This phenomenon was not
an artefact of using bait plants using N. lugens eggs
for a similar effect was apparent when using eggs of
T. pusanus. Thus ‘switching’ from alternative hosts in nonrice habitats to attacking delphacid pests in rice seems to
be accomplished with a partial reduction in performance
that is short in the context of a species with approximately
20 generations per year.
The sex ratio, body size and parasitoid growth rate
of Anagrus optabilis (Perkins) in Chinese rice fields and
adjacent habitats were found to be influenced by host
species, host plants and the surrounding habitat (Yu et al.,
1996). Grass species that were found to be important
for mymarids were Digitaria ciliaris (Retz.), Brachiaria distachya (L.) and Cynodon dactylon (L.) Pers. These habitats
supported A. sp. nr flaveolus, A. optabilis as well as the
trichogrammatids Oligosita naias (Girault) and Oligosita
aesopi (Girault). In these grassy habitats, A. nr. flaveolus
commonly parasitised T. pusanus. More recent Chinese
work on the use of alternative hosts in non-crop habitats
showed that Anagrus spp. used the hosts Saccharosydne
procerus (Matsumura), L. striatellus (Fallén), T. propinqua,
T. tuberculosa, S. panicicola, N. bakeri, T. albovittatum, Delphacodes graminicola (Matsumura), S. furcifera and N. lugens
(Zheng et al., 2003a). The non-rice plants used included
the grasses E. crusgalli, L. hexandra, P. repens, C. dactylon,
P. distichum, Digitaria spp. and L. chinensis.
More concrete evidence for the importance of non-rice
habitats as a source for parasitoids that can exert control
of rice pests comes from studies of the vegetable crop
Zizania caduciflora (Turcz.). This crop supports S. procerus,
a delphacid that is unable to develop on rice so considered
a non-pest species (Yu, 2001). However, this insect
supports the parasitoid A. optabilis which is also an
important parasitoid of N. lugens (Zheng et al., 1999).
There is, however, evidence of an adaptation process.
After rearing two generations on N. lugens, A. optabilis
preferred to parasitise the eggs of N. lugens over the nonpest S. procerus. When these parasitoids are presented
with S. procerus, numbers of progeny were lower than
those that remained on N. lugens (Zheng et al., 2003a).
Other than providing alternative hosts, non-crop
habitats may also offer nectar and this resource is utilised
by A. flaveolus (Yu et al., 1996). Laboratory studies on
A. nilaparvatae showed that longevity was extended by
feeding with honey, corn pollen, soybean flowers and the
honeydew of N. lugens and Toya spp. Of greater relevance
to biological control, egg production by this parasitoid on
161
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
N. lugens was significantly increased when fed with those
nutrient-rich diets except the honeydew excreted by Toya
sp. (Zheng et al., 2003b).
Family: Encyrtidae
The encyrtids Chrysopophagus australiae (Perkins) and
Echthrogonatopus exitiosus (Perkins) have been reported
from N. lugens in the Solomon Islands (Chiu, 1979) but
appear to be relatively unimportant parasitoids of rice
pests in Asia (Table 3). Cheiloneurus exitiosus (Perkins)
has been recorded as a hyperparasitoid of Gonatopus
sp., Haplogonatopus sp., Pseudogonatopus hospes (Perkins),
P. flavifemur on N. lugens and S. furcifera (Guerrieri &
Viggiani, 2005) whilst Cheiloneurus sp. has been recorded
as a hyperparasitoid of dryinids on N. lugens in Vietnam
(Lam, 1992, 1996, 2000, 2002).
Family: Eulophidae
Two genera of eulophids, Ootetrastichus and Tetrastichus
have been reported from delphacid hosts in the
Philippines, Vietnam, Malaysia and Thailand (Table 3).
Overall, however, the limited published information
suggests that this family is relatively unimportant in
terms of biological control of delphacids in Asian rice
systems.
Family: Pteromalidae
Only one pteromalid, Panstenon sp., has been reported
from rice planthoppers from Sri Lanka (Fowler et al.,
1991) and Fujian Province, China (Lo & Zhou, 1980).
Family: Scelionidae
Scelionidae (Superfamily: Scelionoidea) is the only
hymenopteran parasitoid family outside of the Superfamily Chalcidoidea to feature amongst the parasitoids
reported attacking delphacid pests of rice in Asia. It
appears to be a relatively unimportant family, represented by three genera from N. lugens in India (Table 3).
These include a species of Baeus, a genus generally considered to be spider parasitoids but Manjunath et al. (1978)
reports attack of N. lugens. The lack of verification by later
workers may reflect a misidentification or simply a dearth
of research in this region.
Family: Trichogrammatidae
This family of egg parasitoids has four genera that attack
delphacid pests of rice: Aphelinoidea, Oligosita, Paracentrobia
and Trichogramma (Table 3). Drumming the surface of the
162
rice leaves and oviposition occurs in a similar manner
to Anagrus spp. (Chandra, 1980). Unlike mymarids,
however, Trichogrammatidae parasitoids cause the host
egg to become dark grey in colour obscuring the view
of the developing parasitoid. Dissecting the host eggs is
not a good method of determining parasitisation because
larvae and pupae of the wasp are very delicate and easily
destroyed. Larvae within the eggs are difficult to observe
as they are immobile. Adults emerge 11–12 days after
oviposition; males tend to emerge first.
Parasitism rates reported for members of this family
range from 5% and above for Oligosita aesopi (Girault) on
S. furcifera to 68% in the case of Oligosita naias (Girault)
in Malaysia (Watanabe et al., 1992). Oligosita aesopi is
a common parasitoid in Vietnam (Lam, 1992, 1996,
2000, 2002). Oligosita naias is considered an important
egg parasitoid of delphacids in Chinese rice (Yu, 1996).
In Sri Lanka, Oligosita spp. are more abundant than
Anagrus spp. on N. lugens, with parasitism rates up to
32.7% (Fowler et al., 1991). In India, Gupta and Pawar
(1989) reported Oligosita sp./spp. along with Anagrus sp.,
to be the most common parasitoids of N. lugens. Greathead
(1982) reported Oligosita sp./spp. from India, Korea,
Malaysia, Philippines, Sri Lanka, Thailand and China
on N. lugens, S. furcifera, N. cincticeps, N. nigropictus and
N. virescens.
Like Mymaridae, trichogrammatids feed on sugars
(Gurr & Nicol, 2000) and the nature of non-crop habitat
close to rice where nectar may be available is considered
important in population dynamics (Yu et al., 1996).
Non-crop habitat dominated by grasses close to paddy
fields may also act as a reservoir of parasitoids of rice
planthoppers (Yu, 1996). The limited number of studies
available on Trichogrammatidae that attack delphacid
pests of rice shows that this is a relatively poorly studied
area.
Order: Strepsiptera
Although represented by few taxa (Table 4), parasitism
rates (see below) suggest that this group of nymphaladult parasitoids is important in control of delphacid
pests in Asian rice production systems. They reproduce
viviparously, individual females producing 1000–2000
triungulins. These are 0.15 mm long, light yellow, slightly
curved, with well developed eyes, legs and caudal setae
allowing them to crawl and jump. In the laboratory,
most die within an hour. They enter hosts by piercing
intersegmental membranes then shrink and transform
into cylindrical legless larvae that develop over seven
instars. Males pupate with their anterior end protruding
from the host’s abdomen whilst the female pupates within
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 3 Encyrtidae, Eulophidae, Pteromalidae, Scelionidae and Trichogrammatidae parasitoids reported from Hemiptera pests of Asian rice
Parasitoid
Host
Location
References
Nilaparvata lugens
Nilaparvata lugens
Nilaparvata lugens
Vietnam
Solomon Islands
Solomon Islands
Lam (1992, 1996, 2000, 2001, 2002)
Chiu (1979)
Chiu (1979)
Nilaparvata lugens
Philippines
Vietnam
Vietnam
Malaysia (Peninsular)
Thailand
Barrion et al. (1981)
Lam (1992, 1996, 2000, 2001, 2002)
Lam (1992, 1996, 2000, 2001, 2002)
van Vreden & Ahmadzabidi (1986)
Wongsiri et al. (1980)
Nilaparvata lugens
Planthoppers
Sri Lanka
China (Fujian)
Fowler et al. (1991)
Lo & Zhou (1980)
Nilaparvata lugens
Nilaparvata lugens
Nilaparvata lugens
India
India
India
Manjunath et al. (1978)
Manjunath et al. (1978)
Manjunath et al. (1978)
Aphelinoidea sp.
Nilaparvata lugens
China (Taiwan)
Oligosita aesopi (Girault)
Nilaparvata lugens
China
Vietnam
China
Malaysia
Vietnam
China
China
China
India (Tamil Nadu)
Malaysia (Muda)
China
India
China
China
China
China
Indonesia
China (Taiwan)
China
China
China (Guangdong)
China (Taiwan)
China
India (Andhra Pradesh)
India (Andhra Pradesh)
Indonesia
Malaysia (Peninsular)
Thailand
Thailand
India
Korea
Malaysia
Chiu (1979) (citing Fukuda 1934);
Chu & Hirashima (1981)
Yu et al. (1996); Yu et al. (1998)
Lam (1992, 1996, 2000, 2001, 2002)
Yu et al. (1996)
Watanabe et al. (1992)
Lam (1992, 1996, 2000, 2001, 2002)
Yu (1996); Yu et al. (1998)
Yu (1996); Yu et al. (1998)
Yu et al. (1996); Yu et al. (1998)
CAB International (2005)
Watanabe et al. (1992)
Yu et al. (1996)
Randhawa et al. (2006)
Yu (1996); Yu et al. (1998)
Yu (1996); Yu et al. (1998)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Mao et al. (1999); NPPS & ZAU (1991)
Claridge et al. (1999)
Chu & Hirashima (1981)
NPPS & ZAU (1991)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Chu & Hirashima (1981); Mao et al. (1999)
Chu & Hirashima (1981); Mao et al. (1999)
NPPS & ZAU (1991)
CAB International (2005)
CAB International (2005)
Claridge et al. (1999)
van Vreden & Ahmadzabidi (1986)
Wongsiri et al. (1980)
Wongsiri et al. (1980)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Family: Encyrtidae
Cheiloneurus sp.
Chrysopophagus australiae (Perkins)
Echthrogonatopus exitiosus (Perkins)
Family: Eulophidae
Ootetrastichus nr. formosanus
(Timberlake)
Tetrastichus formosanus (Timberlake)
Sogatella furcifera
Nilaparvata lugens
Family: Pteromalidae
Panstenon sp
Family: Scelionidae
Baeus sp.
Gryon sp.
Oxyscella sp.
Family: Trichogrammatidae
Sogatella furcifera
Oligosita naias (Girault)
Tagosodes pusanus
Toya spp.,
Nilaparvata lugens
Sogatella furcifera
Oligosita nephotetticum (Mani)
Oligosita shibuyae (Ishii)
Oligosita tachikawai (Yashiro)
Oligosita yasumatsui (Viggiani
& Subba Rao)
Oligosita sp./spp.
Tagosodes pusanus
Toya spp.
Nephotettix cincticeps
Nilaparvata lugens
Laodelphax striatellus
Nephotettix cincticeps
Nilaparvata lugens
Sogatella furcifera
Nilaparvata lugens
Nilaparvata lugens
Sogatella furcifera
Nephotettix cincticeps
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
163
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 3 Continued
Parasitoid
Host
Nephotettix nigropicta
Nephotettix virescens
Nilaparvata lugens
Location
References
Philippines
Sri Lanka
China (Taiwan)
Thailand
India
Korea
Malaysia
Philippines
Sri Lanka
China (Taiwan)
Thailand
India
Korea
Malaysia
Philippines
Sri Lanka
China (Taiwan)
Thailand
India
Greathead (1982)
Greathead (1982)
Chu & Hirashima (1981); Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982); Gupta & Pawar (1989);
Manjunath et al. (1978)
Claridge et al. (1999)
Greathead (1982)
Greathead (1982); Ooi (1982); van Vreden &
Ahmadzabidi (1986)
Barrion et al. (1981); Greathead (1982)
Fowler et al. (1991); Greathead (1982)
Chiu (1979) citing Lin (1974); Chu & Hirashima
(1981); Greathead (1982)
Chiu (1979) (citing Yasumatsu et al., 1975);
Greathead (1982); Vungsilabutr (1981)
Greathead (1982)
Ooi (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982)
Greathead (1982); Vungsilabutr (1981)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Chu & Hirashima (1981)
Chu & Hirashima (1981)
Mao et al. (1999)
Chiu (1979) (citing Suenaga 1963; Lin, 1974)
Chiu (1979) (citing Suenaga, 1963; Lin, 1974);
Chu & Hirashima (1981); Miura et al. (1979)
Lo & Zhou (1980)
Van vreden & Ahmadzabidi (1986)
Chiu (1979) (citing Yasumatsu et al., 1975)
Van Vreden & Ahmadzabidi (1986)
Chiu (1979) (citing Yasumatsu et al. (1975);
Wongsiri et al. (1980)
Barrion et al. (1981)
Barrion et al. (1981)
Indonesia
Korea
Malaysia
Philippines
Sri Lanka
China (Taiwan)
Thailand
Sogatella furcifera
Paracentrobia andoi (Ishii)
Paracentrobia garuda (Subba Rao)
Nephotettix cincticeps
Nephotettix nigropicta
Nephotettix virescens
Nilaparvata lugens
Planthoppers
Nilaparvata lugens
Paracentrobia yasumatsui
(Subba Rao)
Nilaparvata lugens
Stephanodes sp.
Nilaparvata lugens
the host. Adult males emerge from the host and mate with
adult females via the exposed cephalothorax.
Parasitised hosts have smaller genitalia and are
identifiable by an extended abdomen and discoloured
164
India, Korea
Malaysia
Philippines
Sri Lanka
China (Taiwan)
Thailand
China
China (Taiwan)
China (Taiwan)
China (Guangdong)
Japan
China (Taiwan)
China (Fujian)
Malaysia (Peninsular
Thailand
Malaysia (Peninsular)
Thailand
Philippines
China (Taiwan)
bodies as well as having the male parasitoid extruding
from their abdomina or the female’s cephalothorax
visible. Host insects and female Strepsiptera adults die
soon after triungulins have emerged whilst hosts vacated
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
by males are vulnerable to disease via the exit hole
(Chandra, 1980).
Moist conditions tend to favour strepsiptera with
parasitism higher in rainy seasons (although mostly
below 10%) and in wetland areas (Chandra, 1980).
Strepsiptera parasitoids of hemipteran pests in rice
are reported from Japan, India, Philippines, Thailand,
Sarawak, Malaysia and Vietnam (Table 4). Elenchus japonicus (Esaki & Hashimoto) and Elenchus yasumatsui (Kifune
& Hirashima) are reported attacking N. lugens, L. striatellus
and S. furcifera. In Japan, E. japonicus parasitism rate
of delphacids (predominantly S. furcifera) ranged up to
26.7% in August (Kitamura, 1987). A similar maximum parasitism rate, 25%, was reported from the
Philippines (Peña & Shepard, 1986). In Sri Lanka parasitism by an unidentified species of Elenchus peaked
at 40% (Ôtake et al., 1976). In Thailand, E. yasumatsui
is considered important in controlling N. lugens with
parasitism rates up to 90% (Chiu, 1979). In contrast, only low rates of parasitism are reported from
Vietnam (Lam & Thanh, 1989; Lam, 1992, 1996,
2000, 2002).
Order: Diptera
Represented by three genera in the family Pipunculidae
(Table 5), these nymphal/adult parasitoids generally
favour dryer conditions (Chandra, 1980) and this
may partly explain why they are considered to be
ineffective against N. lugens in Asian rice systems
that are predominantly aquatic (Greathead, 1982).
Low rates of parasitism are reported from Taiwan
(Chiu, 1979) and from Vietnam (Lam 1992, 1996,
2000, 2002).
Table 4 Strepsiptera (Family: Elenchidae) parasitoids reported from Hemiptera pests of Asian rice
Parasitoid
Host
Location
References
Elenchus japonicus
(Esaki & Hashimoto)
Alternative spelling: E. japonica
Laodelphax striatellus
China
Japan (Shimane)
China
India
Japan
NPPS & ZAU (1991)
Kitamura (1987)
Li (1982); NPPS & ZAU, (1991)
Randhawa et al. (2006)
CABI (2005); Chiu (1979) (citing Esaki 1932;
Esaki & Hashimoto, 1932; Sakai, 1932;
Okada, 1971; Kuno 1973)
Kitamura (1987)
NPPS & ZAU (1991)
Randhawa et al. (2006)
Kitamura (1987)
Hirashima & Kifune (1978)
Chandra (1980); Dayanan & Esteban (1996);
Peña & Shepard (1986)
Chiu (1979) (citing FAO 1975; Kifune &
Hirashima 1975; Ôtake, 1976; Yasumatsu
et al., 1975); Wongsiri et al. (1980)
Hirashima et al. (1979)
Chandra (1980); Peña & Shepard (1986)
Wongsiri et al. (1980)
Greathead (1982)
Nilaparvata lugens
Sogatella furcifera
Elenchus yasumatsui
(Kifune & Hirashima)
Nilaparvata lugens
Japan (Shimane)
China
India
Japan (Shimane)
Malaysia (Sarawak)
Philippines
Thailand
Sogatella furcifera
Elenchus sp. spp.
Nephotettix virescens
Nilaparvata lugens
Sogatella furcifera
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
Malaysia (Sarawak)
Philippines
Thailand
India, Indonesia, Japan,
Philippines, Sri Lanka, Thailand
India
Indonesia, Japan
Malaysia
Philippines
Sri Lanka
Thailand
Vietnam
India, Indonesia, Japan
Malaysia
Philippines
Sri Lanka
Thailand
Vietnam
Greathead (1982); Shankar & Baskaran (1992)
Greathead (1982)
Ooi (1982)
Greathead (1982)
Chiu (1979); Greathead (1982)
Greathead (1982)
Lam (1992, 1996, 2000, 2002)
Greathead (1982)
Ooi (1982)
Greathead (1982)
Greathead (1982); Ôtake et al. (1976)
Greathead (1982)
Lam (1992, 1996, 2000, 2002)
165
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 5 Diptera (Family: Pipunculidae) parasitoids reported from Hemiptera pests of Asian rice
Parasitoid
Host
Location
References
Dorylas sp.
Dorylomorpha lini Hardy
Pipunculus javanensis
(de Meijere)
Nilaparvata lugens
Nephotettix cincticeps
Nephotettix cincticeps
Sri Lanka
Chiu (1979)
NPPS & ZAU (1991)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Chiu (1979); Chu & Hirashima (1981); NPPS &
ZAU (1991)
Chiu (1979); Chu & Hirashima (1981); NPPS &
ZAU (1991)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Wongsiri et al. (1980)
Lam (1992, 1996, 2000, 2002)
Wongsiri et al. (1980)
Lam 1992, 1996, 2000 (2002)
Randhawa et al. (2006)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Chiu (1979); Chu & Hirashima (1981); NPPS &
ZAU (1991)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Nilaparvata lugens
China (Guangxi)
China (Taiwan)
China (Guangxi)
China (Taiwan)
Pipunculus mutillatus (Loew)
Nephotettix cincticeps
Nephotettix nigropictus
Nephotettix virescens
Pipunculus orientalis (Koizumi)
Nilaparvata lugens
Nephotettix cincticeps
Pipunculus roralis (Kerterz)
Nephotettix cincticeps
Pipunculus javanensis
(de Meijere)
Nephotettix cincticeps
Nilaparvata lugens
Pipunculus mutillatus (Loew)
Nephotettix cincticeps
Nephotettix nigropictus
Nephotettix virescens
Pipunculus orientalis (Koizumi)
Pipunculus roralis (Kerterz)
Pipunculus sp.
Nilaparvata lugens
Nephotettix cincticeps
Nephotettix cincticeps
Nephotettix cincticeps
Nephotettix nigropictus
Nephotettix virescens
Nilaparvata lugens
Tomosvaryella epichalca
(Perkins)
Nephotettix cincticeps
Nilaparvata lugens
Tomosvaryella inazumae
(Koizumi)
Tomosvaryella oryzaetora
(Koizumi)
Recilia dorsalis
(Motschulsky)
Nephotettix cincticeps
Nephotettix nigropictus
Nephotettix virescens
Nilaparvata lugens
Tomosvaryella subvirescens
(Loew)
Nephotettix cincticeps
Nephotettix nigropictus
Nephotettix virescens
166
China (Guangxi, Hunan, Sichun)
China (Taiwan)
Thailand
Vietnam
Thailand
Vietnam
India
China (Anhui)
China (Taiwan)
China (Guangxi)
China (Taiwan)
China (Guangxi, Taiwan)
China (Guangxi, Taiwan)
China (Guangxi, Hunan,
Sichun, Taiwan)
Thailand
Vietnam
Thailand
Vietnam
India
China (Anhui, Taiwan)
China (Guangxi, Taiwan)
Sri Lanka
China (Taiwan)
China (Taiwan)
Sri Lanka
China (Taiwan)
Sri Lanka
China (Taiwan)
China (Guangxi, Yunnan)
Wongsiri et al. (1980)
Lam (1992, 1996, 2000, 2002)
Wongsiri et al. (1980)
Lam (1992, 1996, 2000, 2002)
Randhawa et al. (2006)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
Greathead (1982)
Greathead (1982); Chu & Hirashima (1981)
Chu & Hirashima (1981)
Greathead (1982)
Greathead (1982); Chu & Hirashima, (1981)
Greathead (1982)
Greathead (1982)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Chiu (1979); Chu & Hirashima (1981); NPPS &
ZAU (1991)
NPPS & ZAU (1991)
China
Thailand
Thailand
India
China
China (Fujian, Guangxi)
China (Taiwan)
Thailand
Vietnam
Thailand
Vietnam
Chu & Hirashima (1981); NPPS & ZAU (1991)
Wongsiri et al. (1980)
Wongsiri et al. (1980)
Randhawa et al. (2006)
Chiu (1979); Chu & Hirashima (1981)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Chu & Hirashima (1981); NPPS & ZAU (1991)
Wongsiri et al. (1980)
Lam (1992 1996, 2000, 2002)
Wongsiri et al. (1980)
Lam (1992, 1996, 2000, 2002)
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
Table 5 Continued
Parasitoid
Host
Location
References
Nilaparvata lugens
China (Fujian, Guangxi)
Chu & Hirashima (1981); Chiu (1979); Yasumatsu
et al. 1975); NPPS & ZAU (1991)
Chu & Hirashima (1981); Chiu (1979); Yasumatsu
et al. 1975); NPPS & ZAU (1991)
Chu & Hirashima (1981); Chiu (1979); Yasumatsu
et al. 1975)
Lam (1992, 1996, 2000, 2002)
Chu & Hirashima (1981)
NPPS & ZAU (1991)
NPPS & ZAU (1991)
Chu & Hirashima (1981) (NPPS & ZAU 1991)
Wongsiri et al. (1980)
Lam (1992 1996, 2000, 2002)
Wongsiri et al. (1980)
Lam (1992, 1996, 2000, 2002)
Chu & Hirashima (1981); Chiu (1979); Yasumatsu
et al. 1975); NPPS & ZAU (1991)
Chu & Hirashima (1981); Chiu (1979); Yasumatsu
et al. 1975)
Lam (1992, 1996, 2000, 2002)
Chu & Hirashima (1981)
NPPS & ZAU (1991)
China (Taiwan)
Thailand
Tomosvaryella sylvatica
(Meigen)
Nilaparvata lugens
Nephotettix cincticeps
Tomosvaryella subvirescens
(Loew)
Nephotettix cincticeps
Nephotettix nigropictus
Nephotettix virescens
Nilaparvata lugens
Vietnam
China (Taiwan)
China (Guangxi, Henan)
China (Taiwan)
China (Fujian, Guangxi, Taiwan)
Thailand
Vietnam
Thailand
Vietnam
China (Fujian, Guangxi, Taiwan)
Thailand
Tomosvaryella sylvatica
(Meigen)
Nilaparvata lugens
Nephotettix cincticeps
Vietnam
China (Taiwan)
China (Guangxi, Henan, Taiwan)
Prospects for enhancing biological control
by parasitoids
Ecological engineering to enhance natural enemy
impact
The floral diversity of non-rice habitats around rice
fields is considered to be important in biological
control of rice pests (Lan et al., 2001), especially for
planthopper parasitoids (Yu et al., 1998). Mechanistically,
the availability of overwintering habitats is critical for egg
parasitoids of planthopper species that do not overwinter
locally. Unlike parasitoids of nymphs/adults, such as
Dryinids, egg parasitoids are by definition not carried
to new areas within the body of dispersing hosts.
Accordingly in Japan, Korea and much of China where
important delphacid pests such as N. lugens and S. furcifera
do not overwinter, grassy refuge areas that support
alternative host Hemiptera are critical in establishing
biological control of rice pests in early season crops.
Non-crop vegetation can also favour biological control
by providing plant foods, chiefly nectar, to natural
enemies. Although there is a surprising lack of studies
of the effects of nectar on parasitoids of rice pests there
is a large literature on enhancement of Hymenoptera
and Diptera natural enemies by food plants in other crop
types (Landis et al., 2000; Gurr et al., 2004). Rice bunds
have been largely overlooked as a means to provide plant
foods to natural enemies. Whilst nectar could maximise
longevity and fecundity of parasitoids, pollen could allow
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
generalist predators to reside even during periods of prey
scarcity (Wäckers, 2005).
Prospects for better biological control of planthoppers
by ecological engineering approaches such as habitat
manipulation appear particularly good in rice. An important reason for this is the heterogeneity, connectivity and
generally small patch size of the habitat. Although rice
crops may dominate landscapes in many rural Asian areas,
several factors combine to make the sizes of individual
crops small, with each bounded by a vegetated earthen
bank (‘bund’). First, rice is often grown in undulating,
even steep, terrain and bunds are critical for controlling
water and forming a series of flat, submerged terraces.
Second, the area of land owned or controlled by individual families is small, often less than 1 ha. Bunds are
important in delineating these and allowing foot traffic through otherwise inundated areas. Accordingly, rice
landscapes are richly innervated by a network of bunds
that offer scope to provide resources to natural enemies.
Although bund vegetation has been identified as a
potentially important factor in rice pest management
(Way & Heong, 1994), its potential is far from being
fully realised (Gurr, 2009). A study of the effects of
bund vegetation in the Philippines suggests that a reason
for the relative lack of progress in this area is the
possible risks (Marcos et al., 2001). Insect pests as well
as natural enemies were more abundant and species
richness was increased in rice paddies surrounded by
bunds with vegetation than in paddies without this
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Parasitoids of Asian rice planthoppers
feature. This illustrates the importance of research to
identify the types of vegetation that will preferentially
favour natural enemies; essentially the same refinement
as ‘selective food plants’ as found to be important in
habitat manipulation to favour parasitoids over potato
moth (Phthorimaea operculella (Zeller) in potato cropping
(Baggen & Gurr, 1998; Baggen et al., 1999) and over
lightbrown apple moth (Epiphyas postvittana Walker) in
vineyards (Begum et al., 2004, 2006).
A broad indication that such selectivity might be
possible for rice bunds comes from the results reported
by Marcos et al. (2001). Natural enemies were most
abundant in bunds with only broadleaf as opposed
to grassy weeds. Furthermore, adding support to the
need for careful selection of bund plant species, the
grasses Panicum repens, Cynodon dactylon, Dichanthium
aristatum and Commelina diffusa were found to be infected
with sheath blight and the adjoining edges of rice
paddies were sometimes also infected (Marcos et al.,
2001). That Philippine study also found that cowpea
(Vigna unguiculata L.) crops were important reservoirs of
natural enemies of rice pests. Parallel work in China
found that soy bean (Glycine max L. Merr.) served the
same function (Liu et al., 2001). Ideally, growing rows
of carefully selected plants on bunds could have the
dual benefit of supporting natural enemies and excluding
the grasses that potentially favour insect pests and plant
diseases such as tungro (Bottenberg et al., 1990) The need
to allow human foot traffic on bunds does not seem
to have been an impediment to the growth of other
crop species including sesame (Sesamum indicum (L.))
and soybean on bunds in recent work (International
Rice Research Institute, 2010b). Such crops can also be
established in wider strips beside rice crops whenever
they are bounded by larger banks such as beside river
banks or roadways, an approach being used in Thai sites
in the IRRI-led study.
Spatial manipulation of natural enemies with
herbivore-induced plant volatiles
Recent advances in chemical ecology suggest scope for
another way to enhance the impact of parasitoids and
other natural enemy guilds in rice. It is well established
that plants under attack by arthropod herbivores produce
volatile chemicals that attract natural enemies (Bruce
& Pickett, 2007). A range of such herbivore-induced
plant volatiles (HIPVs) has been identified, synthesised
and used in slow-release dispensers or as sprays. Under
field conditions HIPVs such as methyl-salicylate, cis3-hexen-1-ol, (Z)-3-hexenyl acetate and benzaldehyde
have resulted in elevated catches of natural enemies
(James, 2005). It also appears that the application to
168
G.M. Gurr et al.
plants of a single HIPV not only acts directly in attracting
natural enemies but can also induce the production of a
natural blend of HIPVs (Lou et al., 2005b). Such findings
suggest that applying synthetic HIPVs to crops can –
both directly and indirectly – attract the predators and
parasitoids that could protect crops from pest damage.
Recent field studies in sweetcorn, broccoli and grapevines
have shown that this approach can elevate catches of a
suite of hymenopteran parasitoid taxa in proximity to
treated plants (Simpson et al., 2010).
Prospects for such an approach to work in rice appear
strong (Gurr, 2009). Work on the role of ethylene signalling in rice showed that this hormone is involved
in induced defences against arthropod herbivores (Lu
et al., 2006). Rice attacked by N. lugens produced ethylene 2–24 h after infestation along with HIPVs. Thereafter, A. nilaparvatae was attracted to emitting plants. In
other work, Lou et al. (2005b) showed that exogenous
applications of jasmonic acid to rice plants dramatically
elevated levels of several volatiles including aliphatic aldehydes, alcohols, monoterpenes, sesquiterpenes, methylsalicylate and n-heptadecane. The potential for such
chemical ecology to be developed into a practical pest
management strategy is evident from a doubling of parasitism of N. lugens eggs by A. nilaparvatae on rice plants
that were surrounded by rice plants to which jasmonic
acid had been applied compared with control plants.
Although much remains to be resolved before HIPVs
can be used commercially to enhance biological control
(Gurr & Kvedaras, 2010) there is scope to develop
an ecological engineering approach based on applying
selected HIPV elicitors to rice to promote their sink
status for natural enemy populations. This would be
especially powerful if coupled with the provision of
nearby vegetation that served as overwintering source
vegetation for planthopper parasitoids. Indeed the whole
viability of this method depends on the presence of
sufficient source vegetation. Geospatial methods are
increasingly being used to shed light on the types and
placement of these habitat patches (Perović et al., 2010)
and these will be important in planning land use in
response to climate change. HIPVs could be used to draw
natural enemies into the crop when light trapping showed
immigration of planthoppers and when egg laying by the
pests was imminent. An additional layer in this strategy
could be the presence of nectar sources on bunds in an
‘attract and reward’ strategy as proposed by Khan et al.
(2008). The ‘reward’ component of this approach aims
to maximise the fitness and performance of attracted
natural enemies by providing appropriate sources of
nectar, pollen and shelter.
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
G.M. Gurr et al.
Impacts of genetically modified rice on planthopper
biological control
Higher rice yields are projected in China under a
scenario where widespread use of genetically modified
rice occurs (US Department of Agriculture, 2010).
Bt rice is likely to reduce problems with lepidopteran
pests, such as the leaffolder, and reduce the need
for insecticide applications. This has direct bearing on
prospects for improving biological control of planthopper
pests. The current high levels of usage of insecticide
applications targeting Lepidoptera are largely responsible
for disrupting biological control as is the case in other
crop systems such as apples (Valentine et al., 1996). This
disruption of ‘top down’ control of the pest population
allows build-up of rice planthoppers (Heong & Schoenly,
1998; Catindig et al., 2009). Reflecting this, a Chinese
study found parasitoid communities were more stable in
IPM areas compared to non-IPM areas where insecticide
use was greater (Mao et al., 2002a). But the extent to
which the advent of genetically modified crop varieties
might reduce insecticide inputs and allow natural enemy
communities to maintain better biological control of pests
depends on a range of ecological and operational issues
(Gurr et al., 2004).
At present there is very limited literature on the
influence of genetically modified Bt rice on parasitoids.
Chen et al. (2003) studied the effect of Bt transgenic
rice on the dispersal of planthoppers, leafhoppers and
their egg parasitoids. They reported that Anagrus spp.
tended to disperse towards non-transgenic rice although
reasons for this are unclear and little weight can be put
on this finding for the study was not replicated. The
consequences for pest management of any dilution of
natural enemy activity would be particularly negative for
planthopper problems because these will not be controlled
by Bt toxins.
Accordingly, the limited literature on the direct effects
of Bt rice on natural enemies and consequences for
planthoppers is inconclusive but there is good reason
to suspect that reductions in insecticide use will lead
to beneficial indirect effects. Planthoppers were only a
minor pest group before the 1960s (SBPH became major
pest around mid-1960s in Japan and China, BPH became
major pest in Asia in late-1960s) when broad-spectrum
insecticides, combined with hybrid rice varieties, resulted
in them becoming a major pest since 1980s (Sogawa
et al., 2003; Cheng et al., 2008). Although it is likely
that Bt rice will still require some insecticide applications,
Wang et al. (2010) conducted a 2-year field study that
compared Bt rice with non-Bt rice that was protected with
insecticides when necessary as well as with unsprayed Bt
and non-Bt rice. Larval densities of the Lepidoptera pests,
Ann Appl Biol 158 (2011) 149–176 2010 The Authors
Annals of Applied Biology 2010 Association of Applied Biologists
Parasitoids of Asian rice planthoppers
Chilo suppressalis (Walker), Tryporyza incertulas (Walker)
and Cnaphalocrocis edinalis (Guenee) were 87.5–100%
lower in unsprayed Bt plots than in unsprayed nonBt plots. Overall, insecticide use was reduced by 60 and
50% in protected Bt versus protected non-Bt plots in
the 2 years of the study. But Bt plants still required some
insecticide protection because its yield was 28–36% lower
than that of protected Bt rice.
A reduction in insecticide inputs of around 50%,
whether achieved by the introduction of Bt rice or
other approaches such as tighter regulation of pesticide
promotion and use, is likely to have significant benefits
for natural enemy activity on planthoppers.
In the work by Chen et al. (2007), no consistent benefit
of Bt rice was apparent on planthopper populations but
the comparison was with non-Bt rice treatment plots that
were not sprayed with insecticide without a comparison
with normal crop management of rice involving multiple
applications of insecticides as in the study by Wang et al.
(2010). Products in widespread use for the control of rice
stem borers and leaffolder in Asia are broad-spectrum
chemicals known to be harmful to natural enemies
(Tanaka et al., 2000).
A further factor that may benefit planthopper biological control if Bt rice is widely grown in China
(or should Lepidoptera specific insecticides become
available and economically viable), is the need for
a resistance management strategy (RMS). That for a
Bt crop would involve refuge areas (High et al., 2004)
that maintain sufficient numbers of wild-type susceptible Lepidoptera adults in the population, individuals
that have not been exposed to the selection pressure.
This reduces the likelihood that the resistant mutants
developing on the Bt rice will mate with each other
and produce resistant progeny. Because refuges need
to produce pest adults they will not be sprayed and
this is likely to also make them sources for natural
enemies that might contribute to better planthopper
control.
Conclusion
Notwithstanding the consequences for biological control
of planthoppers of the possible widespread growth of
Bt rice in China, most countries will continue to grow
conventional rice for the forseable future. Prospects for
better biological control of planthoppers in these areas
appear good given the available information although
reducing the currently high level of insecticide use is
important. The perceived need on the part of farmers
(often with low levels of education, training and literacy)
to protect the yield rice is one of several factors that
have led to high levels of synthetic insecticides being
169
G.M. Gurr et al.
Parasitoids of Asian rice planthoppers
used. This effect extends beyond protection of grain
yield to spraying in response to early season foliar
damage that has no effect on grain yield but can make
farmers lose ‘face’. This is driven by strong marketing
and advertising to exploit farmers’ fears. Further, the
high level of government subsidies, especially during
pest outbreaks, reinforces the notion that spraying is
beneficial and endorsed by the authorities. The present
review of the available literature indicates that, despite
the disruptive effects of insecticide use, parasitoids can
cause high levels of parasitism in delphacid populations
and that their impact can be manipulated ecologically.
Mymarids in particular, are strongly influenced by nonrice vegetation. Adjacent habitat patches can support
host insects and allow the persistence of planthopper
parasitoids during the winter. This is an important factor
because much rice production is in non-tropical parts
of Asia. Here rice is absent during the cooler months
and an absence of overwintering habitat would lead to
local extinction of specialist natural enemies. Providing
overwintering habitat would allow local persistence of a
natural enemy community that facilitates a rapid response
to immigrating pests. This is particularly important for
r-selected pests such as N. lugens that otherwise are able
to flee to enemy free space and rapidly multiply to
damaging densities. With greater pressure on available
land area for agricultural production and urbanisation
there will be pressure to make the best possible use of
those habitats that can be retained by applying optimal
management and establishing the most appropriate plant
species for natural enemy overwintering. Accordingly
research effort is required to systematically investigate
the relative merits for natural enemies of various
non-rice crop species as well as the non-crop species
used for grazing, erosion control or aesthetics. A ‘pull’
strategy based on synthetic HIPVs might be developed
to attract natural enemies into rice crops from other
habitats early in the season and prevent immigrating
planthoppers from reproducing. Rice bunds have long
been overlooked as a networked structure that could
support carefully selected plant species that provide plant
foods to natural enemies. Whilst nectar could maximise
longevity and fecundity of parasitoids, pollen could
allow generalist predators to reside even during periods
of prey scarcity. If ecological engineering approaches
could be expanded beyond delphacid pests, particularly
for lepidopterans, a holistic, biologically based pest
management strategy could emerge that would avoid
the need for exogenous toxins (whether sprayed or the
produce of transgenes) and the plea of Settele et al. (2008)
be answered.
170
Acknowledgements
This work was supported by the Asian Development
Bank 13th RETA project 6489 coordinated by the International Rice Research Institute, Los Baños Philippines
and the NSFC – IRRI International Cooperative Project
30+21140407 by the National Natural Science Foundation of China. The authors would like to thank to
Ms S. Villareal and Dr Ho Van Chien for their support.
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